Skip to main content

Respiratory and digestive responses of postprandial Dungeness crabs, Cancer magister, and blue crabs, Callinectes sapidus, during hyposaline exposure

Abstract

Respiratory responses and gastric processing were examined during hyposaline exposure in two crab species of differing osmoregulatory ability. The efficient osmoregulator, Callinectes sapidus, displayed an immediate increase in oxygen uptake when exposed to low salinity in isolation. In contrast, the weak osmoregulator, Cancer magister, showed no change in oxygen uptake upon acute exposure (<6 h), but slight increases in oxygen uptake tended to occur over longer time scales (12–24 h). These changes were likely attributable to an increase in avoidance activity after 6 h hyposaline exposure. Following feeding in 100% SW, oxygen uptake doubled for both species and remained elevated for 15 h. When postprandial crabs were exposed to low salinities, C. sapidus were able to sum the demands of osmoregulation and digestion. Thus, gastric processes continued unabated in low salinity. Conversely, postprandial C. magister prioritized responses to low salinity over those of digestion, resulting in a decrease in oxygen uptake when exposed to low salinity. This decrease in oxygen uptake corresponded to a reduction in the rate of contraction of the pyloric stomach and a subsequent doubling of gastric evacuation time. The current study is one of the few to illustrate how summation or prioritization of competing physiological systems is manifested in digestive processes.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Andersen JB, Wang T (2003) Cardiorespiratory effects of forced activity and digestion in toads. Physiol Biochem Zool 76:459–470

    Article  PubMed  Google Scholar 

  • Anger K (2003) Salinity as a key parameter in the larval biology of decapod crustaceans. Invert Repro Dev 43:29–45

    Google Scholar 

  • Barnes RSK (1967) Osmotic behaviour of a number of grapsoid crabs with respect to their differential penetration of an estuarine system. J Exp Biol 47:535–551

    CAS  PubMed  Google Scholar 

  • Beamish FWH (1974) Apparent specific dynamic action of largemouth bass, Micropterus salmoides. J Fish Res Board Can 31:1763–1769

    Google Scholar 

  • Bennett AF, Hicks JW (2001) Postprandial exercise: prioritization or additivity of the metabolic responses? J Exp Biol 204:2127–2132

    CAS  PubMed  Google Scholar 

  • Brown AC, Terwilliger NB (1999) Developmental changes in oxygen uptake in Cancer magister (dana) in response to changes in salinity and temperature. J Exp Mar Biol Ecol 241:179–192

    Article  Google Scholar 

  • Carefoot TH (1990a) Specific dynamic action (SDA) in the supralittoral isopod, Ligia pallasii—effect of ration and body size on SDA. Comp Biochem Physiol A 95:317–320

    Article  Google Scholar 

  • Carefoot TH (1990b) Specific dynamic action (SDA) in the supralittoral isopod, Ligia pallasii—identification of components of apparent SDA and effects of dietary amino acid quality and content on SDA. Comp Biochem Physiol A 95:309–316

    Article  Google Scholar 

  • Charmantier G, Charmantier-Daures M (2001) Ontogeny of osmoregulation in crustaceans: the embryonic phase. Am Zool 41:1078–1089

    Article  Google Scholar 

  • Cleaver FC (1949) Preliminary results of the coastal crab (Cancer magister) investigation. Wash Dept Fish Biol Rep 49A:47–92

    Google Scholar 

  • Clemens S, Massabuau JC, Legeay A, Meyrand P, Simmers J (1998) In vivo modulation of interacting central pattern generators in lobster stomatogastric ganglion: influence of feeding and partial pressure of oxygen. J Neurosci 18:2788–2799

    CAS  PubMed  Google Scholar 

  • Cornell JC (1974) Reduction in water exchange-rates in an osmoconforming crab. Am Zool 14:1259

    Google Scholar 

  • Cornell JC (1980) Salt and water-balance in 2 marine spider crabs, Libinia emarginata and Pugettia producta. 3. Some factors involved in short-term adaptation to a dilute medium. Biol Bull 158:16–25

    Article  CAS  Google Scholar 

  • Curtis DL, McGaw IJ (2008) A year in the life of a Dungeness crab: methodology for determining the microhabitat conditions of large decapods inhabiting estuaries. J Zool 274:375–385

    Article  Google Scholar 

  • Curtis DL, Jensen EK, McGaw IJ (2007) Behavioral influences on the physiological responses of Cancer gracilis, the graceful crab, during hyposaline exposure. Biol Bull 212:222–231

    PubMed  Google Scholar 

  • Findley AM, Belisle BW, Stickle WB (1978) Effects of salinity fluctuations on respiration rate of southern oyster drill Thais haemastoma and blue crab Callinectes sapidus. Mar Biol 49:59–67

    Article  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 151:272–304

    Article  CAS  Google Scholar 

  • Haddon M, Wear RG (1987) Biology of feeding in the New Zealand paddle crab Ovalipes catharus (crustacea, portunidae). N Z J Mar Freshw Res 21:55–64

    Article  Google Scholar 

  • Hand SC, Hardewig I (1996) Downregulation of cellular metabolism during environmental stress: Mechanisms and implications. Annu Rev of Physiol 58:539–563

    Article  CAS  Google Scholar 

  • Heinzel HG (1988) Gastric mill activity in the lobster. 1. Spontaneous modes of chewing. J Neurophys 59:528–550

    CAS  Google Scholar 

  • Hicks JW, Bennett AF (2004) Eat and run: Prioritization of oxygen delivery during elevated metabolic states. Respir Physiol Neurobiol 144:215–224

    Article  PubMed  Google Scholar 

  • Hill J, Fowler DL, Van Den Avyle MJ (1989) Species profiles: Life histories and environmental requirements of coastal fishes and invertebrates (mid-atlantic) blue crab. U.S. Fish Wildl Serv Biol Rep 82 (11.100). U.S. Army Corps o f Engineers, TR EL-82-4. 18 pp

  • Houlihan DF, Waring CP, Mathers E, Gray C (1990) Protein synthesis and oxygen consumption of the shore crab Carcinus maenas after a meal. Physiol Zool 63:735–756

    CAS  Google Scholar 

  • Jobling M (1983) Towards an explanation of specific dynamic action (SDA). J Fish Biol 23:549–555

    Article  Google Scholar 

  • Jones LL (1941) Osmotic regulation in several crabs of the pacific coast of North America. J Cell Comp Physiol 18:79–92

    Article  CAS  Google Scholar 

  • Jordan AD, Steffensen JF (2007) Effects of ration size and hypoxia on specific dynamic action in the cod. Physiol Biochem Zool 80:178–185

    Article  PubMed  Google Scholar 

  • Jury SH, Kinnison MT, Howell WH, Watson WH (1994) The effects of reduced salinity on lobster (Homarus americanus milne-edwards) metabolism, implications for estuarine populations. J Exp Mar Biol Ecol 176:167–185

    Article  Google Scholar 

  • King EN (1965) Oxygen consumption of intact crabs and excised gills as a function of decreased salinity. Comp Biochem Physiol 15:93–102

    Article  CAS  PubMed  Google Scholar 

  • Legeay A, Massabuau JC (1999) Blood oxygen requirements in resting crab (Carcinus maenas) 24 h after feeding. Can J Zool 77:784–794

    Article  Google Scholar 

  • Lucu C, Towle DW (2003) Na++/K+ATPase in gills of aquatic crustacea. Comp Biochem Physiol A 135:195–214

    Google Scholar 

  • Lusk G (1905) Theories of metabolism. Science 22:6–12

    Article  PubMed  CAS  Google Scholar 

  • Mantle LH, Farmer LL (1983) Osmotic and ionic regulation. In: Mantel LH (ed) The biology of crustacea. Academic Press, New York, pp 53–161

    Google Scholar 

  • McCue MD (2006) Specific dynamic action: a century of investigation. Comp Biochem Physiol A 144:381–394

    Article  CAS  Google Scholar 

  • McGaw IJ (2006a) Feeding and digestion in low salinity in an osmoconforming crab, Cancer gracilis ii. Gastric evacuation and motility. J Exp Biol 209:3777–3785

    Article  PubMed  Google Scholar 

  • McGaw IJ (2006b) Feeding and digestion in low salinity in an osmoconforming crab, Cancer gracilis i. Cardiovascular and respiratory responses. J Exp Biol 209:3766–3776

    Article  PubMed  Google Scholar 

  • McGaw IJ (2006c) Prioritization or summation of events? Cardiovascular physiology of postprandial Dungeness crabs in low salinity. Physiol Biochem Zool 79:169–177

    Article  PubMed  Google Scholar 

  • McGaw IJ, McMahon BR (1996) Cardiovascular responses resulting from variation in external salinity in the Dungeness crab, Cancer magister. Physiol Zool 69:1384–1401

    Google Scholar 

  • McGaw IJ, Reiber CL (1998) Circulatory modification in the blue crab Callinectes sapidus, during exposure and acclimation to low salinity. Comp Biochem Physiol A 121:67–76

    Article  Google Scholar 

  • McGaw IJ, Reiber CL (2000) Integrated physiological responses to feeding in the blue crab Callinectes sapidus. J Exp Biol 203:359–368

    CAS  PubMed  Google Scholar 

  • McGaw IJ, Reiber CL, Guadagnoli JA (1999) Behavioral physiology of four crab species in low salinity. Biol Bull 196:163–176

    Article  Google Scholar 

  • Mente E, Legeay A, Houlihan DF, Massabuau JC (2003) Influence of oxygen partial pressures on protein synthesis in feeding crabs. Am J Physiol 284:R500–R510

    CAS  Google Scholar 

  • Pan ZC, Ji X, Lu HL, Ma XM (2005) Metabolic response to feeding in the Chinese striped-necked turtle, Ocadia sinensis. Comp Biochem Phys A 141:470–475

    Article  CAS  Google Scholar 

  • Pauley GB, Armstrong DA, Heun TW (1986) Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (Pacific Northwest)—Dungeness crab. US Fish Wildl Serv Biol Rep 82(11.63). US Army Corps of Engineers, TR EL-82-4, 20pp

  • Pequeux A (1995) Osmotic regulation in crustaceans. J Crust Biol 15:1–60

    Article  Google Scholar 

  • Piller SC, Henry RP, Doeller JE, Kraus DW (1995) A comparison of the gill physiology of 2 euryhaline crab species, Callinectes sapidus and Callinectes similis: energy production, transport related enzymes, and osmoregulation as a function of acclimation salinity. J Exp Biol 198:349–358

    CAS  PubMed  Google Scholar 

  • Roast SD, Widdows J, Jones MB (2000) Egestion rates of the estuarine mysid Neomysis integer (peracarida : Mysidacea) in relation to a variable environment. J Exp Mar Biol Ecol 245:69–81

    Article  Google Scholar 

  • Robertson RF, Meagor J, Taylor EW (2002) Specific dynamic action in the shore crab, Carcinus maenas, in relation to acclimation temperature and to the onset of the emersion response. Physiol Biochem Zool 75:350–359

    Article  CAS  PubMed  Google Scholar 

  • Secor SM, Hicks JW, Bennett AF (2000) Ventilatory and cardiovascular responses of a python (Python molurus) to exercise and digestion. J Exp Biol 203:2447–2454

    CAS  PubMed  Google Scholar 

  • Spaargaren DH (1973) Effect of salinity and temperature on heart rate of osmoregulating and osmoconforming shrimps. Comp Biochem Physiol 45:773–786

    Article  CAS  Google Scholar 

  • Stevens BG, Armstrong DA, Hoeman JC (1984) Diel activity of an estuarine population of Dungeness crabs, Cancer magister, in relation to feeding and environmental factors. J Crust Biol 4:390–403

    Article  Google Scholar 

  • Sugarman PC, Pearson WH, Woodruff DL (1983) Salinity detection and associated behavior in the Dungeness crab, Cancer magister. Estuaries 6:380–386

    Article  Google Scholar 

  • Talbot C, Higgins PJ (1983) A radiographic method for feeding studies on fish using metallic iron powder as a marker. J Fish Biol 23:211–220

    Article  Google Scholar 

  • Tan EC, van Engel WA (1966) Osmoregulation in the adult blue crab, Callinectes sapidus rathbun. Chesapeake Sci 7:30–35

    Article  Google Scholar 

  • Taylor EW, Butler PJ, Alwassia A (1977) Effect of a decrease in salinity on respiration, osmoregulation and activity in shore crab, Carcinus maenas at different acclimation temperatures. J Comp Physiol 119:155–170

    CAS  Google Scholar 

  • Wallace JC (1973) Feeding, starvation and metabolic rate in shore crab Carcinus maenas. Mar Biol 20:277–281

    Article  Google Scholar 

  • Wang T, Busk H, Overgaard J (2001) The respiratory consequences of feeding in amphibians and reptiles. Comp Biochem Physiol A 128:535–549

    CAS  Google Scholar 

Download references

Acknowledgments

We wish to thank the director and staff of the Bamfield Marine Sciences Centre for use of facilities. This work was supported by an NSF grant (IBN #0313765) to IJM and an NSERC PGS-D to DLC.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Daniel L. Curtis.

Additional information

Communicated by I. D. Hume.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Curtis, D.L., McGaw, I.J. Respiratory and digestive responses of postprandial Dungeness crabs, Cancer magister, and blue crabs, Callinectes sapidus, during hyposaline exposure. J Comp Physiol B 180, 189–198 (2010). https://doi.org/10.1007/s00360-009-0403-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-009-0403-z

Keywords

  • Crab
  • Crustacean
  • Digestion
  • Osmoregulation
  • Salinity