Skip to main content

Advertisement

Log in

How the green crab Carcinus maenas copes physiologically with a range of salinities

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

To evaluate the physiological ability to adjust to environmental variations of salinity, Carcinus maenas were maintained in 10, 20, 32 (control), 40, and 50 ppt (13.8 ± 0.6 °C) for 7 days. Closed respirometry systems were used to evaluate oxygen consumption (\({\dot{\text{M}}\text{O}}_{{2}}\)), ammonia excretion (Jamm), urea-N excretion (Jurea-N) and diffusive water fluxes (with 3H2O). Ions, osmolality, metabolites, and acid–base status were determined in the hemolymph and seawater, and transepithelial potential (TEP) was measured. At the lowest salinity, there were marked increases in \({\dot{\text{M}}\text{O}}_{{2}}\) and Jamm, greater reliance on N-containing fuels to support aerobic metabolism, and a state of internal metabolic alkalosis (increased [HCO3]) despite lower seawater pH. At higher salinities, an activation of anaerobic metabolism and a state of metabolic acidosis (decreased [HCO3] and increased [lactate]), in combination with respiratory compensation (decreased PCO2), were detected. TEP became more negative with decreasing salinity. Osmoregulation and osmoconformation occurred at low and high salinities, respectively, with complex patterns in individual ions; hemolymph [Mg2+] was particularly well regulated at levels well below the external seawater at all salinities. Diffusive water flux rates increased at higher salinities. Our results show that C. maenas exhibits wide plasticity of physiological responses when acclimated to different salinities and tolerates substantial disturbances of physiological parameters, illustrating that this species is well adapted to invade and survive in diverse habitats.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Bateman JB (1933) Osmotic and ionic regulation in the Shore Crab, Carcinus maenas, with notes on the blood concentrations of Gammarus locusta and Ligia oceanica. J Exp Biol 10(4):355–371

    Article  Google Scholar 

  • Behrens-Yamada S (2001) Global invader: the European green crab. Oregon State University, Corvallis

    Google Scholar 

  • Berlind A, Kamemoto FI (1977) Rapid water permeability changes in eyestalkless euryhaline crabs and in isolated, perfused gills. Comp Biochem Physiol A Mol Integr Physiol 58(4):383–385

    Article  Google Scholar 

  • Binns R (1969) The physiology of the antennal gland of Carcinus maenas (L.) V. Some nitrogenous constituents in the blood and urine. J Exp Biol 51(1):41–45

    Article  CAS  Google Scholar 

  • Boutilier RG, Heming TA, Iwama GK (1984) Appendix: Physicochemical parameters for use in fish respiratory physiology. In: Hoar WS, Randall DJ (eds) Fish physiology, vol 10. Academic Press, pp 403–430

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1):248–254

    Article  CAS  PubMed  Google Scholar 

  • Cameron JN, Heisler N (1983) Studies of ammonia in the rainbow trout: physico-chemical parameters, acid–base behaviour and respiratory clearance. J Exp Biol 105(1):107–125

    Article  CAS  Google Scholar 

  • Dal Pont G, Souza-Bastos LR, Giacomin M, Dolatto RG, Baika LM, Grassi MT, Ostrensky A, Wood CM (2019) Acute exposure to the water-soluble fraction of gasoline (WSFG) affects oxygen consumption, nitrogenous-waste and Mg excretion, and activates anaerobic metabolism in the goldfish Carassius auratus. Comp Biochem Physiol C Toxicol Pharmacol 226:108590

    Article  Google Scholar 

  • Davenport HW (1974) The ABC of acid–base chemistry: the elements of physiological blood-gas chemistry for medical students and physicians. University of Chicago Press, Chicago

    Google Scholar 

  • Dejours P (1981) Principles of comparative respiratory physiology, 2nd edn. Elsevier North-Holland, Amsterdam

    Google Scholar 

  • Durand F, Regnault M (1998) Nitrogen metabolism of two portunid crabs, Carcinus maenas and Necora puber, during prolonged air exposure and subsequent recovery: a comparative study. J Exp Biol 201(17):2515–2528

    Article  CAS  PubMed  Google Scholar 

  • Evans DH (1967) Sodium, chloride and water balance of the intertidal teleost, Xiphister Atropurpureus: III. The roles of simple diffusion, exchange diffusion, osmosis and active transport. J Exp Biol 47(3):525–534

    Article  CAS  PubMed  Google Scholar 

  • Frederich M, Sartoris FJ, Arntz WE, Portner H (2000) Haemolymph Mg2+regulation in decapod crustaceans: physiological correlates and ecological consequences in polar areas. J Exp Biol 203(8):1383–1393

    Article  CAS  PubMed  Google Scholar 

  • Freire CA, Onken H, McNamara JC (2008) A structure–function analysis of ion transport in crustacean gills and excretory organs. Comp Biochem Physiol A Mol Integr Physiol 151(3):272–304

    Article  PubMed  Google Scholar 

  • Giacomin M, Dal Pont G, Eom J, Schulte PM, Wood CM (2019a) The effects of salinity and hypoxia exposure on oxygen consumption, ventilation, diffusive water exchange and ionoregulation in the Pacific hagfish (Eptatretus stoutii). Comp Biochem Physiol A Mol Integr Physiol 232:47–59

    Article  CAS  PubMed  Google Scholar 

  • Giacomin M, Eom J, Schulte PM, Wood CM (2019b) Acute temperature effects on metabolic rate, ventilation, diffusive water exchange, osmoregulation, and acid–base status in the Pacific hagfish (Eptatretus stoutii). J Comp Physiol B 189(1):17–35

    Article  CAS  PubMed  Google Scholar 

  • Greenaway P (1976) The regulation of haemolymph calcium concentration of the crab Carcinus maenas (L.). J Exp Biol 64(1):149–157

    Article  CAS  PubMed  Google Scholar 

  • Harris R, Andrews M (1982) Extracellular fluid volume changes in Carcinus maenas during acclimation to low and high environmental salinities. J Exp Biol 99(1):161–173

    Article  CAS  Google Scholar 

  • Healy TM, Schulte PM (2012) Thermal acclimation is not necessary to maintain a wide thermal breadth of aerobic scope in the common killifish (Fundulus heteroclitus). Physiol Biochem Zool 85(2):107–119

    Article  CAS  PubMed  Google Scholar 

  • Henry RP, Garrelts EE, McCarty MM, Towle DW (2002) Differential induction of branchial carbonic anhydrase and Na+/K+ ATPase activity in the euryhaline crab, Carcinus maenas, in response to low salinity exposure. J Exp Zool 292(7):595–603

    Article  CAS  PubMed  Google Scholar 

  • Henry RP, Gehnrich S, Weihrauch D, Towle DW (2003) Salinity-mediated carbonic anhydrase induction in the gills of the euryhaline green crab, Carcinus maenas. Comp Biochem Physiol A Mol Integr Physiol 136(2):243–258

    Article  PubMed  Google Scholar 

  • Henry RP, Lucu Č, Onken H, Weihrauch D (2012) Multiple functions of the crustacean gill: osmotic/ionic regulation, acid–base balance, ammonia excretion, and bioaccumulation of toxic metals. Front Physiol 3:431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hill A, Taylor A, Strang R (1991) Physiological and metabolic responses of the shore crab Carcinus maenas (L.) during environmental anoxia and subsequent recovery. J Exp Mar Biol Ecol 150(1):31–50

    Article  CAS  Google Scholar 

  • Johnson I, Uglow R (1985) Some effects of aerial exposure on the respiratory physiology and blood chemistry of Carcinus maenas (L.) and Liocarcinus puber (L.). J Exp Mar Biol Ecol 94(1–3):151–165

    Article  CAS  Google Scholar 

  • Klassen GJ, Locke A (2007) A biological synopsis of the European green crab, Carcinus maenas. Can Manusc. Rep Fish Aquat Sci 2818, vii+75pp

  • Lauff R, Wood C (1996) Respiratory gas exchange, nitrogenous waste excretion, and fuel usage during starvation in juvenile rainbow trout, Oncorhynchus mykiss. J Comp Physiol B165(7):542–551

    Article  Google Scholar 

  • Leignel V, Stillman J, Baringou S, Thabet R, Metais I (2014) Overview on the European green crab Carcinus spp. (Portunidae, Decapoda), one of the most famous marine invaders and ecotoxicological models. Environ Sci Pollut Res 21(15):9129–9144

    Article  CAS  Google Scholar 

  • Lucu Č, Siebers D (1986) Amiloride-sensitive sodium flux and potentials in perfused Carcinus gill preparations. J Exp Biol 122(1):25–35

    Article  Google Scholar 

  • McDonald DG, Hõbe H, Wood CM (1980) The influence of calcium on the physiological responses of the rainbow trout, Salmo gairdneri, to low environmental pH. J Exp Biol 88(1):109–132

    Article  CAS  PubMed  Google Scholar 

  • McGaw I, Kaiser MJ, Naylor E, Naylor HRN (1992) Intra-specific morphological variation related to the moult-cycle in colour forms of the shore crab Carcinus maenas. J Zool (lond) 228:351–359

    Article  Google Scholar 

  • McGaw I, Reiber C, Guadagnoli J (1999) Behavioral physiology of four crab species in low salinity. Biol Bull 196(2):163–176

    Article  CAS  PubMed  Google Scholar 

  • McGaw I (1991). Behavioural responses of the shore crab Carcinus maenas to salinity variation. Ph.D. Thesis, University of Wales

  • McNamara JC, Faria SC (2012) Evolution of osmoregulatory patterns and gill ion transport mechanisms in the decapod Crustacea: a review. J Comp Physiol B 182(8):997–1014

    Article  CAS  PubMed  Google Scholar 

  • Moore S, Stein WH (1954) A modified ninhydrin reagent for the photometric determination of amino acids and related compounds. J Biol Chem 211:907–913

    Article  CAS  PubMed  Google Scholar 

  • Morritt D, Spicer JI (1993) A brief re-examination of the function and regulation of extracellular magnesium and its relationship to activity in crustacean arthropods. Comp Biochem Physiol A Mol Integr Physiol 106(1):19–23

    Article  Google Scholar 

  • Quijada-Rodriguez AR, Allen GJ, Nash MT, Weihrauch D (2022) Postprandial nitrogen and acid-base regulation in the seawater acclimated green crab, Carcinus maenas. Comp Biochem Physiol A Mol Integr Physiol 267:111171

    Article  CAS  PubMed  Google Scholar 

  • Rahmatullah M, Boyde TRC (1980) Improvements in the determination of urea using diacetyl monoxime: methods with and without deproteinisation. Clin Chim Acta 107(1):3–9

    Article  CAS  PubMed  Google Scholar 

  • Rainbow P, Black W (2001) Effects of changes in salinity on the apparent water permeability of three crab species: Carcinus maenas, Eriocheir sinensis and Necora puber. J Exp Mar Biol Ecol 264(1):1–13

    Article  Google Scholar 

  • Rasmussen A, Andersen O (1996) Apparent water permeability as a physiological parameter in crustaceans. J Exp Biol 199(12):2555–2564

    Article  CAS  PubMed  Google Scholar 

  • Rasmussen AD, Bjerregaard P (1995) The effect of salinity and calcium concentration on the apparent water permeability of Cherax destructor, Astacus astacus and Carcinus maenas (Decapoda, Crustacea). Comp Biochem Physiol A Mol Integr Physiol 111(1):171–175

    Article  Google Scholar 

  • Rudy PP Jr (1967) Water permeability in selected decapod Crustacea. Comp Biochem Physiol 22(2):581–589

    Article  Google Scholar 

  • Schwabe E (1933) Über die Osmoregulation verschiedener Krebse (Malacostracen). Z Vgl Physiol 19(1):183–236

    Article  Google Scholar 

  • Shaw J (1961) Studies on ionic regulation in Carcinus maenas (L.): I. Sodium balance. J Exp Biol 38(1):135–152

    Article  CAS  Google Scholar 

  • Siebers D, Lucu C, Sperling K-R, Eberlein K (1972) Kinetics of osmoregulation in the crab Carcinus maenas. Mar Biol 17(4):291–303

    Article  CAS  Google Scholar 

  • Siebers D, Leweck K, Markus H, Winkler A (1982) Sodium regulation in the shore crab Carcinus maenas as related to ambient salinity. Mar Biol 69(1):37–43

    Article  CAS  Google Scholar 

  • Siebers D, Winkler A, Lucu C, Thedens G, Weichart D (1985) Na–K-ATPase generates an active transport potential in the gills of the hyperregulating shore crab Carcinus maenas. Mar Biol 87(2):185–192

    Article  CAS  Google Scholar 

  • Siebers D, Lucu Č, Winkler A, Dalla Venezia L, Wille H (1986) Active uptake of sodium in the gills of the hyperregulating shore crab Carcinus maenas. Helgol Meeresunters 40(1):151–160

    Article  Google Scholar 

  • Siebers D, Wille H, Lucu C, Venezia LD (1989) Conductive sodium entry in gill cells of the shore crab, Carcinus maenas. Mar Biol 101(1):61–68

    Article  CAS  Google Scholar 

  • Simonik E, Henry RP (2014) Physiological responses to emersion in the intertidal green crab, Carcinus maenas (L.). Mar Freshw Behav Physiol 47 (2):101–115

  • Smith RI (1970) The apparent water-permeability of Carcinus maenas (Crustacea, Brachyura, Portunidae) as a function of salinity. Biol Bull 139(2):351–362

    Article  PubMed  Google Scholar 

  • Spaargaren D (1982) The ammonium excretion of the shore crab, Carcinus maenas, in relation to environmental osmotic conditions. Neth J Sea Res 15(2):273–283

    Article  CAS  Google Scholar 

  • Stewart PA (1978) Independent and dependent variables of acid-base control. Respir Physiol 33(1):9–26

    Article  CAS  PubMed  Google Scholar 

  • Taylor A (1977) The respiratory responses of Carcinus maenas (L.) to changes in environmental salinity. J Exp Mar Biol Ecol 29(2):197–210

    Article  CAS  Google Scholar 

  • Taylor E (1982) Control and co-ordination of ventilation and circulation in crustaceans: responses to hypoxia and exercise. J Exp Biol 100(1):289–319

    Article  Google Scholar 

  • Taylor E, Butler P, Al-Wassia A (1977) Some responses of the shore crab, Carcinus maenas (L.) to progressive hypoxia at different acclimation temperatures and salinities. J Comp Physiol 122(3):391–402

    Article  CAS  Google Scholar 

  • Truchot J (1973) Fixation et transport de l’oxygène par le sang de Carcinus maenas: variations en rapport avec diverses conditions de température et de salinité. Neth J Sea Res 7:482–495

    Article  Google Scholar 

  • Truchot J (1975) Factors controlling the in vitro and in vivo oxygen affinity of the hemocyanin in the crab Carcinus maenas (L.). Respir Physiol 24(2):173–189

    Article  CAS  PubMed  Google Scholar 

  • Truchot JP (1976a) Carbon dioxide combining properties of the blood of the shore crab Carcinus maenas (L): carbon dioxide solubility coefficient and carbonic acid dissociation constants. J Exp Biol 64(1):45

    Article  CAS  PubMed  Google Scholar 

  • Truchot JP (1976b) Carbon dioxide combining properties of the blood of the shore crab, Carcinus maenas (L.): CO2-dissociation curves and Haldane effect. J Comp Physiol 112(3):283–293

    Article  CAS  Google Scholar 

  • Truchot J, Forgue J (1998) Effect of water alkalinity on gill CO2 exchange and internal PCO2 in aquatic animals. Comp Biochem Physiol A Mol Integr Physiol 119(1):131–136

    Article  CAS  PubMed  Google Scholar 

  • Truchot J-P (1981) The effect of water salinity and acid-base state on the blood acid–base balance in the euryhaline crab, Carcinus maenas (L.). Comp Biochem Physiol A Mol Integr Physiol 68(4):555–561

  • Truchot J-P (1987) Comparative aspects of extracellular acid-base balance, zoophysiology, vol 20. Springer, Berlin

  • Verdouw H, Van Echteld CJA, Dekkers EMJ (1978) Ammonia determination based on indophenol formation with sodium salicylate. Water Res 12(6):399–402

    Article  CAS  Google Scholar 

  • Wang S, Carter CG, Fitzgibbon QP, Smith GG (2021) Respiratory quotient and the stoichiometric approach to investigating metabolic energy substrate use in aquatic ectotherms. Rev Aquac 13(3):1255–1284

    Article  Google Scholar 

  • Webb D (1940) Ionic regulation in Carcinus maenas. Proc R Soc Lond Ser B Biol Sci 129(854):107–136

    CAS  Google Scholar 

  • Weihrauch D, Becker W, Postel U, Luck-Kopp S, Siebers D (1999) Potential of active excretion of ammonia in three different haline species of crabs. J Comp Physiol B 169(1):25–37

    Article  CAS  Google Scholar 

  • Weihrauch D, Fehsenfeld S, Quijada-Rodriguez A (2017) Nitrogen excretion in aquatic crustaceans. Acid–base balance and nitrogen excretion in invertebrates: In: Weihrauch D, O'Donnell MJ (eds) Acid–base balance and nitrogen excretion in invertebrates, pp 1–24. Springer, Cham

  • Wilson CH, Nancollas SJ, Rivers ML, Spicer JI, McGaw IJ (2021) Effects of handling during experimental procedures on stress indices in the green shore crab, Carcinus maenas (L.). Mar Freshw Behav Physiol 54(2):65–86

    Article  CAS  Google Scholar 

  • Winkler A (1986) The role of the transbranchial potential difference in hyperosmotic regulation of the shore crab Carcinus maenas. Helgol Meeresunters 40(1):161–175

    Article  Google Scholar 

  • Zanders I (1980) Regulation of blood ions in Carcinus maenas (L.). Comp Biochem Physiol A Mol Integr Physiol 65(1):97–108

  • Zatta P (1987) The relationship between plasma proteins and intracellular free amino acids during osmotic regulation in Carcinus maenas. J Exp Zool 242(2):131–136

    Article  CAS  Google Scholar 

  • Zimmer AM, Wood CM (2017) Acute exposure to high environmental ammonia (HEA) triggers the emersion response in the green shore crab. Comp Biochem Physiol A Mol Integr Physiol 204:65–75

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank the BMSC staff, especially research co-ordinators Eric Clelland and Tao Eastham, for their support, and we appreciate the constructive reviewer comments.

Funding

The study was funded by an NSERC (Canada) Discovery Grant (RGPIN-2017-03843) to CMW.

Author information

Authors and Affiliations

Authors

Contributions

The study was designed by all authors, and the experiments and measurements were performed by all authors. GDP and CMW wrote the first draft of the manuscript, JW and BP edited it, and all authors approved the final version.

Corresponding author

Correspondence to Chris M. Wood.

Ethics declarations

Conflict of interest

All authors declare that they have no conflict of interest.

Ethics approval

Approval was obtained from Bamfield Marine Sciences Centre Invertebrate AUP RS-18-19; Fisheries and Oceans Canada Collection Permit XR 212 2019.

Additional information

Communicated by B. Pelster.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dal Pont, G., Po, B., Wang, J. et al. How the green crab Carcinus maenas copes physiologically with a range of salinities. J Comp Physiol B 192, 683–699 (2022). https://doi.org/10.1007/s00360-022-01458-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-022-01458-1

Keywords

Navigation