Indian Journal of Geo Marine Sciences Vol. 46 (06), June 2017, pp. 1175-1182

Metazoan parasites of Otolithes ruber (Perciforme: Sciaenidae) of the Persian Gulf off Hendijan Region, Iran

Maryam Khosheghbal, Jamileh Pazooki* & Mohammad Reza Shokri

Department of Marine Biology, Faculty of Biological Sciences, Shahid Beheshti University, G.C., Tehran, Iran

*[E-mail: [email protected]]

Received 29 June 2015 ; revised 16 December 2015

Totally, 110 fish specimens were seasonally caught by gill net and hook from summer 2013 to spring 2014. Parasites were Diplectanum spp. (); Erilepturus hamati, Stephanostomum sp., Pleorchis sp. and Prosorhynchus sp. (Digenea); Philometra otolithi, Dichelyne spinigerus and Hysterothylacium sp. (Nematoda); Parabrachiella otolithi (Copepoda); and Gnathia sp. (Isopoda). No significant differences were found among the parasites analyzed with respect to the sex of the host except in digeneans. There were significant differences in parasites abundance among different seasons. No significant correlation was found between parasites abundance and total length of fish.

[Keywords: Commercial fish, Khozestan Province, tigertooth croaker]

Introduction which are polluted by majority of oil, gas and Fish parasitology is a significant study area in uncontrolled discharge of the sewage and aquatic sciences and fish parasites play a major industrial waste water. All these stresses and role in marine biodiversity. It is estimated that activities are posing a serious threat to the marine there are up to 100000 species of fish parasites1. environment and may be change and affect the As parasites may have negative effects on their parasitic fauna of marine organisms. Present hosts; thus, it is important to determine and study was undertaken to survey on metazoan identify the parasitic biodiversity2,3. Tiger tooth parasites of O. ruber one of commercially croaker Otolithes ruber (Bloch & Schneider, important fish from off Hendijan waters in the 1801) (Perciformes: Sciaenidae) with maximum northern Persian Gulf. Also effect of seasons, host length of 90 cm and maximum weight of 7 kg is a size and sex on incidence and occurrence of tropical commercial fish that occurs in marine and parasites were evaluated. brackish waters in Indo-West Pacific oceans. This benthopelagic species occurs mostly in coastal Material and Methods waters from East Africa, including Madagascar (excluding the Red Sea), eastward to the South A total of 110 specimens of O. ruber were China Sea and waters off Queensland, Australia4. seasonally caught by gill net and hook in Several investigations have been undertaken on Khozestan Province (off Hendijan), in the west parasitic fauna of different species of family northern Persian Gulf, Iran from 29° 45' to 30° 09' Sciaenidae in worldwide5-35. In spite of numerous N and 49° 30' to 50° 00' E (Fig. 1). Fish papers dealing with brackish and freshwater specimens were obtained from summer 2013 to parasitic fauna, only scanty information is spring 2014 and were immediately deep frozen available on parasites infesting marine fish until transfer to the Marine Parasitology Lab at species in Iran36-45. The Persian Gulf is one of Faculty of Biological Sciences of Shahid Beheshti commercially and economically important areas University, Tehran.

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parasites were embedded in permanent glycerine– gelatin preparations. Parasites identification carried out based on morphological features according to standard keys44-49. Identified parasites were deposited at Marine Parasitology Lab at Faculty of Biological Sciences of Shahid Beheshti University, Tehran.

Because data was not normally distributed, significant differences in parasites abundance with respect to the fish gender were explored using non- parametric Mann- Whitney U test. The Fig. 1: Sampling location in Khozestan Province, off significant differences in parasites abundance Hendijan in the north western of the Persian Gulf. among various seasons were determined using

After measuring weight and length of fish, all Kruskal-Wallis test with Mann- Whitney U test external and internal organs of the host were for pairwise comparisons. Non- parametric carefully examined by naked eye, stereo-and light Spearman correlation coefficient was used to microscopes for the presence of parasites based investigate the relationship between parasites on parasitology methods. Samples were studied abundance and total length of fish. Statistical using stereo microscopes NSZ-606 and light analyses were performed by the software package microscopes Nikon YS 100. isolated parasites of SPSS version 16.0. Prevalence, mean intensity were fixed and preserved in 4% formaldehyde and abundance were calculated based on Bush et Solution or in 70% ethanol. Monogeneans al.

Table1- Prevalence, mean intensity (±SD), abundance and site of infection for the metazoan parasites in O. ruber at Hendijan Region in the north western of the Persian Gulf.

Parasites Prevalence (%) Mean Intensity Abundance Site of Infection

Monogenea

Diplectanum sp1. 1.81 1±0.13 0.01 Gills and operculum Diplectanum sp2. 80.90 6.22±8.10 5.03 Gills and operculum

Digenea Pleorchis sp. Stephanostomum 0.90 1±0.09 0.01 Intestine sp. 54.54 3.13±2.46 1.70 Intestine Erilepturus hamati 84.54 5.96±6.21 5.03 Gill- Stomach Prosorhynchus sp. 6.36 2±0.52 0.12 Gill- Stomach

Nematoda Philometra otolithi 12.72 12±7.71 1.52 Gonad Dichelyne spinigerus 46.36 2.98±2.33 1.38 Intestine Hysterothylacium sp. 13.63 1.40±0.55 0.19 Stomach, Intestine and Mesenteries

Copepoda Parabrachiella otolithi 7.27 1.25±0.34 0.09 Gill

Isopoda Gnathia sp. 2.72 1±0.16 0.02 Gill

PAZOOKI et al.: METAZOAN PARASITES OF OTOLITHES RUBER (PERCIFORME: SCIAENIDAE) 1177

Results autumn and winter. The most infected organs were gills and stomach with 48.0% and 23.1%, Eleven species of metazoan parasites were respectively; while, they were less in operculum identified representing by two species of and mesenteries with 3.5% and 0.1%, respectively Monogenea, four species of Digenea, three (Fig. 7). species of Nematoda, one species of Copepoda and one species of Isopoda (Fig. 2−4, Table 1). The result of non- parametric Mann- Whitney U test showed no significant difference between the The results of this study showed that parasites analyzed with respect to the sex of the monogeneans and digeneans had the highest host except for digenetic trematodes (Z= -1.99; df occurrences on the host with 45.1% and 37.2%, = 1; P = 0.04). The result of Kruskal-Wallis test respectively, while copepod and isopod were less revealed significant differences among abundant with 0.8% and 0.1%, respectively (Fig. monogenean, nematode and copepod parasites in 5). As shown in Fig. 6, monogenean parasites different seasons (Table 2) and the Mann- were minimized in summer; while, frequently Whitney U test indicated pairwise comparison of recorded in spring. Highest infection rate of seasons with different parasites (Table 3). No trematodes was detected in winter and the lowest significant correlation was found between was in spring. Among the nematodes, peak parasites abundance and total length of fish. infection occurred in summer and spring, low in

Table 2- The results of Kruskal-Wallis test to determine significant differences among parasites in different season

Mon Dig Nem Cop Iso Chi-square 14.188 5.367 21.006 16.778 3.169 df 3 3 3 3 3 P- value 0.003 0.147 0.000 0.001 0.366

Fig. 2: A. Parabrachiella otolithi B. Gnathia sp. C. Fig. 3: A. Prosorhynchus sp. B. Erilepturus hamati C . Diplectanum sp1. D. Opisthaptor of Diplectanum sp1. E. Pleorchis sp. D. Stephanostomum sp. E. Anterior part Diplectanum sp2. F. Opisthaptor of Diplectanum sp2. of Philometra otolithi, male F. posterior part of P. otolithi, male.

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Fig. 5: Occurrence of parasites on O. ruber (%)

Fig. 4: A. Anterior part of P. otolithi, female B. posterior part of P. otolithi, female C. Anterior part of Hysterothylacium sp. D. posterior part of Hysterothylacium sp. E. Anterior part of Dichelyne spinigerus, female F. posterior part of D. Fig. 6: Occurrence of parasites in different seasons (%) spinigerus, female G. Anterior part of D. spinigerus, male H. posterior part of D. spinigerus, male.

Fig.7: Parasitic infection in different organs of O. ruber (%) Mesen: Mesenteries, Operc: Operculum

Table 3- The results of pairwise comparisons among seasons obtained from Mann- Whitney U test * P<0.05; 1: summer, 2: autumn, 3: winter, 4: spring mongen digen nematode copepod isopod 1 vs. 2 0.92 0.78 0.41 0.08 0.24 1 vs. 3 0.31 0.29 0.06 0.33 1.00 1 vs. 4 0.006* 0.28 0.05 0.08 0.41 2 vs. 3 0.42 0.49 0.24 0.31 0.15 2 vs. 4 0.01* 0.15 0.001* 0.001* 0.55 3 vs. 4 0.001* 0.02* 0.000* 0.006* 0.31

PAZOOKI et al.: METAZOAN PARASITES OF OTOLITHES RUBER (PERCIFORME: SCIAENIDAE) 1179

Discussion et al.56 described different species of Prosorhynchus spp. from some families of fish Fish is one of the important sources of protein in such as Serranidae, Carangidae and Trichuridae in the world. Due to limited marine resources and the off coast of Kuwait. In the current study O. need to artificial aquaculture, parasitic infection ruber was introduced as a new host for this of fish is a serious threat and should not be species and Prosorhynchus sp. was reported for neglected. Parasites are known to potentially the first time in Iran. Peyghan et al.37 reported decrease the survival or the reproduction of host Elythrophallus sp., Lecithocladium sp. and 51 populations , so parasitism is largely considered Alloceraadium sp. from this host in Khozestan in studies of biodiversity. Province, Iran. None of the mentioned trematodes by Peyghan et al.37 were found in this study. This study reports the first record of genus Isopod Likewise, they introduced Pleorchis sp. and Gnathia sp. in tigertooth croaker Otolithes ruber Stephanostum sp. from Lutjanus malabaricus in the northern Persian Gulf. Gnathiids are a small (Perciforme: Lutjanidae) in khozestan province, group of marine isopods with parasitic juveniles Iran. which feed on blood and lymph of and 52 elasmobranch fishes . The free-living adults do In this study three species of nematode parasites not feed and are usually hidden in a cavity or were observed. Philometra otolithi was reported 53 sponge where reproduction will occur . by Moravec and Manoharan32 from O. ruber in 34,35 Previously Rameshkumar et al. reported two eastern of India. Two Philometrid nematodes isopod namely Nerocila longispina and N. were also described by Moravec et al.44 in ovary sundaica from O. ruber in southeastern coast of and caudal fin of the host in Iran namely P. India. otolithi and Clavinemoides annulatus, In the present study, two different species of respectively. Likewise, Moravec et al.45 were Diplectanum spp. were reported in generic level. recorded Dichelyne spinigerus in intestine of O. Species of Diplectanum Diesing, 1858, which are ruber in the Persian Gulf, Iran. In present study characterised by the presence of a dorsal and a no nematode parasites was observed in caudal fin. ventral squamodisc, three bars and two pairs of The result of statistical analyses showed a hamuli on the haptor, and a sclerotised tubular significant difference between digenetic copulatory organ, have been recorded from both trematodes with respect to sex of the host; 54 9 marine and freshwater fishes . Kritsky et al. also whereas, females harbored more parasites than stated two different species of Diplectanum spp. males. According to Siddiqui57 the differences in in generic level from O. argenteus in coastal the infection levels of the parasites in the male waters of the Persian Gulf off Kuwait. D. and female hosts may be due to the physiological 12 squamatum was described by Santos et al. in changes in quantity and quality of steroid another species of Sciaenid fish namely hormone presumably androgens of male and Cynoscion guatucupa in southwest of Atlantic estrogens of female hosts. Singha et al.58 16 Ocean. Sabas and Luque also introduced this suggested the infestation of a number of parasites species from C. guatucupa and Macrodon in females was the results of differences in their ancylodon both from family Sciaenidae in coastal food habits and feeding behavior. Likewise, 13 waters of Brazil. Jianying et al. mentioned D. Siddiqui57 described that difference of distribution furcelamellosum in O. ruber and Domingues and of parasites between the different sexes were not 21 Boeger reported this species and also D. due to any one single factor, but it might be due to maculltum in this host. combination of several factors including host’s

7 diet and their physiology. Alkawari et al. reported Pleorchis sp. in O. ruber 59 16 Bell and Burt stated that parasite species in the Persian Gulf. Sabas and Luque introduced richness could be positively correlated with host P. americanus from two member of this family of local abundance because more abundant hosts fishes (Sciaenidae) in the coastal zone of the State 20 would be more readily sustain populations of of Rio de Janeiro, Brazil. Shaukat and Bilqees parasites. In this study density of hosts was recorded P. heterorchis from the host and unbalanced (up to 110 fish examined, 69 females Lutjunus johinii (Lutjanidae) in Karachi coast, 15 and 41 males) that may be the reason for the Pakistan. Nahhas and Say stated Erilepturus higher parasitism record shown by females which, hamati from the host in off coastal waters of 55 as they were more abundant in ecosystem, seem Kuwait. Bray et al. detected this species from L. to be more exposed to parasites. caronotatus in Lizard Island, Queensland. Nahhas

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Moreover host feeding preferences were Acknowledgements considered to be important for endoparasite species richness because of their complex life Authors would like to thank Dr. Mohsen Safaei cycle59,60. Indeed, a carnivorous diet represents a and Mrs. Zahra Masoumizadeh for providing large number and a taxonomically diverse range sampling facilities. This research was supported of potential intermediate hosts, which may favor by Shahid Beheshti University, G. C. an accumulation of parasite species59. References The maximum infection rate was recorded for monogenean parasites. According to Rohde61,62 1. Jakob, E., & Palm, H.W., Parasites of the diversity of parasites may increase with a commercially important fish species from the decrease in latitudinal distribution. On the other southern Java coast, Indonesia, including the distribution pattern of trypanorhynch cestodes, hand, the number of monogenean species Verh. Ges. Ichthyol. Bd., 5 (2006) 165-191. increases from temperate waters to tropical 2. Poulin, R., & Morand, S., The Diversity of waters. Perhaps one of the reasons for increasing Parasites. Q. Rev. Biol., 75 (2000) 277–293. gill infection is that Hendijan is located in the 3. Simkova, A., Morand, S., Matejusova, I., Jurajda, 3 P., & Gelnar, M., Local and regional influences on tropical area. Simkova revealed that fishes living parasite species richness of central European in calm water (limnophilous) and/or at the bottom fishes, Biodivers. Conserve., 10 (2001) 511-525. of rivers (benthic fish) harbor more ectoparasite 4. Froese, R., & Pauly, D., FishBase, World Wide species than fishes living in running water or Web electronic publication., pelagic fishes. Indeed Simkova3 detected that host http://www.fishbase.org, (2013) (version 04/2013). 5. Williams, A., Some monogenean parasites of the habitat may mainly affect the variability in genera Calceostoma van Beneden, 1852 and ectoparasite species richness. Diplectanum Diesing, 1858 Irom Argyrosomus Furthermore high infection rate on the gills might hololepidotus (Lacepede, 1802) (Sciaenidae: be attributed to fact that the gills are in great Teleostei) in Western Australia, Syst. Parasitol., 14 contact to the external water surrounding as a (1989) 187-201. 63,64 6. Bray, R.A., Hemiuridae (digenea) from marine result of their respiratory activities . According fishes of the southern Indian Ocean: Dinurinae, to Hanzelova and Zitnan65 fish are exposed to the Elytropallinae, Glomericirrinae and Plerurinae, increased monogenean infection during the Syst. parasitol., 17 (1990) 183-217. spawning period. The spawning of O. ruber takes 7. Alkawari, K.S.R., Saoud, M.F.A., & Ramadan, M.M., Biodiversity of helminth parasites of fishes place at the end of winter and earlier spring in the in the Arabian Gulf, with special reference to north west of the Persian Gulf. digenetic trematodes and cestodes, Qatar Univ. Sci. Amin (1975) found that season influenced the J., 16 (1996) 141-153. parasitic infection in two ways. One is the 8. Timi, J.T., & Etchegoin, J.A., A new species of Lernanthropus (Copepoda: Lernanthropidae) influence of change in atmospheric conditions on parasite of Cynoscion striatus (Pisces : Sciaenidae), the definitive host causing physiological changes from Argentinean waters and new records of which in turn influences the occurrence of Lernanthropus trachuri (Brian, 1903), Folia parasitic population and the other is the influence Parasitol., 43 (1996) 71–74. of season on the availability of the suitable 9. Kritsky, D.C., Ruiz, F.A.J., & Sey, O., Diplectanids (Monogenoidae: Dactylogyridea) intermediate host. from the gills of fishes of the Persian Gulf off 57 Siddiqui mentioned that intensity of invasion in Kuwait, Comp. Parasitol., 67 (2000) 145-164. different season is may be due to feeding habit, 10. Alves, D.R., & Luque, J.L., Metazoan parasites of availability of food, physiological changes and Micropogonias furnieri (Osteichthyes: Sciaenidae) from the coastal zone of the State of Rio Janeiro, hydrobiological conditions. Brazil, Parasitol. dia., 24 (2000) 40-45. Seasonal abundance of helminth parasites is 11. Alves, D.R., & Luque, J.L., Community Ecology influenced by various factors such as host of the Metazoan Parasites of White Croaker, hibernation, spawning of the host fish, changes in Micropogonias furnieri (Osteichthyes: Sciaenidae), the immune response of fish at different from the Coastal Zone of the State of Rio de Janeiro, Brazil, Mem. Inst. Oswaldo Cruz., 96 temperatures, and the feeding habits of the host (2001) 145-153. 65,67 fish . 12. Santos, C.P., Timi, J.T., & Gibson, D.I., Fish parasites are an integral part of water Diplectanum squamatum n. sp. (monogenea: ecosystems and they are common in natural and ) from the gills of Cynoscion 68 guatucupa (Sciaenidae) in southwest Atlantic cultured populations of fish . Unfortunately, very waters, Syst. parasitol., 52 (2002) 199-204. little research has been done on identify and 13. Jianying, Z., Tingbao, Y., Lin, L., & Xuejuan, D., pathogenesis of marine fish parasites in Iran and A list of monogeneans from Chinese marine fishes, more researches are needed. Syst. parasitol., 54 (2003) 111-130 PAZOOKI et al.: METAZOAN PARASITES OF OTOLITHES RUBER (PERCIFORME: SCIAENIDAE) 1181

14. Luque, J.L., Alves, D.R., & Ribeiro, R.S., 26. Timi, J.T., Lanfranchi, A.L., Tavares, L.E.R., & Community ecology of the metazoan parasites of Luque, J.L., A new species of Dichelyne Banded Croaker, Paralonchurus brasiliensis (Nematoda, Cucullanidae) parasitizing sciaenid (Osteichthyes: Sciaenidae), from the coastal zone fishes from off the South American Atlantic coast, of the State of Rio de Janeiro, Brazil, Acta Sci. Acta Parasitol., 54 (2009) 45–52. Biol. Sci., 25 (2003) 273-278. 27. Fernandes, B.M.M., Arci, A.D.N., & Cohen, S.C., 15. Nahhas, F.M., & Sey, O., Digenetic trematodes New data on some species of Monogenea and from marine fishes off the coast of Kuwait, Digenea parasites of marine fish from the coast of Arabian Gulf: super family Hemiuroidea, Acta the State of Rio de Janeiro, Brazil, Rev. Bras. Zool. Acad. Sci. Hung., 48 (2002) 1-20. Parasitol. Vet., 18 (2009) 13-18. 16. Sabas, C.S., & Luque, J.L., Metazoan parasites of 28. Iannacone, J., Morón, L., & Guizado. S., Between- weakfish, Cynoscion guatucupa and Macrodon year variation of metazoan parasite fauna on ancylodon (Osteichthyes: Sciaenidae), from coastal Sciaena deliciosa (Tschudi, 1846) (Perciformes: zone of the state of Rio De Janeiro, Brazil, Rev. Sciaenidae) in Lima, Peru, Lat. Am. J. Aquat. Res., Bras. Parasitol. Vet., 12 (2003) 171-178. 38 (2010) 218-226. 17. Bartoli, P., Gibson, D.I., & Bray, R.A., 29. Gupta, R., Johri, S., Chandra, S., & Saxena, A.M., Redescription of Pleorchis polyorchis (Stossich, A discussion of trematode genus Pleorchis Railliet, 1889) (Digenea: Acanthocolpidae), a rare and 1896 ( Digenea: Pleorchiidae Poch, 1926) with poorly known parasite of the intestine of Sciaena description of two new species from the intestine umbra L. (Perciformes: Sciaenidae) from the of marine fishes from the Indian Ocean, Pakistan J. western Mediterranean Sea, Syst. parasitol., 58 Zool., 43 (2011) 191-199. (2004) 81-90. 30. Cardenas, M.Q., Fernandes, B.M.M., Justo, 18. Amin, O.M., & Christison, K.W., M.C.N., Santos, A.L., & Cohen, S.C., Helminth Neoechinorhynchus (Neoechinorhynchus) parasites of Ctenosciaena gracilicirrhus dorsovaginatus n. sp. (Acanthocephala: (Perciformes: Sciaenidae) from the coast of Angra Neochinorhynchidae) from the dusky kob dos Reis, Rio de Janeiro Stat, Brazil, Rev. Mex. Argyrosomus japanicus (Sciaenidae) on the Biodivers., 83 (2012) 31-35. southern coast of South Africa, Syst. Parasitol., 61 (2005) 173- 179. 31. Vijayakumar, P., & Veerappan, N., Endohelminth 19. Boeger, W.A., Fehlauer, K.H., & Marques, E.E., parasites of two scianidae fishes from the south- Neotropical Monogenoidea. 49. Four new species east coast of India, Int. J. Environ. Biol., 2 (2012) of the Diplectanidae (Dactylogyrinea) from the 183-186. gills of some pachyurines (Teleostei: Sciaenidae) 32. Moravec, F., & Manoharan, J., Gonad-infecting from the Rio Tocantins and Rio Doce Basins, with philometrids (Nematoda: Philometridae) including the proposal of Anoplectanum n. g. and four new species from marine fishes off the eastern Spinomatrix n. g., Syst. Parasitol., 64 (2006) 57- coast of India. Folia Parasitol, 60 (2013) 105-22. 68. 33. Al-Jufaili, S., Machkevskyi, V., Al-Sulaimi, S., 20. Shaukat, N., & Bilqees, F.M., Pleorchis Faraj, R.B., & Al-Mazrooei, N., Biological and heterorchis n. sp.(Digenea: Acanthocolpidae Luhe, Ecological Features of Poecilancistrum Sp. 1909) from fishes Lutjunus johinii and, Otolithus Plerocercoid (Cestoda: Trypanorhyncha) Infection argenteus of Karachi coast, Pakistan (Abstract), of Arabian Sea Meager Argyrosomus heinii Bangladesh j. Fish. Res., 10 (2006). (Steindachner, 1907), J. Aquac. Res. Development., 21. Domingues, M.V., & Boeger,W.A., Phylogeny and 5(2014) 3. revision of Diplectanidae Monticelli, 1903 34. Rameshkumar, G., Ravichandran, S., & Trilles, (Platyhelminthes: Monogenoidea), Zootaxa., 1698 J.P., Cymothoidae (Crustacea, Isopoda) from (2008) 1-40. Indian fishes, Acta Parasitol., 56 (2011) 78-91. 22. Mendoza, J.M., Maldonado, G.S., & 35. Rameshkumar, G., Ramesh, M., Ravichandran, S., Mendozapalmero, C.A., Monogenean parasites of Trilles, J.P., & Shobana, C., Nerocila sundaica Carangidae and Sciaenidae marine fish on the (Isopoda, Cymothoidae) parasitizing Otolithes Alvarado coast, Veracruz, Mexico, south Gulf of ruber from Nagapattinam, Southeast coast of India, Mexico, Zootaxa., 1843 (2008) 47-56. J. Parasit. Dis., 38 (2014) 1-4. 23. Sudhakar, S., Anbalagan, T., Veerappan, N., 36. Peyghan, R., Hoghoghi Rod, N., & Desfuli, Y., Soundrapandian, P., & Arumugam, R., Nematodes Determination of parasitic helminthes in Persian parasites from Sciaenids fishes of parangipettai, Gulf grouper, (Epinephelus coioides), and silver southeast coast of India, Curr. Res. J. Biol. Sci., 1 pomfret, (Stromateus cinereus), Vet. J. (Pajouhesh (2009) 6-10. va Sazandegi) 62 (2004) 49–55. 24. Boxshall, G.A., & El-Rashidy, H.H., A review of 37. Peyghan, R., Hoghoghirad, N., Mesbah, M., & the Caligus productus species group, with the Rastkerdar, M., Frequency of helminthic infection description of a new species, new synonymies and in Tiger Tooth croaker, Otolithes ruber, Black supplementary descriptions, Zootaxa., 2271 (2009) pomfret, Parastromateus niger; Javelin grunter, 1–26. Pomdasys kaakan and Malabar blood snapper, 25. Casal, G., Garcia, P., Matos, P., Monteiro, E., Lutjanus malabaricus of Persian Gulf, Iran, J. Vet. Matos, E., & Azevedo, C., Fine structureof Res., 10 (2006) 81-87. Chloromyxum menticirrhi n. sp. 38. Khaleghzadeh, A.H., Malek, M., & Valinasab, T., (Myxozoa)infecting the urinary bladder of the First record of the parasitic copepod, Brachiella marine teleost Menticirrhus americanus trichiuri Gnanamuthu, 1951 (Crustacea: (Sciaenidae) in Southern Brazil, Eur. J. Protistol., Lernaeopodidae) on Trichiurus lepturus L. 45 (2009) 139-146.

1182 INDIAN J. MAR. SCI., VOL. 46, NO. 06, JUNE 2017

(Osteichthyes: Trichiuridae) in the Persian Gulf, 53. Hadfield, K.A., Smit, N.J., & Oldewage, A.A., Iran. J. Anim. Biosyst., 5 (2009) 17-21. Gnathia pilosus sp. nov. (Crustacea, Isopoda, 39. Abdi, K., Mokhayer, B., Jalali, B., Mobedi, I., Gnathiidae) from the East Coast of South Africa, Ahmadi, M.R., Mirzargar, S., Meshgi, B., & Zootaxa., 1894 (2008) 23–41. Bahonar, A., The identification and study of 54. Oliver, G., Les Diplectanidae Bychowsky, 1957 monogenetic parasites in the gills of wild and (Monogenea, , Dactylogyridea) cultured yellow- fin seabreams (Acanthopagrus marqueurs biologiques, temoins de la latus Houttuyn, 1782) in Persian Gulf coasts, J. biogéographie et de l’évolution de leurs hôtes, Bull. Vet. Res., 64 (2009) 301-306. Soc. Zool. Fr., 118 (1993) 25–36. 40. Bagherpour, A., Afsharnasab, M., Mobedi, I., 55. Bray, R.A., Cribb, T.H., & Barker, S.C., Jalali, B., & Mesbah, M., Prevalence and intensity Hemiuridae (Digenea) from marine fishes of the of internal parasitic helminthes infected Black sole Great Barrier Reef, Queensland, Australia. Syst. fish, Brachirus orientalis (Bloch and Schneider, Parasitol., 25 (1993) 37-62. 1801) in the Persian Gulf, Iranian J. Fish. Sci., 10 56. Nahhas, F.M., Sey, O., & Nakahara, G., Digenetic (2011) 570-584. trematodes of marine fishes from the Arabian Gulf 41. Eslami, A., Sabokroo, H., & Ranjbar- Bahadori off the coast of Kuwait. Family Bucephalidae S.H., Infection of Anisakids Larvae in Long Tail Poche, 1907, and the description of a new species, Tuna (Thunnus tonggol) In North Persian Gulf, Helminthologia., 43 (2006) 147 – 157. Iran. J. Parasitol., 6 (2011) 96–100. 57. Siddiqui, A.A., Effects of seasons, host age, size 42. Haseli, M., Malek, M., Valinasab, T., & Palm, and sex on monogenetic trematode, H.w., Trypanorhynch cestodes of teleost fish from Hamatopeduncularia indicus of host fish, Arius the Persian Gulf, Iran, J. Helminthol., 85 (2011) jella, J. Chem. Biol. Phys. Sci., 4 (2014) 1146- 215-224. 1151. 43. Pazooki, J., Khosheghbal, M., & Masoumian, M., 58. Singha, R., Shomorendra, M., & Kar, D., Parasite A survey on Otolithes ruber fish infection to infection of three freshwater fishes in Dolu Lake, metazoan parasites in the Persian Gulf, J. Vet. Res., Silchar, Assam, Int. J. Fish. Aquat. Stud., 2 (2015) 68 (2013) 53-60. 125-127. 44. Moravec, F., Khosheghbal, M., & Pazooki, J., Two 59. Bell, G., & Burt, A., The comparative biology of philometrids (Nematoda: Philometridae) infecting parasite species diversity: intestinal helminths of the tigertooth croaker Otolithes ruber (Bloch & freshwater fishes, J. Anim. Ecol., 60 (1991) 1046- Schneider) (Teleostei: Sciaenidae) off Iran, 1063. including erection of a new genus, Syst. Parasitol., 60. Price, P.W., & Clancy, K.M., Patterns in number of 86 (2013) 33–41. helminth parasite species in freshwater fishes, J. 45. Moravec, F., Khosheghbal, M., & Pazooki, J., Parasit., 69 (1983) 449-454. Dichelyne (Dichelyne) spinigerus sp. 61. Rohde, K., Latitudinal gradients in species nov.(Nematoda: Cucullanidae) from the marine diversity and their causes. I. A review of the fish Otolithes ruber (Sciaenidae) off Iran and first hypotheses explaining the gradients, Biol. description of the male of Philometra otolithi Zentralbl., 97 (1978) 393-403. Moravec et Manoharan, 2013 (Nematoda: 62. Rohde, K., Simple ecological systems, simple Philometridae), Acta Parasit., 59 (2014) 229–237. solution to complex problems, Evol. Theory., 8 46. Yamaguti S, Systema helminthum. Monogenea and (1989) 305-350. aspidocotylea,( Interscience Publishers., New 63. Roberts R J, Fish pathology, (Bailliere Tindall, York) (1963) pp. 699. London) (1978) pp 318. 47. Gibson D I, Jones A & Bray R A, Key to the 64. Bichi, A.H., & Ibrahim, A.A.A., Survey of ecto trematoda, (CAB international and the nature and intestinal parasites of Tilapia zillii (Gervias) in history museum., London) (2002), pp. 521. Tiga Lake, Kano, northern Nigeria, Bayero J. Pure 48. Jones A, Bray R A & Gibson D I, Key to the Appl. Sci., 2 (2009) 79 – 82. trematoda, (CAB international and the nature 65. Hanzelova, V., & Zitnan, R., Epizootiological history museum., London) (2005) pp. 745. importance of the concurrent monogenean invasion 49. Pillai N K, Fauna of India: Parasitic copepods of in the carp, Helminthologia., 22 (1985) 277-283. marine fishes, (Technical and General Press., 66. Amin, O.M., Host and seasonal association of Calcutta) (1985) pp.900. Acanthocephalus parksidei (Acanthocephala: 50. Bush, A.O., Laffertyt, K.D., Lotz, J.M., & Shostak, Echinorhynchidae) in Winconsin fishes, J. A.W., Parasitology meets ecology on its own Parasitol., 61 (1975) 318-329. terms: Margolis et al. Revisited, J. Parasitol., 83 67. Chubb, J.C., Seasonal occurrence of helminths in (1997) 575-583. freshwater fishes. Part I. Monogenea, Adv. 51. Minchella, D.J., & Scott, M.E., Parasitism: a Parasitol., 15 (1977) 133-199. cryptic determinant of community structure. 68. Scholz, T., Parasites in cultured and feral fish, Vet. Trends Ecol. Evol., 6 (1991) 250-253. Parasitol., 84 (1999) 317-335. 52. Smit, N.J., & Davies, A.J., The curious life-style of the parasitic stages of gnathiid isopods, Adv. Parasitol., 58 (2004) 289-391.