American Fisheries Society Symposium 35:69-7 6, 2003 O 2003 by the American Fisheries Society

Shads of Eastern Europe from the : Review of Species and Fisheries

IoN Navooenur DantLbe Deltn National Instítute for Reseatch and Deaelopntertt, Babadng Street, 165 Tilcea 8800, Romanin

JouN R. Walpr,reN HtLdson Rioer Foundntion for Science nnd En-oironmental Research, 77 Bnttery Place, Suite 915, Neu York, Netn York 10004, USA

Abstrnct species beÌonging to are known in the northwestern part of the BÌack -Three Sea, including the : Pontic shad A. pontica (EichwaÌd, 1838), Caspian shad Á. caspia (Etchwald, 1838), and BÌack Sea shad A. mneoticn (Crimm, 1901). Regional populations, and possibly subspecies, occur in the , Dniester, Dnieper, and Don rr'vers. Pontic shad, the most abundant shad of Eastern Europe, migrates 500 km upstream for spawning in the Danube River at the end of March in waters oÍ 3-5'C. The peak of these movements occursinApril May at9-TT"C,withtherunendinginJuly-Augustal22-26"C. Pelagiceggs and larvae drift seaward in the upper 0-0.5-m layer of river water. Young-of-the-year Pontic shad feed in brackish waters near the Danube delta, with juveniles leaving the shoreline in autumn. The adult stock lives at depths oÍ 50-100 m, Íeeding mainly on fish. The longevity of Pontic shad is 5-7 years, with maturity occurring at 3-4 years. Most die after the spawning migration, with less than 10% spawning repeatedly. The other two shad species spawn in brackish water of deltas and lagoon Ìakes. The Pontic shad fishery is the most important, followed by that of Caspian shad; the Black Sea shad fishery has collapsed. Fishing Pressure and pollution are the main threats for Pontic shad. However, spawning habitat Íor Caspian shad and Black Sea shad have drastically decreased due to damming. River fisheries for Pontic shad are managed primarily through season and atea closures. Species behavior, spawning and recÍuitment, year-class strength, and estimation of popuÌation dynamics remain open research and management issues.

lntroduction The Black Sea

Three alosines are native to Eastern Europe: Pontic The Black Sea is a large inland sea measuringT,2l1 shad Alosa pontica (Eichwald, 1838), Caspian shad km from east to west and as much as 560 km from A. caspia nordmanni (Eichwald, 1838), and Black Sea north to south, with an area of more than 400,000 shad Á. mneotica (Grimm, 1901). These shads are km2. It is bordered by Ukraine on the north, Russia heavily Íished and are important commercially and on the northeast, Georgia on the east, Turkey on culturally within their respective distributions. All the south, and Bulgaria and Romania on the west. are found in the Black Sea region, an area of con- The Black Sea is connected with the Mediterranean siderabÌe environmental stress. However, knowl- Sea by a reÌatively narrow water\ rav that includes edge of the biology and conservation status of these the Bosporus, the Sea of Marmara, and the shads is poor. Dardanelles. Because of this, its tides are generalÌy In this paper, we review the biology and sta- less than 10 cm. The Black Sea's largest arm is the tus of all three shads, with an emphasis on the best- Sea of Azov; both the Don and Kuban rivers enter known species, Pontic shad. Both Pontic shad and it. Other major rivers flor.'r'ing into the Black Sea Caspian shad are found in the Black Sea and include the Southern Buh, Danube, Dneister, and Caspian Sea basins; we restrict our treatment to the Dnieper. About 20% of Europe's continental land- BÌack Sea basin. Coverage of these fishes in the mass drains to the Black Sea. Caspian Sea is provided in Coad et al. (2003, this The Black Sea has two lavers of water of dif- volume). ferent densities. The bottom layer is highly saline, rich with hydrogen suÌfide, and hypoxic, has lìttle Ì Corresponding author: [email protected] circulation, and is virtually dead biologicalÌy. The

69 lsu Welou'qN 70 Nevooanu

countercloc'k- laver is less saline' circulates 'nner lire' However' the ì:f5 ";à';";À,i' ,i.n marine ;h.k;;ã,-'iilto"*""thasbeent"";l"t-t"tffo"lï tive sPecies, blue' or viol is leidYi (also flanks' TheY the oPercuÌa bu ected. wj.th the the oPerculum'

origin accoun distinguish mon Ponto-Caspian Thethreespe1L^ +Lrrêê qnê .tntiçn:t:;to u*o"g theiifaunas raker counts are useful ;Ë;;"d where they co-oc Gill ad'ults but not for discriminatory fe es among Young sPecimens

cm.

nlosn wlth Alosn' Banarescu (1964) Distribution shad in the Black signations have Pontic Shad ludes the :1ïi:ïi:.fl-"ï:"Ï il: of Azov to sPawn e.been dis- srdes of the between astern PoPulation ranges Crimean ch near túe southeastern

A. tnnaícn, to be a single A. tnnnicn has PriorìtY shouÌd be considered va Pontic shad and Bl

ern Crimean Peninsula'

on both jaws are well deveioPe tic shad and Black Sea shad a ìn CasPian shad' In all ering ierminates with alae, which iie sYmme caudaÌ fin The ventra 77 Snnos op E,qsreRN Eunopp FRoM rHE Blecr Sre

:ends along the Rom Dur- BiologY jìg some years, it is Lake ìn spawning :nd the Razim-Sinoi escu- There are considerable differences eonte and Munteanu 1968). During spring, it is ;r idespread in the Danube delta and adiacent flood- :lain lakes (Antipa 1905; Leonte 1943; Banarescu r964). Some individuals have been found 375 km Kolarov 1991b) and 496ktn (Kovachev 1922) :up- is known of the spawn- :tream from the Danube River mouth. Berg (1948) rivers or in river deltas' Less shad, but it appears they arrd Svetovidov (1952, 1964) cited Antipa's (1905, ing iocations of Black Sea of deltas and lagoons 1909) opinion that Caspian shad migrate up to km utilize low-salinity waters (1985) discussed two 931 (Iron Gate) from the Danube's mouth, and this Ivanov and Beverton in the ivas recently corroborated by N. Bacalbasa- Íorms of Pontic shad. The larger one spawns part of Dobrovici (Lower Danube University, personal Don River and overwinters in the eastern and Batumi' communication), who caught Caspian shad at river the Black Sea between Novorossisk in the western portion of km 864. Caspian shad is also found in the Dniester The smaller form lives the Danube River to and Bug rivers, but it never migrates far from their the Black Sea and enters is high, it aiso river mouths. In the Dnieper Riveç it does not mi- ance n (Vladimirov 1953a). The r, and Bug rivers. had Á. c. tanaica extends migrated in the 90 Sea, north of Batumi, the Dnieper River to Kiev but now can travel only mouth due to a dam Sea of Azov and the Lower Don River. km from the river ' Pontic shad migrate northward in the Black Black Sea Shad Sea in spring and early summer as they move to- rivers. Historically, Pontic shad This species inhabits (Figure 1) both the Black Sea ward spawning penetrated far up the Danube with specimens cap- and Sãa of Azov (Kolarov 1991c). Large schools of at Budapest (river km 1,650), but the migra- this fish enter in Razim-sinoie Ìake complex on the iured route was reduced to 864 km, aÍter construc- Romanian coast (Borcea 1936; Teodorescu-Leonte tion of the Iron Gate II hydroelectric plant in 1983' and Munteanu 1968). It also appears in some years tion Barrages at river km 943 and 864 appear not to along the Bulgarian coast. In the eastern part of the have Àad a large impact on the river's Pontic shad Blaci Sea, it ranges from the region of the Strait of occurs between river Kerch to Novorossysk and south along the popuiation; most spawning and 500. Caucasus coast. km 180

rrì ìlâ ,| tl \ ii Ìì'1 ag,.1!'ar, -:-'€.\., '

l .- tl .f - tlümáfi1á 6!tl:.- *' I

; I I s

aí'ii Elack5ea

Trrlêy I O

Black Sea shad, and (c) Caspìan shad' from the Figure 1-Distribution of Eastern European shads, (a) Pontic shad, ft) Black Sea. 72 Navooenu aNIo WeloMAN

Adult Pontic shad moving upriver in the tic shad entering the Danube River was strongly Danube for spar,r'ning are composed of age-2 to age- positive (y = 0.4832x - 7 .4397 ; r' = 0.9764), possibly 7 individuaÌs. These proportions shift annualÌy, but compensating for loss of biomass through greater age-3 specimens usually comprise 50ok or more of energy expenditure in migration and reproduction the totaÌ run, with the age-6 and age-7 classes con- at higher water temperatures. There was also a tributing about 1% or less (Navodaru 7996, 1998). strongly positive relationshrp (rt = 0.8551) between The three shad species have similar maximum river migration distance at capture and body con- kno'wn ages: 6 years for Black Sea shad and 7 years dition as assessed by the Fulton index (Figure 3). for the other two species. During this upstream migration, Ponüc shad / Total lengths oÍ Pontic shad males and females spawners lost biomass due to egg maturation and ; are approximately equal for each age-class; femaÌes deposition and energy spent for migration. Analy- r,r'eigh more than males at each age interval, but this sis of nine postspawning individuats in compari- difference is not statistically significant (P < 0.05). son with their biomass entering in-river, calculated The relationship between total length (TL) and to- with the length-weight relationship, indicated that taÌ weight (TW; TW = aTLb), estimated for 6 years these shad iost of 10.3-42.7% of biomass. Biomass oÍ migration (1997-7996), incÌuding 1I,375 indi- loss differs by sex (Íemales lose more biomass than viduaìs, was allometric (b + 3): TW = 0.0563TL, as?. do males; between 10.3% and 30.4'/. for males and Crowth in length by age (Table 1) was linear for 10.342.7% for females) and by age (biomass loss average dimension by age (TL = 2.3081. Age + increases with age with an average loss for age-3 22.031). Pontic shad mns in the Danube River over Íish of 23.1%; Íor age-4 frsh, 23.8%; and for age-S 4 years were dominated by first-time spawners f:LsLr,397%). ' with repeat spawners comprising 4-73./. of total The fecundity of the 1987 Danube River run ' spawners annuaÌly (Figure 2). of Pontic shad was analyzed in detail. Thirty fe- The Pontic shad migration in the Danube River males were examined, ranging between 25 and32 begins in early spring when water temperatures cm (standard length) and 195 and 450 g (TW). The reach 3.0-7.5"C, peaks in April and May at between number of eggs per g ranged between 1,080 and 9"C and 17'C, and ends in June and july when 5,41.4, wífh a mean of 3,122. The gonadosomatic water temperatures reach 22-26"C (Navodaru 1996, index (gonad weight x 100/TW) was as low as 2.61 1998). Early run fish appear to contain less fat than and as high as 9.74, averaging 4.86. Absolute fe- later run individuals (Table 2). The relationship cundity ranged between 13,910 and 88,983 eggs per between body fat and water temperature for Pon- female, with a mean of 39,332. The relationship

Table 1'-Age and size structure of rnigratory Pontic shad into the Danube River between 1988 and 1996 TL - total length (cm), sL = standard Ìength (cm), TW = total weight (g), CV = coefficient of variability, and n - number of individuaÌs.

Ag" n Dimension Mean Range SD CV SE of mean 2 394 TL 26.77 19.3-31.5 2.7 8.03 0.11 SL 22.87 77-27.5 r.823 7 99 0.09 TW 168.65 60-290 39.439 23.39 1. 99 3 5,758 TL 29.02 20.5-39.3 7.957 6.74 0.03 SL 25.37 17.2-33 I.753 69.3 0.02 TW /z/.) 75-550 45.513 20.01 0 6 4 4,577 TL 30.89 23 5-38.5 1.861 6.02 0.03 SL 26.85 20-33.5 7.789 6.66 0.03 TW 269.93 115-520 53.816 79.94 0.8 5 599 TL 33.6 26-39.2 7.785 5.31 0.07 SL 29.22 22.2 34.7 1.725 5.9 0.07 TW 324 160-610 58.119 77.64 237 658TL 35 95 33.5-39.3 7.439 4 0.19 SL 37.77 26 35 7.542 4.95 0.2 TW 389.97 270-600 54.744 14.04 7.79 79TL 38.22 36.6-39.6 0.981 2.57 0.33 SL JJ,Jõ 37.7 35 1.093 3.27 0.36 .1 TW 48.1 .1 400-580 65.931 73.7 27.98 Sseos ol EasrenN Eunopl pRotvL rHr Bl,q.cr Spr /.)

1999 (n=262 ind.)

1997 (n=377 ind.) c o (ú 1996 (n=272 ind.) = 1993 (n=734 ind.)

o% 2Oo/"

n First spawning r Repeated spawning

Figure 2.-Proportion of first and repeated spawning for Pontic shad ìn the Danube River;ind = individuaÌs. was stronger through climatic and hydrological cycles, best ex- =rveen fecundity and total weight plained Pontic shad population dynamics' The last ": = O 536) than bet'r,veen fecundity and standard was tn7999,and population size appears .:,gth (r'z = 0.309). minimum be increasing again. The eggs of Pontic shad remain Pelagic untìl to -::ching, then larvae and juveniles migrate pas- Feeding differences among the three alosines raker counts and body sizes. --. eÌr. toward the sea. In the river, juveniles feed refÌect their gill Caspian shad, with their relatively small size and - -jnly on zooplankton. Historically, some juveniles high gill raker counts, are plankton feeders. The ' -.r,rÌd enter the Danube River floodplain and delta two species reach larger sizes and have lower :

15 -n a c = a 19 =o- Y=-0.0018x+1.378 05I R2 = 0.8551

500 200 100 River migration distance (km)

Flgzre 3.-Relationship between the FuÌton condition coefficient index (F = TW x 100/ standard lengthr) and distance of migration of Pontic shad using during 1988 and 1989 migrations.

Sea are landed in the Russian Federation; this fish- Fortunately, however, the critical Danube River ery has an economic value of about $0.4 million. population has proven to be robust despite bar- Black Sea shad stocks in Romania have collapsed. rages, pollution, exploitation, and environmental Annual landings of Pontic shad (Figure 4) vary changes in the Black Sea. AIso, they may have ben- greatly and appear to be cyclic, with several strong efited from a rise in the overall productivity of the years being foÌÌowed by several low ones. Shads of Black Sea since 1970, possibÌy caused by several the Black Sea do not support sport fisheries because factors: a favorable climatic regime, increased they are not considered suitable for angling. eutrophication, and the effects of trophic cascades attributable to overfishing of predators, However, fishery managers should not be compÌacent con- Discussion cerning the Black Sea shads; experiences with alosines across their Íanges have shown that they This paper attempts to synthesize information on are highly sensitive to these multipÌe stresses. It is the three shads of the Black Sea. Howevet it is clear reasonable to assume that the overall decÌine of the that much information is lacking, particularly for Black Sea environment could bring one or more of the Caspian shad and Black Sea shad. It remains these species below a threshold at which substan- possible that more is actually known but that all tiaÌ population decreases might ensue. It aÌso is knowledge of these species has not been shared likely that stock assessment and management oi among the several nations that fish them or in these species would benefit from a multinationaÌ whose waters they are found. Moreover, manage- approach in order to estimate stock size and exploi- ment of the most important of these species-Pon- tation at regional rather than national levels. tic shad-is hampered by the poor quality of catch Improved predictability of run size in the statistics and fishing effort data among the nations Danube would be a useful management tool. One that harvest this species in the Black Sea drainage. obvious factor is river flow, but the relationship

3p00 y =7E-O7xÊ - o ooolf + 0 O089xa -0j779f - 1.5728f +7o288x- 46.992 ca 25OO '-i zpoo 1,500 cP -c 1000 õ () 500

(O (O o (O O Õ + o N o O

FígtLre 4 {alch statistics of Pontic shad from the Romanian portion of the Danube River, 1920 2000. 75 Sg.cos op EesrEm Eunopr rnolvl rHr Bt-.tcr Sr'q

trends for Pontic shad requires :"::i\-een river Ílow and year-class strength for tion of population ---:.ls is not clear. Aprahamian (2001; for twaite - :-l Á. fallax fuorl the Severn River, UK) and shad Á' -:ecco and Savoy (1987; for American -..'.,lissima from the Connecticut River) argue that mental factors. Monitoring of a jur-enile index of . ,..ort strength is negatively correlated with river valuable inÍormation . ',ç due to mortality driven by turbidity effects' recruitment couid also give de on population trends. Indeed, management of all -ì'tçever, C. Mennesson-Boisneau (Université - of the Black Sea would benefit strongl,v . ,.-rrs) and P. Boisneau (Association Agréée thróe shads -:erdépartementale des Pêcheurs Professionnels from additional scientific research. :: Bassin de la Loire et des cours d'eau Bretons, ,:stract from the 1st Conference on EuroPean References :, :ds, 2000; for allis shad Á. alosa lalso known as , ce shad], from the Loire River, France) and nu- Antipa, G. 1905. Die Clupeinen des westlichen Teiles :.rous studies of Pontic shad in the Danube River à"t Schwarzen Meeres und der :entified a positive Donaumündungen' DenkschriÍten der ::uÌt migratory stock Mathematisch-Naturwissenschaftlichen Klasse Akademie der Wissenschaften, of birih. It is not der Kaiserlichen =:.r Wien 28:1-56. rn is due to species differences, the characteris- 1909. Fauna ichtiologica, a Romaniei' technical differences Antipa, G. .':s of the rivers analyzed, or Ãcdemia Romana, Publicatiile Fondului the case of Pontic shad In Adamachi, Bucuresti, Romania' maY r. River, the flood Pulse AP. .. uctivitY, both in the river -:r.d the Black Sea, leading to fast growth of shads' ,-r,rrr'ever, extreme spring floods in the Danube may .-:\ e a negative influence on early life stages of 362/363:953-973. Republicii Populare Romane' :rntic shad due to high turbiditY. Banarescu, P 1964. Fauna Pisces-Osteichthyes. Editura Academiei Republici second key factor that explains variation in A ucuresti, Romania. is water temperature' ;-rpulation size of shads ter Íishes of the U.S S R and in Ber -pìahamian (2001) found that for twaite shad volume 1. Translated from -:e Severn River, water temPerature from July ex- Program for Scientific Trans- :-aÌned 67.1'% oÍ the variation in year-class lations, jerusalem'

et des eaux intérieurs' population d1'namics us- Roumaine de la Mer Noire rinistic models of shad é asslt 22(1- migration, Annuelle Scientifique de l'Universit J 4):306-344. s and at sea Cautis, I., and R. Teodorescu-Leonte' 1964' Corelatia nd others, dintre viitura si dinamica cârdului de scrumbii nference on (Alosa pontica pontica Eichw.) care intra in Dunare -uropean Shads, 2000). Mennesson-Boisneau and pentru reproducere. Buletinul Institutului cle 'Cercetare 23(1):34- 3oìsneau (conference abstract,2000) argue that the pentru Pescuit si Piscicultura :ecruitment of alÌis shad from the Loire River is in- Jependent of parent stock size' Consequently, their :eiruitment model is based on density-indepen- lent, habitat-related Íactors. Similarly, Stier and Crance (1985) tried to explain the population dy- a namics of American shad through models using Bethesda, MarYland. habitat-suitability index that expresses habitat re- Cre T. 19E7' Fis quirements, especialÌy for vuÌnerable stage of de- shad in the E r eÌopment of fish. rtment of From these observations, we conclude that an f Fisheries, explanation oÍ population dynamics and predic- Hartford. elo W,qLPl'tarl ,h N,cvooA.nu

riversarld Elanidze,- - R. F. 1983. Ichthyofauna of the i"t"i of Ceorgia. Akademy Nauk' Georgia' SSR' (ln Russian.) R H Beverton' 1985 The fisheries -f. -à,-,--."ro.tr.", L., and ] oÍ the Mediterranean' part two: Black oÍ the Sea. Food and Agriculture Organization United Nations, Rome' of -Ivanog * L., and P. Kolarov' 1979' Tine dependencv thá àich of the Danube shad (Alosaponticapontica Eichw.) of the solar activity Jubilã-ums^tagung (In óor,urrio.r.tlnng, SIL-Ban, SoÍia 19:389-395'

Wiesba Kolarov P 1938); P freshw Anguilid Kolarov, P. 1 1001). Pa Íreshwa Anguilidae. Aula-Verlag, Wiesbaden' GeÏn?ny' Bioìogia Kottelaí M. 1997. EuroPean ireshwater fishes