Skip to main content
SpringerLink
Log in

Interactive effects of food deprivation state and hypoxia on the respiratory responses of postprandial rock crabs, Cancer irroratus

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

Abstract

Under the background of climate change, increasing attention has focused on the effects of ocean deoxygenation on marine organisms. However, few studies address the effects of different food deprivation states on hypoxia tolerance. We therefore investigated the metabolic responses of the Atlantic rock crab, Cancer irroratus (starved 28–35 days, fasted 3–5 days and recently fed). Starved-crab exhibited the lowest critical oxygen saturation (Scrit), while fed-crab had the highest Scrit. The fed-crab maintained an elevated postprandial oxygen consumption (MO2) even below the Scrit of fasted-crab indicating reserved aerobic scopes for critical activities in severe hypoxia. Following feeding, hypoxia (50% and 20% oxygen saturation, SO2) retarded the specific dynamic action resulting in lower peak MO2 and longer duration. The starved-crab exhibited a lower peak MO2, prolonged duration and higher energy expenditure than fasted-crab after feeding. The decline in arterial PO2 was most pronounced below the Scrit for both fasted- and starved-crab. The higher hemocyanin concentration ([Hc]) of fasted-crab (than starved-crab) suggested they had improved oxygen transport capacity, but hypoxia did not increase [Hc] during the 72-h experiment. Following feeding, the fasted-crab significantly increased l-lactate concentration ([l-lactate]) in 20% SO2, which was not observed in starved-crab. These results suggest starvation may trigger a cross-tolerance to hypoxia. Because crabs can undergo long periods of food deprivation in their natural environment, future studies should consider how this may affect their ability to deal with environmental perturbations.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Airriess C, McMahon B (1994) Cardiovascular adaptations enhance tolerance of environmental hypoxia in the crab Cancer magister. J Exp Biol 190(1):23–41

    Article  CAS  Google Scholar 

  • Ansell AD (1973) Changes in oxygen consumption, heart rate and ventilation accompanying starvation in the decapod crustacean Cancer pagurus. Neth J Sea Res 7:455–475. https://doi.org/10.1016/0077-7579(73)90066-5

    Article  Google Scholar 

  • Baden SP, Depledge MH, Hagerman L (1994) Glycogen depletion and altered copper and manganese handling in Nephrops norvegicus following starvation and exposure to hypoxia. Mar Ecol Prog Ser 103(1/2):65–72

    Article  CAS  Google Scholar 

  • Bell GW, Eggleston DB, Wolcott TG (2003) Behavioral responses of free-ranging blue crabs to episodic hypoxia. II feeding. Mar Ecol Prog Ser 259:227–235

    Article  Google Scholar 

  • Bernatis JL, Gerstenberger SL, McGaw IJ (2007) Behavioural responses of the Dungeness crab, Cancer magister, during feeding and digestion in hypoxic conditions. Mar Biol 150(5):941–951. https://doi.org/10.1007/s00227-006-0392-3

    Article  Google Scholar 

  • Bonvillain CP, Rutherford DA, Kelso WE, Green CC (2012) Physiological biomarkers of hypoxic stress in red swamp crayfish Procambarus clarkii from field and laboratory experiments. Comp Biochem Physiol A Mol Integr Physiol 163(1):15–21. https://doi.org/10.1016/j.cbpa.2012.04.015

    Article  CAS  Google Scholar 

  • Bradford S, Taylor A (1982) The respiration of Cancer pagurus under normoxic and hypoxic conditions. J Exp Biol 97(1):273–288

    Article  Google Scholar 

  • Breitburg D, Levin LA, Oschlies A, Grégoire M, Chavez FP, Conley DJ, Garçon V, Gilbert D, Gutiérrez D, Isensee K, Jacinto GS, Limburg KE, Montes I, Naqvi SWA, Pitcher GC, Rabalais NN, Roman MR, Rose KA, Seibel BA, Telszewski M, Yasuhara M, Zhang J (2018) Declining oxygen in the global ocean and coastal waters. Science 359(6371):eaam7240. https://doi.org/10.1126/science.aam7240

    Article  CAS  Google Scholar 

  • Bridges CR (2001) Modulation of haemocyanin oxygen affinity: properties and physiological implications in a changing world. J Exp Biol 204(5):1021–1032

    Article  CAS  Google Scholar 

  • Brill RW, Bushnell PG, Elton TA, Small HJ (2015) The ability of blue crab (Callinectes sapidus, Rathbun 1886) to sustain aerobic metabolism during hypoxia. J Exp Mar Biol Ecol 471:126–136. https://doi.org/10.1016/j.jembe.2015.06.003

    Article  Google Scholar 

  • Brown CR, Cameron JN (1991) The induction of specific dynamic action in channel catfish by infusion of essential amino acids. Physiol Zool 64:276–297

    Article  CAS  Google Scholar 

  • Cant JP, McBride BW, Croom WJ Jr (1996) The regulation of intestinal metabolism and its impact on whole animal energetics. J Anim Sci 74(10):2541–2553

    Article  CAS  Google Scholar 

  • Carefoot TH (1990) 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 Physiol 95(3):309–316

    Article  Google Scholar 

  • Carlos R, Evenor M, Gabriela G, Roberto B, Eugenio D-I, Luis AS (1998) Effect of dissolved oxygen on the energy balance and survival of Penaeus setiferus juveniles. Mar Ecol Prog Ser 174:67–75

    Article  Google Scholar 

  • Carter C, Mente E (2014) Protein synthesis in crustaceans: a review focused on feeding and nutrition. Open Life Sci 9(1):1–10. https://doi.org/10.2478/s11535-013-0134-0

    Article  CAS  Google Scholar 

  • Cervellione F, McGurk C, Van den Broeck W (2017) Effect of starvation and refeeding on the ultrastructure of the perigastric organ (hepatopancreas) in the whiteleg shrimp Litopenaeus vannamei (Boone, 1931) (Decapoda:Caridea:Penaeidae). J Crust Biol 37(6):693–700. https://doi.org/10.1093/jcbiol/rux085

    Article  Google Scholar 

  • Chen J-C, Cheng S-y (1993) Studies on haemocyanin and haemolymph protein levels of Penaeus japonicus based on sex, size and moulting cycle. Comp Biochem Physiol B Comp Biochem 106(2):293–296. https://doi.org/10.1016/0305-0491(93)90303-M

    Article  Google Scholar 

  • Chen J-C, Kou T-T (1998) Hemolymph acid-base balance, oxyhemocyanin, and protein levels of Macrobrachium rosenbergii at different concentrations of dissolved oxygen. J Crust Biol 18(3):437–441. https://doi.org/10.2307/1549408

    Article  Google Scholar 

  • Cheng W, Liu C-H, Kuo C-M (2003) Effects of dissolved oxygen on hemolymph parameters of freshwater giant prawn, Macrobrachium rosenbergii (de Man). Aquaculture 220(1):843–856. https://doi.org/10.1016/S0044-8486(02)00534-3

    Article  CAS  Google Scholar 

  • Clemens S, Massabuau J-C, 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(7):2788–2799

    Article  CAS  Google Scholar 

  • Clow KA, Short CE, Driedzic WR (2016) Extracellular glucose supports lactate production but not aerobic metabolism in cardiomyocytes from both normoglycemic Atlantic cod (Gadus morhua) and low glycemic short-horned sculpin (Myoxocephalus scorpius). J Exp Biol 1:jeb. 132720

    Article  Google Scholar 

  • Comoglio L, Gaxiola G, Roque A, Cuzon G, Amin O (2004) The effect of starvation on refeeding, digestive enzyme activity, oxygen consumption, and ammonia excretion in juvenile white shrimp Litopenaeus vannamei. J Shellf Res 23(1):243–249

    Google Scholar 

  • Crear B, Forteath G (2000) The effect of extrinsic and intrinsic factors on oxygen consumption by the southern rock lobster, Jasus edwardsii. J Exp Mar Biol Ecol 252(1):129–147

    Article  CAS  Google Scholar 

  • Curtis DL, Vanier CH, McGaw IJ (2010) The effects of starvation and acute low salinity exposure on food intake in the Dungeness crab, Cancer magister. Mar Biol 157(3):603–612. https://doi.org/10.1007/s00227-009-1345-4

    Article  Google Scholar 

  • da Silva-Castiglioni D, Oliveira GT, Buckup L (2011) Metabolic responses in two species of crayfish (Parastacus defossus and Parastacus brasiliensis) to post-hypoxia recovery. Comp Biochem Physiol A Mol Integr Physiol 159(3):332–338. https://doi.org/10.1016/j.cbpa.2011.03.030

    Article  CAS  Google Scholar 

  • DeFur PL, Mangum CP, Reese JE (1990) Respiratory responses of the blue crab Callinectes sapidus to long-term hypoxia. Biol Bull 178(1):46–54. https://doi.org/10.2307/1541536

    Article  CAS  Google Scholar 

  • Depledge M (1985) The influence of nutritional state on the circulatory and respiratory physiology of the shore crab, Carcinus maenas. J Mar Biol Assoc UK 65(1):69–78

    Article  Google Scholar 

  • DFO (2014) Rock crab, Cancer irroratus, fishery and stock status in the Southern Gulf of St. Lawrence: LFA 23, 24, 25, 26A and 26B. DFO Canadian Science Advisory Secretariat Research Document 2014/032

  • Diaz RJ, Rosenberg R (1995) Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanogr Mar Biol Annu Rev 33:245–203

    Google Scholar 

  • Fraser KPP, Rogers AD (2007) Protein metabolism in marine animals: the underlying mechanism of growth. Adv Mar Biol 52:267–362. https://doi.org/10.1016/S0065-2881(06)52003-6

    Article  Google Scholar 

  • Gäde G (1983) Energy metabolism of arthropods and mollusks during environmental and functional anaerobiosis. J Exp Zool 228(3):415–429

    Article  Google Scholar 

  • Galic N, Hawkins T, Forbes VE (2019) Adverse impacts of hypoxia on aquatic invertebrates: a meta-analysis. Sci Total Environ 652:736–743. https://doi.org/10.1016/j.scitotenv.2018.10.225

    Article  CAS  Google Scholar 

  • Gendron L, Fradette P, Godbout G (2001) The importance of rock crab (Cancer irroratus) for growth, condition and ovary development of adult American lobster (Homarus americanus). J Exp Mar Biol Ecol 262(2):221–241. https://doi.org/10.1016/S0022-0981(01)00297-0

    Article  CAS  Google Scholar 

  • Gilbert D, Sundby B, Gobeil C, Mucci A, Tremblay G-H (2005) A seventy-two-year record of diminishing deep-water oxygen in the St. Lawrence estuary: the northwest Atlantic connection. Limnol Oceanogr 50(5):1654–1666. https://doi.org/10.4319/lo.2005.50.5.1654

    Article  CAS  Google Scholar 

  • Gilbert D, Rabalais N, Diaz R, Zhang J (2010) Evidence for greater oxygen decline rates in the coastal ocean than in the open ocean. Biogeosciences 7(7):2283–2296

    Article  CAS  Google Scholar 

  • Giomi F, Beltramini M (2007) The molecular heterogeneity of hemocyanin: its role in the adaptive plasticity of Crustacea. Gene 398(1):192–201. https://doi.org/10.1016/j.gene.2007.02.039

    Article  CAS  Google Scholar 

  • Gíslason Ó, Halldórsson H, Pálsson M, Pálsson S, Davíðsdóttir B, Svavarsson J (2014) Invasion of the Atlantic rock crab (Cancer irroratus) at high latitudes. Biol Invas 16(9):1865–1877. https://doi.org/10.1007/s10530-013-0632-7

    Article  Google Scholar 

  • Haefner PA Jr (1976) Distribution, reproduction and moulting of the rock crab, Cancer irroratus Say, 1917, in the mid-Atlantic Bight. J Nat Hist 10(4):377–397

    Article  Google Scholar 

  • Hagerman L (1983) Haemocyanin concentration of juvenile lobsters (Homarus gammarus) in relation to moulting cycle and feeding conditions. Mar Biol 77(1):11–17

    Article  CAS  Google Scholar 

  • Hagerman L (1986) Haemocyanin concentration in the shrimp Crangon crangon (L.) after exposure to moderate hypoxia. Comp Biochem Physiol A Physiol 85(4):721–724. https://doi.org/10.1016/0300-9629(86)90283-5

    Article  Google Scholar 

  • Harcet M, Perina D, Pleše B (2013) Opine dehydrogenases in marine invertebrates. Biochem Genet 51(9):666–676

    Article  CAS  Google Scholar 

  • Herreid CF (1980) Hypoxia in invertebrates. Comp Biochem Physiol A Physiol 67(3):311–320. https://doi.org/10.1016/S0300-9629(80)80002-8

    Article  Google Scholar 

  • Hochachka P (1986) Defense strategies against hypoxia and hypothermia. Science 231(4735):234–241

    Article  CAS  Google Scholar 

  • Hochachka PW, Mommsen TP (1983) Protons and anaerobiosis. Science 219(4591):1391–1397

    Article  CAS  Google Scholar 

  • Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, Oxford

    Google Scholar 

  • Hochachka P, Buck L, Doll C, Land S (1996) Unifying theory of hypoxia tolerance: molecular/metabolic defense and rescue mechanisms for surviving oxygen lack. Proc Natl Acad Sci 93(18):9493–9498

    Article  CAS  Google Scholar 

  • Hudon C, Lamarche G (1989) Niche segregation between American lobster Homarus americanus and rock crab Cancer irroratus. Mar Ecol Prog Ser 52(2):155–168

    Article  Google Scholar 

  • Jiang Q, McGaw JI (2022) Effects of food deprivation state on feeding behavior and gastric evacuation of rock crabs, Cancer irroratus, during hypoxia. Mar Freshw Behav Physiol. https://doi.org/10.1080/10236244.2022.2089570

    Article  Google Scholar 

  • Jiang Q (2022) Effects of food deprivation states on behavioral and physiological responses to hypoxia in rock crabs (Cancer irroratus). Dissertation, Memorial University of Newfoundland

  • Johnson NG, Burnett LE, Burnett KG (2011) Properties of bacteria that trigger hemocytopenia in the Atlantic blue crab, Callinectes sapidus. Biol Bull 221(2):164–175

    Article  CAS  Google Scholar 

  • Kalra B, Tamang AM, Parkash R (2017) Cross-tolerance effects due to adult heat hardening, desiccation and starvation acclimation of tropical drosophilid-Zaprionus indianus. Comp Biochem Physiol A Mol Integr Physiol 209:65–73

    Article  CAS  Google Scholar 

  • Keeling RF, Körtzinger A, Gruber N (2010) Ocean deoxygenation in a warming world. Ann Rev Mar Sci 2(1):199–229. https://doi.org/10.1146/annurev.marine.010908.163855

    Article  Google Scholar 

  • Kooijman SALM (2010) Dynamic energy budget theory for metabolic organisation. Cambridge University Press, Cambridge

    Google Scholar 

  • Lallier F, Truchot JP (1989) Hemolymph oxygen transport during environmental hypoxia in the shore crab, Carcinus maenas. Respir Physiol 77(3):323–336

    Article  CAS  Google Scholar 

  • Legeay A, Massabuau J-C (1999) Blood oxygen requirements in resting crab (Carcinus maenas) 24 h after feeding. Can J Zool 77(5):784–794

    Article  Google Scholar 

  • Lehtonen MP, Burnett LE (2016) Effects of hypoxia and hypercapnic hypoxia on oxygen transport and acid–base status in the Atlantic blue crab, Callinectes sapidus, during exercise. J Exp Zool A Ecol Genet Physiol 325(9):598–609. https://doi.org/10.1002/jez.2054

    Article  CAS  Google Scholar 

  • Levin L, Ekau W, Gooday A, Jorissen F, Middelburg J, Naqvi S, Neira C, Rabalais N, Zhang J (2009) Effects of natural and human-induced hypoxia on coastal benthos

  • Lignot J-H, Helmstetter C, Secor SM (2005) Postprandial morphological response of the intestinal epithelium of the Burmese python (Python molurus). Comp Biochem Physiol A Mol Integr Physiol 141(3):280–291

    Article  Google Scholar 

  • Mangum CP (1994) Subunit composition of hemocyanins of Callinectes sapidus: phenotypes from naturally hypoxic waters and isolated oligomers. Comp Biochem Physiol B Comp Biochem 108(4):537–541

    Article  CAS  Google Scholar 

  • Mangum C, Weiland A (1975) The function of hemocyanin in respiration of the blue crab Callinectes sapidus. J Exp Zool 193(3):257–263

    Article  CAS  Google Scholar 

  • Marshall DJ, Bode M, White CR (2013) Estimating physiological tolerances—a comparison of traditional approaches to nonlinear regression techniques. J Exp Biol 216(12):2176–2182

    Google Scholar 

  • Matozzo V, Gallo C, Marin MG (2011) Can starvation influence cellular and biochemical parameters in the crab Carcinus aestuarii? Mar Environ Res 71(3):207–212. https://doi.org/10.1016/j.marenvres.2011.01.004

    Article  CAS  Google Scholar 

  • McCue M (2006) Specific dynamic action: a century of investigation. Comp Biochem Physiol A Mol Integr Physiol 144(4):381–394

    Article  CAS  Google Scholar 

  • McCue MD (2007) Snakes survive starvation by employing supply-and demand-side economic strategies. Zoology 110(4):318–327

    Article  Google Scholar 

  • McCue MD (2010) Starvation physiology: reviewing the different strategies animals use to survive a common challenge. Comp Biochem Physiol A Mol Integr Physiol 156(1):1–18

    Article  Google Scholar 

  • McGaw IJ (2005) Does feeding limit cardiovascular modulation in the Dungeness crab Cancer magister during hypoxia? J Exp Biol 208(1):83–91. https://doi.org/10.1242/jeb.01309

    Article  Google Scholar 

  • McGaw IJ (2008) Gastric processing in the Dungeness crab, Cancer magister, during hypoxia. Comp Biochem Physiol A Mol Integr Physiol 150(4):458–463. https://doi.org/10.1016/j.cbpa.2008.05.007

    Article  CAS  Google Scholar 

  • McGaw IJ, Curtis DL (2013) A review of gastric processing in decapod crustaceans. J Comp Physiol B 183(4):443–465. https://doi.org/10.1007/s00360-012-0730-3

    Article  Google Scholar 

  • McGaw IJ, Van Leeuwen TE (2017) Metabolic costs of the mechanical components of the apparent specific dynamic action in the Dungeness crab, Cancer magister. Comp Biochem Physiol A Mol Integr Physiol 210:22–27. https://doi.org/10.1016/j.cbpa.2017.05.006

    Article  CAS  Google Scholar 

  • McGaw IJ, Curtis D, Ede J, Ong K, van Breukelen F, Goss G (2009) Physiological responses of postprandial red rock crabs (Cancer productus) during emersion. Can J Zool 87(12):1158–1169

    Article  CAS  Google Scholar 

  • McMahon BR (2001) Respiratory and circulatory compensation to hypoxia in crustaceans. Respir Physiol 128(3):349–364. https://doi.org/10.1016/S0034-5687(01)00311-5

    Article  CAS  Google Scholar 

  • McMahon B, Hankinson J (1993) Respiratory adaptations of burrowing crayfish. Freshw Crayfish 9(1):174–182

    Google Scholar 

  • Mente E, Legeay A, Houlihan DF, Massabuau J-C (2003) Influence of oxygen partial pressures on protein synthesis in feeding crabs. Am J Physiol Regul Integr Comp Physiol 284(2):R500–R510. https://doi.org/10.1152/ajpregu.00193.2002

    Article  CAS  Google Scholar 

  • Moreira CFDA (2015) Comparing the response of the brown shrimp Crangon crangon (Linnaeus, 1758) to prolonged deprivation of food in two seasons. J Shellf Res 34(2):521–529

    Article  Google Scholar 

  • Mueller CA, Seymour RS (2011) The regulation index: a new method for assessing the relationship between oxygen consumption and environmental oxygen. Physiol Biochem Zool 84(5):522–532. https://doi.org/10.1086/661953

    Article  Google Scholar 

  • Muhlia-Almazan A, Garcı́a-Carreño FL (2002) Influence of molting and starvation on the synthesis of proteolytic enzymes in the midgut gland of the white shrimp Penaeus vannamei. Comp Biochem Physiol B Biochem Mol Biol 133(3):383–394

    Article  Google Scholar 

  • Nickerson KW, Van Holde KE (1971) A comparison of molluscan and arthropod hemocyanin—I Circular dichroism and absorption spectra. Comp Biochem Physiol B Comp Biochem 39(4):855–872. https://doi.org/10.1016/0305-0491(71)90109-X

    Article  CAS  Google Scholar 

  • Ocampo L, Patiño D, Ramı́rez C (2003) Effect of temperature on hemolymph lactate and glucose concentrations in spiny lobster Panulirus interruptus during progressive hypoxia. J Exp Mar Biol Ecol 296(1):71–77

    Article  CAS  Google Scholar 

  • Penney CM, Patton RL, Whiteley NM, Driedzic WR, McGaw IJ (2016) Physiological responses to digestion in low salinity in the crabs Carcinus maenas and Cancer irroratus. Comp Biochem Physiol A Mol Integr Physiol 191:127–139. https://doi.org/10.1016/j.cbpa.2015.10.007

    Article  CAS  Google Scholar 

  • Piersma T, Lindström Å (1997) Rapid reversible changes in organ size as a component of adaptive behaviour. Trends Ecol Evol 12(4):134–138

    Article  CAS  Google Scholar 

  • Pörtner HO, Grieshaber M (1993) Critical PO2 (s) in oxyconforming and oxyregulating animals gas exchange, metabolic rate and the mode of energy production. In: Bicudo J (ed) The vertebrate gas transport cascade adaptations to environment and mode of life. CRC Press, London, pp 330–357

    Google Scholar 

  • Regnault M (1981) Respiration and ammonia excretion of the shrimp Crangon crangon L.: metabolic response to prolonged starvation. J Comp Physiol 141(4):549–555. https://doi.org/10.1007/bf01101478

    Article  CAS  Google Scholar 

  • Rich P (2003) The molecular machinery of Keilin’s respiratory chain. Biochem Soc Trans 31(6):1095–1105

    Article  CAS  Google Scholar 

  • Sacristán HJ, Rodríguez YE, De los Angeles Pereira N, López Greco LS, Lovrich GA, Fernández Gimenez AV (2017) Energy reserves mobilization: strategies of three decapod species. PLoS One 12(9):e0184060. https://doi.org/10.1371/journal.pone.0184060

    Article  CAS  Google Scholar 

  • Sánchez-Paz A, Garcıa-Carreno F, Muhlia-Almazán A, Hernández-Saavedra NY, Yepiz-Plascencia G (2003) Differential expression of trypsin mRNA in the white shrimp (Penaeus vannamei) midgut gland under starvation conditions. J Exp Mar Biol Ecol 292(1):1–17

    Article  Google Scholar 

  • Sánchez-Paz A, García-Carreño F, Muhlia-Almazán A, Peregrino-Uriarte AB, Hernández-López J, Yepiz-Plascencia G (2006) Usage of energy reserves in crustaceans during starvation: status and future directions. Insect Biochem Mol Biol 36(4):241–249. https://doi.org/10.1016/j.ibmb.2006.01.002

    Article  CAS  Google Scholar 

  • Sánchez-Paz A, García-Carreño F, Hernández-López J, Muhlia-Almazán A, Yepiz-Plascencia G (2007) Effect of short-term starvation on hepatopancreas and plasma energy reserves of the Pacific white shrimp (Litopenaeus vannamei). J Exp Mar Biol Ecol 340(2):184–193. https://doi.org/10.1016/j.jembe.2006.09.006

    Article  CAS  Google Scholar 

  • Sato M, Takeuchi M, Kanno N, Nagahisa E, Sato Y (1993) Distribution of opine dehydrogenases and lactate dehydrogenase activities in marine animals. Comp Biochem Physiol B 106(4):955–960

    Article  Google Scholar 

  • Schmidtko S, Stramma L, Visbeck M (2017) Decline in global oceanic oxygen content during the past five decades. Nature 542:335. https://doi.org/10.1038/nature21399

    Article  CAS  Google Scholar 

  • Schmidt-Rohr K (2020) Oxygen is the high-energy molecule powering complex multicellular life: fundamental corrections to traditional bioenergetics. ACS Omega 5(5):2221–2233

    Article  CAS  Google Scholar 

  • Secor S (2009) Specific dynamic action: a review of the postprandial metabolic response. J Comp Physiol B 179(1):1–56. https://doi.org/10.1007/s00360-008-0283-7

    Article  Google Scholar 

  • Secor SM, Diamond JM (2000) Evolution of regulatory responses to feeding in snakes. Physiol Biochem Zool 73(2):123–141

    Article  CAS  Google Scholar 

  • Secor SM, Stein ED, Diamond J (1994) Rapid upregulation of snake intestine in response to feeding: a new model of intestinal adaptation. Am J Physiol Gastrointest Liver Physiol 266(4):G695–G705

    Article  CAS  Google Scholar 

  • Seibel BA (2011) Critical oxygen levels and metabolic suppression in oceanic oxygen minimum zones. J Exp Biol 214(2):326–336. https://doi.org/10.1242/jeb.049171

    Article  CAS  Google Scholar 

  • Seibel BA, Andres A, Birk MA, Burns AL, Shaw CT, Timpe AW, Welsh CJ (2021) Oxygen supply capacity breathes new life into critical oxygen partial pressure (Pcrit). J Exp Biol 224(8):jeb242210

    Article  Google Scholar 

  • Senkbeil EG, Wriston JC (1981a) Hemocyanin synthesis in the American lobster, Homarus americanus. Comp Biochem Physiol Part B Comp Biochem 68(1):163–171. https://doi.org/10.1016/0305-0491(81)90198-X

    Article  Google Scholar 

  • Senkbeil EG, Wriston JC (1981b) Hemocyanin synthesis in the American lobster, Homarus americanus. Comp Biochem Physiol B Comp Biochem 68(1):163–171. https://doi.org/10.1016/0305-0491(81)90198-X

    Article  Google Scholar 

  • Silva-Castiglioni D, Valgas AAN, Machado ID, Freitas BS, Oliveira GT (2016) Effect of different starvation and refeeding periods on macromolecules in the haemolymph, digestive parameters, and reproductive state in Aegla platensis (Crustacea, Decapoda, Aeglidae). Mar Freshw Behav Physiol 49(1):27–45. https://doi.org/10.1080/10236244.2015.1099205

    Article  CAS  Google Scholar 

  • Simon CJ, Fitzgibbon QP, Battison A, Carter CG, Battaglene SC (2015) Bioenergetics of nutrient reserves and metabolism in spiny lobster juveniles Sagmariasus verreauxi: predicting nutritional condition from hemolymph biochemistry. Physiol Biochem Zool 88(3):266–283. https://doi.org/10.1086/681000

    Article  CAS  Google Scholar 

  • Sokolova IM, Frederich M, Bagwe R, Lannig G, Sukhotin AA (2012) Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates. Mar Environ Res 79:1–15. https://doi.org/10.1016/j.marenvres.2012.04.003

    Article  CAS  Google Scholar 

  • Spicer JI (2014) What can an ecophysiological approach tell us about the physiological responses of marine invertebrates to hypoxia? J Exp Biol 217(1):46–56. https://doi.org/10.1242/jeb.090365

    Article  Google Scholar 

  • Spicer JI, Dando CL, Maltby L (2002) Anaerobic capacity of a crustacean sensitive to low environmental oxygen tensions, the freshwater amphipod Gammarus pulex (L.). Hydrobiologia 477(1–3):189–194

    Article  Google Scholar 

  • Staples JF, Buck LT (2009) Matching cellular metabolic supply and demand in energy-stressed animals. Comp Biochem Physiol A Mol Integr Physiol 153(2):95–105. https://doi.org/10.1016/j.cbpa.2009.02.010

    Article  CAS  Google Scholar 

  • Steinberg CE (2012) One stressor prepares for the next one to come: cross-tolerance. Stress ecology. Springer, Berlin, pp 311–325

    Chapter  Google Scholar 

  • Storey KB (2015) Regulation of hypometabolism: insights into epigenetic controls. J Exp Biol 218(1):150–159. https://doi.org/10.1242/jeb.106369

    Article  Google Scholar 

  • Taylor AC (1976) The respiratory responses of Carcinus maenas to declining oxygen tension. J Exp Biol 65(2):309–322

    Article  CAS  Google Scholar 

  • Taylor EW, Butler PJ, Al-Wassia A (1977) The effect of a decrease in salinity on respiration, osmoregulation and activity in the shore crab, Carcinus maenas (L.) at different acclimation temperatures. J Comp Physiol 119(2):155–170. https://doi.org/10.1007/bf00686563

    Article  CAS  Google Scholar 

  • Team RC (2018) R: a language and environment for statistical computing. R foundation for statistical computing, Austria, 2015. ISBN 3-900051-07-0. http://www.R-project.org

  • Terwilliger NB (2015) Oxygen transport proteins in Crustacea: hemocyanin and hemoglobin. In: Chang ESMT (ed) The natural history of the crustacea, vol 4: physiology. Oxford University Press, New York, pp 359–390

    Google Scholar 

  • Terwilliger NB, Brown AC (1993) Ontogeny of hemocyanin function in the Dungeness crab Cancer magister: the interactive effects of developmental stage and divalent cations on hemocyanin oxygenation properties. J Exp Biol 183(1):1–13

    Article  CAS  Google Scholar 

  • Tommerdahl AP, Burnett KG, Burnett LE (2015) Respiratory properties of hemocyanin from wild and aquacultured penaeid shrimp and the effects of chronic exposure to hypoxia. Biol Bull 228(3):242–252

    Article  CAS  Google Scholar 

  • Truchot JP (1992) Respiratory function of Arthropod hemocyanins. In: Mangum CP (ed) Blood and tissue oxygen carriers. Springer, Berlin, pp 377–410. https://doi.org/10.1007/978-3-642-76418-9_13

    Chapter  Google Scholar 

  • Vaquer-Sunyer R, Duarte CM (2008) Thresholds of hypoxia for marine biodiversity. Proc Natl Acad Sci 105(40):15452–15457. https://doi.org/10.1073/pnas.0803833105

    Article  Google Scholar 

  • Wallace JC (1973) Feeding, starvation and metabolic rate in the shore crab Carcinus maenas. Mar Biol 20(4):277–281. https://doi.org/10.1007/BF00354271

    Article  Google Scholar 

  • Wang T, Hung CCY, Randall DJ (2006) The comparative physiology of food deprivation: from feast to famine. Annu Rev Physiol 68(1):223–251. https://doi.org/10.1146/annurev.physiol.68.040104.105739

    Article  CAS  Google Scholar 

  • Wang S, Fitzgibbon QP, Carter CG, Smith GG (2019) Effect of protein synthesis inhibitor cycloheximide on starvation, fasting and feeding oxygen consumption in juvenile spiny lobster Sagmariasus verreauxi. J Comp Physiol B 189(3):351–365. https://doi.org/10.1007/s00360-019-01221-z

    Article  CAS  Google Scholar 

  • Watson AJ (2016) Oceans on the edge of anoxia. Science 354(6319):1529–1530. https://doi.org/10.1126/science.aaj2321

    Article  CAS  Google Scholar 

  • Wei L, Li Y, Qiu L, Zhou H, Han Q, Diao X (2016) Comparative studies of hemolymph physiology response and HIF-1 expression in different strains of Litopenaeus vannamei under acute hypoxia. Chemosphere 153:198–204. https://doi.org/10.1016/j.chemosphere.2016.03.064

    Article  CAS  Google Scholar 

  • Weissgerber TL, Milic NM, Winham SJ, Garovic VD (2015) Beyond bar and line graphs: time for a new data presentation paradigm. PLoS Biol 13(4):e1002128

    Article  Google Scholar 

  • Whiteley N, Robertson R, Meagor J, El Haj A, Taylor E (2001) Protein synthesis and specific dynamic action in crustaceans: effects of temperature. Comp Biochem Physiol A Mol Integr Physiol 128(3):593–604

    Article  Google Scholar 

  • Wilkes PRH, McMahon BR (1982) Effect of maintained hypoxic exposure on the crayfish Orconectes rusticus: I. Ventilatory, acid-base and cardiovascular adjustments. J Exp Biol 98(1):119–137

    Article  CAS  Google Scholar 

  • Wishner KF, Seibel BA, Roman C, Deutsch C, Outram D, Shaw CT, Birk MA, Mislan KAS, Adams TJ, Moore D, Riley S (2018) Ocean deoxygenation and zooplankton: very small oxygen differences matter. Sci Adv 4(12):eaau5180. https://doi.org/10.1126/sciadv.aau5180

    Article  CAS  Google Scholar 

  • Włodarczyk A, Sonakowska L, Kamińska K, Marchewka A, Wilczek G, Wilczek P, Student S, Rost-Roszkowska M (2017) The effect of starvation and re-feeding on mitochondrial potential in the midgut of Neocaridina davidi (Crustacea, Malacostraca). PLoS One 12(3):e0173563

    Article  Google Scholar 

  • Wood CM (2018) The fallacy of the Pcrit— are there more useful alternatives? J Exp Biol 221(22):jeb163717. https://doi.org/10.1242/jeb.163717

    Article  Google Scholar 

  • Yaikin J, Quiñones R, González R (2002) Aerobic respiration rate and anaerobic enzymatic activity of Petrolisthes laevigatus (Anomura, Porcellanidae) under laboratory conditions. J Crust Biol 22(2):345–352

    Article  Google Scholar 

  • Yannicelli B, Paschke K, González RR, Castro LR (2013) Metabolic responses of the squat lobster (Pleuroncodes monodon) larvae to low oxygen concentration. Mar Biol 160(4):961–976. https://doi.org/10.1007/s00227-012-2147-7

    Article  CAS  Google Scholar 

  • Zeis B, Nies A, Bridges CR, Grieshaber MK (1992) Allosteric modulation of haemocyanin oxygen-affinity by L-lactate and urate in the lobster Homarus vulgaris: I specific and additive effects on haemocyanin oxygen-affinity. J Exp Biol 168(1):93–110

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by a Natural Sciences and Engineering Council Discovery Grant to IJM (#207112) and a Grant of Mitacs Accelerate (IT26355) and China Scholarship Council (201404910484) to QJ. We also thank Roy Murphy for his help with collections of rock crab.

Author information

Authors and Affiliations

  1. Department of Ocean Sciences, Memorial University, 0 Marine Lab Road, St. John’s, NL, A1C 5S7, Canada

    Qiwu Jiang & Iain J. McGaw

Authors
  1. Qiwu Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Iain J. McGaw
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Qiwu Jiang.

Ethics declarations

Conflict of interest

QJ and IJM have no competing interests declared.

Additional information

Communicated by B. Pelster.

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 183 KB)

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

Jiang, Q., McGaw, I.J. Interactive effects of food deprivation state and hypoxia on the respiratory responses of postprandial rock crabs, Cancer irroratus. J Comp Physiol B 193, 37–55 (2023). https://doi.org/10.1007/s00360-022-01462-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-022-01462-5

Keywords

Search

Navigation