Iran. J. Ichthyol. (September 2017), 4(3): 281-289 Received: May 30, 2017 © 2017 Iranian Society of Ichthyology Accepted: September 15, 2017 P-ISSN: 2383-1561; E-ISSN: 2383-0964 doi: 10.22034/iji.v4i3.22902.015 http://www.ijichthyol.org

Research Article

Reproductive biology of female Oxynoemacheilus bergianus (Actinopterygii: Cypriniformes: Nemacheilidae) from the Jajrud River, the Namak Lake basin, central Iran

Amir POURSHABANAN1, 2, Alireza SARI1, Hamed MOUSAVI-SABET*3, 4

1School of Biology and Centre of Excellence in Phylogeny of Living organisms, College of Science, University of Tehran, Tehran, Iran. 2Department of Biology, Faculty of Sciences, Ferdowsi University of Mashhad, Mashhad, Iran. 3Department of Fisheries, Faculty of Natural Resources, University of Guilan, Sowmeh Sara, Guilan, Iran. 4The Caspian Sea Basin Research Center, University of Guilan, Rasht, Guilan, Iran. * Email: [email protected]

Abstract: Loach fishes of the genus Oxynoemacheilus, are found in Iran and adjacent countries, but their reproductive parameters are barely known. The main aim of this study was to obtain reproductive characteristics of Oxynoemacheilus bergianus (Derjavin, 1934). Sampling was carried out at monthly intervals throughout the year and 279 individuals of O. bergianus were caught from the River Jajrud in the Namak Lake basin, central Iran. Age, fecundity, oocyte diameter and Gonado-Somatic Index (GSI) were examined. Regression analyses were used to find relations between fecundity and fish size, gonad weight (Wg) and age. The average egg diameter ranged from 142.8 micrometer (August) to 513.1 micrometer (March). Spawning took place in March, when the water temperature was between 16 and 20°C. The average GSI values for females at the beginning of the reproduction period (February) and in ripe mature females (March), were 9.8% and 22.4%, respectively. The averages of absolute and relative fecundity (relative to body weight) were 2792.4 eggs (SE±692.5) and of 637.9 (SE±119.6) per gram body weight, respectively. The absolute fecundity was significantly related to body weight and ovary weight. Based on the pattern of GSI, it was concluded that this fish has a relatively prolonged active reproductive period. The present knowledge could be used in the conservation and management strategies intended to maintain the O. bergianus stock. Keywords: Life history, Spawning season, Reproductive indices, Nemacheilidae. Citation: Pourshabanan, A.; Sari, A. & Mousavi-Sabet. H. 2017. Reproductive biology of female Oxynoemacheilus bergianus (Actinopterygii: Cypriniformes: Nemacheilidae) from the Jajrud River, the Namak Lake basin, central Iran. Iranian Journal of Ichthyology 4(3): 281-289.

Introduction including the Anzali lagoon, and middle Aras, Shafa, According to Esmaeili et al. (2017), 51 loach species Siyah, Masouleh and Sefid Rivers and its upper belonging to two families Nemacheilidae and tributaries (Qezel Owzan and Shahrud) of Caspian Cobitidae and eight genera have been recorded from Sea basin; Karaj, Jajrud, upper Shur or Abhar, middle 19 water basins of Iran. Of these, 31 species are and upper Qareh Chai and upper Qom rivers of the endemic to Iran including Oxynoemacheilus Namak Lake basin, southern and eastern tributaries bergianus (Jouladeh-Roudbar et al. 2015; Esmaeili et of Lake Urmia basin (Zarineh, Tata'u and Talkheh al. 2017). This species is widely distributed in Iran Rivers), and possibly in the eastern Dasht-e Kavir 281

Iran. J. Ichthyol. (September 2017), 4(3): 281-289

basin (Saadati 1977). The biological aspects of most (energy level: 200–300 V; distance between loach species in Iran are unknown especially the electrodes: 10-50 meters; area covered each time: information is limited about the life history and 100 meters; water depth covered: 40-120 cm; reproduction of Nemacheilidae (Mousavi-Sabet et al. substrate of the fishing areas: with diverse structures 2016b, 2017b; Coad 2017). Additionally, there is an including pools, riffles, gravel bed, sandy shore, etc.) urgent need to determine the habitat state, food habits and hand net from the Jajrud River (35°34′ to and systematic of this species in Iran. Currently, 35°47′N, 51°47′ to 51°40′E) in the Namak Lake basin, biological data on loaches are available on spined Tehran Province, Iran. All specimens were fixed and loaches (genus Cobitis) in the southern Caspian Sea preserved in 4% formaldehyde solution and basin (Mousavi-Sabet et al. 2011, 2012b, 2012c). transferred to the laboratory. For each specimen total According to Saadati (1977), O. bergianus is length (TL), fork length (FL) and standard length categorized as near threatened species. (SL) were measured using digital caliper with a Drought, as a main threatening factor of precision of 0.01 mm; body weight (g) was taken on biodiversity loss in Iran, has dried up many natural a digital balance with 0.001 g accuracy. Sex was springs, marshes, ponds and streams (Mousavi-Sabet determined by examination of the gonad tissue either et al. 2013, 2016a). The water flow is reduced with eye or by microscopic examination of the especially in the most main rivers and tributaries of gonads (using a binocular 25-40×). Gonado-Somatic the Tigris drainage threatening specifically the Index (GSI) index was used to investigate the habitat of small fish either endemic or limited to this monthly changes in gonads in order to estimate the region. In addition, industrial, agricultural and spawning season of the species. In order to determine aquaculture wastes, as the main sources of water GSI, Biswas (1993) was followed: GSI [= (Wg× Wb pollution, have significantly increased in the recent –1)×100]. Also, to determine the number of eggs two decades in Iran that affected the fauna and flora (fecundity), approximately 0.05 g pieces of ovary of freshwater habitats (Mousavi-Sabet et al. 2013, tissue were removed, each from the anterior, medial 2016a). Fisheries management organizations some- and posterior positions of both ovarian lobes times measure the likely impact of fishing on a stock (Mohammadi-Darestani et al. 2016; Mansouri- by estimating its relative spawning potential (Mace Chorehi et al. 2016). The ovary pieces were weighed 1994). Today, it is clear and recognized how and their eggs were counted under a binocular reproductive biology affects population productivity. microscope. The number of eggs in each female was The reproductive potential, i.e., fecundity is an calculated as the proportion of eggs in the sample to important biological parameter that plays a the weight of the whole ovary. To calculate absolute significant role in evaluation the commercial fecundity, ovaries at four or five stages were used. potentials of fish stocks (Gómez-Márquez 2003; The absolute fecundity (Fa) was estimated in 30 Mousavi-Sabet et al. 2017a). The principal object of ovaries by counting the 0.1 g oocytes weight (Biswas this study was to provide data on the reproductive 1993). The stage of gonad maturity was determined biology of O. bergianus, including gonado-somatic visually following the Nikolsky scale (Nikolsky index, fecundity, oocyte diameter, and spawning 1963). The relative fecundity (Fr) was expressed by season duration, which are necessary for dividing the absolute fecundity (Fa) by the fish body conservation and management programs of this fish. weight. The result was the number of eggs per gram of body weight (Bagenal 1967). To determine the Materials and Methods ovum diameter, the ovaries were preserved in 4% Fish individuals were collected monthly from formaldehyde solution. The age of fish was assessed January 2012 to December 2012 by electrofishing based on the annual growth of scales taken from the 282 Pourshabanan et al.- Reproduction of Oxynoemacheilus bergianus

Table 1. Fork length (FL), standard length (SL), total length (TL) and body weight (W) (mean±SD) in different ages of females Oxynoemacheilus bergianus from the Jajrud River.

Age N FL (mm) SL (mm) TL (mm) W (g) 1+ 46 35.7±2.2 30.6±2.1 37.1±2.3 0.33±0.07 2+ 84 43.0±3.0 36.9±3.0 44.9±3.1 0.62±0.15 3+ 74 52.8±2.6 45.2±2.4 55.1±2.7 1.17±0.26 4+ 61 62.1±2.3 53.7±2.2 64.7±2.4 2.30±0.61 5+ 14 69.4±1.7 60.8±2.9 72.6±1.6 3.52±0.70 N: number of specimens; SD: standard deviation. Table 2. Absolute (Fa) and relative (Fr) fecundity in particular ranges (according to age) of Standard length (SL) and body weight (W) for females Oxynoemacheilus bergianus from the Jajrud River.

Parameters Groups N Fa Fr Range Mean±SE Range Mean±SE 30.0-53.2 12 106.1-2850.7 1478.4±366.5 75.8-550.0 289.7±96.8 SL (mm) ≥ 53.2 18 1057.4 -5165.9 3676.7±351.5 470.4-1006.7 768.0±79.0 1.4-2.1 13 106.1-1057.4 581.8±186.9 75.6-498.0 348.0±93.0 W (g) 2.2-4.4 10 1598.9-3806.8 2702.9±494·1 470.4-880.4 616.3±106.0 ≥ 4.5 7 4961.3-5165.9 4196.2±408.4 984.0-1006.7 1163.4±126.7 3+ 15 106.1-1598.9 920.8±195.3 106.1-1598.9 398.5±86.6 Age 4+ 11 3806.8-4961.3 3455.6±516.1 1598.9-3801.9 713.9±101.1 5+ 4 2850.7-5165.9 4496.2±553.2 4961.2-5165.9 835.4±167.7 N = number of specimens; SE = standard error. left side of the body, between the end of the pectoral 72.6mm, 35.8-69.4mm, 30.6-60.8 mm and from 0.33 fin and beginning of the dorsal fin (Mousavi-Sabet et to 3.52g, respectively (Table 1). The obtained results al. 2012a). In order to compare significant showed that age of this species ranged from 1+ to 5+ differences in the GSI index among the samples years. Most of the caught fish were 2+ (30.1%) and taken in various months and various size samples, the 3+ (26.5%) years old, some were 1+ (16.5%) and 4+ analysis of variance and Tukey’s test were applied (21.4%) and only a few belong to 5+ (5.0) years old. (P<0.05). The strength and significance of the According to examination of individual gonads, all relationship between the absolute fecundity (Fa) and female specimens with 30.6mm in standard length selected individual features of the females included and more than one-year old (approximately 2 years in the study (standard length and weight, the gonad old) categorized as mature. weight and the fish’s age) were analyzed by In order to determine the spawning season, the determining Pearson’s correlation coefficient r GSI values were examined (Fig. 1). According to (P<0.05) and regression linear equations (Thulasitha diagram, the peak of GSI is in March. The GSI values & Sivashanthini 2013). The data were analyzed by increased from July until January. There were sharp the SPSS version 16.0 software package and increases in GSI values from February to March (at Microsoft Excel 2010 software. water temperature 17ºC). As seen in Figure 1, this value gradually decreased from March to June. This Results trend of the GSI value shows that the spawning During this study, 279 specimens of O. bergianus occurs in March (Fig. 1). were collected from the Jajrud River in the Namak Individual values of the absolute fecundity varied Lake basin, central Iran. The total length, fork length, in a wide range from 106 to 5165 eggs with an standard length and total weight ranged from 37.1- average of 2792 eggs (SE±692.5) (Table 2). The

283 Iran. J. Ichthyol. (September 2017), 4(3): 281-289

Fig.1. The monthly variation of mean (± SE) gonadosomatic index (GSI) in female Oxynoemacheilus bergianus from the Jajrud River.

Fig.2. The monthly mean of oocyte diameter (in micrometer ±SE) in the gonads of Oxynoemacheilus bergianus from the Jajrud River. Table 3. Correlation coefficients r and regression equations for relationships between absolute fecundity (Fa) and standard length (SL), body weight (W), weight of ovary (Wg) and age.

Relationship N Linear Regression r r2 F P Fa – SL 30 Y = 351.85x-16231.51 0.71 0.56 5.20 0.071 Fa – W 30 Y = 1143.50x-1554.67 0.90 0.81 21.4 0.006 Fa – Wg 30 Y = 4319.90x-392.50 0.98 0.97 19.00 0.000 Fa-Age 30 Y = 818.52x + 835.03 0.593 0.359 2.87 0.413 fecundity relative to total weight was 75.6 to 1006.7 coefficient values were 0.90 and 0.98 for body with a mean of 637.9 (SE±119.6) per gram body weight and gonad weight, respectively. The monthly weight (Table 2). Absolute fecundity was signific- ovum diameters Mean ranged from 142.8 (SE±14.3) antly and positively related to female body weight to 513.1 (SE±114.9) micrometer with a mean of and also gonad weight (Table 3). The regression 285.4 micrometer (SE±35.77). Ovum diameters

284 Pourshabanan et al.- Reproduction of Oxynoemacheilus bergianus

Fig.3. The mean oocyte diameter (in micrometer) in reproductive season in the ovaries of Oxynoemacheilus bergianus from Jajrud River.

increased gradually in September, the highest value Discussion was observed in March and the lowest in August The loach is a short-lived species. The maximum age (Figs. 2-3). reported for loaches is 6+ and commonly previous Also in this study, five age groups were observed, studies show that most of the caught fishes are in 2+, the most abundant age group in the catches fishes was 3+ and 4+ age groups and only few of these are 5+ 2+ (30.10%) with average of standard length nearly years old (Robotham 1981; Safari & Naserizadeh 36.9 mm. The fish abundance with 5+ years old was 2013; Mousavi-Sabet et al. 2011, 2012b, 2012c). low and included only 5% of examined specimens. In In many fish species, in order to the estimate of general, most fish were at 2+ (30.10%) and 3+ reproduction period, gonad weight and its different (26.50%) years old. stage of development is appropriate approach The linear function was found well enough for (Fowler et al. 2000; Brown-Peterson et al. 2001). expressing the Fa–W (g) and Fa–Wg (g) relationships Examination of GSI variation in different months and for these species in the Jajrud River (Table 3). in different stages of development shows that

285 Iran. J. Ichthyol. (September 2017), 4(3): 281-289

O. bergianus has a prolonged active reproductive and 79.5-1285.7 eggs/g, respectively. Absolute period. In species which spawn in late spring and in fecundity and oocyte diameter to fish size (length and summer such as the loach, the index remains low in weight) in P. cristata were directly correlated winter and then rises sharply just before the spawning (Patimar et al. 2011). The amount of energy available season (Wootton 1979; Mohammadi-Darestani et al. for egg production and the egg accommodation 2016; Mansouri-Chorehi et al. 2016). A rapid capacity of the body cavity increased with fish size. increase in the weight of ovaries took place when the In the present study, monthly ovum diameters mean temperature rises and increasing amounts of food are ranged from 142.8 to 513.1 micrometer with a mean consumed (Wootton 1998). Prolonged active of 285.4 micrometer (SE±35.8). In the River reproductive period maybe is a strategy for this fish Zanglanlou (Khorasan Razavi Province, northeastern in order to increase survival of larvae. Mousavi-Sabet Iran) egg diameters for P. cristata ranged from 0.53 et al. (2011, 2012b, 2012c) studied reproductive to 1.46 mm, with a mean value of 0.943±0.196 biology of Cobitis sp., Cobitis saniae and Cobitis (Patimar et al. 2011), also Safari & Naserizadeh faridpaki in the southern Caspian Sea basin, and (2013) reported oocyte diameter ranged from 0.09 to showed a prolonged active reproductive period for 1.58 mm, with a mean value of 0.54±0.42 mm for this these fishes. According to Mousavi-Sabet et al. species from the Radkan River (Khorasan Razavi (2011, 2012b, 2012c), in this genus, spawning occurs province, northeastern Iran). The length seems to be in May when the water temperature is about 19.1- a better indicator of the capacity of oocyte production 25.1°C. Gonadosomatic index variation is related to than the weight, because in fish significant decrease different environmental conditions such as water in size is observed whereas weight may vary along temperature (Conover 1990). Decreases in water the year (Bagenal 1967). Usually, the relative temperature affected the vitellogenises and fecundity (number of eggs per body weight) is higher postponement of the spawning period (Kjesbu 1994). in small females than in large ones (Lobon-Cervia et Safari & Naserizadeh (2013) studied reproductive al. 1997). Bagenal & Braum (1978) asserted that fish biology of Turkmenian crested loach, Paraschistura species exhibit wide fluctuation in fecundity among cristata, in northeastern Iran, and showed that, the fish of the same species, size and age. The fecundity peak of reproduction occurred during April and June, is affected by many factors, food supply and with highest average values in May. The difference temperature (Thrope et al. 1984; Fleming & Gross in the beginning of spawning season may be related 1990). The present obtained knowledge could be to environmental condition such as temperature, used in the conservation and management strategies water level and food viability. In most teleost species intended to maintain the O. bergianus stock. from the region, the process of gonadal recrud- escence is positively correlated with the progress of Acknowledgments the dry season, in such a manner that the maximum We would like to thank Guilan and Tehran maturational stage is achieved by the end of the dry Universities for financial supports. season (Gonzalez 1980; Gentile et al. 1986). The average absolute fecundity of female References O. bergianus from the Jajrud River was about 2792.3 Bagenal, T.B. & Braum, E. 1978. Eggs and early life eggs (SE±692.5), and ranged from 106.1 to 5165.9 history. Methods for assessment of fish production eggs. The fecundity relative to total weight was 75.6 in freshwaters. 3rd edn. Blackwell Scientific. to 1006.7 with a mean of 637.9 (SE±119.6) per gram Oxford. UK. body weight. Absolute and relative fecundity for Bagenal, T.B. 1967. A short review of fish fecundity. Pp. 89–111. In: Gerking S.D. (Ed.) The Biological basis Paraschistura cristata ranged between 114-1246 eggs 286 Pourshabanan et al.- Reproduction of Oxynoemacheilus bergianus

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288 Iran. J. Ichthyol. (September 2017), 4(3): 281–289 Received: May 30, 2016 © 2017 Iranian Society of Ichthyology Accepted: September 15, 2017 P-ISSN: 2383-1561; E-ISSN: 2383-0964 doi: 10.22034/iji.v4i3.22902 http://www.ijichthyol.org

مقاله پژوهشی زیستشناسی تولیدمثل Oxynoemacheilus bergianus )ماهیان استخوانی عالی: کپورماهی شکالن: لوچ ماهیان( از رودخانه جاجرود، حوضه آبریز نمک، مرکز ایران

امیر پورشبانان1، 2، علیرضا ساری1، سیدحامد موسویثابت4،3*

1دانشکده زیستشناسی و قطب تبارزایی جانداران ایران، دانشکده زیستشناسی، پردیس علوم، دانشگاه تهران، تهران، ایران. 2گروه زیستشناسی، دانشکده علوم، دانشگاه فردوسی مشهد، مشهد، ایران. 3گروه شیالت، دانشکده منابع طبیعی، دانشگاه گیالن، صومعهسرا، صندوق پستی 1144، گیالن، ایران. 4پژوهشکده حوضه آبی دریای خزر، دانشگاه گیالن، رشت، گیالن، ایران.

چکیده: لوچ ماهیان جنس Oxynoemacheilus در ایران و کشورهای اطراف آن یافت میشوند، اما شاخص های تولیدمثل آنها کمتر شناخته شده است. هدف اصلی انجام تحقیق حاضر شناخت شاخص های تولیدمثل (O. bergianus (Derjavin, 1934 میباشد. نمونهبرداریها بهصورت ماهانه و به مدت یکسال انجام شد و تعداد 279 عدد ماهی O. bergianus از رودخانه جاجرود، حوضه آبریز نمک، در مرکز ایران صید شد. سن، نسبت جنسی، هماوری، قطر تخمک و شاخص های گنادی-بدنی مورد مطالعه قرار گرفتند. برای پیبردن به ارتباط بین هماوری و اندازه ماهی، وزن گناد و سن آنالیز رگرسیون مورد استفاده قرار گرفت. میانگین قطر تخمک از 142/8 میکرومتر )مرداد( تا 1/513 میکرومتر )فروردین( متغیر بود. تخمریزی در فروردین ماه، زمانی که دمای آب 16 تا 20 درجه سانتیگراد بود، صورت پذیرفت. میانگین شاخص گنادی بدنی برای ماهیان ماده در شروع فصل تولیدمثل )بهمن( و در رسیدگی کامل )فروردین(، بهترتیب 8/9 و 4/22 درصد محاسبه شد. میانگین هماوری مطلق و نسبی )نسبت به وزن بدن( به ترتیب 4/2792 )5/692±( و 637/9 )6/119±( به ازای هر گرم وزن بدن، محاسبه شدند. هماوری مطلق به صورت معنی داری با وزن بدن و وزن تخمدان رابطه داشت. براساس روند ساالنه شاخص گنادی بدنی مشخص گردید که این ماهی دارای دوره نسبتاً طوالنی تولیدمثل فعال میباشد. از اطالعات حاضر میتوان جهت حفاظت و اتخاذ تصمیمات مدیریت ذخایر ماهی O. bergianus استفاده نمود. کلماتکلیدی: چرخه زندگی، فصل تخمریزی، شاخص تولیدمثلی، لوچ ماهیان.

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