Advertisement

Behavioural and physiological responses to low- and high-intensity locomotion in Chinese shrimp Fenneropenaeus chinensis

  • Jiangtao Li
  • Xiuwen Xu
  • Wentao Li
  • Xiumei Zhang
Original paper
  • 31 Downloads

Abstract

We explored stroke behaviour, energy sources, and their related metabolic enzymes during multi-intensity swimming and tail-flipping at low- and high-intensity modes in Chinese shrimp Fenneropenaeus chinensis. In swimming, shrimp were encouraged to swim at velocities of 3, 6, 9 cm s−1 for 200 min (low-intensity), and at 12, 15, 18 cm s−1 until fatigue (high-intensity). In tail-flipping, shrimp were encouraged to tail-flip by tapping cephalothorax at frequencies of 0.020, 0.040, 0.063 Hz (one tap every 50, 25, 16 s) for 5 min (low-intensity), and at 0.083, 0,100, 0.125 Hz (one tap every 12, 10, 8 s) until no response (high-intensity). Results showed that shrimp increased stroke rates of pleopods and uropods to elevate swimming and tail-flipping ability. For low-intensity locomotion, glycogen was burned in aerobic pathway due to low pleopods beat frequency in swimming; however, glycogen was anaerobically burned due to high uropods beat amplitude in tail-flipping. Anaerobic metabolism occurred in high-intensity locomotion in either swimming or tail-flipping. Critical contents of muscle lactate causing locomotion fatigue might be around threefold of rest condition. Shrimp reduced locomotive time to avoid glycogen exhaustion and lactate accumulation during high-intensity locomotion. These findings highlight our understanding of physiological mechanisms of locomotion activities in shrimp.

Keywords

Aerobic metabolism Energy sources Glycolysis Migration Predator evasion 

Notes

Acknowledgements

The authors thank Yongliang Liu in Institute of Oceanology, Chinese Academy of Sciences for help with experiment performance.

Funding

This study was funded by the national program on key basic research project (973 Program) (2015CB453302).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Supplementary material

359_2018_1306_MOESM1_ESM.rar (59 kb)
Supplementary material 1 (RAR 59 KB)
359_2018_1306_MOESM2_ESM.rar (180.1 mb)
Supplementary material 2 (RAR 184444 KB)

References

  1. Albalat A, Gornik SG, Atkinson RJA, Coombs GH, Neil DM (2009) Effect of capture method on the physiology and nucleotide breakdown products in the Norway lobster (Nephrops norvegicus). Mar Biol Res 5:441–450CrossRefGoogle Scholar
  2. Amornpiyakrit T, Arimoto T (2008) Muscle physiology in escape response of kuruma shrimp. Am Fish Soc Symp 49:1321–1334Google Scholar
  3. Anttila K, Jäntti M, Mänttäri S (2010) Effects of training on lipid metabolism in swimming muscles of sea trout (Salmo trutta). J Comp Physiol B 180:707–714CrossRefGoogle Scholar
  4. Arnott SA, Neil DM, Ansell AD (1999) Escape trajectories of the brown shrimp crangon crangon, and a theoretical consideration of initial escape angles from predators. J Exp Biol 202:193–209PubMedGoogle Scholar
  5. Baldwin J, Gupta A, Iglesias X (1999) Scaling of anaerobic energy metabolism during tail flipping behaviour in the freshwater crayfish, Cherax destructor. Mar Freshw Res 50:183–187CrossRefGoogle Scholar
  6. Behbahani SB, Tan XB (2016) Design and modeling of flexible passive rowing joint for robotic fish pectoral fins. Ieee T Robot 32:1119–1132CrossRefGoogle Scholar
  7. Bernatchez L, Dodson JJ (1987) Relationship between bioenergetics and behavior in anadromous fish migrations. Can J Fish Aquat Sci 44:399–407CrossRefGoogle Scholar
  8. Brett JR (1972) The metabolic demand for oxygen in fish, particularly salmonids, and a comparison with other vertebrates. Respir Physiol 14:151–170CrossRefGoogle Scholar
  9. Brizel DM, Schroeder T, Scher RL, Walenta S, Clough RW, Dewhirst MW, Mueller-Klieser W (2001) Elevated tumor lactate concentrations predict for an increased risk of metastases in head-and-neck cancer. Int J Radiat Oncol 51:349–353CrossRefGoogle Scholar
  10. Cheng W, Liu C-H, Yan D-F, Chen J-C (2002) Hemolymph oxyhemocyanin, protein, osmolality and electrolyte levels of whiteleg shrimp Litopenaeus vannamei in relation to size and molt stage. Aquaculture 211:325–339CrossRefGoogle Scholar
  11. Childress JJ, Seibel BA (1998) Life at stable low oxygen levels: adaptations of animals to oceanic oxygen minimum layers. J Exp Biol 201:1223–1932PubMedGoogle Scholar
  12. Cowles DL (1994) Swimming dynamics of the mesopelagic vertically migrating penaeid shrimp Sergestes Similis: modes and speeds of swimming. J Crustacean Biol 14:247–257CrossRefGoogle Scholar
  13. Diaz R, Rosenberg R (1995) Marine benthic hypoxia: A review of its ecological effects and the behavioural response of benthic macrofauna. Oceanogr Mar Biol 33:245–303Google Scholar
  14. Dickson KA, Donley JM, Sepulveda C, Bhoopat L (2002) Effects of temperature on sustained swimming performance and swimming kinematics of the chub mackerel Scomber japonicus. J Exp Biol 205:969–980PubMedGoogle Scholar
  15. Duan Y, Zhang X, Liu X, Thakur DN (2014) Effect of dissolved oxygen on swimming ability and physiological response to swimming fatigue of whiteleg shrimp (Litopenaeus vannamei). J Ocean U China 13:132–140CrossRefGoogle Scholar
  16. Felip O, Ibarz A, Fernandez-Borras J, Beltran M, Martin-Perez M, Planas JV, Blasco J (2012) Tracing metabolic routes of dietary carbohydrate and protein in rainbow trout (Oncorhynchus mykiss) using stable isotopes ([13C]starch and [15N]protein): effects of gelatinisation of starches and sustained swimming. Br J Nutr 107:834–844CrossRefGoogle Scholar
  17. Felip O, Blasco J, Ibarz A, Martin-Perez M, Fernandez-Borras J (2013) Beneficial effects of sustained activity on the use of dietary protein and carbohydrate traced with stable isotopes 15N and 13C in gilthead sea bream (Sparus aurata). J Comp Physiol B 183:223–234PubMedGoogle Scholar
  18. Fluck M (2006) Functional, structural and molecular plasticity of mammalian skeletal muscle in response to exercise stimuli. J Exp Biol 209:2239–2248CrossRefGoogle Scholar
  19. Foulds JB, Roff JC (1976) Oxygen consumption during simulated vertical migration in Mysis relicta (Crustacea, Mysidacea). Can J Zool 54:377–385CrossRefGoogle Scholar
  20. Fricke RA (1984) Development of habituation in the crayfish due to selective weakening of electrical synapses. Brain Res 322:139–143CrossRefGoogle Scholar
  21. Fu C, Cao ZD, Fu SJ (2013) The effects of caudal fin loss and regeneration on the swimming performance of three cyprinid fish species with different swimming capacities. J Exp Biol 216:3164–3174CrossRefGoogle Scholar
  22. Gracey AY, Lee T-H, Higashi RM, Fan T (2011) Hypoxia-induced mobilization of stored triglycerides in the euryoxic goby Gillichthys mirabilis. J Exp Biol 214:3005–3112CrossRefGoogle Scholar
  23. Hagerman L, Vismann B (1995) Anaerobic metabolism in the shrimp Crangon crangon exposed to hypoxia, anoxia and hydrogen sulfide. Mar Biol 123:235–240CrossRefGoogle Scholar
  24. Hammer C (1995) Fatigue and exercise tests with fish. Comp Biochem Phys A 112:1–20CrossRefGoogle Scholar
  25. Head G, Baldwin J (1986) Energy metabolism and the fate of lactate during recovery from exercise in the Australian freshwater crayfish Cherax destructor. Mar Freshwater Res 37:641–646CrossRefGoogle Scholar
  26. Jackson DJ, MacMillan DL (2000) Tailflick escape behavior in larval and juvenile lobsters (Homarus americanus) and crayfish (Cherax destructor). Biol Bull 198:307–318CrossRefGoogle Scholar
  27. Kieffer JD (2010) Perspective—Exercise in fish: 50 + years and going strong. Comp Biochem Phys A 156:163–168CrossRefGoogle Scholar
  28. Kieffer JD, Alsop D, Wood CM (1998) A respirometric analysis of fuel use during aerobic swimming at different temperatures in rainbow trout (Oncorhynchus mykiss). J Exp Biol 201:3123–3133PubMedGoogle Scholar
  29. Krasne FB, Woodsmall KS (1969) Waning of the crayfish escape response as a result of repeated stimulation. Anim Behav 17:416–424CrossRefGoogle Scholar
  30. Lage LPA, Plagnes-Juan E, Putrino SM, Baron F, Weissman D, Guyonvarch A, Brugger R, Nunes AJP, Panserat S (2017) Ontogenesis of metabolic gene expression in whiteleg shrimp (Litopenaeus vannamei): New molecular tools for programming in the future. Aquaculture 479:142–149CrossRefGoogle Scholar
  31. Lang F, Govind CK, Costello WJ, Greene SI (1977) Developmental neuroethology: changes in escape and defensive behavior during growth of the lobster. Science 197:682–685CrossRefGoogle Scholar
  32. Lauff RF, Wood CM (1997) Effects of training on respiratory gas exchange, nitrogenous waste excretion, and fuel usage during aerobic swimming in juvenile rainbow trout (Oncorhynchus mykiss). Can. J Fish Aquat Sci 54:566–571Google Scholar
  33. Li D, Wei XL, Lin XT, Xu ZN, Mu XP (2015) Effects of exercise training on carbohydrate and lipid catabolism in the swimming muscles of Nile tilapia (Oreochromis niloticus). J Anim Physiol Anim Nutr (Berl) 99:893–898CrossRefGoogle Scholar
  34. Li J, Lin X, Xu Z, Sun J (2017) Differences in swimming ability and its response to starvation among male and female Gambusia affinis. Biol Open 6:625–632CrossRefGoogle Scholar
  35. Livesey G, Elia M (1988) Estimation of energy expenditure, net carbohydrate utilization, and net fat oxidation and synthesis by indirect calorimetry: evaluation of errors with special reference to the detailed composition of fuels. Am J Clin Nutr 47:608–628CrossRefGoogle Scholar
  36. McClellan AD, Pale T, Messina JA, Buso S, Shebib A (2016) Similarities and differences for swimming in larval and adult lampreys. Physiol Biochem Zool 89:294–312CrossRefGoogle Scholar
  37. McFarlane WJ, McDonald DG (2002) Relating intramuscular fuel use to endurance in juvenile rainbow trout. Physiol Biochem Zool 75:250–259CrossRefGoogle Scholar
  38. Nauen JC, Shadwick RE (1999) The scaling of acceleratory aquatic locomotion: body size and tail-flip performance of the california spiny lobster Panulirus interruptus. J Exp Biol 202:3181–3193PubMedGoogle Scholar
  39. Nguyen PL, Jackson ZJ, Peterson DL (2016) Comparison of fin ray sampling methods on white sturgeon Acipenser transmontanus growth and swimming performance. J Fish Biol 88:655–667CrossRefGoogle Scholar
  40. Onnen T, Zebe E (1983) Energy metabolism in the tail muscles of the shrimp Crangon crangon during work and subsequent recovery. Comp Biochem Phys A 74:833–838CrossRefGoogle Scholar
  41. Oufiero CE, Garland T (2009) Repeatability and correlation of swimming performances and size over varying time-scales in the guppy (Poecilia reticulata). Funct Ecol 23:969–978CrossRefGoogle Scholar
  42. Peake SJ, Farrell AP (2006) Fatigue is a behavioural response in respirometer-confined smallmouth bass. J Fish Biol 68:1742–1755CrossRefGoogle Scholar
  43. Robles-Romo A, Zenteno-Savín T, Racotta IS (2016) Bioenergetic status and oxidative stress during escape response until exhaustion in whiteleg shrimp Litopenaeus vannamei. J Exp Mar Bio Ecol 478:16–23CrossRefGoogle Scholar
  44. Sánchez-Paz A, Soñanez-Organis JG, Peregrino-Uriarte AB, Muhlia-Almazán A, Yepiz-Plascencia G (2008) Response of the phosphofructokinase and pyruvate kinase genes expressed in the midgut gland of the Pacific white shrimp Litopenaeus vannamei during short-term starvation. J Exp Mar Bio Ecol 362:79–89CrossRefGoogle Scholar
  45. Spangenburg EE, Booth FW (2003) Molecular regulation of individual skeletal muscle fibre types. Acta Physiol Scand 178:413–424CrossRefGoogle Scholar
  46. Tobo S, Takeuchi Y, Hori M (2012) Morphological asymmetry and behavioral laterality in the crayfish, Procambarus clarkii. Ecol Res 27:53–59CrossRefGoogle Scholar
  47. Tyson GE, Sullivan ML (1979) Antennular sensilla of the Brine shrimp, Artemia salina. Biol Bull 156:382–392CrossRefGoogle Scholar
  48. Van Waarde A (1983) Aerobic and anaerobic ammonia production by fish. Comp Biochem Phys B 74:675–684CrossRefGoogle Scholar
  49. Villamar DF, Brusca GJ (1988) Variation in the larval development of Crangon Nigricauda (Decapoda: Caridea), with notes on larval morphology and behavior. J Crustacean Biol 8:410–419CrossRefGoogle Scholar
  50. Walton MJ, Cowey CB (1982) Aspects of intermediary metabolism in salmonid fish. Comp Biochem Phys B 73:59–79CrossRefGoogle Scholar
  51. Wang Q, Zhuang Z, Deng J, Ye Y (2006) Stock enhancement and translocation of the shrimp Penaeus chinensis in China. Fish Res 80:67–79CrossRefGoogle Scholar
  52. Wang M, Wang W, Xiao G, Liu K, Hu Y, Tian T, Kong J, Jin X (2016) Genetic diversity analysis of spawner and recaptured populations of Chinese shrimp (Fenneropenaeus chinensis) during stock enhancement in the Bohai Bay based on an SSR marker. Acta Oceanol Sin 35:51–56Google Scholar
  53. Weber J-M (2011) Metabolic fuels: regulating fluxes to select mix. J Exp Biol 214:286–294CrossRefGoogle Scholar
  54. Wells RMG, Lu J, Hickey AJR, Jeffs AG (2001) Ontogenetic changes in enzyme activities associated with energy production in the spiny lobster, Jasus edwardsii. Comp Biochem Phys B 130:339–347CrossRefGoogle Scholar
  55. Xue SX, Wei JL, Li JJ, Geng XY, Sun JS (2017) Effects of total ammonia, temperature and salinity on the mortality and viral replication of WSSV-infected Chinese shrimp (Fenneropenaeus chinensis). Aquac Res 48:236–245CrossRefGoogle Scholar
  56. Yu X, Zhang X, Zhang P, Yu C (2009a) Critical swimming speed, tail-flip speed and physiological response to exercise fatigue in kuruma shrimp, Marsupenaeus japonicus. Comp Biochem Physiol A 153:120–124CrossRefGoogle Scholar
  57. Yu X, Zhang X, Zhang P, Yu C (2009b) Swimming ability and physiological response to swimming fatigue in kuruma shrimp, Marsupenaeus japonicus. Afr J Biotechnol 8:1316–1321Google Scholar
  58. Yu X, Zhang X, Duan Y, Zhang P, Miao Z (2010) Effects of temperature, salinity, body length, and starvation on the critical swimming speed of whiteleg shrimp, Litopenaeus vannamei. Comp Biochem Physiol A 157:392–397CrossRefGoogle Scholar
  59. Zenteno-Savín T, Saldierna R, Ahuejote-Sandoval M (2006) Superoxide radical production in response to environmental hypoxia in cultured shrimp. Comp Biochem Physiol C 142:301–308Google Scholar
  60. Zhang P, Zhang X, Li J, Huang G (2006) Swimming ability and physiological response to swimming fatigue in whiteleg shrimp, Litopenaeus vannamei. Comp Biochem Physiol A 145:26–32CrossRefGoogle Scholar
  61. Zhang P, Zhang X, Li J, Huang G (2007) The effects of temperature and salinity on the swimming ability of whiteleg shrimp, Litopenaeus vannamei. Comp Biochem Physiol A 147:64–69CrossRefGoogle Scholar
  62. Zhu Z, Song B, Lin X, Xu Z (2016) Effect of sustained training on glycolysis and fatty acids oxidation in swimming muscles and liver in juvenile tinfoil barb Barbonymus schwanenfeldii (Bleeker, 1854). Fish Physiol Biochem 42:1807–1817CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  • Jiangtao Li
    • 1
  • Xiuwen Xu
    • 1
  • Wentao Li
    • 1
  • Xiumei Zhang
    • 1
    • 2
  1. 1.The Key Laboratory of Mariculture, Ministry of EducationOcean University of ChinaQingdaoChina
  2. 2.Laboratory for Marine Fisheries Science and Food Production ProcessesQingdao National Laboratory for Marine Science and TechnologyQingdaoChina

Personalised recommendations