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Turkish Journal of Fisheries and Aquatic Sciences 12: 429-434 (2012)www.trjfas.orgISSN 1303-2712DOI: 10.4194/1303-2712-v12_2_33Assessment of Food Supply of Small Pelagic Fish in the Black Sea Based onTheir Lipid ContentVictor Nikolsky 1, *, Georgiy Shulman 1 , Alla Shchepkina 1 , Tatjana Yuneva 1 , Levent Bat 2 ,Yalçin Kaya 2 , Ahmet Kideyş 3 , Kadir Seyhan 41 Institute of the Biology of the Southern Seas, 2 Nakhimov av., 99011, Sevastopol, Ukraine.2 Sinop University, Fisheries Faculty, 57000 , Sinop, Turkey.3 Institute of Marine Sciences, Middle East Technical University, Erdemli, Mersin, Turkey.4 Karadeniz Technical University, Faculty of Marine Sciences, 61530, Trabzon, Turkey.* Corresponding Author: Tel.: +380.692 544110; Fax: +380.692 557813;E-mail:Received 15 March 2012Accepted 29 June 2012AbstractTotal lipids in anchovy and sprat were measured and interpreted as indicators of their nutritional condition and foodsupply for the period 2005 to 2010. High lipid content in anchovies suggested that they were able to found sufficient food andfavorable environmental condition supporting their stock biomass on a certain level which was strongly limited by heavyfishing. Wide inter-annual fluctuations in anchovy landings could be caused by variability in yearly recruitment and due toshifts in the spatial distribution patterns of the exploited stock. Unlike anchovy, lipid reserves in sprat declined remarkably tothe lowest levels recorded during the 50-year observations period. Such a significant worsening in sprat nutritional conditionfollowed the evident warming of the Black Sea and coincided with a sharp decline in sprat catches off Crimea. Thus, thedeterioration of food supply together with intensive fishing could have contributed to the reduction of that local sprat stock.Keywords: Anchovy, sprat, water temperature, stock biomass.IntroductionThe most abundant small pelagic forage fishes,anchovy Engraulis encrasicolus ponticus and spratSprattus sprattus phalericus, are the key fish speciesin Black Sea food web. They are important grazers ofzooplankton and a main food resource for toppredators (dolphins, spiny dogfish, mackerel, whiting,turbot etc). Their early life stages are components ofthe diet of horse-mackerel and predatory zooplankton(Prodanov et al., 1997). Massive populations ofanchovy and sprat display strong fluctuationsdepending on environmental conditions. Food supplyis one of the most important conditions determiningthe population size of small pelagics (Nikolsky,1965). In theory, the definition of ‘food supply’implies the amount and nutritional value of food, thenumber of all consumers including competitors, andspecific feeding conditions. These include amongothers the temperature and transparency of water,availability and nutritional value of prey items etc(Shulman and Love, 1999).Food supply of organisms or populations can beexpressed numerically as the ratio between foodconsumed and food required but direct determinationsof these two variables are very difficult whenstudying fish in nature. An indirect approach is toevaluate fish condition that ultimately depends onquantity and quality of consumed food. Many authorsproposed fat content (triacylglycerols) or total lipidcontent as a good indicator of the fish nutritionalcondition (Håkanson, 1989; Lasker, 1970; Shulman,1974; Garcia-Franco et al., 1999; Marshall et al.,1999; Shulman and Love, 1999; Orlova et al., 2010and others). However, few publications used the lipidbasedindicators with emphasis on estimation of longtermvariability in food supply of fish.The objective of this research was to determinethe nutritional condition of these fish over the pastdecade compared to earlier historical data. The longrangegoal is to develop a method for forecasting thefish stocks nutritional condition and hence, foodsupply. A long-term data series (1960 to present) oflipid accumulation in sprat populations provides a richresource for retrospective data analyses of the fishcondition which are thought to be driven byanthropogenic effects and climatic impact. Evidentiallinks between the condition of the sprat and theenvironmental characteristics of the Black Sea havebeen found (Shulman et al., 2005), and initialattempts to predict probable changes in the nutritionalcondition of sprat have been made (Nikolsky andShulman, 2005; Nikolsky et al., 2009).© Published by Central Fisheries Research Institute (CFRI) Trabzon, Turkeyin cooperation with Japan International Cooperation Agency (JICA), Japan

430 V. Nikolsky et al. / Turk. J. Fish. Aquat. Sci. 12: 429-434 (2012)Materials and MethodsTo monitor inter-annual changes in fishnutritional condition, anchovy and sprat had beenexamined at the end of their feeding periods (June-July for sprat and October-November for anchovy)between 2005 and 2010. The techniques of samplingand determination of lipid content in small pelagicfish had been explicitly described earlier (Shulman etal., 2005). Specimens (not less than 100 fish) weresampled from each catch. Fish were sized at 5 mmintervals, and then every size group was separatelyhomogenized. About 10–15 g of homogenate wasdried at 100–105°C to a steady weight. Lipid contentof fish was estimated using the relationship betweentotal lipid and dry matter contents (Nikolsky et al.,2009). An average weighted value was calculatedthen for each sample by equation:1X Nk1n i x i,where n i is number of fish in size group i, x i islipid content in size group i, k is number of sizegroups, and N is number of all fish analyzed. Then thelipid content indicator (LCI) was calculated as asimple arithmetic mean of all samples collected eachyear. The food supply index (FSI t ) was calculated asthe difference between the lipid content attained byfish at the end of feeding in a certain year (LCI t ) andaverage lipid content (LCI)deducted from data of thesame period obtained over many years andnormalized by standard deviation (SD):FSItLCIt LCISDwhile LCI does not differ from (LCI)more than± SD, the FSI does not exceed ± 1, and the foodsupply of the population is considered adequate; atFSI

432 V. Nikolsky et al. / Turk. J. Fish. Aquat. Sci. 12: 429-434 (2012)18.0Lipid content indicator, %16.014.012.010.08.0SpratAnchovy6.060 70 80 90 100 110 120 130Fork length, mmFigure 5. Variations in lipid stores of anchovy (October–November) and sprat (June–July) of different sizes. The plot wasgenerated using monitoring data for the period 2005 to 2010. Horizontal lines indicate long-term levels of the LCI.DiscussionThe fishery statistics data clearly show arecovering fishery of small pelagic fish after itscollapse occurred between the end of the 1980s andthe beginning of the 1990s. Since 1995, annuallandings of anchovy in Turkey have approachedlevels recorded before the collapse. However, widefluctuations in anchovy landings within the range of100-400 thousand tons are still evident (Figure 6).Such extensive fluctuations could be caused byseveral reasons affecting the stock biomass such asdue to variability in annual recruitment, predation orcompetition as well as changes in the spatialdistribution pattern of parent stock.It is known that anchovy spatial distributionduring wintering depends on stored lipid reserves andis strongly controlled by the water temperature(Shulman, 1974; Chashchin and Akselev, 1990). Thisrule was clearly observed during the fishing season of2005 when anchovy fatness was low and the watertemperature off Crimea being higher than off theAnatolian coast (Figure 7). As a result, a considerableportion of the anchovy stock remained wintering inwarmer waters off Crimea. Fishing continued therethroughout the winter and even spring months whilethe lowest yield was recorded from Turkish waterssince anchovy stocks had recovered after the collapse.A similar situation was observed in 2009: thetemperature off Crimea was higher than off theAnatolian coast, lipid content in anchovy was not veryhigh and Turkish anchovy catch decreased noticeably.On the contrary, a local peak in anchovy catchoccurred in 2007 when water temperature off Crimeadecreased abruptly following the destructive cyclonethat happened in the north-western Black Sea inNovember.It is noticeable, that annual anchovy catches forthe period of 2002 to 2009 show significant positivecorrelations with water temperature gradients betweenthe two areas examined. Furthermore, the pronouncedpeaks in anchovy catches off Crimea occurred duringthe 2002/03, 2005/04, 2007/08, and 2009/10 fishingseasons (Zuev et al., 2011) when the lowest andhighest Turkish annual catches were recorded (Figure8).The significant decrease in sprat nutritionalcondition was followed by evident warming of the seaand coincided with sharp reduction in Ukrainiancatches from the shelf of Crimea (Figure 9). It led tothe conclusion that food abundance in the westernshelf of Crimea was too low to support existing spratstocks. Analyses of the fish stomach contents showedthat sprats were lacking their main food items (coldwatercopepods) and were forcing to consumezooplankton species which play a secondary role intheir diet (Glushchenko, 2011). As a result, adultsprats had apparently to avoid that traditional localfishing ground. According to official statistics, fishingof sprat had developed remarkably during that sametime in the south-eastern Black Sea by Turkey. Totalsprat landings by all countries exceeded 91 thousandtons in 2009 and approached close to the criticalmaximal level of the 1980s (FAO, 2011).AcknowledgementsThe authors are grateful to their Turkish andUkrainian colleagues whose roles in sample collectionwere very useful. This work was supported byTUBITAK-NASU Projects (numbers 105Y028 and105Y341).ReferencesChashchin, A.K. and Akselev, O.I. 1990. Migrations of thestocks and availability of Black Sea anchovy to thefishery to the autumn and winter. V. A. Shlyakhov(Ed.), Biological Resources of the Black Sea, VNIRO,Moscow: 80-93 (in Russian).Garcia-Franco, W., Vidal-Talamantes, R., Cota-Villavicencio, A., Ramon-Corrales, J. and Prieto-Montalvo, I. 1999. Variation in fat content of northernanchovy (Engraulis mordax) in relation to the BajaCalifornia environment. CalCOFI Rep., 40: 165-169.

V. Nikolsky et al. / Turk. J. Fish. Aquat. Sci. 12: 429-434 (2012) 4336000005000001Catch, tons400000300000200000210000001970 1975 1980 1985 1990 1995 2000 2005 2010Figure 6. Total anchovy landings by all countries (1) including Turkey (2) from the Black Sea (FAO, 2011).19.0217.0TL, %17.015.013.011.09.07.0116.015.014.013.0SST, o C5.02005 2006 2007 2008 2009 2010Figure 7. Inter-annual changes of lipid content (% wet mass) in anchovy body at the end of feeding period in October-November (bars) and monthly average sea surface temperature in the Crimean (1) and Turkish (2) fishing areas. Thetemperatures were calculated using the NOAA/NASA satellite data.12.04002007R 2 = 0.6920022004Catch, 10 3 mt300200200920102003200620082005100-1.0 0.0 1.0 2.0 3.0Thermal gradient, °СFigure 8. Turkish anchovy landings for the period 2002 to 2010 against the sea water temperature gradient between Sinop andCrimea regions. The thermal gradients were calculated for November using the NOAA/NASA MODIS-Aqua satellite data.Glushchenko, T.I. 2011. Nutrition and assessment of BlackSea sprat in 2009-2010. Tr. YugNIRO, 49: 34-39 (inRussian).FAO 2011. Fishery statistics. GFCM Capture Production1970-2009. http:// www.fao.org.Håkanson, J.L. 1989. Analysis of lipid components fordetermining the condition of anchovy larvae,Engraulis mordax. Mar. Biol., 102: 143-151.Lasker, R. 1970. Utilization of zooplankton energy by aPacific sardine population in the California Current.In: J.H. Steele (Ed.), Marine Food Chains, Edinburgh:265-284.Marshall, C.T., Yaragina, N.A., Lambert, Y. and Kjesbu, O.1999. Total lipid energy as a proxy for total eggproduction by fish stocks. Nature, 402: 288-290.Nikolsky, G.V. 1965. Theory of fish stock dynamics.Nauka, Moscow, 382 pp. (In Russian).Nikolsky, V.N. and Shulman, G.E. 2005. The sprat fat

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