Biological impacts of deep-sea carbon dioxide injection inferred from indices of physiological performance
1 Monterey Bay Aquarium Research Institute, 7700 Sandholdt Road, Moss
Landing, CA 95039, USA
2 Marine Biology and Fisheries, National Institute of Environmental Health
Sciences, Marine and Freshwater Biomedical Science Center, Rosenstiel School
of Marine and Atmospheric Sciences, 4600 Rickenbacker Causeway, University of
Miami, Miami, FL 33149, USA
* Author for correspondence (e-mail: bseibel{at}mbari.org)
Accepted 12 November 2002
![]() |
Summary |
---|
Key words: carbon dioxide, global warming, deep sea, hypercapnia, acidbase balance, sequestration, cephalopoda, metabolism
![]() |
Introduction |
---|
Addition of CO2 to seawater will result in a decrease in pH due
to the bicarbonate buffer system in the ocean (equation 1):
![]() | (1) |
A variety of disposal schemes are being discussed
(Adams et al., 1997). Shallow
gas injection to form a dense sinking fluid, injection of ultra-cold liquid
CO2 to form a dense ice skin-hydrate phase, formation of a lake of
CO2 on the seafloor, and dissolution of a rising plume of liquid
CO2 are among the possible scenarios. The environmental
`friendliness' of CO2 sequestration is thought to depend primarily
on the method of CO2 injection, general circulation models at the
depth and location of CO2 injection, and the general tolerance of
deep-living organisms to reductions in pH and increased CO2
(hypercapnia). This latter point is the focus of this paper.
![]() |
Environmental stability and the evolution of physiological strategies |
---|
However, the projected perturbations in pH and CO2 partial
pressure (PCO2) due to CO2 disposal
are large relative to the pH variation experienced by most organisms in the
deep-sea. While CO2 and pH vary diurnally, or even hourly, within
some shallow-water habitats (Truchot and
Duhamel-Jouve, 1980; Burnett,
1997
), PCO2 (pH) in most of the
deep-sea, like oxygen, is dependent on regional productivity and the age of
bottom water (Miyake and Saruhashi,
1956
; Park, 1968
)
and is, thus, stable over thousands of years
(Kennett and Ingram, 1995
).
Deep-sea animals have evolved in the absence of substantial environmental
variability and, as a result, lack the capacity adaptations that facilitate
regulation of their internal milieu in the face of changing environmental
characteristics (Childress and Seibel,
1998
; Seibel et al.,
1999
). Angel (1992
)
stated that, as a result of environmental stability, deep-sea communities
"can be expected to contain the most highly tuned species with
possibly the least tolerance of environmental change of all on
earth". Haedrich
(1996
) affirmed this sentiment
stating "any disturbance that takes place too quickly to allow for a
compensating adaptive change within the genetic potential of finely adapted
deep-water organisms is likely to be harmful. Deep-water faunas are sure to be
sensitive to any change that occurs over a few generations and is
significantly outside the probably rather narrow range of environmental
conditions under which the fauna evolved". Therefore, even small
perturbations in CO2 or pH could have important consequences for
deep-sea organismal physiology and, by extrapolation, the ecology of the
entire deep sea.
![]() |
Physiological responses of animals to acidbase disturbance |
---|
|
In the shallow-living species for which acidbase balance has been
studied, elevated environmental PCO2 leads
directly to elevated internal PCO2 until a new
steady-state gradient sufficient to restore CO2 excretion is
established. When this occurs, the extracellular pH (pHe=blood pH) is
depressed, and the bicarbonate concentration rises according to the
bicarbonate buffer characteristics of the animal's extracellular fluid (see
equation 1; Cameron, 1986).
Extracellular pH and bicarbonate values directly impact intracellular pH (pHi;
Pörtner et al., 1998
). A
secondary rise in bicarbonate ions due to active transport, ion exchange
(Cameron, 1986
;
Cameron and Iwama, 1987
;
Pörtner et al., 1998
) or
dissolution of CaCO3 exoskeletons
(Lindinger et al., 1984
)
results in an increase in pHe towards control values over a time course of
hours to days (Fig. 2).
Intracellular compensation is typically completed within 48-72 h in the
animals tested to date, and some return towards control values is usually
observed within 24 h (Pörtner et al.,
1998
), often at the expense of pHe. An inability to control
acidbase imbalances in the intra- and extracellular spaces may, as
discussed in more detail below, lead directly to metabolic suppression,
reduced scope for activity or loss of consciousness due to disruption of
oxygen transport mechanisms and, ultimately, death.
|
Seibel and Walsh (2001)
briefly reviewed the literature available for deep-sea organisms with
relevance to acidbase physiology. We concluded that, as a result of the
relative environmental stability and low rates of metabolism in the deep-sea,
organisms living there have little need, and thus little capacity, for robust
acidbase regulation. Here, we reiterate these arguments and detail the
extreme sensitivity of deep-sea organisms to even small changes in seawater
chemistry. While great variation in CO2 tolerance presumably exists
within diverse animal assemblages at any given depth, enough data exist to
illustrate differences in the magnitude of acidbase imbalance between
generalized deep- and shallow-living species predicted to result from deep-sea
injection of CO2. However, precise thresholds for individual
species cannot yet be predicted. Furthermore, it should be pointed out that
regulation of acidbase balance typically occurs at the expense of ionic
homeostasis and cell volume regulation
(Cameron and Iwama, 1987
;
Whiteley et al., 2001
) such
that mechanisms for compensation of short-term hypercapnia may not be possible
during longer exposures.
![]() |
Metabolism |
---|
|
![]() |
Buffering capacity |
---|
The ability to buffer metabolic end products correlates with metabolic
capacity. Thus, non-bicarbonate buffering capacities are as much as 100 times
higher in muscles of shallow-living species than in comparable deep-living
species (Fig. 3;
Castellini and Somero, 1981;
Morris and Baldwin, 1984
;
Pörtner, 1990
;
Seibel et al., 1997
). The
muscles of deep-sea organisms have low amounts of both dialyzable buffers and
proteins (Somero, 1985
). The
consequences of reduced intracellular buffering capacity are illustrated
clearly in Fig. 4. A doubling
of PCO2 causes only a 0.02 pH change in the
intracellular space of the shallow-living squid Stenoteuthis
oualaniensis. However, a similar increase in
PCO2 leads to a 0.2 pH change in the
deep-living pelagic octopod Japetella heathi. The ability to buffer
extracellular fluids against pH change is similarly dependent on the
concentration of proteins in the blood
(Wells et al., 1988
). The
majority of deep-living animals measured have extremely low extracellular
protein contents compared with closely related shallow-living relatives
(Douglas et al., 1976
;
Brix, 1983
;
Childress and Seibel, 1998
;
Seibel et al., 1999
).
Respiratory protein concentrations generally decrease with metabolic rate and,
therefore, depth.
|
![]() |
Ion-exchange capacity |
---|
Gas-exchange (e.g. gill) tissue has been identified as the primary site
responsible for acidbase regulation in both fishes and invertebrates
(McDonald, 1983;
McDonald et al., 1991
;
Whiteley et al., 2001
),
although significant gas and ion exchange may take place across all epithelial
surfaces in some organisms (e.g. cephalopods;
Pörtner, 1994
). Reduced
gill surface area among deep-sea species may, therefore, limit ion-exchange
capacity. Aside from those adapted for residence in oxygen minimum layers
(Childress and Seibel, 1998
),
the few deep-sea species studied have much lower gill surface areas than their
more-active, shallower-living counterparts
(Henry et al., 1990
;
Marshall, 1971
;
Voss, 1988
).
Gibbs and Somero (1990)
reported greatly reduced capacities for active ion regulation via
ATPases in gills of deep-sea fishes relative to shallower species. Although
their study focused on Na+/K+-ATPases, their data show
that activities of total ATPases declined with increasing depth as well.
Similarly, deep-sea animals, other than those inhabiting hydrothermal vents,
appear from limited data to have activities of carbonic anhydrase (CA) in
gas-exchange tissue that are lower than those of shallower-living species
(Henry, 1984
;
Kochevar and Childress, 1996
).
CA catalyzes the reversible hydration/dehydration reaction of CO2
and water (equation 1) and, thus, plays an important role in CO2
excretion and acidbase balance in marine animals by maintaining
availability of H+ and HCO3- for transporters
(Burnett, 1997
;
Henry, 1984
). Deep-sea species
presumably have a much lower requirement for branchial ion transport due to
the extreme ionic stability of seawater at depth and their low rates of
metabolic and locomotory activity (Henry
et al., 1990
).
![]() |
Oxygen transport, pH sensitivity and metabolism |
---|
![]() | (2) |
These interactions are well understood in a variety of organisms (see
Bridges and Morris, 1989;
Toulmond, 1992
for a review).
However, the specific effects of CO2 and pH on respiratory
protein-mediated gas exchange vary widely between taxa. For example, limited
data suggest that CO2 increases the affinity of hemocyanin
(molluscs and crustaceans) but decreases the affinity of Hb (vertebrates and
annelids) for oxygen (Bridges and Morris,
1989
; Toulmond,
1992
). Only a few measurements of the specific effect of
CO2 on oxygen binding have been made in deep-sea species other than
those inhabiting hydrothermal vents. No specific effect of CO2 was
found for vertically migrating mesopelagic shrimps
(Sanders and Childress, 1990b
)
or for the deep-sea benthic shrimp Glyphocrangon vicaria
(Arp and Childress, 1985
). The
specific CO2 effect observed for the midwater shrimp Notostomus
gibbosus was slight and masked by physiological concentrations of
ammonium used for buoyancy in this species
(Sanders et al., 1992
).
Regardless, increased CO2 will result in decreased pH and a
subsequent reduction of oxygen-binding affinity in most species. In addition
to a large Bohr effect, many fish Hbs possess a Root effect, where a
respiratory acidosis, as incurred during exposure to hypercapnia, can result
in a dramatic reduction in hemoglobin-oxygen carrying capacity (up to 50%).
The Root effect is thought, in some cases, to facilitate excretion of oxygen
into a gas-filled swim-bladder following acid loading in the blood at the Rete
Mirable. Most fishes that possess a Root effect also possess the ability to
regulate red blood cell pH (pHi) during an acidosis through the release of
catecholamines (adrenaline and noradrenaline) that indirectly activate
Na+/H+ exchange
(Tufts and Randall, 1989
).
Several deep-sea fishes investigated appear to possess a Root effect
(Noble et al., 1986
;
Pelster, 1997
). However, there
are no data on whether deep-sea fishes have the ability to regulate pHi in the
face of an acidosis that might be incurred during exposure to hypercapnia.
Pörtner and Reipschläger
(1996) predicted that
extremely active animals, in particular, squids, would be disproportionately
impacted by anthropogenic decreases in seawater pH. Epipelagic squids such as
Illex illecebrosus have extremely high rates of oxygen consumption
and low blood-oxygen carrying capacity relative to fishes with intracellular
respiratory proteins. Therefore, squids have little venous oxygen reserve and
are highly dependent on a large Bohr shift to ensure complete release of
oxygen at the tissues. Not surprisingly, pHe is tightly controlled in squids
(Pörtner, 1994
). A blood
pH change of as little as 0.15 units is predicted to reduce the scope for
activity in species such as I. illecebrosus, while a change of 0.25
units is lethal (Pörtner and
Reipschläger, 1996
).
Conversely, they argued that the specific effect of pH on oxygen binding is
small in animals with low metabolic rates, such as those in the deep-sea, and
that such species will be less affected by CO2 disposal
(Pörtner and Reipschläger,
1996). Although some deep-living species have respiratory proteins
with low pH sensitivities (e.g. the vampire squid Vampyroteuthis
infernalis; Seibel et al.,
1999
), no relationship exists between metabolic rate and the Bohr
coefficient or between the Bohr coefficient and depth for a variety of deep
and shallow-living marine species (Fig.
3). The shrimp Glyphocrangon vicaria, for example, living
on the sea floor at depths near 3000 m (oxygen=30% air saturation) has a Bohr
coefficient similar to those of its shallow-living relatives despite having a
low metabolic rate (Arp and Childress,
1985
). Similarly, all octopodids (Cephalopoda) measured, like
squids, have hemocyanins that are extremely sensitive to pH
(
logP50/
pH>-1.0) regardless of depth,
oxygen or metabolic rate (Bridges,
1994
). For example, in the deep-sea octopod Benthoctopus
sp., a drop in arterial pH by just 0.3 units would reduce oxygen saturation of
the blood by 40% at ambient oxygen levels
(Fig. 5B; A. Seibel unpublished
data).
|
Mickel and Childress (1978)
examined the effects of reduced pH on oxygen consumption of Gnathophausia
ingens, a crustacean living in extreme hypoxia at mid-depths off
California where seawater pH values are as low as 7.6. They found no specific
effect of pH on the rates of oxygen consumption or the abilities of this
species to regulate its oxygen consumption rate. However, they did note a
large increase in the percentage of oxygen extracted from the respiratory
stream at pH 7.1 as opposed to pH 7.9. They reasoned that, as the increase in
oxygen extraction does not improve the ability of G. ingens to
regulate its oxygen uptake, there must be a loss in effectiveness of oxygen
uptake at some other point along the oxygen-transport pathway at low pH. If,
as is suggested by the large negative Bohr coefficient for this species
(Sanders and Childress,
1990a
), hemocyanin-oxygen affinity is reduced by low extracellular
pH, then perhaps G. ingens is slowing either the respiratory or
circulatory stream at low pH in order to increase the amount of oxygen
extracted. Such a strategy would greatly reduce the scope for activity at low
pH for this species.
Animals without well-developed circulatory systems, such as cnidarians and
echinoderms, may also be sensitive to hypercapnia and reduced pH. As far as is
known, they depend solely on a favorable tissue-environment gradient for
CO2 excretion. Elevated environmental
PCO2 therefore, will lead directly to
intracellular pH reductions. During brief bouts of environmental hypercapnia,
echinoderms may use their large volume of coelomic fluid to buffer
environmental changes (Spicer,
1995; Burnett et al.,
2002
); however, this mechanism will be ineffective during longer
exposures (see below). Echinoderms and bivalves may also rely on dissolution
of calcareous tests and shells to buffer pH changes (see below;
Burnett et al., 2002
;
Lindinger et al., 1984
;
Spicer, 1995
).
![]() |
Metabolic suppression |
---|
Not all animals are able to suppress metabolism. Organisms unable to reduce
oxygen demand sufficiently are subject to depletion of high-energy phosphate
levels during energy limitation, resulting in death. Although not specifically
investigated, metabolic suppression is suspected for midwater (mesopelagic)
species migrating diurnally into low oxygen regions as well as for deep-sea
benthic fauna living in burrows, crevices or shells that may become hypoxic
periodically (Hunt and Seibel,
2000; Seibel and Childress,
2000
). Furthermore, metabolism of some deep-living macrofauna is
depressed nearly fivefold between periods of feeding
(Smith and Baldwin, 1982
), and
many copepod species are known to overwinter in a dormant state in deep water
(Alldredge et al., 1984
;
Hand, 1991
).
The mechanisms that bring about reductions in metabolism are under active
investigation. Metabolic suppression is typically associated with a decrease
in pHi that may lead to rapid adjustments in pH-sensitive metabolic processes
such as glycolysis in muscle tissue via alterations in the activities
of glycolytic enzymes (reviewed by Somero,
1985). For example, phosphorylation of glycolytic enzymes is
involved in the transition into dormancy in some marine molluscs
(Brooks and Storey, 1997
). In
some cases, high CO2 levels trigger metabolic suppression
independently of pH (Hand,
1998
; Pörtner et al.,
1998
), but reduced pH is also sometimes sufficient to trigger
metabolic suppression (Hand,
1998
; Kwast and Hand,
1996
).
Suppression of metabolism is accomplished, at least in part, by shutting
down expensive cellular processes such as protein synthesis
(Guppy and Withers, 1999). For
example, Reid et al. (1997
)
found that low pH inhibited protein synthesis in trout living in lakes
rendered acidic through anthropogenic input. Mitochondrial protein synthesis
in brine shrimp is also acutely sensitive to pH changes
(Kwast and Hand, 1996
).
Metabolic suppression under conditions of environmental hypercapnia is
accompanied by changes in nitrogen excretion in the marine worm Sipunculus
nudus, which is attributable, in part, to a reduction in protein
synthesis rates (Langenbuch and
Pörtner, 2002
). Reduced protein synthesis, by definition,
restricts both growth and reproduction.
Takeuchi et al. (1997)
investigated growth rate in one deep-and several shallow-living nematode
species in relation to pH. Growth rate in the deep-sea species was reduced by
nearly 50% at pH 6.9, while the shallow-living species showed similar growth
rates to the control at pH 6.2. This may reflect the suppression of metabolic
rate due to an inability to compensate for an intracellular acidosis in the
deeper-living species.
![]() |
Mortality |
---|
In situ investigations suggest that deep-sea echinoid (sea urchin)
shells are extremely susceptible to fatal dissolution when caged near small
pools of liquid CO2 on the seafloor at 3600 m depth
(Barry et al., 2002). Equation
3 demonstrates clearly how addition of CO2 may enhance
CaCO3 dissolution:
![]() | (3) |
![]() |
Mobility of deep-sea fauna |
---|
Tamburri et al. (2000)
recently conducted the first in situ experiments attempting to
directly assess the impacts of liquid CO2 on deep-sea organisms. By
mixing a fish slurry with liquid CO2, they were able to attract
fish (primarily hagfish, Myxinidae) to the liquid CO2 itself.
Hagfish appeared not to detect the CO2 and swam directly to the
beaker that contained the CO2/fish slurry. Upon contact with the
CO2, the fish immediately lost consciousness and fell to the
bottom. Rattails (Macrouridae), by far the dominant fishes near the
deep-sea floor, rely on olfaction to find food. Studies with baited cameras on
the deep-sea floor have shown that fish abundance increases dramatically, up
to 1 per m2, with the intensity of the current carrying the bait
smell (Gage and Tyler, 1991
).
Rattails are known to root about in the ooze, sucking in the top layer of
sediment and straining off small infaunal invertebrates
(Gage and Tyler, 1991
).
Preliminary in situ observations suggest that rattails are also not
able to detect liquid CO2 or accompanying pH decreases. Individual
rattails did, however, demonstrate dramatic reactions upon making direct
contact with liquid CO2 (B. A. Seibel, personal observation). These
results are worrying because they suggest that the smell of decaying animals
that is certain to accompany the initial impact from any sequestered
CO2 may attract additional scavengers.
![]() |
Perspective |
---|
Given the substantial research investment in deep-sea biology over the past few decades, and the relatively limited understanding of deep-sea processes that endures, a very aggressive research campaign must be initiated in order to provide the necessary information within a relevant time frame, unless a `no effect' strategy is adopted.
Priorities should include:
Many deep-living species, if captured carefully, can be kept alive
indefinitely at atmospheric pressure (e.g.
Seibel and Childress, 2000).
Methods are also available for successful maintenance of deep-sea animals
under their respective habitat pressures in the laboratory (e.g.
Girguis et al., 2002
) and for
laboratory culture (Omori et al.,
1998
; Young and George,
2000
). Such methods allow long-term hypercapnia studies that are
essential prior to instigating deep-sea CO2 injection.
What can be stated with confidence, based on our present knowledge, is that
shallow-living organisms are already generally intolerant of hypercapnia
(Knutzen, 1981) and that
deep-sea organisms will be even more so. Slow recolonization of deep-sea
habitats and a tendency towards slow growth and longevity among deep-sea
organisms (Gage and Tyler,
1991
) suggests that recovery from any anthropogenic insult will be
slow at best. Should deep-sea CO2 injection be deemed necessary,
great care and caution must be employed and further research initiated to
ensure that it is done in the most environmentally benign manner possible.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
Adams, E. E., Caulfield, J. A., Herzog, H. J. and Auerbach, D. I. (1997). Impacts of reduced pH from ocean CO2 disposal: sensitivity of zooplankton mortality to model parameters. Waste Man. 17,375 -380.
Alldredge, A. L., Robison, B. H., Fleminger, A., Torres, J. J., King, J. M. and Hamner, W. M. (1984). Direct sampling and in situ observation of a persistent copepod aggregation in the mesopelagic zone of the Santa Barbara Basin. Mar. Biol. 80,75 -81.
Angel, M. V. (1992). Managing biodiversity in the oceans. In Diversity of Oceanic Life: An Evaluative Review (ed. M. N. A. Peterson), pp.23 -62. Washington, DC: The Center for Strategic and International Studies.
Arp, A. J. and Childress, J. J. (1985). Oxygen binding properties of the blood of the deep-sea shrimp, Glyphocrangon vicaria. Physiol. Zool. 58,38 -45.
Barry, J., Seibel, B. A., Drazen, J., Tamburri, M., Lovera, C. and Brewer, P. (2002). Field experiments on direct ocean CO2 sequestration: the response of deep-sea faunal assemblages to CO2 injection at 3200 m off Central California. Eos Trans. AGU 83,OS51F-02 .
Brewer, P. G., Friederich, G., Peltzer, E. T. and Orr, F. M.
J. (1999). Direct experiments on the ocean disposal of fossil
fuel CO2. Science
284,943
-945.
Bridges, C. R. (1994). Bohr and Root effects in cephalopod haemocyanins paradox or pressure in Sepia officinalis? In Physiology of Cephalopod Molluscs: Lifestyle and Performance Adaptations (ed. H. O. Pörtner, R. K. O'Dor and D. L. MacMillan), pp. 121-130. Basel, Switzerland: Gordon and Breach.
Bridges, C. R. and Morris, S. (1989). Respiratory pigments: interactions between oxygen and carbon dioxide transport. Can. J. Zool. 67,2971 -2985.
Brix, O. (1983). Giant squids may die when exposed to warm currents. Nature 303,422 -423.
Brooks, S. P. and Storey, K. B. (1997). Glycolytic controls in estivation and anoxia: A comparison of metabolic arrest in land and marine molluscs. Comp. Biochem. Physiol. A 118,1103 -1114.[CrossRef][Medline]
Burnett, L., Terwilliger, N., Carroll, A., Jorgensen, D. and
Scholnick, D. (2002). Respiratory and acidbase
physiology of the purple sea urchin, Stronglyocentratus purpuratus,
during air exposure: presence and function of a facultative lung.
Biol. Bull. 203,42
-50.
Burnett, L. E. (1997). The challenges of living in hypoxic and hypercapnic aquatic environments. Am. Zool. 37,633 -640.
Cameron, J. N. (1986). Acidbase equilibria in invertebrates. In Acidbase Regulation in Animals (ed. N. Heisler), pp. 357-394. New York: Elsevier.
Cameron, J. N. (1989). The Respiratory Physiology of Animals. New York: Oxford University Press.
Cameron, J. N. and Iwama, G. K. (1987). Compensation of progressive hypercapnia in channel catfish and blue crabs. J. Exp. Biol. 133,183 -197.
Castellini, M. A. and Somero, G. N. (1981). Buffering capacity of vertebrate muscle: correlations with potentials for anaerobic function. J. Comp. Physiol. 143,191 -198.
Caulfield, J. A., Auerbach, D. I., Adams, E. and Herzog, H. J. (1997). Near field impacts of reduced pH from ocean CO2 disposal. Energy Convers. Man. 38,343 -348.
Childress, J. J. (1995). Are there physiological and biochemical adaptations of metabolism in deep-sea animals? Trends Ecol. Evol. 10,30 -36.[CrossRef]
Childress, J. J. and Seibel, B. A. (1998). Life
at stable low oxygen levels: Adaptations of animals to oceanic oxygen minimum
layers. J. Exp. Biol.
201,1223
-1232.
Davies, J. K. (1991). Reactions of sand smelt to low pH sea-water. Mar. Poll. Bull. 2, 74-77.
Douglas, E. L., Friedl, W. A. and Pickwell, G. V. (1976). Fishes in oxygen-minimum zones: blood oxygenation characteristics. Science 191,957 -959.[Medline]
Drange, H., Alendal, G. and Johannessen, O. M. (2001). Ocean release of fossil fuel CO2: a case study. Geophys. Res. Lett. 28,2637 -2640.
Gage, J. D. and Tyler, P. A. (1991). Deep-Sea Biology: A Natural History of Organisms of the Deep-sea Floor. Cambridge: Cambridge University Press.
Gibbs, A. H. and Somero, G. N. (1990). Na+-K+ adenosine triphosphatase activities in gills of marine teleost fishes, changes with depth, size and locomotory activity level. Mar. Biol. 106,315 -321.
Girguis, P. R., Childress, J. J., Freytag, J. K., Klose, K. and
Stuber, R. (2002). Effects of metabolite uptake on
proton-equivalent elimination by two species of deep-sea vestimentiferan
tubeworm, Riftia pachyptila and Lamellibrachia cf
luymesi: proton elimination is a necessary adaptation to
sulfide-oxidizing chemoautotrophic symbionts. J. Exp.
Biol. 205,3055
-3066.
Goffredi, S. K., Childress, J. J., Desaulniers, N. T., Lee, R.
W., Lallier, F. H. and Hammonds, D. (1997). Inorganic carbon
acquisition by the hydrothermal vent tubeworm Riftia pachyptial
depends upon high external PCO2 and upon
proton-equivalent ion transport by the worm. J. Exp.
Biol. 200,883
-896.
Guppy, M. and Withers, P. (1999). Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol. Rev. 74, 1-40.[CrossRef][Medline]
Haedrich, R. L. (1996). Deep-water fishes: evolution and adaptation in the Earth's largest living spaces. J. Fish Biol. 49,40 -53.[CrossRef]
Halmann, M. M. and Steinberg, M. (1999). Greenhouse Gas Carbon Dioxide Mitigation: Science and Technology. Washington, DC: Lewis Publishers.
Hand, S. C. (1991). Metabolic dormancy in aquatic invertebrates. In Advances in Comparative and Environmental Physiology, vol. 8 (ed. R. Gilles), pp.1 -47. New York: Springer-Verlag.
Hand, S. C. (1998). Quiescence in Artemia
franciscana embryos: reversible arrest of metabolism and gene expression
at low oxygen levels. J. Exp. Biol.
201,1233
-1242.
Haugan, P. M. (1997). Impacts on the marine environment from direct and indirect ocean storage of CO2. Waste Man. 17,323 -327.
Heisler, N. (1989). Interactions between gas exchange, metabolism, and ion transport in animals: an overview. Can. J. Zool. 67,2923 -2935.
Henry, R. P. (1984). The role of carbonic anhydrase in blood ion and acidbase regulation. Am. Zool. 24,241 -251.
Henry, R. P., Handley, H. L., Krarup, A. and Perry, H. M. (1990). Respiratory and cardiovascular physiology of two species of deep-water crabs, Chaceon fenneri and C. quinquidens: in normoxia and hypoxia. J. Crust. Biol. 10,413 -422.
Hochachka, P. W. and Somero, G. N. (2002). Biochemical Adaptation. Oxford: Oxford University Press.
Houghton, J. T., Ding, Y., Griggs, D. J., Noguer, M., van der Linden, P. J. and Xiaosu, D. (2001). Climate Change 2001: The Scientific Basis. In PICC Third Assessment Report: Climate Change 2001, pp. 944. Cambridge: Cambridge University Press.
Hunt, J. C. and Seibel, B. A. (2000). Life history of Gonatus onyx (Teuthoidea: Cephalopoda): ontogenetic changes in habitat, behavior and physiology. Mar. Biol. 136,543 -552.[CrossRef][Medline]
Ikeda, T. (1988). Metabolism and chemical composition of crustaceans from the Antarctic mesopelagic zone. Deep-Sea Res. 35,1991 -2002.
Kennett, J. P. and Ingram, B. L. (1995). A 20,000-year record of ocean circulation and climate change from the Santa Barbara basin. Nature 377,510 -514.
Kerr, R. A. (2001). Bush backs spending for a
`global problem'. Science
292, 1978.
Knutzen, J. (1981). Effects of decreased pH on marine organisms. Mar. Poll. Bull. 12, 25-29.
Kochevar, R. E. and Childress, J. J. (1996). Carbonic anhydrase in deep-sea chemoautotrophic symbioses. Mar. Biol. 125,375 -383.
Kwast, K. E. and Hand, S. C. (1996). Oxygen and pH regulation of protein synthesis in mitochondria from Artemia franciscana embryos. Biochem. J. 313,207 -213.[Medline]
Langenbuch, M. and Pörtner, H. O. (2002).
Changes in metabolic rate and N excretion in the marine invertebrate
Sipunculus nudus under conditions of environmental hypercapnia:
identifying effective acidbase variables. J. Exp.
Biol. 205,1153
-1160.
Lindinger, M. I., Lauren, D. J. and McDonald, D. G. (1984). Acidbase balance in the sea mussel, Mytilus edulis. III. Effects of environmental hypercapnia on intra- and extracellular acidbase balance. Mar. Biol. Lett. 5,371 -381.
Marchetti, C. (1977). On geoengineering and the CO2 problem. Climate Change 1, 59-68.
Marshall, N. B. (1971). Exploration in the Life of Fishes. Cambridge, MA: Harvard University Press.
McDonald, D. G. (1983). The effects of H+ upon the gills of freshwater fish. Can. J. Zool. 61,691 -703.
McDonald, D. G., Freda, J., Cavdek, V., Gonzalez, R. and Zia, S. (1991). Interspecific differences in gill morphology of freshwater fish in relation to tolerance to low-pH environments. Physiol. Zool. 64,124 -144.
Mickel, T. and Childress, J. J. (1978). The effect of pH on respiration and activity in the bathypelagic mysid Gnathophausia ingens. Biol. Bull. 154,138 -147.
Miyake, Y. and Saruhashi, K. (1956). On the vertical distribution of the dissolved oxygen in the ocean. Deep-Sea Res. 3,242 -247.
Morris, G. M. and Baldwin, J. (1984). pH buffering capacity of invertebrate muscle: correlations with anaerobic muscle work. Mol. Physiol. 5,61 -70.
Noble, R. W., Kwiatkowski, L. D., Young, A. D., Davis, B. J., Haedrich, R. L., Tam, L. and Riggs, A. F. (1986). Functional properties of hemoglobins from deep-sea fish: correlations with depth distribution and presence of a swimbladder. Biochim. Biophys. Acta 870,552 -563.[Medline]
Omori, M., Norman, C. P. and Ikeda, T. (1998). Oceanic disposal of CO2: potential effects on deep-sea plankton and micronketon a review. Plankton Biol. Ecol. 45, 87-99.
Park, K. (1968). Alkalinity and pH off the coast of Oregon. Deep-Sea Res. 15,171 -183.
Pelster, B. (1997). Buoyancy at depth. In Fish Physiology, vol. 16 (ed. D. J. Randall and A. P. Farrell), pp. 195-237. New York: Academic Press.
Perry, S. F. and Laurent, P. (1993). Environmental effects on fish gill structure and function. In Fish Ecophysiology (ed. J. C. Rankin and F. B. Jensen), pp.231 -264. London: Chapman & Hall.
Pörtner, H. O. (1990). Determination of intracellular buffer values after metabolic inhibition by fluoride and nitrilotriacetic acid. Resp. Physiol. 81,275 -288.[Medline]
Pörtner, H. O. (1994). Coordination of metabolism acidbase regulation and haemocyanin function in cephalopods. In Physiology of Cephalopod Molluscs: Lifestyle and Performance Adaptations (ed. H. O. Pörtner, R. K. O'Dor and D. L. MacMillan), pp. 131-148. Basel, Switzerland: Gordon and Breach.
Pörtner, H. O. and Reipschläger, A. (1996). Ocean disposal of anthropogenic CO2: physiological effects on tolerant and intolerant animals. In Ocean Storage of Carbon Dioxide. Workshop 2 Environmental Impact (ed. B. Ormerod and M. V. Angel), pp.57 -81. Cheltenham, UK: IEA Greenhgouse Gas R&D Program.
Pörtner, H. O., Reipschläger, A. and Heisler, N.
(1998). Acidbase regulation, metabolism and energetics in
Sipunculus nudus as a function of ambient carbon dioxide level.
J. Exp. Biol. 201,43
-55.
Reid, S. D., Dockray, J. J., Linton, T. K., McDonald, D. G. and Wood, C. M. (1997). Effects of chronic environmental acidification and a summer global warming scenario: protein synthesis in juvenile rainbow trout (Oncorhynchus mykiss). Can. J. Aquat. Sci. 54,2014 -2024.[CrossRef]
Roos, A. and Boron, W. F. (1981). Intracellular
pH. Physiol. Rev. 61,296
-434.
Sanders, N. K. and Childress, J. J. (1990a).
Adaptations to the deep-sea oxygen minimum layer: oxygen binding by the
hemocyanin of the bathypelagic mysid, Gnathophausia ingens Dohrn.
Biol. Bull. 178,286
-294.
Sanders, N. K. and Childress, J. J. (1990b). A comparison of the respiratory function of the hemocyanins of vertically migrating and non-migrating oplophorid shrimps. J. Exp. Biol. 152,167 -187.
Sanders, N. K., Morris, S., Childress, J. J. and McMahon, B. R. (1992). Effects of ammonia, trimethylamine, L-lactate and CO2 on some decapod crustacean haemocyanins. Comp. Biochem. Physiol. A 101,511 -516.
Seibel, B. A., Chausson, F., Lallier, F. H., Zal, F. and Childress, J. J. (1999). Vampire blood: respiratory physiology of the vampire squid (Cephalopoda: Vampyromorpha) in relation to the oxygen minimum layer. Exp. Biol. Online 4, 1-10. ISSN: 1430-3418.
Seibel, B. A. and Childress, J. J. (2000). Metabolism of benthic octopods (Cephalopoda) as a function of habitat depth and oxygen concentration. Deep-Sea Res. 47,1247 -1260.
Seibel, B. A., Thuesen, E. V., Childress, J. J. and Gorodezky,
L. A. (1997). Decline in pelagic cephalopod metabolism with
habitat depth reflects differences in locomotory efficiency. Biol.
Bull. 192,262
-278.
Seibel, B. A. and Walsh, P. J. (2001).
Potential impacts of CO2 injection on deep-sea biota.
Science 294,319
-320.
Smith, K. L., Jr (1983). Metabolism of two dominant epibenthic echinoderms measured at bathyal depths in the Santa Catalina Basin. Mar. Biol. 72,249 -256.
Smith, K. L., Jr and Baldwin, R. J. (1982). Scavenging deep-sea amphipods: effects of food odor on oxygen consumption and a proposed metabolic strategy. Mar. Biol. 68,287 -298.
Smith, K. L., Jr and Hessler, R. R. (1974). Respiration of benthopelagic fishes: in situ measurements at 1230 meters. Science 184,72 -73.
Somero, G. N. (1985). Intracellular pH, buffering substances and proteins: imidazole protonation and the conservation of protein structure and function. In Transport Processes, Iono- and Osmoregulation (ed. R. Gilles and M. Gilles-Baillien), pp.454 -468. Berlin: Springer-Verlag.
Spicer, J. J. (1995). Oxygen and acidbase status of the sea urchin Psammechinus miliaris during environmental hypoxia. Mar. Biol. 124, 71-76.
Takeuchi, K., Fujioka, Y., Kawasaki, Y. and Shirayama, Y. (1997). Impacts of high concentrations of CO2 on marine organisms: a modification of CO2 ocean sequestration. Energy Convers. Man. 38,S337 -S341.
Tamburri, M. N., Peltzer, E. T., Friederich, G. E., Aya, I., Yamane, K. and Brewer, P. G. (2000). A field study of the effects of CO2 ocean disposal on mobile deep-sea animals. Mar. Chem. 72,95 -101.[CrossRef]
Thuesen, E. V., Miller, C. B. and Childress, J. J. (1998). Ecophysiological interpretation of oxygen consumption rates and enzymatic activities of deep-sea copepods. Mar. Ecol. Prog. Ser. 168,95 -107.
Torres, J. J., Aarset, A. V., Donnelly, J., Hopkins, T. L., Lancraft, T. M. and Ainley, D. G. (1994). Metabolism of antarctic micronektonic crustacea as a function of depth of occurrence and season. Mar. Ecol. Prog. Ser. 113,207 -219.
Toulmond, A. (1992). Chapter 9. Properties and functions of extracellular heme pigments. In Advances in Comparative and Environmental Physiology, vol.13 , pp. 231-256. Heidelberg: Springer-Verlag.
Truchot, J. P. (1987). Comparative Aspects of Extracellular Acidbase Balance. Berlin: Springer-Verlag.
Truchot, J. P. and Duhamel-Jouve, A. (1980). Oxygen and carbon dioxide in the marine intertidal environment: diurnal and tidal changes in rockpools. Resp. Physiol. 39,241 -254.[Medline]
Tufts, B. L. and Randall, D. J. (1989). The functional significance of adrenergic pH regulation in fish erythrocytes. Can. J. Zool. 67,235 -238.
Voss, G. L. (1988). Evolution and phylogenetic relationships of deep-sea octopods (Cirrata and Incirrata). Mollusca 12,253 -276.
Walsh, P. J. and Milligan, C. L. (1989). Coordination of metabolism and intracellular acidbase status: ionic regulation and metabolic consequences. Can. J. Zool. 67,2994 -3004.
Wells, R. M. G., Summers, G., Beard, L. A. and Grigg, G. C. (1988). Ecological and behavioral correlates of intracellular buffering capacity in the muscles of antarctic fishes. Polar Biol. 8,323 -325.
Wheatly, M. G. and Henry, R. P. (1992). Extracellular and intracellular acidbase regulation in crustaceans. J. Exp. Zool. 263,127 -142.
Whiteley, N. M., Scott, J. L., Breeze, S. J. and McCann, L.
(2001). Effects of water salinity on acidbase balance in
decapod crustaceans. J. Exp. Biol.
204,1003
-1011.
Yamada, Y. and Ikeda, T. (1999). Acute toxicity of lowered pH to some oceanic zooplankton. Plankton Biol. Ecol. 46,62 -67.
Young, C. M. and George, S. B. (2000). Larval
development of the tropical deep-sea echinoid Aspidodiadema jacobyi:
phylogenetic implications. Biol. Bull.
198,387
-395.