Assessment of the main drivers of the Black Sea ecosystem functioning Mnemiopsis leidyi and Beroe ovata impact on

the Black Sea ecosystem. Modeling approach.

Tamara Shiganova

P.P.Shirshov Institute of oceanology RAS, Moscow, RUSSIIA

Paul NivalLaboratoire d'Oceanographie de Villefranche Villefranche-sur-Mer, FRANCE

Distribution of M. leidyi in the native and invaded areas

Costello J. H., J. E. Purcell, K. M. Bahya, H. W. Mianzan & T. A. Shiganova, 2011

Native area

Invaded area

In the Black Sea, native gelatinous species belong to moderately cold-water species: the ctenophore Pleurobrachia pileus, scyphomedusa Aurelia aurita, and the pyrophyte alga Noctiluca scintillans. Two warm water invasive ctenophores arrived and established in the heated upper layer

Cold water species Warm water species

Subdivision of the gelatinous species in their relation to mean seasonal, annual and minimal winter SST: analyses of field data according to main component method )

Population genetic analyses supported its invasion from the Gulf of Mexico (e.g., Tampa Bay) into the Black Sea, then secondary into the Azov, northern Aegean and into the Caspian Sea and the Mediterranean (Ghaboolia, Shiganova et al., 2010)

1982

1988

1992

19901999

1993

2009

2005

2005

20092009

2006

2005

2006

2006

2007

2007

Dispersal of Mnemiopsis leidyi in the Eurasian seasDispersal of Mnemiopsis leidyi in the Eurasian seasMnemiopsis leidyi

19971997

1999

2004

2011

20052000

Dispersal of Beroe ovata in the Eurasian seasBeroe ovata

Black Sea

Sea of Azov

Aegean Sea

Caspian Sea

Baltic Sea

The dark areaCorresponds to theperiod of Mnemiopsis leidyi occurance(observations)

Environmental data and

M.leidyi invasion in the seas of Eurasia

After Shiganova et al., in press

Interannual variation of M.leidyi and B.ovata in the Black Sea

0

500

1000

1500

2000

2500

19841988

1989

1990

1991

1992

1993

1994

1995

1996

1997

1998

Years

Abun

danc

e, ind

.m-2

M.leidyi,ind.m2

0

500

1000

1500

2000

2500

1999

2000

2001

2002

2003

2004

2005

2006

2007

2008

0

200

400

600

800

1000

1200

M.leidyi,ind.m2

B.ovata,ind.m2

Zooplankton are the main food of M.leidyiChange of interannual variability of edible zooplankton after

appearance of invasive ctenophores in the inshore and offshore waters in August in the northeastern Black Sea

Zooplankton in the inshore waters,ind.m2

0

50000

100000

150000

200000

250000

300000

350000

400000

450000

500000

VIII.1989

VIII.1993

VIII.1994

VIII.1995

VII.1996

VIII.1998

VIII.1999

IX.2000

VIII.2001

VIII.2002

VIII.2003

VIII.2004

VIII.2005

VIII.2006

VIII.2007

VIII.2008

Years

Zoop

lank

ton,

ind.

m-2

Calanus euxinus Paracalanus parvusPseudocalanus elongatus Acarthia clausiOithona similis Pontella mediterraneaLarvae_Bivalvia Larvae_PolychaetaLarvae_Decapoda Larvae GastropodaCirripedia Larvae Parasagitta setosaCladocera without Penilia Penilia avirostrisCentropages ponticus Oikopleura dioicaHarpacticoida

Zooplankton in the offshore waters,ind.m2

0

50000

100000

150000

200000

250000

300000

350000

400000

450000

VIII.1989

VIII.1993

VIII.1994

VIII.1995

VII.1996

VIII.1998

VIII.1999

IX.2000

IX.2002

VIII.2003

VIII.2004

IX.2005

VIII.2006

VIII.2007

VIII.2008

zoop

lankto

n,ind

.m2

Calanus euxinus Paracalanus parvusPseudocalanus elongatus Acarthia clausiOithona similis Pontella mediterraniaOithona nana Oikopleura dioicaParasagitta setosa Larvae_BivalviaLarvae_Polychaeta Larvae_DecapodaLarvae Gastropoda Cirripedia LarvaeCladocera without Penilia Penilia avirostrisCentropages ponticus IsopodaOthers

Mnemiopsis leidyi seasonal cycle in cold (1993) and warm (1994) year before B.ovata arrival

Field data in the coastal area

r=0,6-08, p<0,001Cold yearCold year Warm year

Before the arrival of B.ovata, M.leidyi abundance was controlled by temperature and zooplankton prey

1994

0

1

2

3

4

5

6

7

8

9

I II III IV V VI VII VIII IX X XI XII

mn

emio

psi

s,г.

м-3

0

1

2

3

4

5

6

7

8

9

Zo

op

lan

kto

n,g

.m-3

Mnemiopsis Zooplankton

1992

0

1

2

3

4

5

6

7

8

9

I II III IV V VI VII VIII IX X XI XII

Mn

emio

psi

s,g

.m-3

0

1

2

3

4

5

6

7

8

9

Zo

op

lan

kto

n,m

g.m

-3

Mnemiopsis Zooplankton

2001

0

5

10

15

20

25

30

0 20 40 60 80 100 120 140 160 180 200 220 240 260 280 300 320 340 360

Time (days

Tem

pera

ture

, 0C

2003

0

5

10

15

20

25

30

0 20 40 60 80 100 120 140 160 180 200 220 240 260 280 300 320 340 360

Time (days)

Tem

pera

ture

, 0 C

2008

0

5

10

15

20

25

30

0 20 40 60 80 100 120 140 160 180 200 220 240 260 280 300 320 340 360

Time (days)

Tem

pera

ture

, 0 C

0

100

200

300

400

500

600

0 20 40 60 80 96 101 120 140 166 210 235 236 237 249 254 264 276 300 320 340 360

Zo

op

lan

kto

n, m

g.m

-3

0

100

200

300

400

500

600

20 40 60 80 100 120 148 160 180 200 220 240 250 260 266 270 280 300 320 340 350Z

oo

pla

nkt

on

,mg

.m-3

0

50

100

150

200

250

300

350

400

450

500

550

600

0 20 40 60 80 100 115 139 162 168 169 200 220 234 252 280 300 320 340 360

Zo

op

lan

kto

n,

mg

.m-3

0

20

40

60

80

100

120

140

160

180

200

220

240

260

0 20 40 60 80 100 120 140 160 180 200 220 240 260 280 300 320 340 360

Mn

emio

psi

s, i

nd

. m

-3

Mn.adult 1

Mn.Juv

Mn.eggs

Mn.larvae

0

20

40

60

80

100

120

140

160

180

200

220

240

260

0 20 40 60 80 100 120 140 160 180 200 220 240 260 280 300 320 340 360

Mn

emio

psi

s, i

nd

.m-3

0

20

40

60

80

100

120

140

160

180

200

220

240

260

0 20 40 60 80 100 120 140 160 180 200 220 240 260 280 300 320 340 360

Mn

emio

psi

s, i

nd

.m3

0

10

20

30

40

50

60

70

80

90

100

0 20 40 60 80 100 120 140 160 180 200 220 240 260 280 300 320 340 360Days

Ber

oe,

in

d.

m-3

0

10

20

30

40

50

60

70

80

90

100

0 20 40 60 80 100 120 140 160 180 200 220 240 260 280 300 320 340 360

Time (days)

Ber

oe,

ind

.m3

0

10

20

30

40

50

60

70

80

90

100

0 20 40 60 80 100 120 140 160 180 200 220 240 260 280 300 320 340 360Days

Ber

oe,

ind

.m-3

Ber.adult 1

Ber.Juv

Ber.eggs

Ber.larva

Temperature

Zooplankton

M.leidyi

B.ovata

A

JL

E

E

A

A

JL

Interannual variability of phenology of ctenophores M. leidyi and B.ovata in the coastal area of the NE Black Sea

Interannual variability of phenology of ctenophores M. leidyi and B.ovata in the coastal area of the NE Black Sea

Time of appearance of B.ovataTime of beginning reproduction of B.ovata

Time of appearance of M.leidyiTime of pick of reproduction of M.leidyi

120

140

160

180

200

220

240

260

280

300

320

340

360

1999 2000 2001 2002 2003 2004 2005 2006 2007 2008Year

Tim

e (d

ays)

appearance B.ovata Reproduction start of M.leidyiReproduction start of B.ovata Peak of M.leidyi reproduction Peak of B.ovata reproduction Disappearance M.leidyi larvaeDisappearance B.ovata larvae

--- M.leidyi

--- B.ovata

Life stages and forcing factors

for M.leidyi and B.ovataL J

E

A

food

Temperature

Individual based modeling approach was used to take into account life cycle and physiological features

E – eggsL-larvaJ-juvenaleA-adult

-mortality

0 50 100 150 200 250 300 350 4000

5

10

15

20

25

time (days)

biom

asse

zoo

pk (

mm

olN

.m-3

)

0 50 100 150 200 250 300 350 4005

10

15

20

25

30

temps days

Tem

pera

ture

(°C

)

Forcing functions

Zooplankton biomass

Temperature

Mortality rate

00.1

0.20.3

0.4

0

10

20

30

400

0.5

1

1.5

2

2.5

3

mmA1

0

0,5

1

1,5

2

2,5

0 5 10 15 20 25 30 35

Temperature (°C)

Ad

ult

mo

rta

lity

(d

ay

-1)

mm

A1

mortality

0

0,2

0,4

0,6

0,8

1

1,2

0 0,1 0,2 0,3 0,4

food concentration (mmol N.m-3)

mo

rtal

ity

rate

FoodTemperature

Mor

talit

y ra

te

Model

ZE

A

J

A

J

L

L

ETemperature

food

Prey – predator individual based model structure

M.leidyi

B.ovata

Age classes

L

A

J1

1

1

1

2

2

2

2

no

nL

nJ

nAprocess

ageing

Age classes

L

A

J1

1

1

1

2

2

2

2

no

nL

nJ

nAprocess

ageing

0% 50% 100%

fast growing

0

5

10

15

20

25

0 10 20 30 40 50

age (days)

length (

unit

s)

slow growing

egg

egg

larva juvenile

juvenilelarva

Adult

Adult

fast

slow

Change in stage duration depending on physiology (food, temperature)

0 5 10 15 20 25 300

50

100

150

temps days

n in

divi

dus

per

unit

volu

me

eggs

larvae

juveniles

adults

old adults

Time (days)

Num

ber

indi

vidu

als

per

unit

of

volu

me

first larva

first egg

first adult

first juvenile

Model

Ontogenetic cycle of M.leidyi and B.ovata development

5 10 15 20 25 300

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.9

1

temperature (°C)

spaw

ning

rat

e co

ef.

(d-1

)

Reproduction rate

0

100

200

300

400

500

600

700

20 21 22 23 24 25 26 27 28

Temperature, 0C

WW

,g,e

gg-

2.d

ay-1

0

20

40

60

80

100

120

140

160

180

20 21 22 23 24 25 26 27 28

Temperature, C

egg.

gWW

-1,d

ay

Experiments Model

M.leidyi

B.ovata

0 0.05 0.1 0.15 0.2 0.25 0.30

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.9

1

available food concentration

inge

stio

n ra

te c

oef.

(d-

1)

Ingestion rate coefficient (0 – 1)

C2= (Food- minFood)/ (Kf+ (Food-minFood))

C2 = 0 when Food < minFood

FoodminFood

0

0,5

1

1,5

2

2,5

3

3,5

4

0 2000 4000 6000 8000 10000 12000

zooplankton,ind.m-3

Ratio

n,DW

.day

-1

experiment Model

Ingestion rate

0

0.05

0.1

0.15

0.2 5 10 15 20 25 30 35

0

5

10

15

20

Stage duration

age to 50% transfer

Temperature (°C)

Ingestion

Sta

ge d

urat

ion

(day

s

optimum conditions

0 50 100 150 200 250 300 350 4000

50

100

150

200

250

300

350

400

temps (days)

num

bers

(n

m-3

)

First stage: M.leidyi present

B.ovata absent

A

L

J

E

0 50 100 150 200 250 300 350 4000

50

100

150

200

250

300

350

400

temps (days)

num

bers

(n

m-3

)

0 50 100 150 200 250 300 350 4000

50

100

150

200

250

time (days)

num

be

rs (

n m

-3)

M.leidyi

B.ovata

A

L

A

L

Second stage

B.ovata appears in surface water at time 200th day

Simulation of input of B.ovata in surface water at time 200th day.M.leidyi develops a bloom, which is grazed by B.ovataPredation on larvae, juveniles and adult on M.leidyi makes them disappear

Model

E

JE

J

0 50 100 150 200 250 300 350 4000

50

100

150

200

250

300

350

400

temps (days)

num

bers

(n

m-3

)

0 50 100 150 200 250 300 350 4000

50

100

150

200

250

time (days)

nu

mb

ers

(n

m-3

)

M.leidyi

B.ovata

A

L

A

L

0

20

40

60

80

100

120

140

160

180

200

220

240

260

0 20 40 60 80 100 120 140 160 180 200 220 240 260 280 300 320 340 360

Time days

Mne

mio

psis

, ind

. m-3

Mn.adult 1 Mn.Juv Mn.ova Mn.larvae

0

10

20

30

40

50

60

70

80

90

100

0 20 40 60 80 100 120 140 160 180 200 220 240 260 280 300 320 340 360Time days

Ber

oe,

ind

.m-3

Ber.adult 1 Ber.Juv Ber.ova Ber.larva

Model Field observations

M.leidyi

B.ovata B.ovata

L

J

A

L

E

A

JE

Conclusions

In present Black Sea ecosystem there is a bottom up control from zooplankton to its consumer Mnemiopsis leidyi and finally to its predator Beroe ovata.

Annual changes in temperature and food availability are considered as the main factors that control these predators’ dynamics and their impact on pelagic ecosystem of the Black Sea.Both field data analyses and individual based modeling confirmed that, with appearance B. ovata that controlled M. leidyi population, a recovering shift of the ecosystem appeared but was controlled by climate forcing.

Now in any case it is another ecosystem with two ctenophores that affected ecosystem but the time of high effect of M.leidyi is much shorter.

Acknowledgement

The research was performed in framework of project GK-0422

Thank you for attention