1. Biological impact of elevated ocean CO2 concentrations: lessons from animal physiology and earth history
Hans O. Pörtner

2. Observations: Atmospheric O2 and CO2 levels in earth history
Present Level
600
400
300
200
100
500 35
0.5
0.4
0.3
0.2
0.1 30 25 20 15 10 5
Concentration (%)
CO2 C O Tr P S D T J K O2
Perm
Trias
Jurassic
Cretaceous
Tertiary
Cambrian
Ordovician
Silurian
Devonian
Carboni-
ferous
MY before present
Late evolution of high species nos.
high performance, high activity lifeforms dependent on low CO2 levels?
important
mass
extinction
periods
Levels are long term means,
did short term oscillations occur?
after Ruben 1995, 1996, Dudley, 1998

3. Parallel oscillations of temperature and oxygen levels
CO2 „experiments“ in earth history: Water CO2 oscillations in Perm / Trias mass extinctions A
warm CO 2
Preconditions in Perm/Trias:
No surface to deep ocean currents
Pangaea as a super-continent d 13 C
Photosynthesis CO 2
Sulfate reduction d 13 C
HCO - H H 2 2 S S
cold 3 CO B 2
Glacier H 2 S -
up to 1 %
( ppm) CO 2
HCO 3
Did such a situation exist before in earth history?
redrawn after Knoll
et al.
, 1996
Parallel oscillations of temperature and oxygen levels
CO2 critical in mass extinctions?

4. 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 (~ ppm).
- excessive respiration occurs in confined areas
hypoxic: rock­pools, sandy sediments, oxygen minimum layers
anoxic: marine sediments, stratified bottom waters (up to ppm)

5. Anthropogenic CO2 in the world‘s ocean over time
5000 GtC
released,
no intentional
storage
surface waters:
up to – 0.77 ΔpH,
1900 ppm CO2
variable bodies of water with
- 0.2 to 0.4 pH units
550 ppm CO2
Depth (km)
5000 GtC
550 ppm stabilized
<90 % in geol. stor.,
10 % leakage
5000 GtC
550 ppm stabilized
<100% stored
no leakage
Biological impact?
modified after Caldeira and Wickett, 2003, 2004

6. A role for ecological and evolutionary physiology
What makes organisms susceptible to CO2? Sensitivities differ between organisms, why? Which levels are critical?
A role for ecological and evolutionary physiology

7. Competition with vertebrates led to maximized performance levels and metabolic rates (10 x fish!).
Acute effects of high CO2 levels: Squid, elite athletes of the ocean: Illex illecebrosus Lolliguncula brevis Loligo pealei

8. Squid haemocyanin function during exercise, pH / saturation analysis: extreme pH sensitivity
Illex illecebrosus
50 %
100 %
0 %
14.7
PO2
(mm Hg)
146 97 59 28
100 80 60 40 20
7.0
7.4
7.8
8.2
% Saturation
24.8
pHe Ca Ev Ea
2000 ppm
6500 ppm
Haemocyanin
molecule
not relevant for leakage
- ∆blood pH > 0.15 (∆Pco2 > ppm) reduced scope for activity (sublethal).
- ∆blood pH > 0.25 (∆Pco2 > ppm) asphyxiation (acutely lethal).
Pörtner et al., 2004

9. CO2 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)
CO2
Hoegh-Guldberg, 2004, Source: J. Kleypas

10. Long term effects in non-calcifying animal species tolerant to CO2 oscillations? Sipunculus nudus
eurybathic:
found between 0 and 2300 m depths

11. S. nudus: Extra- and intracellular acid-base status
CO2 induced metabolic depression: physiological background
S. nudus: Extra- and intracellular acid-base status
partial compensation
Blood
Only partial compensation of extracellular acidosis causing metabolic depression:
A typical finding in invertebrates!
full compensation
Muscle
after Pörtner et al. 1998

12. Reduced exercise capacity
Not just pH! Metabolic and behavioral depression caused by adenosine accumulation in nervous tissue of S. nudus
Reduced exercise capacity
and activity
Reipschläger et al., 1997

13. Metabolic depression and 55 % (
Metabolic depression and 55 % (!) growth reduction in mussels (Mytilus galloprovincialis) under CO2 (permanent extracellular acidosis!!)
© M.S. Calle
control
Water pH 7.3: Maximum pH drop as expected from business as usual scenarios by 2300
(Caldeira and Wickett, 2003)
hypercapnia
Michailidis et al. (2004)

14. Control animals repeatedly reburying into sediment
1 % CO2 early
1% CO2 late
3 % CO2
However, tolerance is time limited: Delayed onset of enhanced mortality during long term „disturbed“ maintenance under 1 % CO2 in S. nudus
Control animals repeatedly reburying into sediment
% Survivors
no decrease in body energy stores
behavioral incapacitation involved
Days of incubation
Langenbuch et al. (2004)

15. Uncompensated acidosis and metabolic depression in several invertebrates
Mytilus
galloprovincialis
Sipunculus nudus
…contributing to lower resistance and enhanced mortality?
Sepia officinalis
©CephBase
Compensated acidosis and, therefore, no metabolic depression in most fish
…a reason for enhanced resistance to high CO2?
Pachycara
brachycephalum
Atlantic
cod
Gadus morhua
Antarctic
eelpout
Heisler, 1986, Larsen et al. 1997, Ishimatsu et al., 2004

16. Further findings Shirayama and colleagues:
- long term reduction of growth, survival, and reproduction in Pacific shallow water sea urchins and snails at 550 ppm CO2,
- reduced fertilization of copepod eggs at CO2 levels beyond 1000 ppm.
Rates of higher functions are reduced under
moderate CO2 elevations. Effects set in early in invertebrates.

17. Mortality independent on CO2 level and exposure time
Principle considerations: Role of time scales and levels for CO2 exposure to become lethal
Incipient lethal
CO2 level
(long term critical threshold)
arbitrary
units
Mortality independent
of exposure time
Zone of resistance
Mortality dependent
on CO2 level and exposure time
Zone of
tolerance
Upper median lethal CO2 level (LD50)
log exposure time (days, weeks, months, years) →
†Acute asphyxiation: squid, fish
…..do we know the key physiological mechanisms affected by CO2?
No such complete
data set exists
Critical level and
mechanism unknown
Tolerable organism and
ecosystem (?) responses
Pörtner et al., 2004

18. …..mechanisms also affected by hypoxia and temperature extremes!!
CO2 effects: complex physiological background shifting whole animal functioning
still incomplete!!
…..mechanisms also affected by hypoxia and temperature extremes!!
complex physiological background behind higher functions
Pörtner et al. 2004

19. a unifying principle in ectotherms (!) and endotherms (!?).
Temperature, hypoxia, CO2 interactions?
A recent hypothesis:
The first level of thermal intolerance at low and high temperature extremes in METAZOA is a loss in whole organism metabolic flexibility (aerobic scope),
a unifying principle in ectotherms (!) and endotherms (!?).
Am. J. Physiol 279, R1531-R1538, 2000.
Naturw. 88, , 2001
Am. J. Physiol. 283, R1254- R1262, 2002
Comp. Biochem. Physiol. 132A, , 2002

20. affecting growth, exercise, behaviours, reproduction, ….fitnessTp Tp
: Pejus T‘s: onset of limitation
in aerobic scope
Hypoxia, CO2 and thermal extremes act synergistically via the same physiological mechanisms!!
Hypoxia, CO2
affecting growth, exercise, behaviours, reproduction, ….fitness
100 Tc
% oxygen
limited
aerobic
scope Tc
: Critical T‘s:
onset of
anaerobic
metabolism
Temperature
Cardiac +
ventila-
tory
output
functional capacity of oxygen supply
Qrest •
Qmax
after Farrell
max
Aerobic scope and performance are maximal at the upper pejus temperature.
rate of
aerobic
perfor-
mance
temperature
after Frederich and Pörtner 2000, Mark et al. 2002
Pörtner et al. 2000, 2004, Pörtner 2001, 2002,

21. …..interaction with CO2 effects?
Temperate crustacean,
Maja squinado
EXAMPLES
Temperate cephalopod,
Sepia officinalis
Antarctic bivalve,
Laternula elliptica
O2 dependent temperature limits verified across phyla: annelids, sipunculids, molluscs (bivalves, cephalopods), crustaceans, fish and some air breathers, limited evidence in endotherms incl. man.
…..interaction with CO2 effects?
Atlantic cod,
Gadus morhua
Antarctic and
temperate zoarcids,
Pachycara brachycephalum,
Zoarces viviparus

22. Combined effects of CO2 accumulation and global warming:
Marginalization of coral reef cover as a special case
Pre-industrial
pCO2 : 280 ppm
carbonate saturation state (Warag) ;
pCO2 : 517 ppm
warmer temperatures
Hoegh-Guldberg (2004)

23. Animal limitations in high CO2 oceans
Progressive (not beyond critical thresholds?) effects already expected in 450 to 750 ppm surface ecosystems
shifted ecosystem equilibra caused by:
reduced calcification rates
higher ratios of non-calcifiers over calcifiers
reduced tolerance to thermal extremes
enhanced geographical distribution shifts
reduced distribution ranges
reduced behavioral capacity, growth, productivity and life span
food chain length and composition
reduced population densities, ……biodiversity (critical!)?
Research needs to further identify mechanisms, titrate/quantify (lab and field) scenarios,
address micro-evolutionary potential

24. CLIMATE CHANGE, CO2 effects, ENERGY BUDGETS
Dr. Christian Bock
Carsten Burkhard
Dr. Martina Langenbuch
Dr. Vasilis Michailidis
Dr. Anke Reipschläger
Susann Schmidt
Rolf-M. Wittig

25. CO2 limitations relevant in evolution?
Number of genera
severest losses
Permian-Triassic mass extinctions Loss of marine invertebrate genera due to CO2?
Articulates = Crinoids belonging to echinoderms
Obs: highest activity forms were not yet existent!!
Physiological characters
of eliminated forms?
moderately active,
moderate calcification
sessile, hypometabolic,
calcified: larger effect?
Pörtner et al., 2004
after Knoll et al., 1996

26. Processes and Limits: Effects of integrated CO2, O2 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 CO2 alone have likely shaped
evolutionary scenarios!
Pörtner et al., 2004

27. Long term effects at moderate CO2 levels: decreased calcification
CO2 + H2O + CaCO3 <=> 2 HCO3 + Ca2+
Warag = [Ca2+][CO32-] / K’sp
K’sp: solubility product for aragonite.
Warag > 1: super-saturation, required for calcification

28. Close correlation between dry / wet weight and shell length
Reduced growth affects shell and soft body alike
not just calcification!!
dry weight
Michailidis et al. (2004)

29. © M.S. Calle
Oxygen consumption
control
hypercapnia
hypercapnia
Mytilus galloprovincialis under hypercapnia (water pH 7.3): 65% (!) metabolic depression associated with enhanced N excretion, i.e. protein degradation during permanent (extracellular) acidosis (as seen in S. nudus)
control
Ammonia excretion
Pörtner et al. (1998)
Michailidis et al. (2004)

30. Reduced cellular protein synthesis during acidosis favouring amino acid catabolism in S. nudus ….likely causing reduced growth rates
Langenbuch et al

31. Animals died despite return to normocapnia!!!
Recent data: Uncompensated intracellular acidosis in cuttlefish (S. officinalis) brain under 24 h of hypercapnia (1%)
Sepia officinalis
intracellular pH
Animals died despite return to normocapnia!!!
S. Schmidt, C. Bock, H.O. Pörtner, unpubl.