Biological impact of elevated ocean COBiological impact of elevated ocean CO22

concentrations: concentrations: lessons from animal physiology and earth historylessons from animal physiology and earth history

Hans O. Pörtner

after Ruben 1995, 1996, Dudley, 1998

importantmass extinctionperiods

Observations: Atmospheric OObservations: Atmospheric O22 and CO and CO22 levels in earth history levels in earth history

Levels are long term means, Levels are long term means, did short term oscillations occur?did short term oscillations occur?

Late evolution of Late evolution of high species nos.high species nos.high performance, high performance, high activity high activity lifeforms dependent lifeforms dependent on low COon low CO22 levels? levels?

Present Level

600 400 300 200 100500

35

0.50.4

0.3

0.2

0.1

30252015105

Con

cent

ratio

n (%

)

CO2

C O C TrPS D TJ K

O2

Per

mT

rias

Jura

ssic

Cre

tace

ous

Ter

tiary

Cam

bria

n

Ord

ovic

ian

Silu

rian

Dev

onia

nC

arbo

ni-

fero

us

Present Level

MY before present0

C

CO2

CO2

Photosynthesis

C Sulfate reductionCO2

HCO3- H2SH2S

CO2 HCO3-H2S

A

B

redrawn after Knoll et al., 1996

Glacier

COCO22 „experiments“ in earth history: „experiments“ in earth history:

Water COWater CO22 oscillations in Perm / Trias mass extinctions oscillations in Perm / Trias mass extinctions

Preconditions in Perm/Trias:

No surface to deep ocean currents

Pangaea as a super-continent

Parallel oscillations of Parallel oscillations of temperature and oxygen levelstemperature and oxygen levels

COCO2 2 critical in mass extinctions?critical in mass extinctions?

warmwarm

coldcold

up to 1 %(10 000 ppm)

CO2 as a natural factor nowadays, in areas with marine life:

- constantly low in most of the pelagic zones of the sea (<500 ppm).

- fluctuates when - volcanic emissions occur in the sea (~ 80 000 ppm).

- excessive respiration occurs in confined areas hypoxic: rock pools, sandy sediments, oxygen

minimum layersanoxic: marine sediments, stratified bottom

waters (up to 16 000 ppm)

Dep

th

Dep

th

(km

)(k

m)

5000 GtC5000 GtCreleased, released, no intentionalno intentionalstoragestorage

5000 GtC5000 GtC550 ppm stabilized 550 ppm stabilized <90 % in geol. stor.,<90 % in geol. stor.,10 % leakage10 % leakage

5000 GtC5000 GtC550 ppm stabilized550 ppm stabilized<100% stored<100% storedno leakageno leakage

modified after Caldeira and Wickett, 2003, 2004

Anthropogenic COAnthropogenic CO22 in the in the

world‘s ocean over timeworld‘s ocean over time

surface waters: surface waters: up to – 0.77 up to – 0.77 ΔΔpH, pH, 1900 ppm CO1900 ppm CO22

variable variable bodies of bodies of water with water with - 0.2 to 0.4 - 0.2 to 0.4 pH unitspH units550 ppm CO550 ppm CO22

Biological impact?Biological impact?

What makes organisms susceptible to COWhat makes organisms susceptible to CO22??

Sensitivities differ between organisms, why?Sensitivities differ between organisms, why?Which levels are critical?Which levels are critical?

A role for ecological and evolutionary physiology

Acute effects of high Acute effects of high COCO22 levels: levels:

Squid, elite athletes Squid, elite athletes of the ocean:of the ocean:

Illex illecebrosusIllex illecebrosus

Lolliguncula brevisLolliguncula brevis

Loligo pealeiLoligo pealei

Competition with vertebrates led to maximized performance levels and metabolic rates (10 x fish!).

Squid haemocyanin function during exercise,Squid haemocyanin function during exercise,pH / saturation analysis: pH / saturation analysis: extreme pH sensitivityextreme pH sensitivity

Illex illecebrosus

50 %

100 %

0 %

14.7PO2

(mm Hg)146 97 59 28

100

80

60

40

20

0

7.0 7.4 7.8 8.2

% S

atur

atio

n

24.8

pHe

Ca

Ev

Ea

- ∆blood pH > 0.15 (∆Pco2 > 2 000 ppm) reduced scope for activity (sublethal).

- ∆blood pH > 0.25 (∆Pco2 > 6 500 ppm) asphyxiation (acutely lethal).

Pörtner et al., 2004

HaemocyaninHaemocyaninmoleculemolecule

2000 ppm2000 ppm

6500 ppm6500 ppm

Hoegh-Guldberg, 2004, Source: J. Kleypas

Long term effects at moderate CO2 levels:

15 to 85 % reduction in calcification rates…

…due to reduced carbonate levels with a doubling of CO2 (Sabine et al., 2004)

COCO22

Long term effects Long term effects in non-calcifying in non-calcifying

animal species animal species tolerant to COtolerant to CO2 2

oscillations?oscillations?SSipunculusipunculus nudus nudus

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

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 statusacid-base status

after Pörtner et al. 1998

partial compensation

full compensation

Only partial Only partial compensation of compensation of

extracellular extracellular acidosis causing acidosis causing

metabolic metabolic depression: depression:

A typical finding A typical finding in invertebrates!in invertebrates!

COCO22 induced metabolic depression: physiological background induced metabolic depression: physiological backgroundB

loo

dM

usc

le

Not just pH!Not just pH!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

Metabolic depression and 55 % (!) growth Metabolic depression and 55 % (!) growth reduction in mussels reduction in mussels

((Mytilus galloprovincialis) Mytilus galloprovincialis) under COunder CO22

(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)

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

% S

urv

ivor

s%

Su

rviv

ors

Days of incubation

• no decrease in body energy stores

• behavioral incapacitation involved

Langenbuch et al. (2004)

Control animals repeatedly

reburying into sediment

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

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

MytilusMytilus

galloprovincialisgalloprovincialis

Atlantic Atlantic codcod

Antarctic Antarctic eelpouteelpout

Further findingsFurther findings

Shirayama and colleagues:Shirayama and colleagues:

- long term reduction of growth, survival, and - long term reduction of growth, survival, and reproduction in Pacific shallow water sea reproduction in Pacific shallow water sea urchins and snails at urchins and snails at 550 ppm550 ppm CO CO22, ,

- reduced fertilization of copepod eggs at CO- reduced fertilization of copepod eggs at CO22

levels beyond levels beyond 1000 ppm1000 ppm. .

Rates of higher functions are reduced underRates of higher functions are reduced undermoderate COmoderate CO22 elevations. Effects set in early in elevations. Effects set in early in

invertebrates.invertebrates.

Principle considerations: Principle considerations: Role of time scales and levels for CORole of time scales and levels for CO22 exposure to become lethal exposure to become lethal

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

†Acute asphyxiation: squid, fish

Pörtner et al., 2004

……..do we know the key physiological ..do we know the key physiological mechanisms affected by COmechanisms affected by CO22??

COCO22 effects: complex physiological background shifting whole animal functioning effects: complex physiological background shifting whole animal functioning

……..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 metabolic flexibility (aerobic scope),metabolic flexibility (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?

0

% oxygen limitedaerobicscope

Tc

Tp Tp : Pejus 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, 2004, 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 pejus are maximal at the upper pejus 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

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.

……..interaction with CO..interaction with CO22 effects? effects?

Pre-industrialpCO2 : 280 ppm

2060-69; pCO2 : 517 ppmwarmer temperatures

Combined effects of CO2 accumulation and global warming: Marginalization of coral reef cover as a special case

Hoegh-Guldberg (2004)

carbonate saturation state (arag)

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!)?

Research needs to further identify mechanisms, titrate/quantify (lab and field) scenarios, address micro-evolutionary potential

CLIMATE CHANGE, CO2 effects, ENERGY BUDGETS

Dr. Christian Bock Carsten BurkhardDr. Martina LangenbuchDr. Vasilis MichailidisDr. Anke ReipschlägerSusann Schmidt Rolf-M. Wittig

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

Obs: highest Obs: highest activity forms activity forms were not yet were not yet existent!!existent!!

Pörtner et al., 2004

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

Metabolic flexibility (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 et al., 2004

Long term effects at moderate CO2 levels:decreased calcification

CO2 + H2O + CaCO3 <=> 2 HCO3 + Ca2+

arag = [Ca2+][CO32-] / K’sp

K’sp: solubility product for aragonite.

arag > 1: super-saturation, required for calcification

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

not just calcification!!not just calcification!!

Michailidis et al. (2004)

wet weightwet weight

dry weightdry weight

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

Pörtner et al. (1998)Michailidis et al. (2004)

Oxygen consumption

Ammonia excretion

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.

Recent data: Recent data: Uncompensated intracellular Uncompensated intracellular acidosisacidosis in cuttlefish ( in 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!!!