BULGARIAN ACADEMY OF SCIENCESInstitute of Oceanology — Varna, Bulgaria

LONG – TERM SHIFTS IN THE BLACK SEA PLANKTON COMMUNITY

(BULGARIAN COAST)

K. Stefanova, S. Moncheva, V. Doncheva, L. Kamburska

The Black Sea is one of the world’s semi-enclosed seas particularly sensitive to anthropogenic impacts due to its isolation and large river inflow. The identified key ecological problems are the anthropogenic eutrophication, the unsustainable exploitation of the biological resources and the invasion and expansion of exotic species. Three periods are differentiated in the Black Sea ecosystem evolution in terms of the anthropogenic pressure - reference near natural state period (up to the early 70-ties) – pre-eutrophication , period of early and intensive eutrophication (from the 70-ties to the early 90-ties) and the recent period manifesting signs of ecosystem recovery (last 10 years).

The 1970s are recognized as a period of extremely high nutrient loading into the basin; the 1980s are renowned for gelatinous and aliens outbreaks, and overfishing, while the 1990s are known as predisposed to the climatic forcing (Moncheva et al., 2001; Oguz, 2005-a). These ecological issues have provoked remarkable ecosystem alterations which have been well documented.

Problem

.

VarnaVarnaVarnaVarna

Hot Spots Along the Black Sea

Case study area

27.6 27.8 28 28.2 28.4 28.6 28.8 29 29.2

4 2 . 2

4 2 . 4

4 2 . 6

4 2 . 8

4 3

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4 3 . 4

4 3 . 6 101 102 103 104

201 202 203 204 205 206 300

301 302 303 304 305 306 307 308

401 402 403 404 405 406 407 408 409

500

501 502 503 504 505 506 507 508 509

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601 602 603 604 605 606 607

Varna

Burgas

c. Kaliakra

c. Galata

c. Emine

Shabla

Area of long term monitoring

The map represents the monitoring area along the Bulgarian Black Sea coast during the last ten years. The long term shifts are assessed mainly on data collected from 3 miles in front of c. Galata, which is under the indirect impact of various influence .

Long term measurements

Parameter Abbreviation

Total zooplankton biomass ZBCopepoda abundance

Cladocera abundance

Noctiluca scintillans abundance N. sciBacillariophycea bloom abundance

Dinophyceae bloom abundance DinTotal catches of Bulgaria TCTemperature TDanube river discharge DD

Sun spot activity SSA

A long term data array of physical,

chemical and biotic

parameters presented in the

table are discussed in the

study.

Zooplankton Key groups

0

10000

20000

30000

40000

Cladocera Copepoda

abun

danc

e [in

d.m

- 3]

The diversity and community structure of Copepods and Cladoceras – typical for the Black Sea ecosystem decreased substantially from pre-eutrophication period to nowadays. Many of the dominant mesozooplankton species, supporting fish populations were replaced by smaller, less-valuable species. The average abundance of both key groups demonstrate similar changes among the years (Konsulov et. al., 1998; Konsulov & Kamburska, 1997, 1998).

Species

Year

1954-1967

1984 -

19871991-1995

1996 1998 1999 2000

Acartia clausi * * * * * * *Paracalanus parvus * * * * * * *Oithona similis * * * * * * *Pseudocalanus elongatus * * * * * * *

Calanus euxinus * * * * * * *Anomalocera patersoni

* - - - - * *

Pontella mediterranea * - - - - * *Oithona nana * * - - * * -Centropages ponticus * * - - - * *

0

1

2

3

4

5

6

7

1970-1980 1980-1990 1990-1997 1998-2001

Oithona nana Centropages kroyeri

biom

ass

[mg.

m-3

]

Figure The average biomass of O. nana and C. ponticus (syn. C. kroyeri) in front of Bulgarian

Black Sea coast

Warm-water and eurythermal copepods such as O. nana, C. ponticus, inhabiting the upper mixed layer, and reproducing predominantly in the warm season (Gubanova et al, 2000) have disappeared during 1980s and 1990s . The species density and biomass decline could most probably be related to a combination of two factors, gelatinous predatory pressure and pollution.

Other groups

11 6 11

6 2 5

64 6

11 2 3

0%

20%

40%

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100%

1970-1980 1981-1990 1991-2001Copepodа Cladocera Meroplankton Ctenophora

20012000

19991998

0

2

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10

num

ber

of sp

ecie

s

groups

years

Zooplankton biomass dynamic

0

50

100

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300bi

omas

s [m

g.m-3

]

years

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350

catches Bulgaria zooplankton biomass

bio

ma

ss [mg

.m-3]

catc

he

s [t

]

years

Mnemiopsis leidyi

Figure Long-term dynamic of fodder summer zooplankton biomass (without N. scintillans) along the Bulgarian Black Sea coast in the period 1967-2001 and total fish catches (Prodanov, Konsulov et. al. 2001)

The eutrophic Black Sea ecosystem has produced more zooplankton biomass than it used to in its pre-eutrophication phase. The combination of eutrophication-induced bottom- up control and top-down control by gelatinous carnivores and small pelagic fishes lead to strong variations in the mesozooplankton (Oguz, 2005-b). Critically low zooplankton biomass of the Bulgarian Black Sea coast is registered in the middle of 1980-ies when the highest fishing efforts were registered and after M. leidyi introduction (Prodanov, Konsulov et. al. 2001).

Beroe ovata

Box & W his ker Plot: Copepoda

-2000

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Co

pep

od

a ab

un

dan

ce (ind

/m3 )

Pre -e utrophication

Mean Mean±SE Mean±1.96*SE

Ear ly e utrophication

In te ns ive e utrophication

Pos t e utrophication

Box & W his ker Plot: Cladoc era

-5000

0

5000

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30000

Cla

do

cera

ab

un

dan

ce (

ind

/m3 )

Pre -e utrophication

Ear ly e utr ophication

Mean Mean±SE Mean±1.96*SE

In te ns ive e utr ophication

Pos t e u tr ophication

The regime shifts of summer biomass prove the significant alteration of zooplankton qualitative and quantitative structure. The large fluctuations of copepods and cladoceras contributed mostly to the overall mesozooplankton biomass deviation. Cladocera in the early 70-ies overdominated the mesozooplankton composition, whereas Copepoda maintained high density in pre- and early eutrophication phases. In general key groups gradually diminished during eutrophication.

Shifts in the mean for summer biomass (Galata) , 1967-2004Probability = 0.01, cutoff length = 10, Huber parameter = 1

0

100

200

300

400

500

600

1967

1969

1971

1973

1975

1977

1979

1981

1983

1985

1987

1989

1991

1993

1995

1997

1999

2001

2003

Regime-shift of summer mesozooplankton biomass (by Radionov, 2005)

Box & W his ker Plot

2000

4000

6000

8000

10000

12000

14000

Fis

h c

atc

h (t

ones

)

Mean Mean±SE Mean±1.96*SE

Pre -e utrophication

Ear ly e utrophication

Inte ns ive e utrophication

Pos t e utrophication

Box & W his ker Plot:

-100

0

100

200

300

400

500

600

700

Zo

op

lan

kto

n s

um

mer b

iom

ass (m

g/m

3 )

Pre -e utrophication Inte ns ive e utrophication

Ear ly e utrophication

Pos t e utrophication

Mean Mean±SE Mean±1.96*SE

Overfishing caused the reduction of medium and large pelagic fish catches and their removal from the system made the smaller and less-valuable planktivorous fishes (anchovy, sprat) the dominant predators in the ecosystem (Oguz, 2005-b). This change doubled the exploited stock of anchovy and sprats, and subsequently their total catch at the end of the 1970s to middle of the 1980s (Prodanov et. al. 1997). As a result, a different type of top-down control started operating on the lower levels of the food web lead to two-fold decline in mesozooplankton biomass and a comparable increase in phytoplankton biomass (Daskalov 2002). This was not a result of eutriphication only, but a process that also included overfishing (i.e. top-down effect). The catches of small fishes started decreasing during the post eutropication phase. The niche vacated by these fish groups was gradually replaced by gelatinous zooplankton (the jellyfish Aurelia aurita followed by M. leidyi) and other opportunistic species as N. scintillans (Mutlu, 1999 Oguz, 2005-b).

Shifts in the mean for Northwest, 1965-2001Probability = 0.05, cutoff length = 10, Huber parameter = 1

0

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700

1965

1967

1969

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1999

2001

Box & W his ker Plot

-10000

-5000

0

5000

10000

15000

20000

25000

30000

35000

40000N

.sci

nti

llan

s a

bu

nda

nce (

ind

/m3 )

Mean Mean±SE Mean±1.96*SE

Pre -e utrophication

Ear ly e utrophication

In te ns ive e utrophication

Pos t e utrophication

Regime-shifts of A. aurita (by Radionov, 2005)

The increase in density and biomass of moon jelly in the 1970s might have been associated with overfishing and removal of mackerel, which was a main predator of Aurelia in Black Sea (Arai, 2001). Because of their competitive advantage for food as compared to small pelagics, and their predation on eggs and larvae of small pelagics, the total gelatinous biomass, mostly of the jellyfish Aurelia aurita, reached its peak in the beginning of 1980s, and finally attained the low value when the population of the ctenophore Mnemiopsis leidyi exploded.

N. scintillans an indicator species of eutrophication become dominant with frequent and massive blooms in the two phases of eutriphication.

catc

hes B

ulg

ari

aN

. scin

till

an

s a

bu

nd

an

ce

(ind/m

3)

zo

op

lan

kto

n b

iom

ass

Year max.: 2001

N-catch-ZB.tab - 21.10.2005 17:43 h PANGAEA/PanPlot

1967 1977 1987 1997

0

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In pre-eutrophication period N. scintillans average abundance was low, while in the next periods (1978-1988) it increased about 7 fold (9087 ind/m3) with a higher range of summer oscillations. Two extremely high maxima are evident in 1977 and in 1989 (Kamburska et. al. 2003-a), the decrease of fodder zooplankton biomass during the 80-ies being concurrent with increased fish catches.

-2 -1 0 1 2C ladocera, C opepoda (ind/m 3), -Phytop lankton B loom s (cells /l),

-2

-1

0

1

2

N.s

cintil

lans

(ind/m

3 ), f

ish c

atc

h (t/y

)

1967

1968

1969

1970

197119721973

1974 1975

1976

1977

1978

1979

1980

1981

1982

1983 1984

1985

1986 1987

1991

1994

1995

1996

1997

1998

19992000

-2.0

-1.5

-1.0

-0.5

0.0

0.5

1.0

1.5

2.0

-2.0

-1.5

-1.0

-0.5

0.0

0.5

1.0

1.5

2.0

A

B

A1

C

The comparison between the different periods reveal a high variability of plankton community characteristics (abundance of dominant groups and N. scintillans, phytoplankton blooms and catches of pelagic fishes) resulting in dissimilarity between the years suggested by the PCA analysis.

The PCA analysis extracts 2 components to which variability could be attached (PC1) and (PC2).

PC1 correlates positively with Copepoda and Cladocera abundance and negatively with phytoplankton blooms.

PC2 corresponds to increasing of N. scintillnas abundance and fish catches. A PCA plot displays a discrimination between the 1970 (cluster A split into two subgroups), 80s (cluster B), and the 90s (cluster C).

A. The A group, corresponding to the pre-eutrophication period of the ecosystem is characteristic with low blooms densities and frequency, high copepods and cladoceras density and low N. scintillans abundance, while A1 subgroup (1975- 1979) marks the transition between the reference (the 70ies) and the intensive eutrophication (the 80ies) episodes.

B. The 1980-1988 (B group ) – e.g. intensive eutrophication corresponds to highest fish catches, phytoplankton blooms and N. scintillans abundance, and low ZB.

C. Typical for the recent period (post eutrophication) –group C includes years characterized with decreasing phytoplankton blooms and low abundance of N. scintillans.

A

B

C

0%

20%

40%

60%

80%

100%

1986-1991 1992-1999 2000 2001 2002 2003

diatoms dinoflagellates other groups

Phytoplankton communities similar to zooplankton manifest parallel structural changes in terms of major taxonomic groups (Bacillariophyceae, Dinophyceae) during the different phases of the Black Sea ecosystem evolution.

The share of dinoflagellates in the blooms increased from 15% prior to1970 to 60% during the 80s and 90s on the account of diatoms relative decrease. After 70s summer blooms occurred regularly in addition to the typical spring blooms, dominated mainly by dinоflagellates, coccolitophores and euglenophytes.

The Bac:Din biomass ratio is considered normally an indicator of the taxonomic structure of phytoplankton communities, the classical spring-summer value for undisturbed system reported to be 10:1 (Petrova-Karadjova,1984, Moncheva et. al., 1997). Thus the inversion of this ratio during the 80-ies reflects the higher dominance of opportunistic Dinophyceae species.

In contrast to the 80ies in the recent period the ratio Bacillariophyceae: Dinophyceae increased in favour of the diatoms, (about 3 times in spring and twice in summer) suggesting a trend of diatom dominance recovery as typical for the reference period of the evolution of the Black Sea coastal ecosystem (Moncheva et. al., 2001).

-1.2

-1

-0.8

-0.6

-0.4

-0.2

0years

[log

Bac

illar

ioph

icea

&D

inop

hyce

a]

Bacillariophycea Dinophycea

Cluster B - The split of the 1980s (B) into two subgroups - B (1980-1985) and B1 (1986-1989) is more apparent along the PC1 axis (blooms/grazing). It is parallel to the different amplitude of Din blooms increase (maximum values recorded during 1986-1989) and the contrasting trend of ZB dynamic (reduction of ZB, more explicit since 1986). Both subgroups are projected at coordinates corresponding to the highest level of eutrophication component.

Cluster A - (1960-70s), corresponding to the reference period of the ecosystem, is characteristic with low blooms densities and frequency, high grazing and low N. sci., relatively high temperature and low level of eutrophication component.

B

C

-2 -1 0 1 2 3PC1:Din , -ZB, N.sci

-3

-2

-1

1

2

PC

2:

-T,

DD

, S

SA

C1

C2

C3

A

B1

Cluster C - The 1990-1993 (C1 subgroup) of the recent period marks the transition between the reference (the 70s) and the intensive eutrophication (the 80s) episodes. The association of 1994-1996 (C2 subgroup) to the reference A, reflects more the similarity of the interaction fashion between the selected determinants despite the differences of the real values. A decreasing trend of nutrients and phytoplankton blooms and an increasing trend of ZB was observed but sustained at a higher level (respectively lower for ZB), in comparison to the reference period, at higher T and similar SSA The C3 subgroup corresponds to a blooms/grazing mode characteristic for the transition episode (C1) at higher T and maintained decreasing trend of eutrophication componen (Moncheva et. al., 2001)

The PCA performed on data array including additional parameters – Danube discharge, sun spot activity, temperature, zooplankton biomass, Dinophyceae blooms the same clusters were discriminated.

Exotic species

Mnemiopsis leidyi

Beroe ovata

•The undesirable effect over the Black Sea ecosystem is the invasion of the ctenophore Mnemiopsis leidyi (Agassiz, 1865) in the early 1980s. Introduced by ballast waters from the Northern Atlantic coast, M.leidyi emerged to a key controlling factor for the ecosystem in the late 80ies- 90ies mainly due to zooplankton reduction by feeding.

predator

Recently (1997), a new ctenophore species, Beroe ovata (Mayer, 1912) has been introduced into Black Sea basin. Тhis species is the only one predator of M.leidyi. Possible recovery of the Black Sea zooplankton diversity, community structure and dynamic could be expected as a result of efficient predation of Beroe on Mnemiopsis

2.5

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1967 1970 1973 1978 1981 1984 1987 1994 1997 2000

0

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Copepods+Cladocera M.leidyi B.ovata

log

[M.leid

yi, B

.ov

ata abu

nd

ance]

log

[C

op

epo

ds,

Cla

do

cera

ab

un

dan

ce]

years

R=0.74

The long-term summer dynamic of the dominant mesozooplankton groups, the exotic ctenophores M.leidyi and B.ovata manifest significant inter-annual variability. Despite of the existing oscillations before the invasion of M. leidyi, during the 80ies-90ies, the average abundance of the two zooplankton groups sustain a lower level compared to the previous period (1967 ‑ 1982). Although the dominant groups maintained a long-term decreasing trend more explicit since 80ies (R= 0.74), most likely the occurrence of both exotic ctenophores contributed substantially to the recent pattern of mesozooplankton variability (Kamburska et. al. 2003-b)

Figure Long-term dynamic of dominant mesozooplankton groups and exotic ctenophores abundance in summer at 3 miles -transect Galata (by Kamburska et al. 2003-b).

2.5

3

3.5

4

4.5

5

1967 1970 1973 1976 1979 1982 1985 1988 1991 1994 1997 2000-2

-1

0

1

2

3

4

Copepods+Cladocera Cop+Clad/M.leidyi M.leidyi/B.ovata

[lo

g c

op

ep

od

s,cla

do

cera

ab

un

dan

ce]

[log

pre

y/ p

red

ato

r ratio

s]

The coupling copepods /cladocera versus M. leidyi/B. ovata interacting in a strong trophic relationship (typical prey-predator modes) is more significant and effective in summer-autumn period. Before the introduction of Beroe, the M. leidyi abundance was higher, which led to a decrease of mesozooplankton abundance. The ratios mesozooplankton / M.leidyi were higher in 1991-1992, and varied in a huge range (from 3 to 1100). The lowest ratio was less than classical one of 10:1 (at least 3), recorded in 1995. The occurrence of Beroe in the late 90ies resulted in a sharp decline of its prey. The prey-predator coupling M.leidy‑ B.ovata modified the mesozooplankton growth as well. When the ratio Mnemiopsis/ Beroe abundance was higher, as a consequence Mnemiopsis grazing pressure on copepods and cladocera abundance was low and an increasing of dominant groups was evident. However, that prey-predator ratio did not reach the classical one (maximum was 5), which could suggest an effective trophic utilization of secondary produced organic matter (Kamburska et. al. 2003-b). .

Conclusions The long–term shifts of diversity, abundance and biomass of dominant

mesozooplankton groups (copepods and cladocera) reflect the four phases of Black Sea ecosystem development (pre-etrophication, early, intensive and post eutrophication periods).

The recent performances of mesozooplankton community structure (diversity, growth) points at recovery, related mainly to the reduction of top-down Mnemiopsis control. Yet, Mnemiopsis is a key controlling factor, especially in summer.

Signs of recovery of the pelagic flora and fauna are recognized during the post eutrophication period - increasing diversity, abundance and biomass of sensitive to eutrophication zooplankton species, reduced amplitude of seasonal oscillations and year to year variations of phytoplankton blooms.

However, indications such as high fluctuation of dominant zooplankton groups, mass development of zooplankton tolerant to eutrophication species as well as the still significant impact of Mnemiopsis leidyi on zooplankton structure in summer, persisting in the current period, testify for sustained anthropogenic impact on the ecosystem.

ReferencesArai, M. N., 2001. Pelagic coelenterates and eutrophication: a review. Hydrobiologia 451:69-87.Daskalov G. M, 2002. Overfi shing drives a trophic cascade in the Black Sea. Marine Ecology Progress Series 225:53-63.Gubanova A., Yu. Prusova, U. Niermann, N. Shadrin, I. Polikarpov, 2001. Dramatic Change in the Copepod Community in Sevastopol Bay (Black Sea) during Two Deacds (1976-1996)., Seckenbergiana marit., 31 (1): 17-27.Konsulov A., Tz. Konsulova, K. Prodanov, S. Moncheva, K. Dencheva, A. Velikov, L. Kamburska , 1998. State of the art and tendencies for changes in the Black Sea biodiversity in front of the Bulgarian Black Sea coast. V. Kotlyakov et al. (eds.), Conservation of the Biological diversity as a Prerequisite for Sustainable Development in the Black Sea Region, Kluwer Academic Publishers, 101-128. Konsulov A., L. Kamburska, 1997. Sensitivity to anthropogenic factors of the plankton fauna adjacent to the Bulgarian coast of the Black Sea. NATO ASI Series ‘Sensitivity to Change: Black Sea, Baltic Sea and North Sea”, Environment, Kluwer Academic publishers, vol. 2/27, 95-104.Konsulov A., L.Kamburska, 1998. Black Sea zooplankton structural dynamic and variability off the Bulgarian Black Sea coast during 1991‑1995. NATO ASI Series, 2.Environment-vol.2/27, “Ecosystem Modeling as a Management Tool for the Black Sea, Symposium on Scientific Results”, L. Ivanov & T. Oguz (eds.), v. 1, Kluwer Academic Publishers, 281‑293 Moncheva S., A. Krastev, 1997.Some aspects of phytoplankton long term alterations off Bulgarian Black Sea shelf. NATO ASI Series 2/27, Environment, E.Oszoy &E.Mykaelian, eds., Kluwer Academic Publishers, 79-94 .Moncheva S., V. Doncheva, L. Kamburska, 2001. On the long-term response of harmful algal blooms to the evolution of eutrophication off the Bulgarian Black Sea coast: are the recent changes a sign of recovery of the ecosystem‑the uncertainties. Proceedings of IX International conference on “Harmful Algal Blooms”, Hobart, Tasmania; G.M.Hallegraff et al., Eds. (UNESCO-IOC, Paris, 2001), 177-182

Kamburska L., S. Moncheva, A. Konsulov, A. Krastev, K. Prodanov, 2003-a. The invasion of Beroe ovata in the Black Sea a warning signal for ecosystem concern. Proceeding of Institute of Oceanology, vol. 4, 111-123.Kamburska L., V. Doncheva, K. Stefanova, 2003-b. On the recent changes of zooplankton community structure along the Bulgarian Black Sea coast –a post invasion effect of exotic ctenophores interactions. Proceedings of First International Conference on Environmental Research and Assessment, Bucharest, Romania, 69-85 pp. Mutlu, E., 1999. Distribution and abundance of ctenophores and their zooplankton food in the Black Sea. II. Mnemiopsis leidyi. Marine Biology 135: 603-613.Oguz, T., 2005-a. Black Sea ecosystem response to climatic teleconnections. Oceanography, Special issue features: Black Sea Oceanography, vol.18, 2, 122-133.Oguz, T., 2005-b. Long-term impacts of anthropogenic forcing on the Black Sea ecosystem. Oceanography, Special issue features: Black Sea Oceanography, vol. 18, 2, 112-121.Petrova-Karadjova, V., 1984. Changes in planktonic flora in Bulgarian Black Sea waters under the influence of eutrophication, Proc. Inst. Fish. 21, 105-112.Prodanov K., K. Mikhailov, G. Daskalov, K. Maxim E. Ozdamar, V. Shlyakhov, A. Chashcin, A. Arkhipov, 1997. Environmental management of fish resources in the Black Sea and their rational exploitation. General Fisheries Council of the Mediterranean Studies and Reviews 68:1-178.Prodanov K, S. Moncheva, A. Konsulov, L. Kamburska, Tz. Konsulova, K. Dencheva, 2001. Recent ecosystem trends along the Bulgarian Black Sea coast. Proceeding of Institute of Oceanology-BAS, Varna, vol.3, 110-127. Radionov , S. 2005. Report of the regime shifts detection group. UNESKO Workshop "Large-scale disturbances (regime shifts) and recovery in aquatic ecosystems: challenges for management towards sustainability", 13-17 June 2005, Varna, Bulgaria, http://biocore.ecolab.bas.bg/events/unesco-ws/