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Journal of Comparative Physiology B

, Volume 188, Issue 4, pp 591–598 | Cite as

Mass scaling of the resting and maximum metabolic rates of the black carp

  • Xiao Lv
  • Hang Xie
  • Danyang Xia
  • Cong Shen
  • Jian Li
  • Yiping Luo
Original Paper

Abstract

We investigated the body mass (M) scaling of resting metabolic rate (RMR), maximum metabolic rate (MMR), excess post-exercise oxygen consumption (EPOC), blood parameters, and organ masses of black carp (Mylopharyngoden piceus). The results showed that RMR scaled with M of the fish by an exponent (b) of 0.833 (bR), which was significantly larger than 0.75. MMR scaled with M by a power of 0.775 (bM), which was significantly lower than 1 and may be due to a small size proportion of red muscle. No difference between bR and bM or correlation between factorial aerobic scope and M was found. However, EPOC scaled positively with M by a power of 1.231, suggesting a constant aerobic capacity and an enhanced anaerobic capacity with fish growth. Mass of the inactive organs scaled with M by a power of 1.005, which was significantly larger than 1 and was negatively correlated with RMR, suggesting that the proportion of inactive organs increases with fish growth, which may contribute to the negative scaling of RMR. Red blood cell surface area (S) did not increase with increasing M, suggesting that the ontogenetic decrease in the surface area to volume ratio of cells may not contribute to the negative scaling of RMR. The predicted bR value (0.846) by the average S (1.746 µm²) differs by only 1.62% from the observed bR value using our previously reported S − bR function in carp, suggesting that the species-specific cell size, rather than its ontogenetic change, affects the metabolic scaling of a species.

Keyword

Oxygen consumption Allometry Body size Metabolic level Surface area 

Abbreviations

M

Body mass

MR

Metabolic rate

RMR

Resting metabolic rate

MMR

Maximum metabolic rate

FAS

Factorial aerobic scope

EPOC

Excess post-exercise oxygen consumption

b

Scaling exponent

bR

Scaling exponent of RMR

bM

Scaling exponent of MMR

\({{M}_{{{\text{O}}_2}}}\)

Oxygen consumption rate

Hb

Hemoglobin concentration

RBCC

Red blood cell count

S

Red blood cell surface area

MActive organs

Total mass of active organs

MInactive organs

Total mass of inactive organs

Notes

Acknowledgements

This work was supported by the National Natural Science Foundation of China (no. 31672287) and the Start-up Research Grant from Qinzhou University (no. 2017KYQD107). We thank Mr. Bo Zhang for his help in fish collection and thank the anonymous reviewers for their comments on the manuscript.

Supplementary material

360_2018_1154_MOESM1_ESM.xls (22 kb)
Supplementary material 1 ESM_1. Datasets generated and analyzed in this study (XLS 21 KB)
360_2018_1154_MOESM2_ESM.doc (26 kb)
Supplementary material 2 ESM_2. Relationship between the body mass (M, g) and factorial aerobic scope (FAS) (DOC 26 KB)
360_2018_1154_MOESM3_ESM.doc (33 kb)
Supplementary material 3 ESM_3. Relationship between the body mass (M, g) and several hematological parameters in the black carp. A: red blood cell surface area, S (μm2); B: red blood cell count, RBCC (109 mL-1); C: hematological concentration, Hb (mg mL-1) (DOC 33 KB)
360_2018_1154_MOESM4_ESM.doc (26 kb)
Supplementary material 4 (DOC 25 KB)

References

  1. Auer SK, Killen SS, Rezende EL (2017) Resting vs. active: a meta-analysis of the intra- and inter-specific associations between minimum, sustained, and maximum metabolic rates in vertebrates. Funct Ecol 31:1728–1738CrossRefPubMedPubMedCentralGoogle Scholar
  2. Beamish FWH (1978) Swimming capacity. In: Hoar WS, Randall DJ (eds) Fish physiology, vol VII. Academic Press, LondonGoogle Scholar
  3. Bokma F (2004) Evidence against universal metabolic allometry. Funct Ecol 18:184–187CrossRefGoogle Scholar
  4. Brett JR (1965) The relation of size to rate of oxygen consumption and sustained swimming speed of sockeye salmon (Oncorhynchus nerka). J Fish Res Board Can 22:1491–1501CrossRefGoogle Scholar
  5. Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789CrossRefGoogle Scholar
  6. Clarke A, Johnston NM (1999) Scaling of metabolic rate with body mass and temperature in teleost fish. J Anim Ecol 68:893–905CrossRefGoogle Scholar
  7. Davison J (1955) Body weight, cell surface and metabolic rate in anuran Amphibia. Biol Bull 109:407–419CrossRefGoogle Scholar
  8. Gao ZX, Wang WM, Abbas K, Zhou XY, Yang Y, Diana JS, Wang HP, Wang HL, Li Y, Sun YH (2007) Haematological characterization of loach Misgurnus anguillicaudatus: comparison among diploid, triploid and tetraploid specimens. Comp Biochem Physiol A 147:1001–1008CrossRefGoogle Scholar
  9. Glazier DS (2005) Beyond the ‘3/4-power law’: variation in the intra- and interspecific scaling of metabolic rate in animals. Biol Rev 80:611–662CrossRefPubMedGoogle Scholar
  10. Glazier DS (2009) Activity affects intraspecific body-size scaling of metabolic rate in ectothermic animals. J Comp Physiol B 179:821–828CrossRefPubMedGoogle Scholar
  11. Glazier DS (2010) A unifying explanation for diverse metabolic scaling in animals and plants. Biol Rev 85:111–138CrossRefPubMedGoogle Scholar
  12. Glazier DS (2014a) Metabolic scaling in complex living systems. Systems 2:451–540CrossRefGoogle Scholar
  13. Glazier DS (2014b) Scaling of metabolic scaling within physical limits. Systems 2:425–450CrossRefGoogle Scholar
  14. Huang QD, Zhang YR, Liu ST, Wang W, Luo YP (2013) Intraspecific scaling of the resting and maximum metabolic rates of the crucian carp (Carassius auratus). PLoS One 8:e82837CrossRefPubMedPubMedCentralGoogle Scholar
  15. Itazawa Y, Oikawa S (1983) Metabolic rates in excised tissues of carp. Experientia 39:160–161CrossRefGoogle Scholar
  16. Killen SS, Costa I, Brown JA, Gamperl AK (2007) Little left in the tank: metabolic scaling in marine teleosts and its implications for aerobic scope. Proc R Soc B 274:431–438CrossRefPubMedGoogle Scholar
  17. Killen SS, Atkinson D, Glazier DS (2010) The intraspecific scaling of metabolic rate with body mass in fishes depends on lifestyle and temperature. Ecol Lett 13:184–193CrossRefPubMedGoogle Scholar
  18. Killen SS, Glazier DS, Rezende EL, Clark TD, Atkinson D, Willener AS, Halsey LG (2016) Ecological influences and morphological correlates of resting and maximal metabolic rates across teleost fish species. Am Nat 187:592–606CrossRefPubMedGoogle Scholar
  19. Kozłowski J, Konarzewski M, Gawelczyk AT (2003) Cell size as a link between noncoding DNA and metabolic rate scaling. Proc Natl Acad Sci USA 100:14080–14085CrossRefPubMedPubMedCentralGoogle Scholar
  20. Kozłowski J, Czarnołęski M, Françoiskrassowska A, Maciak S, Pis T (2010) Cell size is positively correlated between different tissues in passerine birds and amphibians, but not necessarily in mammals. Biol Lett 6(6):792–796CrossRefPubMedPubMedCentralGoogle Scholar
  21. Luo YP, He DC, Li G, Xie H, Zhang RY, Huang QD (2015) Intraspecific metabolic scaling exponent depends on red blood cell size in fishes. J Exp Biol 218(10):1496–1503CrossRefPubMedGoogle Scholar
  22. Maciak S, Janko K, Kotusz J, Choleva L, Boron A, Juchno D, Kujawa R, Kozłowski J, Konarzewski M (2011) Standard metabolic rate (SMR) is inversely related to erythrocyte and genome size in allopolyploid fish of Cobitis taenia hybrid complex. Funct Ecol 25:1072–1078CrossRefGoogle Scholar
  23. Norin T, Malte H (2012) Intraspecific variation in aerobic metabolic rate of fish: relations with organ size and enzyme activity in brown trout. Physiol Biochem Zool 85:645–656CrossRefPubMedGoogle Scholar
  24. Oikawa S, Takemori M, Itazawa Y (1992) Relative growth of organs and parts of a marine teleost, the porgy, Pagrus major, with special reference to metabolism size relationships. Jap J Ichthyol 39:243–249Google Scholar
  25. Pang X, Fu SJ, Zhang YG (2015) Individual variation in metabolism and swimming performance in juvenile black carp (Mylopharyngodon piceus) and the effects of hypoxia. Mar Freshw Behav Physiol 48(6):431–443CrossRefGoogle Scholar
  26. Pang X, Fu SJ, Li XM, Zhang YG (2016) The effects of starvation and re-feeding on growth and swimming performance of juvenile black carp (Mylopharyngodon piceus). Fish Physiol Biochem 42(4):1203CrossRefPubMedGoogle Scholar
  27. Rubner M (1883) Über den einfluss der körpergrösse auf stoff-und kraftwechsel. Zeit Biol 19:535–562Google Scholar
  28. Savage VM, Allen AP, Brown JH, Gillooly JF, Herman AB, Woodruff WH, West GB (2007) Scaling of number, size, and metabolic rate of cells with body size in mammals. Proc Natl Acad Sci USA 104:4718–4723CrossRefPubMedPubMedCentralGoogle Scholar
  29. Starostová Z, Konarzewski M, Kozłowski J, Kratochvĺl L (2013) Ontogeny of metabolic rate and red blood cell size in eyelid geckos: species follow different paths. PLoS One 8(5):e64715CrossRefPubMedPubMedCentralGoogle Scholar
  30. Wang QQ, Wang W, Huang QD, Zhang YR, Luo YP (2012) Effect of meal size on the specific dynamic action of the juvenile snakehead (Channa argus). Comp Biochem Physiol A 161:401–405CrossRefGoogle Scholar
  31. West GB, Brown JH, Enquist BJ (1997) A general model for the origin of allometric scaling laws in biology. Science 276:122–126CrossRefPubMedGoogle Scholar
  32. Wieser W (1985) Developmental and metabolic constraints of the scope for activity in young rainbow trout (Salmo gairdneri). J Exp Biol 118:133–142Google Scholar
  33. Yan GJ, He XK, Cao ZD, Fu SJ (2013) An interspecific comparison between morphology and swimming performance in cyprinids. J Evolution Biol 26:1802–1815CrossRefGoogle Scholar
  34. Zhang YR, Huang QD, Liu ST, He DC, Wei G, Luo YP (2014) Intraspecific mass scaling of metabolic rates in grass carp (Ctenopharyngodon idellus). J Comp Physiol B 184:347–354CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Key Laboratory of Freshwater Fish Reproduction and Development, Ministry of Education, School of Life SciencesSouthwest UniversityChongqingChina
  2. 2.Luzhou Agricultural BureauNational Nature Reserve of Rare and Endemic Fish in the Upper Yangtze River for Luzhou WorkstationLuzhouChina
  3. 3.Guangxi Key Laboratory of Beibu Gulf Marine Biodiversity Conservation, Ocean CollegeQinzhou UniversityQinzhouChina

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