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

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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.

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References

  • 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 5:441–450

    Article  Google Scholar 

  • Amornpiyakrit T, Arimoto T (2008) Muscle physiology in escape response of kuruma shrimp. Am Fish Soc Symp 49:1321–1334

    Google Scholar 

  • 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 180:707–714

    Article  CAS  PubMed  Google Scholar 

  • 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 202:193–209

    PubMed  Google Scholar 

  • 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 50:183–187

    Article  Google Scholar 

  • Behbahani SB, Tan XB (2016) Design and modeling of flexible passive rowing joint for robotic fish pectoral fins. Ieee T Robot 32:1119–1132

    Article  Google Scholar 

  • Bernatchez L, Dodson JJ (1987) Relationship between bioenergetics and behavior in anadromous fish migrations. Can J Fish Aquat Sci 44:399–407

    Article  Google Scholar 

  • Brett JR (1972) The metabolic demand for oxygen in fish, particularly salmonids, and a comparison with other vertebrates. Respir Physiol 14:151–170

    Article  CAS  PubMed  Google Scholar 

  • 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 51:349–353

    Article  CAS  Google Scholar 

  • 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 211:325–339

    Article  CAS  Google Scholar 

  • Childress JJ, Seibel BA (1998) Life at stable low oxygen levels: adaptations of animals to oceanic oxygen minimum layers. J Exp Biol 201:1223–1932

    CAS  PubMed  Google Scholar 

  • Cowles DL (1994) Swimming dynamics of the mesopelagic vertically migrating penaeid shrimp Sergestes Similis: modes and speeds of swimming. J Crustacean Biol 14:247–257

    Article  Google Scholar 

  • Diaz R, Rosenberg R (1995) Marine benthic hypoxia: A review of its ecological effects and the behavioural response of benthic macrofauna. Oceanogr Mar Biol 33:245–303

    Google Scholar 

  • 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 205:969–980

    PubMed  Google Scholar 

  • 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 13:132–140

    Article  Google Scholar 

  • 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 107:834–844

    Article  CAS  PubMed  Google Scholar 

  • 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 183:223–234

    CAS  PubMed  Google Scholar 

  • Fluck M (2006) Functional, structural and molecular plasticity of mammalian skeletal muscle in response to exercise stimuli. J Exp Biol 209:2239–2248

    Article  CAS  Google Scholar 

  • Foulds JB, Roff JC (1976) Oxygen consumption during simulated vertical migration in Mysis relicta (Crustacea, Mysidacea). Can J Zool 54:377–385

    Article  Google Scholar 

  • Fricke RA (1984) Development of habituation in the crayfish due to selective weakening of electrical synapses. Brain Res 322:139–143

    Article  CAS  PubMed  Google Scholar 

  • 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 216:3164–3174

    Article  PubMed  Google Scholar 

  • 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 214:3005–3112

    Article  CAS  PubMed  Google Scholar 

  • Hagerman L, Vismann B (1995) Anaerobic metabolism in the shrimp Crangon crangon exposed to hypoxia, anoxia and hydrogen sulfide. Mar Biol 123:235–240

    Article  CAS  Google Scholar 

  • Hammer C (1995) Fatigue and exercise tests with fish. Comp Biochem Phys A 112:1–20

    Article  Google Scholar 

  • 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 37:641–646

    Article  CAS  Google Scholar 

  • Jackson DJ, MacMillan DL (2000) Tailflick escape behavior in larval and juvenile lobsters (Homarus americanus) and crayfish (Cherax destructor). Biol Bull 198:307–318

    Article  CAS  PubMed  Google Scholar 

  • Kieffer JD (2010) Perspective—Exercise in fish: 50 + years and going strong. Comp Biochem Phys A 156:163–168

    Article  CAS  Google Scholar 

  • 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 201:3123–3133

    PubMed  Google Scholar 

  • Krasne FB, Woodsmall KS (1969) Waning of the crayfish escape response as a result of repeated stimulation. Anim Behav 17:416–424

    Article  CAS  PubMed  Google Scholar 

  • 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 479:142–149

    Article  CAS  Google Scholar 

  • Lang F, Govind CK, Costello WJ, Greene SI (1977) Developmental neuroethology: changes in escape and defensive behavior during growth of the lobster. Science 197:682–685

    Article  CAS  PubMed  Google Scholar 

  • 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 54:566–571

    Google Scholar 

  • 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) 99:893–898

    Article  CAS  Google Scholar 

  • 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 6:625–632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 47:608–628

    Article  CAS  PubMed  Google Scholar 

  • McClellan AD, Pale T, Messina JA, Buso S, Shebib A (2016) Similarities and differences for swimming in larval and adult lampreys. Physiol Biochem Zool 89:294–312

    Article  PubMed  Google Scholar 

  • McFarlane WJ, McDonald DG (2002) Relating intramuscular fuel use to endurance in juvenile rainbow trout. Physiol Biochem Zool 75:250–259

    Article  CAS  PubMed  Google Scholar 

  • 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 202:3181–3193

    PubMed  Google Scholar 

  • 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 88:655–667

    Article  CAS  PubMed  Google Scholar 

  • 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 74:833–838

    Article  Google Scholar 

  • Oufiero CE, Garland T (2009) Repeatability and correlation of swimming performances and size over varying time-scales in the guppy (Poecilia reticulata). Funct Ecol 23:969–978

    Article  Google Scholar 

  • Peake SJ, Farrell AP (2006) Fatigue is a behavioural response in respirometer-confined smallmouth bass. J Fish Biol 68:1742–1755

    Article  Google Scholar 

  • 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 478:16–23

    Article  CAS  Google Scholar 

  • 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 362:79–89

    Article  CAS  Google Scholar 

  • Spangenburg EE, Booth FW (2003) Molecular regulation of individual skeletal muscle fibre types. Acta Physiol Scand 178:413–424

    Article  CAS  PubMed  Google Scholar 

  • Tobo S, Takeuchi Y, Hori M (2012) Morphological asymmetry and behavioral laterality in the crayfish, Procambarus clarkii. Ecol Res 27:53–59

    Article  Google Scholar 

  • Tyson GE, Sullivan ML (1979) Antennular sensilla of the Brine shrimp, Artemia salina. Biol Bull 156:382–392

    Article  CAS  PubMed  Google Scholar 

  • Van Waarde A (1983) Aerobic and anaerobic ammonia production by fish. Comp Biochem Phys B 74:675–684

    Article  Google Scholar 

  • 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 8:410–419

    Article  Google Scholar 

  • Walton MJ, Cowey CB (1982) Aspects of intermediary metabolism in salmonid fish. Comp Biochem Phys B 73:59–79

    Article  Google Scholar 

  • Wang Q, Zhuang Z, Deng J, Ye Y (2006) Stock enhancement and translocation of the shrimp Penaeus chinensis in China. Fish Res 80:67–79

    Article  Google Scholar 

  • 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 35:51–56

    Google Scholar 

  • Weber J-M (2011) Metabolic fuels: regulating fluxes to select mix. J Exp Biol 214:286–294

    Article  CAS  PubMed  Google Scholar 

  • 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 130:339–347

    Article  CAS  Google Scholar 

  • 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 48:236–245

    Article  CAS  Google Scholar 

  • 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 153:120–124

    Article  CAS  Google Scholar 

  • 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 8:1316–1321

    CAS  Google Scholar 

  • 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 157:392–397

    Article  CAS  Google Scholar 

  • Zenteno-Savín T, Saldierna R, Ahuejote-Sandoval M (2006) Superoxide radical production in response to environmental hypoxia in cultured shrimp. Comp Biochem Physiol C 142:301–308

    Google Scholar 

  • 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 145:26–32

    Article  CAS  Google Scholar 

  • 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 147:64–69

    Article  CAS  Google Scholar 

  • 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 42:1807–1817

    Article  CAS  PubMed  Google Scholar 

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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).

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Correspondence to Xiumei Zhang.

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Li, J., Xu, X., Li, W. et al. Behavioural and physiological responses to low- and high-intensity locomotion in Chinese shrimp Fenneropenaeus chinensis. J Comp Physiol A 205, 87–102 (2019). https://doi.org/10.1007/s00359-018-1306-9

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  • DOI: https://doi.org/10.1007/s00359-018-1306-9

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