Fish Physiology and Biochemistry

, Volume 43, Issue 6, pp 1531–1542 | Cite as

Metabolic, behavioral, and locomotive effects of feeding in five cyprinids with different habitat preferences

Article

Abstract

Fish generally perform routine swimming behaviors during food digestion; thus, changes in swimming performance and adjustments to spontaneous behavior resulting from digestion can have important ecological significance for wild fishes. The effects of feeding on metabolism, spontaneous activity, fast-start escape movement, and critical swimming speed (U crit) were investigated in five cyprinids with different habitat preferences, specifically the Chinese crucian carp (Carassius auratus), common carp (Cyprinus carpio), black carp (Mylopharyngodon piceus), Chinese bream (Parabramis pekinensis), and qingbo (Spinibarbus sinensis). Generally, species in still water exhibited increased feeding metabolism, whereas species in flowing water showed higher spontaneous activity and locomotion performance. Digestion had no significant effects on either spontaneous activity or fast-start escape movement in the five cyprinids. These results could be due to the small meal sizes (approximately 2% body mass) and active foraging modes of cyprinids. The changes in aerobic swimming performance due to feeding were more complex. No effect of digestion on U crit was observed in crucian carp (still water, high feeding metabolism, and low U crit), common carp (widely distributed, high feeding metabolism, and high U crit), and qingbo (flowing water, low feeding metabolism, and high U crit), but digestion resulted in a significant decrease in the U crit of Chinese bream (moderate feeding metabolism but high U crit) and black carp (moderate feeding metabolism and low U crit), suggesting no connection between postprandial U crit changes and feeding metabolism (or between U crit and preferred habitat). The maximum metabolic rate (MMR) of common carp and crucian carp increased after feeding, whereas the corresponding values for the other three cyprinids remained the same. The oxygen uptake capacity appears to meet the oxygen demand of both aerobic swimming and digestion in common carp and crucian carp, whereas qingbo sacrifices digestion for locomotion, and black carp and Chinese bream sacrifice locomotion for digestion under postprandial swimming conditions. The locomotion-priority mode of qingbo is adaptive to its active foraging mode in the demanding swimming habitat of rapidly flowing water, whereas the high respiratory capacities of postprandial crucian carp and common carp and hence the maintenance of their aerobic swimming performances might be a by-product of natural selection for hypoxia tolerance rather than for swimming speed.

Keywords

Competition Cyprinids Digestion Priority Swimming performance 

Notes

Acknowledgements

This study was funded by a grant from the National Science Foundation of China (NSFC 31670418).

Compliance with ethical standards

This study was approved by the Animal Care and Use Committee of the Key Laboratory of Animal Biology of Chongqing (permit number: Zhao-20140313-02) and performed in strict accordance with the recommendations in the Guide for the Care and Use of Animal at the Key Laboratory of Animal Biology of Chongqing, China.

References

  1. Alsop D, Wood C (1997) The interactive effects of feeding and exercise on oxygen consumption, swimming performance and protein usage in juvenile rainbow trout (Oncorhynchus mykiss). J Exp Biol 200:2337–2346PubMedGoogle Scholar
  2. Altimiras J, Claireaux G, Sandblom E, Farrell AP, McKenzie DJ, Axelsson M (2008) Gastrointestinal blood flow and postprandial metabolism in swimming sea bass Dicentrarchus labrax. Physiol Biochem Zool 81:663–672. doi: 10.1086/588488 CrossRefPubMedGoogle Scholar
  3. Asaeda T, Priyadarshana T, Manatunge J (2001) Effects of satiation on feeding and swimming behavior of planktivores. Hydrobiologia 443:147–157. doi: 10.1023/A:1017560524056 CrossRefGoogle Scholar
  4. Brauner CJ, Matey V, Zhang W, Richards JG, Dhillon R, Cao ZD, Wang Y, Fu SJ (2011) Gill remodeling in crucian carp during sustained exercise and the effect on subsequent swimming performance. Physiol Biochem Zool 84:535–542. doi: 10.1086/662664 CrossRefPubMedGoogle Scholar
  5. Brett JR (1964) The respiratory metabolism and swimming performance of young sockeye salmon. J Fish Res Bd Can 21:1183–1226. doi: 10.1139/f64-103 CrossRefGoogle Scholar
  6. Dan XM, Yan GJ, Zhang AJ, Cao ZD, Fu SJ (2014) Effects of stable and diel-cycling hypoxia on hypoxia tolerance, postprandial metabolic response, and growth performance in juvenile qingbo (Spinibarbus sinensis). Aquaculture 428–429:21–28. doi: 10.1016/j.aquaculture.2014.02.025 CrossRefGoogle Scholar
  7. Dhillon RS, Yao L, Matey V, Chen BJ, Zhang AJ, Cao ZD, Fu SJ, Brauner CJ, Wang YS, Richards JG (2013) Interspecific differences in hypoxia-induced gill remodeling in carp. Physiol Biochem Zool 86:727–739. doi: 10.1086/673180 CrossRefPubMedGoogle Scholar
  8. Domenici P, Blake R (1997) The kinematics and performance of fish fast-start swimming. J Exp Biol 200:1165–1178PubMedGoogle Scholar
  9. Fu S, Xie X, Cao Z (2005) Effect of dietary composition on specific dynamic action in southern catfish Silurus meridionalis Chen. Aquac Res 36:1384–1390. doi: 10.1111/j.1365-2109.2005.01356.x CrossRefGoogle Scholar
  10. Fu SJ, Cao ZD, Peng JL (2006) Effect of meal size on postprandial metabolic response in Chinese catfish (Silurus asotus Linnaeus). J Comp Physiol B 176:489–495. doi: 10.1007/s00360-006-0070-2 CrossRefPubMedGoogle Scholar
  11. Fu SJ, Fu C, Yan GJ, Cao ZD, Zhang AJ, Pang X (2014) Interspecific variation in hypoxia tolerance, swimming performance and plasticity in cyprinids that prefer different habitats. J Exp Biol 217:590–597. doi: 10.1242/jeb.089268 CrossRefPubMedGoogle Scholar
  12. Fu SJ, Zeng LQ, Li XM, Pang X, Cao ZD, Peng JL, Wang YX (2009) The behavioral, digestive and metabolic characteristics of fishes with different foraging strategies. J Exp Biol 212:2296–2302. doi: 10.1242/jeb.027102 CrossRefPubMedGoogle Scholar
  13. Gill AB, Hart PJB (1994) Feeding behavior and prey choice of the threespine stickleback: the interacting effects of prey size, fish size and stomach fullness. Anim Behav 47:921–932. doi: 10.1006/anbe.1994.1124 CrossRefGoogle Scholar
  14. Gill AB, Hart PJB (1996) Unequal competition between three-spined stickleback, Gasterosteus aculeatus, L., encountering sequential prey. Anim Behav 51:689–698CrossRefGoogle Scholar
  15. Gotanda KM, Reardon EE, Murphy SMC, Chapman LJ (2012) Critical swim speed and fast-start response in the African cichlid Pseudocrenilabrus multicolor victoriae: convergent performance in divergent oxygen regimes. Can J Zool 90:545–554. doi: 10.1139/z2012-019 CrossRefGoogle Scholar
  16. He XK, Cao ZD, Fu SJ (2011) Fast-start swimming performances of juvenile Cyprinus carpio and the effects of electrical stimulation parameters. Chinese J Ecol 30:2523–2527Google Scholar
  17. Jourdan-Pineau H, DuPont-Prinet A, Claireaux G, McKenzie DJ (2010) An investigation of metabolic prioritization in the European sea bass, Dicentrarchus labrax. Physiol Biochem Zool 83:68–77. doi: 10.1086/648485 CrossRefPubMedGoogle Scholar
  18. Kieffer JD (2010) Perspective—exercise in fish: 50+ years and going strong. Comp Biochem Physiol A Mol Integr Physiol 156:163–168. doi: 10.1016/j.cbpa.2010.02.009 CrossRefPubMedGoogle Scholar
  19. Killen SS, Marras S, Steffensen JF, McKenzie DJ (2012) Aerobic capacity influences the spatial position of individuals within fish schools. Proc Biol Sci 279:357–364. doi: 10.1098/rspb.2011.1006 CrossRefPubMedGoogle Scholar
  20. Lee CG, Farrell AP, Lotto A, MacNutt MJ, Hinch SG, Healey MC (2003) The effect of temperature on swimming performance and oxygen consumption in adult sockeye (Oncorhynchus nerka) and coho (O. kisutch) salmon stocks. J Exp Biol 206:3239–3251. doi: 10.1242/jeb.00547 CrossRefPubMedGoogle Scholar
  21. Lyon JP, Ryan TJ, Scroggie MP (2008) Effects of temperature on the fast-start swimming performance of an Australian freshwaterfish. Ecol Freshwat Fish 17:184–188. doi: 10.1111/j.1600-0633.2007.00244.x CrossRefGoogle Scholar
  22. Pang X, Cao ZD, Fu SJ (2011) The effects of temperature on metabolic interaction between digestion and locomotion in juveniles of three cyprinid fish, Carassius auratus, Cyprinus carpio and Spinibarbus sinensis. Comp Biochem Physiol A Mol Integr Physiol 159:253–260. doi: 10.1016/j.cbpa.2011.03.013 CrossRefPubMedGoogle Scholar
  23. Pang X, Fu SJ, Li XM, Zhang YG (2016a) The effects of starvation and re-feeding on growth and swimming performance of juvenile black carp (Mylopharyngodon piceus). Fish Physiol Biochem 42:1203–1212. doi: 10.1007/s10695-016-0210-x CrossRefPubMedGoogle Scholar
  24. Pang X, Fu SJ, Zhang YG (2016b) Acclimation temperature alters the relationship between growth and swimming performance among juvenile common carp (Cyprinus carpio). Comp Biochem Physiol A Mol Integr Physiol 199:111–119. doi: 10.1016/j.cbpa.2016.06.011 CrossRefPubMedGoogle Scholar
  25. Peng J, Cao ZD, Fu SJ (2014a) The effects of constant and diel-fluctuating temperature acclimation on the thermal tolerance, swimming capacity, specific dynamic action and growth performance of juvenile Chinese bream. Comp Biochem Physiol A Mol Integr Physiol 176:32–40. doi: 10.1016/j.cbpa.2014.07.005 CrossRefPubMedGoogle Scholar
  26. Peng J, Cao ZD, Fu SJ (2014b) Effects of temperature and digestion on the swimming performance of juvenile Chinese bream. Aquat Biol 21:183–189. doi: 10.3354/ab00584 CrossRefGoogle Scholar
  27. Penghan LY, Cao ZD, Fu SJ (2014) Effect of temperature and dissolved oxygen on swimming performance in crucian carp. Aquat Biol 21:57–65. doi: 10.3354/ab00571 CrossRefGoogle Scholar
  28. Plaut I (2001) Critical swimming speed: its ecological relevance. Comp Biochem Physiol A Mol Integr Physiol 131:41–50. doi: 10.1016/S1095-6433(01)00462-7 CrossRefPubMedGoogle Scholar
  29. Robinson CJ, Pitcher TJ (1989) The influence of hunger and ration level on shoal density, polarization and swimming speed of herring, Clupea harengus L. J Fish Biol 34:631–633. doi: 10.1111/j.1095-8649.1989.tb03341.x CrossRefGoogle Scholar
  30. Sims DW, Davies SJ (1994) Does specific dynamic action (SDA) regulate reture of appetitie in the lesser spotted dogfish, Scyliorhinus canicula? J Fish Biol 45:341–348Google Scholar
  31. Sollid J, De Angelis P, Gundersen K, Nilsson GE (2003) Hypoxia induces adaptive and reversible gross morphological changes in crucian carp gills. J Exp Biol 206:3667–3673. doi: 10.1242/jeb.00594 CrossRefPubMedGoogle Scholar
  32. Sollid J, Weber RE, Nilsson GE (2005) Temperature alters the respiratory surface area of crucian carp Carassius carassius and goldfish Carassius auratus. J Exp Biol 208:1109–1116. doi: 10.1242/jeb.01505 CrossRefPubMedGoogle Scholar
  33. Steffensen JF (1989) Some errors in respirometry of aquatic breathers: how to avoid and correct for them. Fish Physiol Biochem 6:49–59. doi: 10.1007/BF02995809 CrossRefPubMedGoogle Scholar
  34. Thorarensen H, Farrell AP (2006) Postprandial intestinal blood flow, metabolic rates, and exercise in Chinook salmon (Oncorhynchus tshawytscha). Physiol Biochem Zool 79:688–694. doi: 10.1086/505512 CrossRefPubMedGoogle Scholar
  35. Walker JA, Ghalambor CK, Griset OL, McKenney D, Reznick DN (2005) Do faster starts increase the probability of evading predators? Funct Ecol 19:808–815. doi: 10.1111/j.1365-2435.2005.01033.x CrossRefGoogle Scholar
  36. Wang Q, Wang W, Huang Q, Zhang Y, Luo Y (2012) Effect of meal size on the specific dynamic action of the juvenile snakehead (Channa argus). Comp Biochem Physiol A Mol Integr Physiol 161:401–405. doi: 10.1016/j.cbpa.2011.12.015 CrossRefPubMedGoogle Scholar
  37. Webb PW (1976) The effect of size on the fast-start performance of rainbow trout Salmo gairdneri, and a consideration of piscivorous predator-prey interactions. J Exp Biol 65:157–177PubMedGoogle Scholar
  38. Webb PW (1986) Effect of body form and response threshold on the vulnerability of four species of teleost prey attacked by largemouth bass (Micropterus salmoides). Can J Fish Aquat Sci 43:763–771. doi: 10.1139/f86-094 CrossRefGoogle Scholar
  39. Yan GJ, He XK, Cao ZD, Fu SJ (2015) Effects of fasting and feeding on the fast-start swimming performance of southern catfish Silurus meridionalis. J Fish Biol 86:605–614. doi: 10.1111/jfb.12595 CrossRefGoogle Scholar
  40. Zhang W, Cao ZD, Fu SJ (2012) The effects of dissolved oxygen levels on the metabolic interaction between digestion and locomotion in cyprinid fishes with different locomotive and digestive performances. J Comp Physiol B 182:641–650. doi: 10.1007/s00360-012-0644-0 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  1. 1.Laboratory of Evolutionary Physiology and Behavior, Chongqing Key Laboratory of Animal BiologyChongqing Normal UniversityChongqingChina

Personalised recommendations