Effects of COEffects of CO22 on marine animals on marine animals Time scales, processes, and limits of adaptationTime scales, processes, and limits of adaptation

Hans O. Pörtner, Martina Langenbuch, Basile Michaelidis

Alfred-Wegener-Institute, Bremerhaven, Germany,

Aristotle University of Thessaloniki, Greece.

Interactions with temperature and hypoxia regimes

Scenarios: • Business as usual, • Direct disposal, • Indirect disposal

(Fe fertilization)

Principle considerations: Role of time scales in CO2 exposure experiments

Incipient lethalCO2 level

(long term critical threshold)

arbitraryunits

Mortality independent

of exposure time

Zone of resistanceMortality dependent on CO2 level and

exposure time

Zone of tolerance

Up

per

med

ian

leth

al C

O2 l

evel

(L

D50

)

log exposure time (days, weeks, months, years) →

No such complete data set exists

Tolerable organism and ecosystem (?) responses

critical level and mechanism unknown

†Asphyxiation: squid and fish

Pörtner, in prep.

Example of an Example of an animal species animal species tolerant to COtolerant to CO2 2

oscillations:oscillations:SSipunculusipunculus

nudusnudus

eurybathic: eurybathic: found between 0 and found between 0 and 2300 m depths2300 m depths

However, tolerance However, tolerance is limited: is limited:

Delayed onset of Delayed onset of enhanced mortality enhanced mortality

during long term during long term „disturbed“ „disturbed“

maintenance under 1 maintenance under 1 % CO% CO22 in in S. nudusS. nudus

0 50 100 150 200 250

0

20

40

60

80

100

120 ControlControl

1 % CO1 % CO2 2 earlyearly

1% CO1% CO2 2 latelate

3 % CO3 % CO22

% M

orta

lity

% M

orta

lity

Days of incubation

• no decrease in body energy stores

• behavioral incapacitation involved

Langenbuch et al. (2004)

Control animals repeatedly

reburying into sediment

Permian-Permian-Triassic Triassic

mass mass extinctionsextinctions

Loss of Loss of marine marine

invertebrate invertebrate generagenera

due to COdue to CO22??

moderately active,moderate calcification

sessile, hypometabolic, calcified: larger effect?

after Knoll et al., 1996

Physiological characters of eliminated forms?

severest losses

COCO22 limitations relevant in evolution? limitations relevant in evolution?

Number of genera

Time (h)

7,0

7,2

7,4

7,6

7,8

8,0

1 % CO2 pH

pl

-48 0 48 96 144

7,2

7,4

pHi

ControlS. nudusS. nudus::

Extra- and Extra- and intracellular intracellular

acid-base status acid-base status during during

hypercapniahypercapniain vivoin vivo

after Pörtner et al. 1998

partial compensation

full compensation Partial Partial compensation of compensation of

extracellular extracellular acidosis: acidosis:

A typical finding A typical finding in invertebrates?in invertebrates?

Physiological background??Physiological background??

55 % (!) growth reduction in55 % (!) growth reduction inMytilus galloprovincialis Mytilus galloprovincialis under hypercapniaunder hypercapnia

(permanent extracellular acidosis!!)(permanent extracellular acidosis!!)

0 20 40 60 80 10012

14

16

18

20

22

24

26

28

30

Time (days)

Mea

n sh

ell l

engt

h (m

m) Water pH 7.3:

Maximum pH drop as expected from business as usual scenarios by 2300(Caldeira and Wickett, 2003)

hypercapniahypercapnia

controlcontrol

© M.S. Calle

Michailidis et al. (2004)

Close correlation Close correlation between between

dry / wet weight dry / wet weight and shell lengthand shell length

Shell length (mm)

5 10 15 20 25 30 35

Dry

wei

ght

(gr)

0.00

0.02

0.04

0.06

0.08

0.10

0.12

0.14

0.16

0.18

Log shell lenght (mm)1.0 1.1 1.2 1.3 1.4 1.5

Log

dry

wei

ght (

gr)

-2.6

-2.4

-2.2

-2.0

-1.8

-1.6

-1.4

-1.2

-1.0

-0.8

r2 0,9877

r2 0,9726

Shell length (mm)

5 10 15 20 25 30 35

Wet

wei

ght

of s

oft

body

(gr

)

0.0

0.2

0.4

0.6

0.8

1.0

1.2

1.4

1.6

1.8

2.0

Log shell lenght (mm)

1.0 1.1 1.2 1.3 1.4 1.5 1.6

Log

fres

h w

eigh

t (gr

)

-1.6

-1.4

-1.2

-1.0

-0.8

-0.6

-0.4

-0.2

0.0

0.2

0.4

r2 0,9786

r2 0,9822

Reduced growth Reduced growth affects shell and affects shell and soft body alikesoft body alike

Michailidis et al. (2004)

Reduced cellular Reduced cellular protein synthesis protein synthesis during acidosis during acidosis

favouring amino favouring amino acid catabolismacid catabolism

in in S. nudusS. nudus

….likely causing….likely causing reduced growth reduced growth

ratesrates

Langenbuch et al. 2004.Langenbuch et al. 2004.

Mytilus galloprovincialisMytilus galloprovincialis under hypercapniaunder hypercapnia

(water pH 7.3):(water pH 7.3):

65% (!) metabolic 65% (!) metabolic depression associated with depression associated with enhanced N excretion, i.e. enhanced N excretion, i.e.

protein degradationprotein degradationduring permanent during permanent

(extracellular) acidosis (extracellular) acidosis ((as seen in as seen in S. nudusS. nudus))

Time (days)

0 5 10 15 20 25

Rat

e of

oxy

gen

cons

umpt

ion

(%

of c

ont

rol)

20

40

60

80

100

120

140

*

*

*

Time (days)

0 5 10 15 20 25

Rat

e of

NH

3 e

xcre

tion

(% o

f con

trol

)

20

40

60

80

100

120

140

160

180*

* *

(a)

(b)

hypercapniahypercapnia

controlcontrol

hypercapniahypercapnia

controlcontrol

© M.S. Calle

Michailidis et al. (2004)

Uncompensated intracellular acidosis in Uncompensated intracellular acidosis in cuttlefish (cuttlefish (S. officinalisS. officinalis)) brainbrain under under

24 h of hypercapnia (1%) 24 h of hypercapnia (1%)

7.2

7.25

7.3

7.35

7.4

7.45

7.5

7.55

-3 1 5 9 13 17 21 25 29 33

time (h)

Hypercapnia Normocapnia* *

intr

acel

lula

r p

HSepia officinalisSepia officinalis

S. Schmidt, C. Bock, H.O. Pörtner, unpubl.

Animals died despite return to normocapnia!!!Animals died despite return to normocapnia!!!

Uncompensated acidosisUncompensated acidosisand metabolic depression in several invertebratesand metabolic depression in several invertebrates

…contributing to lower resistance and enhanced mortality?

Compensated acidosis Compensated acidosis and, therefore, no metabolic depression in most fishand, therefore, no metabolic depression in most fish

…a reason for enhanced resistance to high CO2?

Sepia officinalisSepia officinalis Sipunculus nudusSipunculus nudus

PachycaraPachycarabrachycephalumbrachycephalum

Gadus morhuaGadus morhua

©CephBase

see Poster Heisler, 1986, Larsen et al. 1997, Ishimatsu et al., 2004

MytilusMytilus

galloprovincialisgalloprovincialis

Mortality involves Mortality involves metabolic and metabolic and

behavioralbehavioral depression depression

caused by adenosine caused by adenosine accumulation in nervous accumulation in nervous

tissue of tissue of S. nudusS. nudus

Time (h)

Infusion

- Saline- Adenosine, 15 nmol·g-1

(m

ol ·

g-1

· h

-1)

0.2

0.3

0.4

*

0 5 10 15

*

**

0

2

4

6

8

10*

Control Anoxia Hypercapnia Anoxia + Hypercapnia

(nm

ol ·

g n

ervo

us ti

ssue

-1)

Ade

nosi

neO

xyge

n co

nsum

ptio

nA role for adenosine in metabolic depression

0 6 12 18 24 30 360

1

2

3

Normocapnia1 % CO2

Time (h)

Ven

tila

tion

fre

quen

cy (

min

-1)

Reipschläger et al., 1997

Reduced exercise capacity and activity

Unifying principles of COUnifying principles of CO22 effects in animals effects in animals

……..mechanisms also affected by hypoxia and ..mechanisms also affected by hypoxia and temperature extremes!!temperature extremes!!

still incomplete!!

Pörtner et al. 2004

A recent hypothesis:A recent hypothesis:The first level of thermal intolerance at low and high The first level of thermal intolerance at low and high

temperature extremes in METAZOA is a loss in whole organism temperature extremes in METAZOA is a loss in whole organism aerobic scope,aerobic scope,

a unifying principle in ectotherms (!) and endotherms (!?).a unifying principle in ectotherms (!) and endotherms (!?).

Am. J. Physiol 279, R1531-R1538, 2000.Am. J. Physiol 279, R1531-R1538, 2000.Naturw. 88, 137-146, 2001Naturw. 88, 137-146, 2001Am. J. Physiol. 283, R1254- R1262, 2002Am. J. Physiol. 283, R1254- R1262, 2002Comp. Biochem. Physiol. 132A, 739-761, 2002Comp. Biochem. Physiol. 132A, 739-761, 2002

Temperature, hypoxia, CO2 interactions?

Temperate crustacean,Temperate crustacean,Maja squinadoMaja squinado

Temperate Temperate cephalopod,cephalopod,Sepia officinalisSepia officinalis

Antarctic bivalve,Antarctic bivalve,Laternula ellipticaLaternula elliptica

Atlantic cod,Atlantic cod,Gadus morhuaGadus morhua

Antarctic andAntarctic andtemperate zoarcids,temperate zoarcids,Pachycara Pachycara brachycephalum,brachycephalum,Zoarces viviparusZoarces viviparus

EXAMPLESEXAMPLES

OO22 dependent temperature limits verified across phyla: dependent temperature limits verified across phyla:

annelids, sipunculids, molluscs (bivalves, cephalopods), annelids, sipunculids, molluscs (bivalves, cephalopods), crustaceans, fish and some air breathers, limited evidence in crustaceans, fish and some air breathers, limited evidence in

endotherms incl. man.endotherms incl. man.

0

% oxygen limitedaerobicscope

Tc

Tp Tp : Peius T‘s: onset of limitation in aerobic scope

Tc : Critical T‘s:

affecting growth, affecting growth, exercise, behaviours, exercise, behaviours,

reproduction,reproduction,….fitness….fitness

Temperature

onset ofanaerobic metabolism

after Frederich and Pörtner 2000, Mark et al. 2002Pörtner et al. 2000, Pörtner 2001, 2002

100

Cardiac +ventila-toryoutput

0

functional capacity of oxygen supply

Qrest•

Qmax•

after Farrell

max Aerobic scope and performance Aerobic scope and performance are maximal at the upper peius are maximal at the upper peius temperature.temperature.

rate of aerobicperfor-mance

0temperature

Hypoxia, COHypoxia, CO22 and thermal and thermal

extremes act synergistically extremes act synergistically via the same physiological via the same physiological mechanisms!!mechanisms!!

Hypoxia, COHypoxia, CO22

Hypoxia, COHypoxia, CO22

Processes and Limits:Processes and Limits: Effects of integrated CO Effects of integrated CO22, O, O22 and temperature fluctuations and temperature fluctuations

CO2 impacts on:

Hypoxia tolerance ↑→ Improved extension of passive survival (limited!)

BUT

Aerobic scope ↓→ Long term performance and growth functions ↓ → Thermal tolerance ↓

(tolerance to thermal fluctuations ↓)

These interactions and not COThese interactions and not CO2 2 alone have likely shaped alone have likely shaped

evolutionary scenarios!evolutionary scenarios!Pörtner and Langenbuch, in prep.

Animal limitations in high COAnimal limitations in high CO22 oceans oceansProgressive (not beyond critical thresholds?) effects already Progressive (not beyond critical thresholds?) effects already

expected in 450 to 750 ppm surface ecosystemsexpected in 450 to 750 ppm surface ecosystemsshifted ecosystem equilibrashifted ecosystem equilibra caused by: caused by:- reduced calcification ratesreduced calcification rates

- higher ratios of non-calcifiers over calcifiershigher ratios of non-calcifiers over calcifiers- reduced tolerance to thermal extremes reduced tolerance to thermal extremes

- enhanced geographical distribution shiftsenhanced geographical distribution shifts- reduced distribution rangesreduced distribution ranges

- reduced behavioral capacity, growth, productivity and life reduced behavioral capacity, growth, productivity and life spanspan**- food chain length and compositionfood chain length and composition**- reduced population densities, ……biodiversity (critical!)?reduced population densities, ……biodiversity (critical!)?**

*effects transferred to deep with ocean disposal (direct and indirect)Research needs to further identify mechanisms, titrate/quantify (lab and field) scenarios, address micro-evolutionary potential

Pörtner and Langenbuch, in prep.

Ocean COOcean CO22 disposal: disposal:

Are their methods of choice?Are their methods of choice? Preliminary insight from COPreliminary insight from CO22, T, hypoxia impact studies in animals, T, hypoxia impact studies in animals

• Avoid business as usual scenarios • (thermal changes, direct impact of CO2!)

• Avoid large scale disposal strategies • (towed pipe or Fe fertilization)

• If feasible, use CO2 lake option in environments protected from physical disturbance („dump site“ strategy)

• Apply direct pH neutralization of injected CO2?

• Dispose in thermally stable environments• Avoid hypoxia aggravation (eutrophication)

Pörtner and Langenbuch, in prep.

CLIMATE CHANGE, CO2 effects, ENERGY BUDGETS

Dr. Christian Bock Carsten BurkhardDr. Martina LangenbuchDr. Anke ReipschlägerSusannSchmidt Rolf-M. Wittig

Dr. Vasilis Michailidis