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Water bicarbonate modulates the response of the shore crab Carcinus maenas to ocean acidification

Abstract

Ocean acidification causes an accumulation of CO2 in marine organisms and leads to shifts in acid–base parameters. Acid–base regulation in gill breathers involves a net increase of internal bicarbonate levels through transmembrane ion exchange with the surrounding water. Successful maintenance of body fluid pH depends on the functional capacity of ion-exchange mechanisms and associated energy budget. For a detailed understanding of the dependence of acid–base regulation on water parameters, we investigated the physiological responses of the shore crab Carcinus maenas to 4 weeks of ocean acidification [OA, P(CO2)w = 1800 µatm], at variable water bicarbonate levels, paralleled by changes in water pH. Cardiovascular performance was determined together with extra-(pHe) and intracellular pH (pHi), oxygen consumption, haemolymph CO2 parameters, and ion composition. High water P(CO2) caused haemolymph P(CO2) to rise, but pHe and pHi remained constant due to increased haemolymph and cellular [HCO3]. This process was effective even under reduced seawater pH and bicarbonate concentrations. While extracellular cation concentrations increased throughout, anion levels remained constant or decreased. Despite similar levels of haemolymph pH and ion concentrations under OA, metabolic rates, and haemolymph flow were significantly depressed by 40 and 30%, respectively, when OA was combined with reduced seawater [HCO3] and pH. Our findings suggest an influence of water bicarbonate levels on metabolic rates as well as on correlations between blood flow and pHe. This previously unknown phenomenon should direct attention to pathways of acid–base regulation and their potential feedback on whole-animal energy demand, in relation with changing seawater carbonate parameters.

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Abbreviations

3-APP:

3′-Aminopropylphosphonate

α :

Solubility coefficient; level of significance

ADP:

Adenosin-5′-diphosphate

AEP:

2′-Aminoethylphosphonate

ANOVA:

Analysis of variance

ATP:

Adenosin-5′-triphosphate

[B]T :

Total boron concentration

bpm:

Beats per minute

°C:

Degree celsius

c :

Concentration

Ca2+ :

Calcium ion

Cl :

Chloride ion

CO2 :

Carbon dioxide

δ:

Chemical shift

FLASH:

Fast low angle shot

g:

Gramm

GABA:

Gamma-aminobutyric acid

H+ :

Hydrogen ion/proton

h:

Hour(s)

HCO3 :

Hydrogen carbonate/bicarbonate ion

HCl:

Hydrochloric acid

K+ :

Potassium ion

L:

Liter

M:

Molar (mol/L)

m:

Meter

m :

Mass

Mg2+ :

Magnesium ion

min:

Minute(s)

mol:

Mol

\(\dot {M}{{\text{O}}_2}\) :

Metabolic-/respiration rate

MRI:

Magnetic resonance imaging

n :

Amount of substance; group size

Na+ :

Sodium ion

NH4 + :

Ammonium ion

NMR:

Nuclear magnetic resonance

O2 :

Oxygen

P:

Phosphorous

P :

(Partial-)pressure; probability

P(CO2)e :

Partial pressure of CO2 in haemolymph

P(CO2)w :

Partial pressure of CO2 in seawater

Pi :

Inorganic phosphate

pH:

− log10[H+]

pHe :

Extracellular pH

pHi :

Intracellular pH

pHw :

Sea water pH (free scale)

pK a :

− log10 of dissociation constant in an acid–base equilibrium

\({\text{p}}{K_{\text{a}}}^{{\prime \prime \prime }}\) :

pKa under defined conditions

PLA:

Phospho-l-arginine

PSU:

Practical salinity unit

ppm:

Parts per million

RARE:

Rapid acquisition with relaxation enhancement

RMR:

Routine metabolic rate

S :

Seawater salinity

SID:

Strong ion difference

SMR:

Standard metabolic rate

SO4 2− :

Sulfate ion

T:

Tesla

T :

Temperature

t :

Time

V :

Volume

w f :

Wet weight/fresh weight

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Acknowledgements

The authors thank Fredy Veliz Moraleda and Silvia Hardenberg for assistance in animal maintenance. We thank Dr. Franz-Josef Sartoris for expertise on ion chromatography, Timo Hirse for assistance with the GC and Rolf Wittig for post-processing the MR data. We would like to thank three anonymous reviewers for their helpful comments, improving the manuscript.

Funding

The study is a contribution to the PACES II research program (WP 1.6) of the Alfred Wegener Institute, funded by the Helmholtz Association.

Author information

BM, CB and HP conceived and designed the experiments, and wrote and drafted the manuscript. BM carried out the experiments, with help from CB on MR experiments. BM performed the statistical analyses. All authors approved the final version of the manuscript.

Correspondence to Christian Bock.

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No competing interests declared.

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Communicated by G. Heldmaier.

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Maus, B., Bock, C. & Pörtner, H. Water bicarbonate modulates the response of the shore crab Carcinus maenas to ocean acidification. J Comp Physiol B 188, 749–764 (2018) doi:10.1007/s00360-018-1162-5

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Keywords

  • Crustacean
  • Bicarbonate
  • Cardiac MRI
  • In vivo 31P NMR spectroscopy
  • Extracellular pH marker
  • Cardiovascular system