Journal of the Persian Gulf (Marine Science)/Vol. 8/No. 28/ June 2017/8/61-68

Possible effects of Rainbow trout escape from cages on Salmo caspius in the

Mehdi Naderi Jolodar1*, Arefeh Sadat Mirhejazi2 1- Ministry of Agriculture, Country Fisheries Science Research, Ecological Institute of Caspian Sea, Khazar Blvd., Sari, . 2-Graduated from MSc in Fisheries, Fisheries group, Khazar Higher Education Institution. E-mail: [email protected] Received: December 2016 Accepted: June 2017

© 2017 Journal of the Persian Gulf. All rights reserved. Abstract This study was conducted to investigate the possibility of population forming of Oncorhynchus mykiss in competition with Salmo caspius on the southern shores of the Caspian Sea in , Iran. One hundred specimens were collected seasonally from commercial purse seine from October 2017 to April 2018. Brown trout diet was analyzed and a total of 90 individuals belonging to 12 taxa (groups) were identified. Except for algae which were general prey, the other food items in the diet were rare for rainbow trout. Atherina caspia and Clupeonella cultriventris were the other prey items, accordingly. Analysis of the brown trout diet, a total number of 2 taxa was identified summing a total of 10 individuals. The Atherina caspia for brown trout was a specialty food and the most important A% and FO% found in the diet of its had. Although the feeding habits were both carnivorous and used more than fish as food prey, but rainbow trout fed a wide range of food items. Therefore, in the competition between two species, Oncorhynchus mykiss is more successful, and under adverse

Downloaded from jpg.inio.ac.ir at 11:47 IRST on Thursday October 7th 2021 habitat conditions it is possible to remove Salmo caspius. In some rainbow trout caught, all stages of sexually transmitted infections (II to V) were observed, of which stages 4 and 5 had the lowest number. Escaped farmed salmon are able to spawn successfully in rivers.

Keywords: Oncorhynchus mykiss; Salmo caspius; Competition; Feeding habits; Reproduction; Caspian Sea.

1. Introduction native to the rivers and lakes of the Pacific Ocean from North America and Asia is exotic to the Among the 79 fish species identified in the southern Caspian basin (Abdoli et al., 2008). southern Caspian basin, approximately 13 species Invasion by exotic species is a serious threat to the belong to exotic fish species (Kiabi et al., 1999). conservation of freshwater ecosystems (Fuller et al., Rainbow trout (Oncorhynchus mykiss) which is 1999; Rahel, 2002). Rainbow trout is the species with the biggest impact on biological diversity, as * Email: [email protected] listed in ‘100 of the World’s Worst Invasive Alien

61 Naderi Jolodar1 and Mirhejzai / Possible effects of Rainbow trout escape from cages on…

Species’ by the IUCN (2018). Rainbow trout impacts Sea species. population dynamics and composition of Caspian Sea species because it grows in number fast and 2. Material and Methods competes with native fish for common food resources (Coad and Abdoli, 1993). This study was conducted on the southern shores Many species of salmonids have been introduced of the Caspian Sea in Mazandaran province. for recreational and commercial purposes to regions Considering the cages at the sea and the distribution throughout the world where they did not occur of rainbow trout escaped from cages on the southern naturally, with little regard to the effects on native shores of the Caspian Sea, Oncorhynchus mykiss and species (Fausch, 1988). In most cases, salmonid Salmo caspius specimens (N = 100) were collected introductions have been widely implicated in seasonally from commercial purse seine and mesh declines of native biota (Polhemus, 1993; Lassuy, size of net was (a=28 mm), from October 2017 to 1995). Currently, the most important strategy of April 2018. In the laboratory, O. mykiss and S. Iranian fisheries in response to supplying the caspius were measured (nearest mm in total length) country's food needs is the development of rainbow weighed (nearest g in fish weight) and dissected for trout in the Caspian Sea using breeding in cage sex determination (male/female), sexual maturity (I, methods. Since Caspian Sea has acceptable potential II, III, IV and V), gonad weight (g), immediately for cage culturing of rainbow trout, and since there is after landing. Classification of gonads was as the high risk of fish escape from cages (Rikardsen, follows: stage I - immature; stage II - immature or 2002), extreme care must be given to environmental recovery; stage III - maturing; stage IV – mature, and considerations and compatibility with their stage V - spent. Age of fish was determined by ecosystems. observing growth rings on Scales using stereoscopic Salmo caspius is an anodromous and endemic microscope. Gut content of each fish was evacuated species of the Caspian Sea ecosystem (Abdoli and and fixed in 4% formalin solution, and then Naderi Jalodar, 2008). This species lives and feeds in identified in the laboratory following (Kasimov, the sea and enters the river for spawning, and has 2000; Merritt et al., 2008). In addition, gut length of

Downloaded from jpg.inio.ac.ir at 11:47 IRST on Thursday October 7th 2021 high economic value (Kazancheyev, 1981). The main samples was measured and its ratio to fish total area of the habitat is the western and southern coasts length was determined. of the Caspian Sea, with limited distribution in Concerning the measurement of fullness index northern and the eastern shores (Sayyad Bourani et (FI), the whole stomach was detached from the al., 2013). The overfishing and habitat destruction, alimentary system by removing the posterior part of especially its reproductive habitats in rivers, has led the esophagus and intestine. The stomachs weight to its listing as critically endangered species (Kiabi et including its contents (TSW) were measured, and al., 1999). Considering competetion of this species dissected emptying their contents a Petri dish. The with the Salmo caspius for food and the possibility of weight of the empty stomach (ES) was then growing its population in the southern Caspian basin, recorded. The difference of the two weights gives the the present study investigates possible effects of weight of food (FW) (Kagwade 1964): WF (g) = escaped rainbow trout from cages on Salmo caspius TSW (g) - ES (g). The measurement of ingested food and the potential impact of exotic trout on native weight (FW) is expressed as a percentage of total fauna and presents suggestions for managing the risk fish weight (W) according to the formula defined by of exotic trout invasion and its impact on Caspian Hureau (1969): FI = FW / W x 100, where FI is the

62 Journal of the Persian Gulf (Marine Science)/Vol .8/No. 28/ June 2017/8/61-68

fullness index. Feeding intensity is also evaluated via weight of specimens of fish caught for rainbow trout the vacuity index (VI) of sampled stomach which 31.82± 1.03, 546.05± 44.02 and for brown trout corresponds to the percentage of empty stomachs 31.82± 1.03, 546.05± 44.02, respectively (Table 1). (ES) with respect to all analyzed stomachs (TS): VI= All S. caspius specimens were male and male to ES / TS x 100. female ratio was 1.7 for O. mykiss, which did not To estimate the dietary importance of each prey show significant differences between them (p>0.05). category, we calculated the prey specific abundance There was no significant difference between mean of of each food category (A%) and the frequency of total male and female (p>0.05), but the difference in occurrence (FO%). The Costello (1990) graphical between mean weight of male and female was method was applied to describe the feeding strategy statistically significant (p<0.05). and prey importance (Fig 1). A total number of 12 taxa/groups were identified in the gut contents of rainbow trout and brown trout (Table 2). The most abundant of food items in the rainbow trout gut were as follows: Balanus sp., Clupeonella cultriventris, Plastic, wood, Bivalvia, Neogobius fluviatilis, Atherina caspia, Liza saliens, Chinavia hilaris, Taxiphyllum barbieri, kutum, Cumacea, Syngnathus caspius and Gasterosreus aculeatus respectively (Fig. 1). In the gut of the brown trout, only two fish species Atherina caspia and Clupeonella cultriventris were identified, with the most prey related to Atherina caspia. Also, from the total of 100 gut contents

analysed, 90 belonged to O. mykiss and 10 to S. Fig 1: Feeding strategy displayed by the Costello (1990) trutta (Fig 1). graphical method The average Fullness index of rainbow trout was

Downloaded from jpg.inio.ac.ir at 11:47 IRST on Thursday October 7th 2021 At first, the obtained data was normalized and 389.39 ± 25.33 and its value in brown trout was tested by Kolmogorov-Smirnov method. Data 396.28 ± 89.58, which was not significantly different analysis was performed using SYSTAT software and between them (P> 0.05). Fullness index of this one-way ANOVA analysis. Duncan's test was used species in the autumn was minimal and it had a at a level of 5% (P = 0.05) to compare the means. maximum value in spring, there was a significant Data was computed and the diagrams were plotted difference between them (P <0.05). The number of using the Excel software package (Conover, 1980). specimens for the seasonal variation of this index was not sufficient for brown trout. Although, the 3. Results and Discussion feeding habits were both carnivorous and used more than fish as food prey, but rainbow trout fed a 3.1. SPM concentration broader range of food items (Fig 2). Following the analysis of the brown trout diet, a In this study, 90 O. mykiss and 10 S. caspius were total number of 12 taxa/groups were identified collected from central and western parts of summing a total of 90 individuals. Except algae, the Mazandaran (Table 1). Average total length and total food items used were rare for Rainbow trout, and

63 Naderi Jolodar1 and Mirhejzai / Possible effects of Rainbow trout escape from cages on…

Table 1. Total Length (cm) and Total Weight (g) of O. mykiss and S. caspius specimens from the western part and the central part on the southern shores of the Caspian Sea

Species Total Length Total Weight Oncorhynchus mykiss Mean± SD Min Max Mean±SD Min Max Number Male 33.17± 1.05 19 48 48097± 40.27 200 1100 46 Female 30.42± 1.78 13 56 604.67± 79.21 156 2230 44 Total 31.82± 1.03 13 56 546.05± 44.02 156 2230 90 Salmo caspius Male 34.50± 3.46 21 42 540.00± 123.18 195 970 10 Female ------Total 34.50± 3.46 21 42 540.00± 123.18 195 970 10

Table 2. Total Length (cm) and Total Weight (g) of O. mykiss and S. caspius specimens from the western part and the central part on the southern shores of the Caspian Sea

Phylum Class Order Family Species

Chordata Mugiliformes Mugilidae L. saliens Mollusca Bivalvia Veneroida Cardiidae C. lamarcki Chordata Actinopterygii C. cultriventris Chordata Actinopterygii Gobiiformes Gobiidae N. fluviatilis Arthropoda Malacostraca Cumacea - - Arthropoda Hexanauplia Sessilia Balanidae B. glandula Chordata Actinopterygii Syngnathidformes Syngnathidae S. caspius Chordata Actinopterygii Gasterosteiformes Gasterosteidae G. aculeatus Plant Bryopsida Hypnales Hypnaceae T. barbieri Chordata Actinopterygii Atheriniformes Atherinidae A. caspia Downloaded from jpg.inio.ac.ir at 11:47 IRST on Thursday October 7th 2021 Arthropoda Insecta Hemiptera Pentatomidae C. hilaris Chordata Actinopterygii R. kutum

Frequency Frequency

35 80 30 25 20 60 15 10 40 5 0 20

0 Atherina C. cultriventris

Salmo caspius Oncorhynchus mykiss Fig 2: Presence and abundance of each taxon/group identified in the gut contents of rainbow trout, and of brown trout

64 Journal of the Persian Gulf (Marine Science)/Vol .8/No. 28/ June 2017/8/61-68

algae were considered as generalization prey (Fig. 3). food and the most important A% and FO% found in After algae, the most important A% found in the diet the diet of its had (Fig 3). of rainbow trout were Atherina caspia and The maturity stages of reproductive cycle can be Clupeonella cultriventris (Fig 3). Also, although grouped into five phases (Fig 4). The samples of Balanus sp. has the highest FO% for this species, it immature Rainbow trout had the highest relative has a very low nutritional value. frequency (Fig 5). In some rainbow trout caught, all In analysis of the brown trout diet, a total number stages of sexually transmitted infections (II to V) of 2 taxa were identified swith a total 10 individuals. were observed, of which stages 4 and 5 had the The Atherina caspia for Brown trout was a specialty lowest number (Fig 5).

100 100

50 50

0 0 0 50 100 0 50 100 Algae Atherina C.Cultriventris Kutum Atherina C. cultriventris Liza Balanus Oncorhynchus mykiss Salmo caspius

Fig 3: Feeding strategy displayed by the Costello (1990) graphical method for the Oncorhynchus mykiss and Salmo caspius.

Female 3 Female 4 Female 5 Male Downloaded from jpg.inio.ac.ir at 11:47 IRST on Thursday October 7th 2021

Fig 4: Developmental stages be observed from Rainbow trout Gonads in the southern Caspian Sea

%Frequency

45 40 35 30 25 20 15 10 5 0 Immature II III IV V

Fig 5: Frequency of sexual stages be observed from rainbow trout gonads in the southern Caspian Sea

65 Naderi Jolodar1 and Mirhejzai / Possible effects of Rainbow trout escape from cages on…

4. Conclusions and Conslusion (Afrahei Bandpei et al., 2009; Stergiou, 1988; Geetha et al., 1990; Dadzie, 2007 ). Reducing Identification, distribution, abundance and temperature affects metabolic activity and during ecological assessment of aquatic , including reproductive periods due to physiological and fish in a lake and river, are important issues that behavioral changes on the fullness index of fish unfortunately have not received enough attention. which has been confirmed by the researchers So, the study of the sources showed that there is little (Nikoliskii, 1963; Miller, 1989; Biswas, 1993). information about most species in different rivers of The results of this study showed that rainbow trout Iran (Coad, 1995; Abdoli and Naderi Jolodar, 2008). escaped from the cage with carnivorous behavior and Most studies have been done on the effects of habitat used a wide range of food, so it is possible to on fish with a focus on abiotic factors (Shepherd and compete with this species with many fish species of Cousens, 1984; Myers, 1998). the Caspian Sea. Since, this carnivore is very The results of this study showed that meat foods, demanding and occupies top of the ecological food such as fish species were fed by this species, as in pyramid of the Caspian Sea, it has been exposed to studies (Tajallipour and Akbarnejad, 1978; species, such as S. caspius, which are endemic Zarinkamar, 1996; Afrahei Bandpei et al., 2009). species of the Caspian Sea and are critically Results present study is in agreement with endangered as a result of completion for common importance of nutrition under the influence of food sources. Effects of rainbow trout, as an invasive behavioral, physiological and ecological adaptations and very demanding specie, goes beyond S. caspius, and mechanismse (Alexander and Fichter, 1977). and affect many more species of the Caspian Sea The results of this study showed that fish, such as rendering possibly serious damage to their resources. Atherina caspia and Clupeonella cultriventris was the most important food used for rainbow trout and References brown trout. Although, the feeding habits were both Abdoli, A., and Naderi Jolodar, M. 2008. The biodiversity carnivorous and used more than fish as food prey, of South Caspian Sea Basin . Aquatic science but rainbow trout fed on a wide range of food items publications. 242 p. Downloaded from jpg.inio.ac.ir at 11:47 IRST on Thursday October 7th 2021 (Fig 2). Therefore, in the competition between two species, O. mykiss is more successful, and under Ahmet, A., Cemil, K. and Hakan Murat, B. 2003. Age, adverse habitat conditions it is possible to remove S. Growth and Diet Composition of the Resident Brown caspius. These results are consistent with studies by Trout, Salmo trutta macrostigma Dumeril 1858, in other researchers (Steven and Ruth, 2000; Ahmet, et Firniz Stream of the River Ceyhan, Turkey, Turk J Vet al., 2003). Anim Sci 29 (2005) 285-295 © TÜBITAK. Fullness index of O. mykiss was the lowest in the Alexander, T.R. and Fichter, G.S. 1977. Ecology. autumn and significantly highest in spring (P <0.05). Translation by: Karimmi, A. U.S.A. 208 P. The reproductive season is most of the Caspian Sea Afrahei Bandpei, M.A., Mashhor, M., Abdolmaleki, S. fish in the spring and summer, due to the high of and El-Sayed, M.A.F. 2009. Food and feeding habits of fullness index in spring, more fish fingerlings in the Caspian Kutum ( kutum (Cyprinidae)) in Caspian Sea are damaged. Several studies have Iranian waters of the Caspian Sea. Cybium. 33(3): 193- shown that fullness index in fish is time- dependent 198. and decreases or increases at reproduction period Bagenal, T. 1978. Method for assessment of fish with lowering or hiking of temperature, respectively production in freshwater. T.B.P, handbook no.3.

66 Journal of the Persian Gulf (Marine Science)/Vol .8/No. 28/ June 2017/8/61-68

Blackwell publication, oxford, U.K. 365 p. Fausch, K. D. and White, R. J. 1986. Competition between Berg, L.S. 1949. Freshwater fishes of the USSR and brook trout and brown trout for positions in a Michigan adjacent countries. Israeli program for scientific stream. Canadian Journal of Fisheries and Aquatic translations, Jerusalem, 1964, Vol. 2. Sciences, 38: 1220-1227. https://doi.org/10.1139/f81-164 Biswas, S.P. 1993. Manual of methods in fish biology. South Asian Publisher Pvt. Ltd. New Delhi. Fuller, P. L., Nico, L. G. and Williams, J. D. 1999. Non- International Book Co. Absecon highlands. N.J. Borcea, indigenous fishes introduced to inland waters of the I (1933) 1934. Revision systematiqueet distribution United States. American Fisheries Society, Bethesda, geographique des gobiides de la mer Noire et Maryland, USA. 613 p. particulierement deseaux Roumanies. Ann. Sci. Univ. Geetha, M., Suryanarayanan, H. and Balakrishnann, N. Jassy.19(1/4): 1-136. 1990. Food and feeding of puntius vittatus (Daw.). Brishtin, A. A. 1970. Invertebrate Atlas of the Caspian Indian Nat.Sci.Acad..B 56: 327-334. Sea. Moscow food industry. 610 pp. IUCN-Environmental Law Centre. 2018. Survey of Coad, B.W. and Abdoli, A. 1993. Exotic Fish Species in International Instruments and Institutions with the Fresh Waters of Iran, Zoology in the Middle East, Provisions and/or Programmes with regard to Alien (9):65-80. Invasive Species (update of Glowka in collaboration with de Klemm. 1996. NonIndigenous Species Coad, B.W. 1995. Fresh Water fishes of Iran. Institute of Introductions: References in International Instruments. landscape Ecology of the Academy of Sciences of the Chart distributed for comments at the Norway/United Czech Republic , BRNO. Nations Conference on Alien Species, Trondheim, Coblentz, B. E. 1990. Exotic organisms: A Dilemma for Norway, 1 July 1996, and in revised form to CBD COP Conversation Biology, Conversation biology wiley IV, 1998). See Appendix I. Also available on URL: online library, volume 4, Issue 3. http://www.iucn.org/themes/law/. https://doi.org/10.1111/j.1523-1739.1990.tb00287.x Jester, D.B. 1973. Variations in catchability of fishes with Conover, W.J. 1980. Practical nonparametric statistics, color of gill nets. Transactions American Fisheries 2nd edition. Wiley. New York. pp: 219. Downloaded from jpg.inio.ac.ir at 11:47 IRST on Thursday October 7th 2021 Society. 102: 109- 15. Costello, M. J. 1990. Predator feeding strategy and prey https://doi.org/10.1577/1548- importance: a new graphical analysis, Journal of Fish 8659(1973)102<109:VICOFW>2.0.CO;2 Biology, Vol. 36, Issue: 2, 261-263 p. Kagwade, P. V. 1964. The food and feeding habits of the https://doi.org/10.1111/j.1095-8649.1990.tb05601.x Indian oil sardine Sardinella longiceps valenciennes. Dadzie, S. 2007. Food and feeding habits of the black Indian Journal of Fisheries 11:345-370 pomfret Parastromateus niger (Carangidae) in the Kasimov, A. 2000. Methods of monitoring in Caspian Sea. Kuwait waters of the Arabian Gulf . Cybium.31: 77- 84. QAPPPOLIQRAF., 57 pp. Euzen, O. 1987. Food habits and diet composition of some Kazancheyev, E.N. 1981. Fishes of the Caspian Sea. fish of Kuwait, Kuwait, Bull, Mar, Sci, (9):65-85p. Moscow. 168P. Fausch, K. D. 1988. Tests of competition between native Kim C.H., Park M.K. and Kang E.J. 2008. Minute and introduced salmonids in streams: what have we tubercles on the skin surface of larvae in the Korean learned? Canadian Journal of Fisheries and Aquatic endemic bitterling, Rhodeus Pseudosericeus . J. App. Science, 45: 2238-2246. Ichthyol. 24:269-275. https://doi.org/10.1139/f88-260 https://doi.org/10.1111/j.1439-0426.2007.01030.x

67 Naderi Jolodar1 and Mirhejzai / Possible effects of Rainbow trout escape from cages on…

Lassuy, D. R. 1995. Introduced species as a factor in Rahel, F. J. and Hubert, W. A. 1991. Fish assemblages extincttion and endangerment of native fish species. and habitat gradients in a Rocky Mountain Great Plains American Fisheries Society Symposium, 15: 391-396 stream: biotic zonation and additive patterns of Merritt, R.W., Cummins, K.W. and Berg, M.B. 2008. An community change. Transactions of the American Introduction to the Aquatic Insects of North America. Fisheries Society 120:319-332. 4th ed. Dubuque: Kendall Hunt Publishing. https://doi.org/10.1577/1548- 8659(1991)120<0319:FAAHGI>2.3.CO;2 Miller, P.J. 1989. The tokology of gobioid fishes. pp. 119- 153. In fish reproduction, strategies and Tactics. Ed. Rikardsen, A. 2002. Foraging behavior changes of Arctic Potts, G.V. and Wootton, R.J. Academic press Limited. charr during smolt migration in northen Norway, Third printing. Printed in Great Britain. 410 p. Journal of Fish Biology, 60(2): 489-491. https://doi.org/10.1111/j.1095-8649.2002.tb00297.x Myers, R.A. 1998. When do environmentrecruitment correlations work? Rev. Fish Biol. Fish. 8: 285-305. Shepherd, J.G., Pope, J.G. and Cousens, R.D. 1984. https://doi.org/10.1023/A:1008828730759 Variations in fish stocks and hypotheses concerning their links with climate. Rapp. P.-v. reun. Cons, int Mer Nikoliskii, G.V. 1963. Ecology of fishes. Moskova. 185: 255-267. Gorudarsvennoe izdatelstov. Sovetskayanaaka. Translated to English in 1963. 538 p. Shorygin, A.A. 1952. Feeding and nutritional interrelations of fish in the Caspian Sea. Penczak, T., Galicka W., Molinski M. and Zalewski M. Pishchepromizdat. Moscow. 268 p. 1982. The Enrichment of a Mesotrophic Lake by Carbon, Phosphorous and Nitrogen from the Cage Stergiou, K.I. 1988. Feeding habits of the Lessepsian Aquaculture of Rainbow trout, Salmo gairdneri, Journal migrant Siganus luridus in the eastern Mediterranean its of Applied Ecology 19(2). new environment. J. Fish Biol. 33: 531- 543. https://doi.org/10.2307/2403474 https://doi.org/10.1111/j.1095-8649.1988.tb05497.x Pimental, D. and Morrison D. 2005. Update on the Steven, J.K. and Ruth, E.G. 2000. Ecological impacts of environmental and economic costs associated with fish introductions: evaluating the risk. Fish and Wildlife alien-invasive species in the united states. Ecological Branch, Ontario Ministry of Natural Resources, Downloaded from jpg.inio.ac.ir at 11:47 IRST on Thursday October 7th 2021 Economics, Elsevier . Sciencedirect, Volume 52, Issue Peterborough, Ontario, 473 p. 3, pp:273-288 Tajallipour, B. and Akbarnejad, A. 1978. Study of Kutum https://doi.org/10.1016/j.ecolecon.2004.10.002 natural food. Board of Faculty of medicine University Polhemus, D. A. 1993. Conservation of aquatic insects: of Tehran's veterinary letter. Volume 34. Number 2. 15 worldwide crisis or localized threats? American p. Zoology, 33, 588-598. Zarinkamar, H. 1996. Servey feeding habits of Kutum in https://doi.org/10.1093/icb/33.6.588 Bandar Anzali coastal. M.Sc. Thesis. 150 p. Islamic Azad Univ. Unit Tehran. (in Persian).

Naderi Jolodar1 and Mirhejzai / Possible effects of Rainbow trout escape from cages on… Journal of the Persian Gulf (Marine Science)/Vol .8/No. 28/ June 2017/8/61-68 Journal of the Persian Gulf (Marine Science)/Vol. 8/No. 28/ June 2017/8/61-68

68