Effects of ocean acidification on marine animals in times of ocean warming Physiological mechanisms linking climate to ecosystem change Hans Pörtner

Searching for unifying physiological principles in animal ecology and evolution

Trends and projections of ocean warming: IPCC 2007 IPCC 2007

Many open questions ….however… …clear ecological impact is observed …physiological knowledge which explains ecological impact is available and emerging Temperature anomalies in different oceans between 1906 and 2005 compared to 1901 to  1950. Projections until 2100 according to emission scenarios B1, A1B, A2. Antragsskizze BIOACID – Biological Impact of Ocean ACIDification Bonn, 10. Dezember 2007

The „emerging The „ emerging“  “ danger danger: : Ocean Ocean Acidification (through CO2 enrichment enrichment)… )… ...associated with a pH‐decrement in surface water by 0.02 units per decade since 1980

Canaries

Hawaii

Even more questions…. …ecological l i l impact i setting i in (calcification) i ( l ifi i ) …emerging hypotheses and knowledge about physiological basis BEYOND calcification Bermuda

IPCC 2007

Analysing ecosystem effects of ocean acidification …..against against the background of ongoing change - on species level - on ecosystem level What do we need? To identify…. identify • Physiological mechanisms: …for a consistent cause and effect understanding beyond empirical observations! • Response of those mechanisms to various levels of OA! • Thresholds and time scales of effects: effects …at at species & ecosystem levels! • Realistic R li ti scenarios: i …on top t off ongoing i change! h !

↔ Integrating teg at g with t tthermal e a e effects ects a and d mechanisms ec a s s ↔ Building a thermal matrix for OA effects

Current ecological phenomena:: phenomena East Atlantic species are moving North …..to various degrees (!)

Anglerfish

Cod Snake blenny

~ Different thermal sensitivities → Changes in community composition

Cod (Gadus morhua) Anglerfish (Lophius piscatorius) Data : 1977 - 2001

Perry A.L. et al., 2005

Snake blenny (Lumpenus lampretaeformis)

Thermal specialization explaining ecological phenomena? The climate‐induced  “regime regime shift shift“ from sardines  from sardines to anchovies (Japanese Sea)  is linked to the thermal  windows of growth of the  two species.  Takasuka et al. 2007

Climate induced changes in the food web Regime shift from LARGE to SMALLer copepods in the North Sea…… driven by warmer temperatures.

LARGE Calanus finmarchicus SMALL C l Calanus helgolandicus

Percentage of C. helgolandicus in total Calanus

Different thermal windows of predator and d prey organisms i co--define prey co availability:: availability Affecting food web structure Smaller food items contributing t ib ti to t the th decline of cod stocks in the North Sea? Sea ?

(Beaugrand et al., 2003 Helaouët and Beaugrand, 2007)

Explaining thermal windows from animal physiology: Concept of oxygen and capacity limited thermal tolerance Tpejus Aerobic window

onset of hypoxemia Tp

O2-deficit Tcritical

Tc

cell damage

Tdenaturation Td Climate sensitivity is based on the specialization of animals on limited thermal windows set by aerobic 0 Optimum capacity Fitness measures: measures: Aerobic performance

growth, Specific Dynamic growth, Action (SDA), exercise, exercise, behaviours,, immune behaviours capacity,, capacity reproduction….. reproduction …..fitness fitness

0 Temperature

After Pörtner, 2001, 2002, Pörtner et al., 2005, Pörtner and Knust, Science 2007

Range of tolerance (passive)

Shelford‘s law of tolerance applicable to thermal limitations?

Range of maximum aerobic capacity Pessimum Pejus Optimum

Haemolym mph PO2 (mmHg g)

Tc I

Tp I

Pejus

Tp II

Pessimum Tc II

140 120 100 80

C Concept t off oxygen and d capacity it lilimited it d th thermall Limited cardiocirculatory and First verified inanimal Maja squinado tolerance supported by data from various ventilatory performance phyla: setting….. sipunculids,, annelids, molluscs (bivalves, sipunculids cephalopods), Commonalities crustaceans, vertebrates, …..air breathers 60

40 20 0

0

5

10

15

20

25

30

Succinate (μmol/g wet w wt.-1)

16

12

40

*

Musculature (leg) Hepatopancreas Heart Haemolymph

14

35

Tp:: pejus temperature, Tp temperature,

10

onset of hypoxemia

8

4

( j (pejus: getting tti worse))

*

6

*

Tc:: critical temperature Tc temperature,,

*

2

* 0

-0.3

7.9

12.5

control

21.6

33.3

Temperature (°C) Frederich and Pörtner, AJP 2000

loss of aerobic scope scope,, onset of anaerobic metabolism

CO2 enhances heat stress Heat stress enhances CO2 sensitivity sensitivity.. Tp

Tp

Normocapnia 10-22°C 1 % Hypercapnia 10-22°C

Cancer pagurus

PO2 (kPa)

15

10

Δ 4-5°C: High sensitivity of thermal thresholds to CO2

Tc

5

0 10

12

14

16

18

T Temperature t (°C)

Warming

Metzger et al., 2007

20

22

Enhanced hypoxemia under CO2: causes narrower thermal windows windows, lower performance optima? Organism thermal windows: optima, limits (Ι) and acclimation / adaptation (     ) loss of performance

Aerrobic scopee

Topt

Tpej

? Tpej

onset of anaerobiosis

CO2

onset of denaturation

hypoxia

Tcrit

Tcrit

Tden

T (°C) short

‐ long ‐ short term tolerance

Pörtner and Farrell, Science 2008

Are these physiological principles suitable to explain ecological phenomena phenomena? ? Eelpout (Zoarces viviparus) viviparus) abundance in the German g summer mean temperatures p Wadden Sea falls at high

relattive abunda ance

10

8

Early loss of LARGE i di id l due individuals d to the h allometry of oxygen limitation

6

4

2 17

18

19

mean summer temperature (°C) ( C)

20

To Tp

Climate effects in the field…..

Tc

Relative abunndance versus max. suummer temperatuure

10

(A)

8 6

Abundance

4 2

Eelpout

0 0

6

12

18

24

Daily grrowth ( mm / day )

0,6

(B)

0,4

G Growth th

0,2

0,0 0

Arterial blood flow (A AU )

30 25 20

Z Zoarces viviparus i i

North Sea At the limits of acclimation capacity the loss of …explained by oxygen limitations fitness (performance capacity)) beyond pejus limits capacity (C) causes reduced growth and field abundance abundance!! 6

12

18

24

15

Bl d flflow Blood

10 5 0

Liveer succinate (µmol//g wet weight)

0

6

12

18

24

(D)

1,0

(72 h)

0,8

O2-deficit

0,6 (24 h)

0,4 0,2 0,0 0

6

12

18

24

Temperature ( °C )

Pörtner and Knust, Science, 315, 95 – 97, 2007

Not all thermal windows are the same: Climate dependence and temporal dynamics

Thermal window widths across life stages (fishes)

Populations,  food web  interactions, phenologies

Spawners Growing adults Juveniles

Performance

Climate zone, Ecosystem

Sequen nce of life stages

Life history

Steno Stenotherm

Eurytherm

CoExistance

Eggs, early larvae A bi th Aerobic thermal window l i d

T clines T dynamics

Metabolic implications: Co-defining Co defining CO2-sensitivity? sensitivity? Pörtner and Farrell, Science

Hypothesis: CO2 dependent changes at ecosystem level in a climate change context

CoExistance

T clines T dynamics

Reduced Red ced spatial and temporal overlap under CO2 Performance

Perfo ormance

Populations,  food Populations food web  web interactions, phenologies

CoExistance

Differential sensitivities Relative changes in  performance: ‐ Δ competition ‐ Δ susceptibility to predation

T clines T dynamics

THERMAL WINDOWS: g changes g in food web dynamics y and a suitable matrix for understanding ecosystem functioning caused by Ocean Acidification Pörtner and Farrell, Science

Performance proxies (possibly) affected by OA • • • • • • •

Growth: Shirayama, Michaelidis….et al. Development: Shirayama, Dupont, Gutowska, Havenhand, Findlay….et al. F Foraging i capacity, it behaviours: b h i … Capacity for competition: … Exercise capacity: Melzner… Melzner et al al. Fecundity, recruitment: Boersma… et al. Immune capacity: Burnett, Bibby, Beesley…. et al.

(In)tolerance proxies (possibly) affected by OA • • • • •

Quality of carbonate skeletons: multiple authors... Predation resistance: Bibby… Bibby et al al. Mortality: Ishimatsu, Shirayama, Hall-Spencer… et al. Heat tolerance, cold tolerance: Baumgartner, g Metzger, g Walther… et al. Hypoxia tolerance: Reipschläger… et al.

Understanding differential sensitivities: Study of specific CO2 effects on changes g in p performance,e.g. , g g growth Mediterranean mussels M til Mytilus galloprovincialis

© M.S. Calle

560 ppm CO2 pHw 7.3

Mean she ell length (mm)

26 24

Growth Effective reduced d db by 55 control % (!)

140

mechanisms mechanisms? ? 100

22 20 18 16

hypercapnia

14

control

120

Cumu ulative percentage w et w eigh ht increase

30 28

Pacific sea urchin Hemicentrotus pulcherrimus l h i

80

60

hypercapnia yp p 40

12 0

20

40

60

80

100

20

Time (days)

Michaelidis et al. (2005)

0 2

4

6

8

10

12

14

16

Weeks from start

18

20

22

24

26

Data courtesy: Y. Shirayama

Tissue wet weight

M. galloprovincialis

Michailidis et al. (2005)

2.0 0.4 0.2 0.0 -0.2 -0.4 -0.6 -0.8 -1.0 -1.2 -1.4 -1.6

Wet weight off soft body (gr)

16 1.6 1.4 1.2 1.0

Log fresh weight (grr)

1.8

0.8

Searching for mechanisms: Close coordination in the reduction of tissue dry / wet weight and shell length

r2 0,9786 r2 0,9822

1.0

1.1

0.6

1.2

1.3

1.4

1.5

1.6

Log shell lenght (mm)

0.4 0.2 0.0 5

10

15

Shell length

Which parameter is coordinating di ti BOTH soft ft body growth and calcification rates rates? ?

r2 0,9877

Log dry weight ((gr)

Dry weight (gr)

0.10

35

-1.0 -1.2

0.12

30

-0.8

0.16 0.14

25

Shell length (mm)

Ti Tissue d weight dry i h 0.18

20

-1.4 1.4

r2 0,9726

-1.6 -1.8 -2.0 -2.2 -2.4

0.08

-2.6

0.06

1.0

1.1

1.2 1.3 Log shell lenght (mm)

1.4

1.5

Coordination disrupted in lower calcifiers (echinoderms, brachipods)?

0.04 0.02 0.00

5

10

15

20

Shell length (mm)

25

30

Shell length

35

Wood et al. 2008, J. Barry POSTER

Partially compensated extracellular acidosis in haemolymph of Mytilus galloprovincialis 5 (a)

7.60

(b) 4

7.55

Pco o2 (mmHg)

Extracelllular pH (pHe)

7.65

7.50 7.45 7.40 7.35 7 25 7.25 0

2

4

6

8

0

10

0

4.5 ((c)) (mM)

3.5

2+

3.0 25 2.5

Ca a

[HCO O3-]e mM

2 1

7.30

40 4.0

Hypercapnia (pHw 7.3) causes

3

2.0 1.5 10 1.0 0

2

4

6

8

32 30 28 26 24 22 20 18 16 14

10 Time (days)

2

4

6

8

10

2

4

6

8

10

(d)

0

- lowered pHe - elevated PCO2 - bicarbonate accumulation - Ca2+ accumulation in haemolymph.

Michailidis et al. (2005)

Reduced cellular protein synthesis during acidosis associated with reduced metabolic rates ….likely causing reduced growth rates

Langenbuch et al. 2006

Disentangling effective acid-base parameters by experiments manipulating acid-base status under normo- and dh hypercapnia. i Effects on metabolic rate, S. nudus muscle

Extracellular pH only is consistentlyy related to metabolic rate. Reipschläger and Pörtner, 1996

Teleost fish 10,000 ppm CO2 (=1%)

Atlantic Cod Gadus morhua

Full compensation of extracellular acidosis Lower sensitivity than in (l (lower) ) invertebrates? i t b t ? Decrements in performance depending on pH regulation capacity?

(Larsen et al. 1997)

The importance of defending extracellular pH:  Long term acclimation via gene expression of pH–regulation  mechanisms in fish gills Eelpout  (Z. viviparus) Na+K+‐ATPase Na+HCO3‐‐ Cotransporter

Expression  studied by real‐ studied by real‐ time PCR

6 weeks Deigweiher et al. 2008

Complete pHe compensation under expected CO2 accumulation scenarios: maintained thermal optimum in teleost fishes, at narrower thermal windows? Organism thermal windows: optima, limits thermal windows: optima limits (Ι) and acclimation / adaptation (     ) loss of performance, abundance

Aerobic sccope

Topt

Tpej onset of anaerobiosis

Tpej onset of denaturation CO2

Tcrit

hypoxia

Tcritit

Tden

T (°C) short

‐ long ‐ short term tolerance Pörtner and Farrell, Science

Uncompensated acidosis HYPOTHESES and metabolic depression in several lower invertebrates Mytilus spec spec..

Sipunculus nudus …contributing to reduced calcification, lower Regulation acid-performance, f resistance i t and dof extracellular acid Sea urchin enhanced mortality. base status as a major factor in Hemicentrotus pulcherrimus

Compensated acidosis d fi i sensitivity? defining sensitivity iti it ? and,, therefore, and therefore, no metabolic depression in most fish …contributing to maintained performance, enhanced resistance.

Acidosis causes performance decrements… decrements … ….the …. the link toGadus thermal tolerance? ? Antarctic morhua tolerance

Pachycara brachycephalum

eelpout l t

Sepia officinalis

High performance invertebrates invertebrates:: …developing p g fish-like p performance and resistance

©CephBase

Atlantic cod

Functional consequences of thermal adaptation: importance p of climate zone ((temperature p stability), y) hypoxia preadaptation, life history, lifestyle and phylogeny p y g y in setting g metabolic and pH compensation capacity

Sequen nce of life sstages

Thermal window widths across life stages (fishes): Relevance for CO2 sensitivity Spawners Growing adults Juveniles

Climate zone,, Ecosystem y Variable width and positioning of thermal  windows Performan nce

Life historyy

StenoSteno therm

Eurytherm

CoExists ance

Eggs, early larvae Aerobic thermal window

T clines T dynamics

e.g. pH compensation capacity p y less in crabs from the deep sea (Chionoecetes tanneri) than from shallow waters (Cancer magister, Necora puber) (Pane and Barry, 2007, Spicer et al., al 2007)

Pörtner and Farrell, Science 2008

Addressing CO2 effects and sensitivities in warming a g oceans, ocea s, hypotheses ypot eses First lines of CO2 sensitivity (with ecological relevance relevance)) likely depend on • CO2 effects on temperature dependent performance in rel rel. to compensation capacity for extracellular acid acid--base status. • This includes disturbance of calcification through extracellular acidification.. acidification Implications to be considered: considered: • seasonal shifts in performance windows • climate dependent functional specialization • temperature dependent biogeography • climate dependent growth growth,, fecundity • synergistic interactions with factors in addition to temperature (hypoxia hypoxia,, pollutants pollutants,, …))

Germany

United Kingdom

Pörtner et al. 2005, 2008

Low ocean pH and reduced HCO3‐ ion equilibria ion equilibria Calcification site

‐

‐

Na+/H+‐exchange etc. exchange etc Epithelia (gill, gut, kidney)

H+ Ω CO2 H2O

HCO3‐

Brain Chemosensory Neurons pHi ↓

H2O

ventilatio on rate      (some groups) Opercullum

metaabolic equilibria proteein synthesis rate

calcification

and high CO2

2 K+ Thermal windows:+ ATP ATP‐ ‐ ase He Adenosine 3 Na+ a suitable matrix to investigate and understand the accumulation  Na in the context of climate + specific effects of OA d l and release ‐ H sensitivity of ecosystems

H+i

+

+

Heart

HCO3‐ Cl‐

‐

gene expression ( + or ‐ ) expression (      or     ) intracellular space

mem mbrane

H+ Na+

‐ blood  pigment

extracellular space

Muscle

functional  capacity 

Tissues

‐

CLICOFI CLICOFI Effects of climate induced temperature change on marine coastal fishes EU PROJECT ENV4-CT-0596

SCAR: EASIZ, EVOLANTA, EBA CLIMATE CHANGE, THERMAL LIMITS and ADAPTATION, ENERGY

AWI:

BUDGETS , OCEAN ACIDIFICATION

National / International Partners Dr. Christian Bock Dr Katrin Deigweiher Magdalena Gutowska Dr Olaf Heilmayer Dr. Timo Hirse Nils Koschnick Dr. Rainer Knust Dr. Gisela Lannig Dr. Felix Mark Dr. Franz-J. Sartoris Dr. Daniela Storch Rolf-M. Wittig et al.

Dr. Frank Melzner; IFM Geomar Kiel Prof. Vasilis Michaelidis, Thessaloniki Prof. f Lloyd l d Peck, k BAS Dr. Simon Morley, BAS Prof. Inna Sokolova, UNCC Charlotte P f Al Prof. Alex Sukhotin, S kh ti Zool Z l Inst. I t St. St P Petersburg t b

BAS