Nicole Aberle, Henriette Horn,Aleksandra Lewandowska, Ulrich Sommer

MAY 2016ICES/PICES 6TH ZOOPLANKTON PRODUCTION SYMPOSIUM

BERGEN

Microzooplankton in a changing environment: shifts in phenology and

trophic relations

1

Kraberg et al. 2008

2

Climate changes effects on oceans

temperature

increase

elevated pCO2

elevated concentrations of

green house gases e.g. CO2

enhancedUV radiation

acidfication

sea levelrise

higher airtemperatures

changes in air pressure

higher storm frequencies

melting sea ice

salinity changes

changes incurrent systems

changes in upwhelling

anthropogenic impacts

temperature increase

elevated pCO2

elevated concentrations of

green house gases e.g. CO2

sun

enhancedUV radiat.

acidfication

sea levelrise

higher airtemperat.

changes in air pressure

higher storm frequ.

melting sea ice

salinity changes

changes incurrent systems

changes inupwhelling

anthropogenic impacts

3Warming: Aquatic food webs become more microbial

Sarmento et al.

Phil. Trans. R. Soc. B

2010;365:2137-2149

Microbial food webs in a warming ocean

DFG Priority Programme AQUASHIFT:

Kiel Plankton Mesocosm Cluster

Bacteria, Phyto- and Zooplankton, Biogeochemistry, Modelling

Experimental design

Baltic Sea spring bloom:

2005-2009

• Indoor mesocosms (1400 L): 12

• Temperatures (ΔT): 0 and 6°C

• Additional manipulations:

light regime and copepod density

• Treatments: 2 replicates each

0 40 80 120 160 200

Julian Days

0

4

8

12

16

20

Tem

pera

ture

in °

C

deltaT 6

deltaT 4

deltaT 2

deltaT 0

Spring temperature modell

0 40 80 120 160 200

Julian Days

0

4

8

12

16

20

Tem

pera

ture

in °

C

deltaT 6

deltaT 4

deltaT 2

deltaT 0

Spring temperature modell

Te

mpe

ratu

re in

°C

Julian day

Δ0°C: decadal mean (1993-2002)

Bio

ma

ss

Spring season

Spring scenario (temperate regions)

Seasonal succession patterns of spring plankton

Phytoplankton Microzooplankton Fish larvaeMesozooplankton

Heterotrophic processes are more vulnerable to

temperature changes than autotrophic ones

‘Metabolic Theory of Ecology’ (Brown et al. 2014)

Phenology shifts with warming

• Reduced time-lags between autotrophs and

heterotrophs with warming

• Shifts in timing (and magnitude) of MZP biomass

• Stronger top-down control of phytoplankton by MZP

• Alterations in energy transfer (enhanced dietary

competition between MZP and mesozooplankton)

WARMING

‘Trophic link’ ‘Trophic sink’

?

Day of the year

40 50 60 70 80 90 100

Cu

mu

lati

ve b

iom

ass (

%)

0

20

40

60

80

100

120

6°C: 64%

6°C: 48%

6°C: 32%

°C: 64%

°C: 48%

°C: 32%

Qend= 75% threshold

Qstart= 25% threshold

Qmedian= 50% threshold

Aberle et al. Mar Biol 2012→ Earlier timing of MZP in the mesocosms

7

MZP biomass (2008)

Time-lags between ciliates and phytoplankton

Bio

masse in µ

g C

L-1

Julianischer Tag

ΔT=0 ΔT=2 ΔT=4 ΔT=6

40 60 80 100 12040 60 80 100 12040 60 80 100 120

10-2

10-1

100

101

102

103

40 60 80 100 120

CilPhyto

Data: Sommer, Lengfellner, Aberle

Temperature treatment ΔT (°C)

Bio

ma

ss

(µg

C L

-1)

→ Reduced time-lags between phytoplankton and MZP with warming

8

Phenology shifts

Aberle et al. (Mar Biol, 2012)

6°C: 62%

Y A

xis

30

20

40

60

80

100

MZ

P b

iom

ass (

µg

C l

-1)

0

10

20

30

40

°C: 62%

Day of the year

40 50 60 70 80 90 100

Y A

xis

3

0

20

40

60

80

100

MZ

P b

iom

ass (

µg

C l

-1)

0

10

20

30

40

A

6°C: 57%

B

6°C: 49%

Co

pep

od

bio

mass (µ

g C

l-1

)

0

20

40

60

80

100

Ph

yto

pla

nkto

n b

iom

ass (µ

g C

l-1

)

1

10

100

1000

Col 1 vs Col 4 Col 14

Col 15

Col 1 vs Col 4

Col 9 vs Col 12

C

D

°C: 57%

Day of the year

40 50 60 70 80 90 100

Y A

xis

3

0

20

40

60

80

100

E

°C: 49%

Day of the year

40 50 60 70 80 90 100

Ph

yto

pla

nkto

n b

iom

ass (µ

g C

l-1

)

1

10

100

1000

Co

pep

od

bio

mass (µ

g C

l-1

)

0

20

40

60

80

100F

Copepods

small phytoplankton

Ciliates

Dinoflagellates

medium phytoplankton

→ Reduced temporal occurrence of MZP9

Phenology shifts (2008)

Hypotheses:

1. High overwintering copepod densities will affect MZP

biomass (size classes/community composition)

2. Warming at high copepod densities will lead to a strong

top-down control on MZP→ MZP functions as a ‘trophic link’

3. Warming at low copepod densities will lead to an earlier

timing of MZP and a shortened temporal occurrence → MZP functions as a ‘trophic sink’

Test for the combined effects of warming and densities of

overwintering copepods on MZP biomass and phenology

Warming & overwintering copepod densities

11

Aberle et al. (MEPS 2015)→ MZP bloom intensity was highly affected by copepod density

→ Strong suppression of MZP (especially ciliates <30 µm) at elevated

temperatures

Top-down control by copepods

Initial copepod density (copepods L-1

)

1,5 4 6

Blo

om

in

ten

sit

y (

BP a

t D

ma

x)

in µ

g C

l-1

-50

0

50

100

150

200

250

300

D 6°C: 1.5 cop L-1

_A

D 6°C: 4 cop L-1

_A

D 6°C: 10 cop L-1

_A

D 6°C: 1.5 cop L-1

_B

D 6°C: 4 cop L-1

_B

D 6°C: 10 cop L-1

_B

Linear regression D 6°C

D 0°C: 1.5 cop L-1

_A

D 0°C: 4 cop L-1

_A

D 0°C: 10 cop L-1

_A

D 0°C: 1.5 cop L-1

_B

D 0°C: 4 cop L-1

_B

D 0°C: 10 cop L-1

_B

Linear regression D 0°C

D 6°C

r²= 0.67

b= -36,9

D 0°C

r²= 0.87

b= -112.3

1.5 4 10

Initial copepod density (copepods l-1)

MZ

P b

loo

min

ten

sit

y(µ

g C

l-1

)

Kraberg et al. 2008

12

Effects of warming & ocean acidification (OA)

temperature

increase

elevated pCO2

elevated concentrations of

green house gases e.g. CO2

enhancedUV radiation

acidfication

sea levelrise

higher airtemperatures

changes in air pressure

higher storm frequencies

melting sea ice

salinity changes

changes incurrent systems

changes in upwhelling

anthropogenic impacts

temperature increase

elevated pCO2

elevated concentrations of

green house gases e.g. CO2

sun

enhancedUV radiat.

acidfication

sea levelrise

higher airtemperat.

changes in air pressure

higher storm frequ.

melting sea ice

salinity changes

changes incurrent systems

changes inupwhelling

anthropogenic impacts

Will OA affect lower food web dynamics?

Phytoplanktonn

Microzooplankton

Mesozooplankton

Bacteria

POCDOC

HNF

Warming vs. OA: an indoor mesocosm study (BIOACID II 2012-2015)

• 12 mescocosms filled with Baltic

Sea plankton communities

• Two different temperatures levels:

cold and warm (Δ 6°C)

• CO2 gradients: 500 ppm (low) to

max. 3000 ppm (high)

Will the combined effects of warming and OA induce

direct or indirect effects on the phenology, community

composition and carrying capacity of MZP?

Horn et al. (ICES J Mar Sci 2015)

Ciliate biomass (BIOACID II 2012)

cold warm

→ Warming: earlier timing and higher growth rates

→ No effects of pCO2 on total ciliate biomass

Species composition (BIOACID II 2012)

Horn et al. (ICES J Mar Sci 2015)

Cil

iate

bio

ma

ss

(%)

Low CO2 High CO2

Cold

Warm

→ No effect of pCO2 conditions

→ Changes in MZP composition and succession

patterns with warming

Species composition (BIOACID II 2013)

Horn et al. (ICES J Mar Sci 2015)

Cil

iate

bio

ma

ss

(%)

Horn et al. (unpublished data)

• Warming affects MZP timing, growth, community

composition and succession

• Warming leads to reduced time-lags between

phytoplankton and MZP

• Reduced temporal occurrence of MZP with warming

• Stronger top-down control by copepods on MZP at high

temperature conditions

• High tolerance of MZP to changes in pCO2 (peak timing,

biomass and community composition remained

unaffected)

Conclusions: OA & warming

• Co-operating partners of the AQUASHIFT

Kiel Mesocosm Cluster

• T. Hansen, S. Schröder & C. Rautenstrauch

for technical support

19

Phytoplanktonn

Microzooplankton

Mesozooplankton

Bacteria

POCDOC

HNF

Key role of microzooplankton (MZP)

Traditionally the role of micrograzers

as phytoplankton consumers has

been neglected

Zooplankton grazing on phytoplankton

21

60% of the primary production consumed daily by

MZP and only 10% by mesozooplankton

Calbet et al. 2008

Warming will lead to:

1. Reduced time-lags between autotrophic and

heterotrophic processes with warming

2. Shifts in timing and magnitude of MZP biomass

3. Stronger top-down bloom control by MZP

4. Enhanced trophic overlap and dietary competition

between MZP and mesozooplankton

WINTER WARMING SZENARIO

22

Hypotheses

23

Aberle et al. (Mar Biol, 2012)

→ Strong suppression of the ciliate Lohmaniella oviformis

PZP community composition

6°C

Initial copepod density (copepods L-1

)

Y D

ata

0

50

100

150

200

250

0°C

Initial copepod density (copepods L-1

)

PZ

P b

iom

as

s (

µg

C l

-1)

0

50

100

150

200

250

A B

1.5 4 10 1.5 4 10

Myrionecta rubra

Lohmaniella oviformis

Protoperidinium bipes

Protoperidinium pellucidum

Gyrodinium spp.

Gymnodinium spp.

Tintinnida

Rimostrombidium sp.

Euplotes sp.

Time course of small algae (yellow), diatoms (green), ciliates (red),

dinoflagellates (black) and copepods (blue)

∆6°C

∆0°C

Q10=2 Q10=4 Q10=6

5 15 25 35 450

500

1000

1500

a

5 15 25 35 450

500

1000

1500

b

5 15 25 35 450

500

1000

1500

c

5 15 25 35 450

500

1000

1500

d

5 15 25 35 450

500

1000

1500

e

5 15 25 35 450

500

1000

1500

f

Aberle et al.

Mar Biol 2012

→ With increasing Q10 of copepods a tighter coupling between PZP

and copepods occurs (strong top-down control of PZP) 24

Predator prey model (2008)

Relationship MZP-copepods

Klauschies et al. (Mar Biol 2012)

0.5 1 1.5 2 2.50

0.5

1

1.5

2

log10

mean biomass COP

log

10 m

ean b

iom

ass C

S

a (high-light)

0 1 2 3-2

-1

0

1

log10

mean biomass COP

log

10 m

ean b

iom

ass C

L

b (high-light)

0 0.5 1 1.5 2 2.5-0.5

0

0.5

1

1.5

2

log10

mean biomass COP

log

10 m

ean b

iom

ass D

INO

c (high-light)

0.5 1 1.5 2-0.5

0

0.5

1

log10

mean biomass COP

log

10 m

ean b

iom

ass C

S

d (low-light)

0 0.5 1 1.5 2-1

-0.5

0

0.5

1

log10

mean biomass COP

log

10 m

ean b

iom

ass C

L

e (low-light)

0.5 1 1.5 2-2

-1.5

-1

-0.5

log10

mean biomass COP

log

10 m

ean b

iom

ass D

INO

f (low-light)

• Mean biomass of small (CS) and large ciliates (CL) and

heterotrophic dinoflagellates (DINO)

• Black (ΔT=4°C, ΔT=6°C) and grey (ΔT=0°C, ΔT=2°C) linear regressions

(P<0.05)

→ Strong suppression by coperpods

log

10

me

an

bio

ma

ss

log

10

mean

bio

mass

log

10

mean

bio

mass

log10 mean COPEPOD biomass

small ciliates large ciliates heterotrophic dinoflagellates

Phytoplankton: green

MZP: orange

Copepods: grey areas26

Aberle et al. (Mar Biol, 2012)→ No top-down control of MZP at low temperatures + copepod

density

Plankton succession (2009)

6°C: 10 cop L-1

co

p b

iom

as

s (µ

g C

l-1

)

0

5

10

15

20

25

30

flu

ore

sc

en

ce

(in

viv

o)

0.1

1

10

100

1000CB

PZ

P b

iom

as

s (

µg

C l-1

)

0.1

1

10

100

1000A

D

6°C: 1.5 cop L-16°C: 4 cop L-1

°C: 10 cop L-1

Day of the year

40 50 60 70 80 90

co

p b

iom

as

s (µ

g C

l-1

)

0

5

10

15

20

25

30

flu

ore

sc

en

ce

(in

viv

o)

0.1

1

10

100

1000F

°C: 4 cop L-1

Day of the year

40 50 60 70 80 90

E

°C: 1.5 cop L-1

Day of the year

40 50 60 70 80 90

PZ

P b

iom

as

s (

µg

C l-1

)

0.1

1

10

100

1000

Co

pe

po

db

iom

as

s(µ

g C

l-1

)

MZ

P b

iom

as

s(µ

g C

l-1

)

Winder et al. Mar Biol 2012 → Advanced peak timing of PZP 27

Peak timing (2005-2009)

Winder et al.

Mar Biol 2012

Winder et al.

Mar Biol 2012

→ No impact on peak magnitudes of PZP 28

Peak magnitude (2005-2009)