American Fisheries Society Symposium 35:69-7 6, 2003
O 2003 by the American Fisheries Society
Shads of Eastern Europe from the Black Sea:
Review of Species and Fisheries
IoN Navooenur
for Reseatch and Deaelopntertt,
DantLbe Deltn National Instítute
Babadng Street, 165 Tilcea 8800, Romanin
JouN R. Walpr,reN
Rioer Foundntion for Science nnd En-oironmental
Research,
HtLdson
77 Bnttery Place, Suite 915, Neu York, Netn York 10004, USA
species beÌonging to Alosa are known in the northwestern part of the BÌack
-Threethe Sea of Azov: Pontic shad A. pontica (EichwaÌd, 1838), Caspian shad Á.
including
Abstrnct
Sea,
(Etchwald, 1838), and BÌack Sea shad A. mneoticn (Crimm, 1901). Regional populations,
and possibly subspecies, occur in the Danube, 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.
caspia
lntroduction
The Black Sea
Three alosines are native to Eastern Europe: Pontic
shad Alosa pontica (Eichwald, 1838), Caspian shad
A. caspia nordmanni (Eichwald, 1838), and Black Sea
shad Á. mneotica (Grimm, 1901). These shads are
heavily Íished and are important commercially and
The Black Sea is a large inland sea measuringT,2l1
km from east to west and as much as 560 km from
north to south, with an area of more than 400,000
km2. It is bordered by Ukraine on the north, Russia
on the northeast, Georgia on the east, Turkey on
the south, and Bulgaria and Romania on the west.
The Black Sea is connected with the Mediterranean
Sea by a reÌatively narrow water\ rav that includes
the Bosporus, the Sea of Marmara, and the
culturally within their respective distributions. All
are found in the Black Sea region, an area of considerabÌe environmental stress. However, knowledge of the biology and conservation status of these
Dardanelles. Because of this, its tides are generalÌy
less than 10 cm. The Black Sea's largest arm is the
Sea of Azov; both the Don and Kuban rivers enter
it. Other major rivers flor.'r'ing into the Black Sea
include the Southern Buh, Danube, Dneister, and
Dnieper. About 20% of Europe's continental landmass drains to the Black Sea.
The Black Sea has two lavers of water of different densities. The bottom layer is highly saline,
rich with hydrogen suÌfide, and hypoxic, has lìttle
circulation, and is virtually dead biologicalÌy. The
shads is poor.
In this paper, we review the biology and status of all three shads, with an emphasis on the bestknown species, Pontic shad. Both Pontic shad and
Caspian shad are found in the Black Sea and
Caspian Sea basins; we restrict our treatment to the
BÌack Sea basin. Coverage of these fishes in the
Caspian Sea is provided in Coad et al. (2003, this
volume).
Ì
Corresponding author: [email protected]
69
Nevooanu
70
lsu
Welou'qN
is less saline' circulates countercloc'k'nner laver
,i.n marine lire' However' the
ì:f5 ";à';";À,i'
;h.k;;ã,-'iilto"*""thasbeent"";l"t-t"tffo"lï
tive sPecies, blue' or viol
is leidYi
(also
the
ected. wj.th
mon Ponto-Caspian origin
the oPercuÌa
the oPerculum' bu
accoun
1L^
+Lrrêê qnê
Thethreespe
u*o"g theiifaunas
;Ë;;"d
flanks' TheY
where they co-oc
discriminatory fe
TaxonomY
distinguish
are useful
counts
raker
Gill
not for
but
ad'ults
among
es
.tntiçn:t:;to
Young sPecimens
cm.
nlosn
wlth Alosn'
Banarescu
(1964)
shad in the Black
signations
have
Pontic
Distribution
Shad
ludes the
of Azov
to sPawn
:1ïi:ïi:.fl-"ï:"Ï il:
e.been dissrdes of the
ranges between
astern PoPulation
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'
well deveioPe
Sea shad a
Black
tic shad and
all
In
shad'
ìn CasPian
on both jaws are
ering ierminates with
alae, which iie sYmme
caudaÌ
fin
The ventra
Snnos op E,qsreRN Eunopp
jìg some years, it is
:nd the Razim-Sinoi
Lake
escu-
77
Blecr Sre
Dur-
Rom
:ends along the
FRoM rHE
BiologY
There are considerable differences ìn spawning
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-
:tream from the Danube River mouth. Berg (1948)
arrd Svetovidov (1952, 1964) cited Antipa's (1905,
1909) opinion that Caspian shad migrate up to km
931 (Iron Gate) from the Danube's mouth, and this
ivas recently corroborated by N. BacalbasaDobrovici (Lower Danube University, personal
communication), who caught Caspian shad at river
km 864. Caspian shad is also found in the Dniester
and Bug rivers, but it never migrates far from their
river mouths. In the Dnieper Riveç it does not min (Vladimirov 1953a). The
had Á. c. tanaica extends
Sea, north of Batumi, the
Sea of Azov and the Lower Don River.
Black Sea Shad
This species inhabits (Figure 1) both the Black Sea
and Sãa of Azov (Kolarov 1991c). Large schools of
this fish enter in Razim-sinoie Ìake complex on the
Romanian coast (Borcea 1936; Teodorescu-Leonte
and Munteanu 1968). It also appears in some years
along the Bulgarian coast. In the eastern part of the
Blaci Sea, it ranges from the region of the Strait of
Kerch to Novorossysk and south along the
Caucasus coast.
rrì
ìlâ
tl
rivers or in river deltas' Less is known of the spawning iocations of Black Sea shad, but it appears they
utilize low-salinity waters of deltas and lagoons
Ivanov and Beverton (1985) discussed two
Íorms of Pontic shad. The larger one spawns in the
Don River and overwinters in the eastern part of
the Black Sea between Novorossisk and Batumi'
The smaller form lives in the western portion of
the Black Sea and enters the Danube River to
ance is high, it aiso
r, and Bug rivers.
migrated in the
travel only 90
can
now
but
to
Kiev
Dnieper River
km from the river mouth due to a dam
' Pontic shad migrate northward in the Black
Sea in spring and early summer as they move toward spawning rivers. Historically, Pontic shad
penetrated far up the Danube with specimens capiured at Budapest (river km 1,650), but the migration route was reduced to 864 km, aÍter construction of the Iron Gate II hydroelectric plant in 1983'
Barrages at river km 943 and 864 appear not to
have Àad a large impact on the river's Pontic shad
popuiation; most spawning occurs between river
km
180 and 500.
,|
\
ii'1
Ìì
ag,.1!'ar,
-:-'€.\.,
-
'
.- tl
tlümáfi1á
6!tl:.-
.f*'
;
l
I
I
I
s
aí'ii
Trrlêy I
O
Figure 1-Distribution of Eastern European shads, (a) Pontic shad,
Black Sea.
Elack5ea
ft) Black Sea shad, and (c) Caspìan shad' from
the
72
Navooenu aNIo WeloMAN
Adult Pontic shad moving upriver in the
Danube for spar,r'ning are composed of age-2 to age7 individuaÌs. These proportions shift annualÌy, but
age-3 specimens usually comprise 50ok or more of
the totaÌ run, with the age-6 and age-7 classes con-
tributing about 1% or less (Navodaru 7996, 1998).
The three shad species have similar maximum
kno'wn ages: 6 years for Black Sea shad and 7 years
for the other two species.
Total lengths oÍ Pontic shad males and females
/
; are approximately equal for each age-class; femaÌes
r,r'eigh more than males at each age interval, but this
difference is not statistically significant (P < 0.05).
The relationship between total length (TL) and totaÌ weight (TW; TW = aTLb), estimated for 6 years
oÍ migration (1997-7996), incÌuding 1I,375 individuaìs, was allometric (b + 3): TW = 0.0563TL, as?.
Crowth in length by age (Table 1) was linear for
average dimension by age (TL = 2.3081. Age +
22.031). Pontic shad mns in the Danube River over
4 years were dominated by first-time spawners
' with repeat spawners comprising 4-73./. of total
' spawners annuaÌly (Figure 2).
The Pontic shad migration in the Danube River
begins in early spring when water temperatures
reach 3.0-7.5"C, peaks in April and May at between
9"C and 17'C, and ends in June and july when
water temperatures reach 22-26"C (Navodaru 1996,
1998). Early run fish appear to contain less fat than
later run individuals (Table 2). The relationship
between body fat and water temperature for Pon-
tic shad entering the Danube River was strongly
positive (y = 0.4832x - 7 .4397 ; r' = 0.9764), possibly
compensating for loss of biomass through greater
energy expenditure in migration and reproduction
at higher water temperatures. There was also a
strongly positive relationshrp (rt = 0.8551) between
river migration distance at capture and body condition as assessed by the Fulton index (Figure 3).
During this upstream migration, Ponüc shad
spawners lost biomass due to egg maturation and
deposition and energy spent for migration. Analysis of nine postspawning individuats in comparison with their biomass entering in-river, calculated
with the length-weight relationship, indicated that
these shad iost of 10.3-42.7% of biomass. Biomass
loss differs by sex (Íemales lose more biomass than
do males; between 10.3% and 30.4'/. for males and
10.342.7% for females) and by age (biomass loss
increases with age with an average loss for age-3
Íish of 23.1%; Íor age-4 frsh, 23.8%; and for age-S
f:LsLr,397%).
The fecundity of the 1987 Danube River run
of Pontic shad was analyzed in detail. Thirty females were examined, ranging between 25 and32
cm (standard length) and 195 and 450 g (TW). The
number of eggs per g ranged between 1,080 and
5,41.4, wífh a mean of 3,122. The gonadosomatic
index (gonad weight x 100/TW) was as low as 2.61
and as high as 9.74, averaging 4.86. Absolute fecundity ranged between 13,910 and 88,983 eggs per
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
2
394
TL
SL
3
5,758
TW
TL
4,577
TW
TL
SL
4
SL
5
599
TW
TL
SL
Mean
26.77
22.87
168.65
29.02
25.37
/z/.)
30.89
26.85
269.93
33.6
29.22
TW
324
SL
TW
35 95
37.77
389.97
SL
JJ,Jõ
658TL
79TL
38.22
TW
48.1 .1
.1
Range
SD
19.3-31.5 2.7
77-27.5 r.823
60-290 39.439
20.5-39.3 7.957
17.2-33 I.753
75-550 45.513
23 5-38.5 1.861
20-33.5 7.789
115-520 53.816
26-39.2 7.785
22.2 34.7
1.725
160-610 58.119
33.5-39.3 7.439
26 35
7.542
270-600 54.744
36.6-39.6 0.981
37.7 35
1.093
400-580 65.931
CV
SE
8.03
7 99
23.39
6.74
69.3
20.01
6.02
6.66
79.94
5.31
5.9
77.64
4
4.95
14.04
2.57
3.27
73.7
of mean
0.11
0.09
1.
99
0.03
0.02
06
0.03
0.03
0.8
0.07
0.07
237
0.19
0.2
7.79
0.33
0.36
27.98
Sseos
ol
EasrenN Eunopl
pRotvL
/.)
rHr Bl,q.cr Spr
1999 (n=262 ind.)
c
o
1997 (n=377 ind.)
(ú
1996 (n=272 ind.)
=
1993 (n=734 ind.)
o%
2Oo/"
n First spawning
Figure
r
Repeated spawning
2.-Proportion of first and repeated spawning for Pontic shad ìn the Danube River;ind =
individuaÌs.
was stronger
=rveen fecundity and total weight
": = O 536) than bet'r,veen fecundity and standard
.:,gth
(r'z = 0.309).
The eggs of Pontic shad remain Pelagic untìl
-::ching, then larvae and juveniles migrate pas--. eÌr. toward the sea. In the river, juveniles feed
-jnly on zooplankton. Historically, some juveniles
' -.r,rÌd enter the Danube River floodplain and delta
: <es; however, due to construction of embank-:nts, most drift directly to the sea (Navodaru
- '1). Later, juveniÌes and also some yearlings in-..:it coastal waters, moving offshore as they grow.
Vladimirov (1953b), Niculescu-Duvaz and
'.,-..lbant (1965), and Cautis and Teodorescu-Leonte
ról) stated that there is a positive relationship
--r\ een recruitment of Pontic shad and river flow
r ihe Danube. Also, in an analysis of a iong data
-;:ies of catch statistics and solar activity, Ivanov
.:rì Kolarov (1979) established a negative correla-.n between catch and solar activity with a cycle
:
11 years. They concluded
through climatic and hydrological cycles, best explained Pontic shad population dynamics' The last
minimum was tn7999,and population size appears
to be increasing again.
Feeding differences among the three alosines
refÌect their gill raker counts and body sizes.
Caspian shad, with their relatively small size and
high gill raker counts, are plankton feeders. The
other two species reach larger sizes and have lower
numbers of gill rakers, consistent with their partly
piscivorous habits..Pontic shad feed mainly on small
fishes such as anchovies Engraulis spp. and sprats
Clupeonella spp. and Sprnttus spp. (Zaytseva1953),
but they also consume crustaceans such as Crangon
spp., mud shrimps upogebin spp', Idothea spp., and
Gammarus spp. Caspian shad are considered to be
a warmwater species, whereas Black Sea shad Íavor cooler temperatures, as cold as 3-4'C. Wintering occurs at substantial depths, 40-100 m for Pontic shad and 50-70 m for Caspian shad.
that solar activity,
Fisheries
'.-'2.-Average fat content (% dry substance) per month
. . ::acted from migratory Pontic shad enterìng the Danube
:
.
er
in 1985.1986, and
n
.:ril
1995
1995
,:re 1995
1996
1.1:v 1996
:re 1996
l.
l:r
-:ril
-.-:ri1 1997
'.' 2.: 1997
'
-ne 1997
6
46
4
B
72
2
6
10
6
1987.
(%)
TemPerature ("C)
82
48.81
67.57
35 88
50.11
79 78
36.10
37.61.
46.21
9.84
75.96
22 06
8.77
18.89
22.22
7.83
15 36
27.78
Fat
37
Average 1995-7997
-:frÌ
I Í.rr
_:ne
20
68
12
36.60
45.51
62.52
8 81
76.74
22.02
All three alosine species are fished in the Black Sea
drainage, with the particular nations fishing each
species reflecting its geographic availability. Some
catch data are mixed among species, making species-speciÍic summaries less precise. Pontic shad are
harvested in the Danube River by a totaÌ of about
5,000 fishermen from Romania, Bulgaria, Serbia,
and Ukraine. PresentÌy, the Pontic shad fishery is
productive but variable, with an economic value
òf about US$2 million and annual Ìandings of about
1,000 metric tons. About 70'k of the fish are taken
by Romanian fishermen. Caspian shad are more
actively pursued in the Caspian Sea, but approxrmately 400 metric tons per year of Caspian shad
captured in the northwestern Portion of the BÌack
l
Nevoonuu eNo W,cLoN4eN
a
15
-n
c
19=
a
Y=-0.0018x+1.378
o=
05I
R2 = 0.8551
200
500
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.
landed in the Russian Federation; this fishery has an economic value of about $0.4 million.
Sea are
Black Sea shad stocks in Romania have collapsed.
Annual landings of Pontic shad (Figure 4) vary
greatly and appear to be cyclic, with several strong
years being foÌÌowed by several low ones. Shads of
the Black Sea do not support sport fisheries because
they are not considered suitable for angling.
Discussion
This paper attempts to synthesize information on
the three shads of the Black Sea. Howevet it is clear
that much information is lacking, particularly for
the Caspian shad and Black Sea shad. It remains
possible that more is actually known but that all
knowledge of these species has not been shared
among the several nations that fish them or in
whose waters they are found. Moreover, management of the most important of these species-Pontic shad-is hampered by the poor quality of catch
statistics and fishing effort data among the nations
that harvest this species in the Black Sea drainage.
3p00
y =7E-O7xÊ - o
a
c
25OO
i
'-
zpoo
P
c
-c
õ
()
ooolf
+ 0 O089xa
Fortunately, however, the critical Danube River
population has proven to be robust despite barrages, pollution, exploitation, and environmental
changes in the Black Sea. AIso, they may have ben-
efited from a rise in the overall productivity of the
Black Sea since 1970, possibÌy caused by several
factors: a favorable climatic regime, increased
eutrophication, and the effects of trophic cascades
attributable to overfishing of predators, However,
fishery managers should not be compÌacent concerning the Black Sea shads; experiences with
alosines across their Íanges have shown that they
are highly sensitive to these multipÌe stresses. It is
reasonable to assume that the overall decÌine of the
Black Sea environment could bring one or more of
these species below a threshold at which substan-
tiaÌ population decreases might ensue. It aÌso is
likely that stock assessment and management oi
these species would benefit from a multinationaÌ
approach in order to estimate stock size and exploitation at regional rather than national levels.
Improved predictability of run size in the
Danube would be a useful management tool. One
obvious factor is river flow, but the relationship
-0j779f
- 1.5728f
+7o288x- 46.992
1,500
1000
500
(O
<f
\f, @ N (O
$ o N (O O
Õ +
o
N N
ó o
õ O
+ s @N
s n to O
o o (o F.- Ì'- c)
@ @ @ o) o) o
-oj N
o) o) o) o) ó o) o) o, o) o) o) o) o) o) o) o) o) o) o)
rN I
FígtLre
4 {alch
1920 2000.
statistics of Pontic shad from the Romanian portion of the Danube River,
75
Sg.cos op EesrEm Eunopr rnolvl rHr Bt-.tcr Sr'q
:"::i\-een river Ílow and year-class strength for
---:.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
river
. ,..ort strength is negatively correlated with
. ',ç due to mortality driven by turbidity effects'
C. Mennesson-Boisneau (Université de
- -ì'tçever, P. Boisneau (Association Agréée
. ,.-rrs) and
-:erdépartementale des Pêcheurs Professionnels
:: Bassin de la Loire et des cours d'eau Bretons,
,:stract from the 1st Conference on EuroPean
:, :ds, 2000; for allis shad Á. alosa lalso known as
, ce shad], from the Loire River, France) and nu:.rous studies of Pontic shad in the Danube River
:entified a positive
::uÌt migratory stock
is not
=:.r of birih. It
rn is due to species differences, the characteris.':s of the rivers analyzed, or technical differences
In the case of Pontic shad
r.
..
River, the flood Pulse maY
uctivitY, both in the river
tion of population trends for Pontic shad requires
mental factors. Monitoring of a jur-enile index of
recruitment couid also give valuable inÍormation
on population trends. Indeed, management of all
thróe shads of the Black Sea would benefit strongl,v
from additional scientific research.
References
Antipa, G. 1905. Die Clupeinen des westlichen Teiles
à"t Schwarzen Meeres und der
Donaumündungen' DenkschriÍten der
Mathematisch-Naturwissenschaftlichen Klasse
der Kaiserlichen Akademie der Wissenschaften,
Wien 28:1-56.
Antipa, G. 1909. Fauna ichtiologica, a Romaniei'
Ãcdemia Romana, Publicatiile Fondului
Adamachi, Bucuresti, Romania'
AP.
-: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
:rntic shad due to high turbiditY.
A second key factor that explains variation in
;-rpulation size of shads is water temperature'
in
-pìahamian (2001) found that for twaite shad
362/363:953-973.
Banarescu, P 1964. Fauna Republicii Populare Romane'
Pisces-Osteichthyes. Editura Academiei Republici
ucuresti, Romania.
ter Íishes of the U.S S R and
volume 1. Translated from
Program for Scientific Trans-
Ber
-:e Severn River, water temPerature from July ex-
:-aÌned 67.1'% oÍ the variation in year-class
rinistic models of shad population d1'namics usmigration,
s
and at sea
nd others,
nference on
-uropean Shads, 2000). Mennesson-Boisneau and
3oìsneau (conference abstract,2000) argue that the
:ecruitment of alÌis shad from the Loire River is inJependent of parent stock size' Consequently, their
:eiruitment model is based on density-indepenlent, habitat-related Íactors. Similarly, Stier and
Crance (1985) tried to explain the population dynamics of American shad through models using a
habitat-suitability index that expresses habitat requirements, especialÌy for vuÌnerable stage of der
eÌopment of fish.
From these observations, we conclude that an
explanation oÍ population dynamics and predic-
lations, jerusalem'
Roumaine de la Mer Noire et des eaux intérieurs'
Annuelle Scientifique de l'Universit é J asslt 22(14):306-344.
Cautis, I., and R. Teodorescu-Leonte' 1964' Corelatia
dintre viitura si dinamica cârdului de scrumbii
(Alosa pontica pontica Eichw.) care intra in Dunare
reproducere. Buletinul Institutului
pentru
'Cercetare
cle
pentru Pescuit si Piscicultura 23(1):34-
Bethesda, MarYland.
Cre
T. 19E7' Fis
shad in the
rtment of E
f
Hartford.
Fisheries,
N,cvooA.nu
,h
elo
R. F. 1983. Ichthyofauna of the riversarld
Elanidze,
-i"t"i of Ceorgia. Akademy Nauk' Georgia' SSR'
(ln Russian.)
L., and R ] H Beverton' 1985 The fisheries
f.
--."ro.tr.",
- -à,-,
oÍ the Mediterranean' part two: Black
oÍ the
Sea. Food and Agriculture Organization
Rome'
United Nations,
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
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