ZHOU Long-Yan, LI Xiu-Ming, FU Shi-Jian. THE EFFECT OF PREDATION ACCLIMATION ON SWIMMING BEHAVIOR, STRESS AND IMMUNE RESPONSES OF JUVENILE MYXOCYPRINUS ASIATICUS AND SPINIBARBUS SINENSIS[J]. ACTA HYDROBIOLOGICA SINICA, 2021, 45(5): 1112-1119. DOI: 10.7541/2021.2020.015
Citation: ZHOU Long-Yan, LI Xiu-Ming, FU Shi-Jian. THE EFFECT OF PREDATION ACCLIMATION ON SWIMMING BEHAVIOR, STRESS AND IMMUNE RESPONSES OF JUVENILE MYXOCYPRINUS ASIATICUS AND SPINIBARBUS SINENSIS[J]. ACTA HYDROBIOLOGICA SINICA, 2021, 45(5): 1112-1119. DOI: 10.7541/2021.2020.015

THE EFFECT OF PREDATION ACCLIMATION ON SWIMMING BEHAVIOR, STRESS AND IMMUNE RESPONSES OF JUVENILE MYXOCYPRINUS ASIATICUS AND SPINIBARBUS SINENSIS

Funds: Supported by the National Natural Science Foundation of China (31670418); the National Natural Science Foundation of Chongqing Committee (cstc2018jcyjAX0150; cstc2017jcyjAX0347)
  • Received Date: January 16, 2019
  • Rev Recd Date: March 03, 2020
  • Available Online: July 15, 2021
  • Published Date: September 08, 2021
  • Whether fish species can adjust their physiological and behavioral traits well to the change of environmental condition of their habitats are key for the future fate of the local population. The aim of the present study was to investigate the physiological and behavioral responses of two endangered fish species, i.e. Chinese sucker (Myxocyprinus asiaticus) and Qingbo (Spinibarbus sinensis) subjected to short-term predation acclimation. We measured the maximum acceleration swimming speed (Ucat), spontaneous shoal behavior (percent time spent moving, median swimming speed and inter-individual distance), innate immune indicator (plasma lysosome activity), specific immune indicator (plasma IgM level), and antioxidant defense ability (plasma SOD activity) of either predation acclimated (reared with snakehead, Channa argus without direct contact) or non-acclimated (as control) juveniles of Chinese sucker and Qingbo for a period of 1 week. The plasma cortisol level and spontaneous activity were measured under both predator present and predator absent conditions. The main results of this study are as follows: (1) Qingbo showed stronger swimming capacity, more active spontaneous behavior, higher plasma cortisol and IgM levels as well as more profound response of both plasma cortisol and IgM level to predation acclimation, compared to those of Chinese sucker. (2) predation acclimation elicited higher plasma cortisol and IgM levels and higher plasma lysosome activity, especially in Qingbo. (3) acute predator exposure resulted in higher plasma cortisol and shorter inter-individual distance whereas the later only manifested in non-acclimated groups. In conclusion, both non-specific and specific immune function up-regulated after predation acclimation possible via the increased release of cortisol which might evolved with purpose to a fast recovery after possible non-lethal hunting. These adjustments indicated that predation training might act as a potential training process for fisheries releasing in the Yangtze River water system. The distinct difference in behavior, immune system and their response to predation acclimation or acute predator exposure suggested that these two fish species might have different fate in near future due to the unpredictable change in environmental factor such as predation.
  • [1]
    周龙艳. 长江流域几种珍稀鱼类对环境因子胁迫的生理与行为响应研究. 重庆: 重庆师范大学, 2020, 36-46.

    Zhou L Y. Physiological and behavioral responses to environmental stress of several endangered fish species in the Yangtze River[D]. Chongqing: Chongqing Normal university, 2020, 36-46.
    [2]
    董纯, 杨志, 龚云, 等. 三峡库区干流鱼类资源现状与物种多样性保护 [J]. 水生态学杂志, 2019, 40(1): 17-23.

    Dong C, Yang Z, Gong Y, et al. Fish resource status and biodiversity conservation in the main channel of Three Gorges Reservior [J]. Journal of Hydroescology, 2019, 40(1): 17-23.
    [3]
    Rousseau Y, Watson R A, Blanchard J L, et al. Evolution of global marine fishing fleets and the response of fished resources [J]. Proceedings of the National Academy of Sciences of The United States of America, 2019, 116(25): 12238-12243. doi: 10.1073/pnas.1820344116
    [4]
    成为为, 汪登强, 危起伟, 等. 基于微卫星标记对长江中上游胭脂鱼增殖放流效果的评估 [J]. 中国水产科学, 2014, 21(3): 574-580.

    Cheng W W, Wang D Q, Wei Q W, et al. Effect of restocking enhancement of Chinese sucker in the middle and upper reaches of Yangtze River based on miscrosatellite loci [J]. Journal of Fishery Sciences of China, 2014, 21(3): 574-580.
    [5]
    Brown C, Day R L. The future of stock enhancements: Lessons for hatchery practice from conservation biology [J]. Fish and Fisheries, 2002, 3(2): 79-94. doi: 10.1046/j.1467-2979.2002.00077.x
    [6]
    Neff B D, Garner S R, Pitcher T E. Conservation and enhancement of wild fish populations: Preserving genetic quality versus genetic diversity [J]. Canadian Journal of Fisheries and Aquatic Science, 2011, 68(6): 1139-1154. doi: 10.1139/f2011-029
    [7]
    Solås M R, Skoglund H, Salvanes A G V. Can structural enrichment reduce predation mortality and increase recaptures of hatchery-reared Atlantic salmon Salmo salar L. fry released into the wild [J]? Journal of Fish Biology, 2019, 95(2): 575-588. doi: 10.1111/jfb.14004
    [8]
    Olla B L, Davis M W, Ryer C H. Understanding how hatchery environment represses or promotes the development of behavioral survival skills [J]. Bulletin of Marine Science, 1998, 62(2): 531-550.
    [9]
    Petersson E, Valencia A C, Järvi T. Failure of predator conditioning: An experimental study of predator avoidance in brown trout (Salmo trutta) [J]. Ecology of Freshwater Fish, 2014, 24(3): 329-337.
    [10]
    Fu S J. Flow and stress acclimation both enhance predator avoidance in a common cyprinid fish [J]. Aquatic Biology, 2015, 24(1): 1-8. doi: 10.3354/ab00633
    [11]
    Karvonen A, Aalto‐Araneda M, Virtala AM, et al. Enriched rearing environment and wild genetic background can enhance survival and disease resistance of salmonid fishes during parasite epidemics [J]. Journal of Applied Ecology, 2016, 53(1): 213-221. doi: 10.1111/1365-2664.12568
    [12]
    Langenhof M R, Komdeur J. Why and how the early life environment affects development of coping behaviours [J]. Behavioral Ecology and Sociobiology, 2018, 72(3): 34. doi: 10.1007/s00265-018-2452-3
    [13]
    Brown C, Laland K N. Social learning and life skills training for hatchery reared fish [J]. Journal of Fish Biology, 2005, 59(3): 471-493.
    [14]
    Fu S J, Fu C, Yan G J, et al. Interspecifific variation in hypoxia tolerance, swimming performance and plasticity in cyprinids that prefer different habitats [J]. Journal of Experimental Biology, 2014, 217(4): 590-597.
    [15]
    Hellström G, Magnhagen C. Balancing past and present: How experience influences boldness over time in Eurasian perch [J]. Current Zoology, 2017, 63(2): 159-164.
    [16]
    Tang Z H, Wu Q, Fu S J. Inspection behaviour and inter-individual cooperation in juvenile qingbo: the effects of prior predator exposure and food deprivation [J]. Journal of Ethology, 2018, 36(5-6): 181-190.
    [17]
    Fu C, Fu S J, Wu Q Y, et al. Predation threat modifies relationships between metabolism and behavioural traits but not their ecological relevance in Chinese bream [J]. Marine and Freshwater Behaviour and Physiology, 2017, 50(5-6): 329-344. doi: 10.1080/10236244.2017.1411158
    [18]
    Mesa M G, Poe T P, Gadomski D M, et al. Are all preys created equal? A review and synthesis of differential predation on prey in substandard condition [J]. Journal of Fish Biology, 1994, 45(Supplement A): 81-96.
    [19]
    Barcellos L J G, Ritter F, Kreutz L C, et al. Whole body cortisol increases after direct and visual contact with a predator in zebrafish, Danio rerio [J]. Aquaculture, 2007, 272(1-4): 774-778. doi: 10.1016/j.aquaculture.2007.09.002
    [20]
    Breves J P, Specker J L. Cortisol stress response of juvenile winter flounder (Pseudopleuronectes americanus, Walbaum) to predators [J]. Journal of Experimental Marine Biology and Ecology, 2005, 325(1): 1-7. doi: 10.1016/j.jembe.2005.04.019
    [21]
    Scott G R, Sloman K A, Rouleau C, et al. Cadmium disrupts behavioural and physiological responses to alarm substance in juvenile rainbow trout (Oncorhyncus mykiss) [J]. Journal of the Experimental Biology, 2003, 206(11): 1779-1790. doi: 10.1242/jeb.00353
    [22]
    Lima S L, Bednekoff P A. Temporal variation in danger drives antipredatory behavior: The predation risk allocation hypothesis [J]. The American Naturalist, 1999, 153(6): 649-659. doi: 10.1086/303202
    [23]
    Brown C, Gardner C, Braithwaite. Differential stress response in fish from areas of high and low predation pressure [J]. Journal of Comparative Physiology B, 2005, 175(5): 305-312. doi: 10.1007/s00360-005-0486-0
    [24]
    Byrnes E E, Brown C. Individual personality differences in Port Jackson sharks Heterodontus portusjacksoni [J]. Journal of Fish Biology, 2016, 89(35): 1142-1157.
    [25]
    Réale D, Garant D, Humbries M M, et al. Personality and the emergence of the pace of life syndrome concept at the population level [J]. Philosophical transactions of the Royal Society B, 2010, 365(1560): 4051-4063. doi: 10.1098/rstb.2010.0208
    [26]
    Xu J J, Fu S J, Fu C. Physiological and behavioral stress responses to predators are altered by prior predator experience in juvenile qingbo (Spinibarbus sinensis) [J]. Biology Open, 2019, 8(5): bio041012.
    [27]
    Fischer E K, Harris R M, Hofmann H A, et al. Predator exposure alters stress physiology in guppies across timescales [J]. Hormones and Behavior, 2014, 65(2): 165-172. doi: 10.1016/j.yhbeh.2013.12.010
    [28]
    Lawrence M J, Godin J G J, Cooke S J. Does experimental cortisol elevation mediate risk-taking and antipredator behaviour in a wild teleost fish [J]? Comparative Biochemistry and Physiology A, 2018, 226(1): 75-82.
    [29]
    夏继刚, 李秀明, 付世建. PFOS对中华倒刺鲃幼鱼爆发游泳及运动后代谢恢复的影响 [J]. 水生生物学报, 2019, 43(2): 356-361. doi: 10.7541/2019.044

    Xia J G, Li X M, Fu S J. Effect of PFOS on burst swimming performance and metabolic recovery in juvenile Spinibarbus sinensis [J]. Acta Hydrobiologica Sinica, 2019, 43(2): 356-361. doi: 10.7541/2019.044
    [30]
    李秀明, 张耀光, 何春梅, 等. 力竭追赶训练对两种鲤科鱼类呼吸循环系统参数和力竭运动后代谢特征的影响 [J]. 水生生物学报, 2019, 43(1): 78-85. doi: 10.7541/2019.010

    Li X M, Zhang Y G, He C M, et al. The effect of exhaustive chasing training on parameters of respiratory and circulatory system and excess post-exercise oxygen consumption in juvenile qingbo (Spinibarbus sinensis) and rock carp (Procypris rabaudi) [J]. Acta Hydrobiologica Sinica, 2019, 43(1): 78-85. doi: 10.7541/2019.010
    [31]
    Bermejo-Poza R, FernándeZ-Muela M, De la Fuente J, et al. Physio-metabolic response of rainbow trout during prolonged food deprivation before slaughter [J]. Fish Physiology and Biochemistry, 2019, 45(1): 253-265. doi: 10.1007/s10695-018-0559-0
    [32]
    Dar S A, Srivastava P P, Varghese T, et al. Temporal changes in superoxide dismutase, catalase, and heat shock protein 70 gene expression, cortisol and antioxidant enzymes activity of Labeo rohita fingerlings subjected to starvation and refeeding [J]. Gene, 2019, 692(1): 94-101.
    [33]
    McCord J M, Fridovich I. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein) [J]. Journal of Biological Chemistry, 1969, 244(22): 6049-6055. doi: 10.1016/S0021-9258(18)63504-5
    [34]
    Filho D W. Reactive oxygen species, antioxidants and fish mitochondria [J]. Frontiers in Bioscience, 2007, 12(1): 1229-1237. doi: 10.2741/2141
    [35]
    庞旭, 付世建, 曹振东, 等. 饥饿和温度驯化对中华倒刺鲃静止代谢和游泳能力的影响 [J]. 生态学报, 2016, 36(7): 1854-1860.

    Pang X, Fu S J, Cao Z D, et al. The effects of fasting and acclimation temperature on the resting metabolism and swimming performance in qingbo (Spinibarbus sinensis) [J]. Acta Ecologica Sinica, 2016, 36(7): 1854-1860.
    [36]
    Liu H S, Zeng L Q, Cao Z D, et al. Effects of different predator stress on vulnerability to predation and the underlying physiological and behavioral mechanisms of this vulnerability in juvenile qingbo (Spinibarbus sinensis) [J]. Acta Ecologica Sinica, 2016, 36(2): 85-90. doi: 10.1016/j.chnaes.2016.01.005
    [37]
    张伟, 曹振东, 付世建. 溶氧水平对鲫鱼代谢模式的影响 [J]. 生态学报, 2012, 32(18): 5806-5812. doi: 10.5846/stxb201108051147

    Zhang W, Cao Z D, Fu S J. Effect of dissolved oxygen level on metabolic mode in juvenile crucian carp et al [J]. Acta Ecologica Sinica, 2012, 32(18): 5806-5812. doi: 10.5846/stxb201108051147
    [38]
    付世建, 聂利娟, 吴慧, 等. 群体大小对青幼鱼群体特征的影响 [J]. 生态学报, 2016, 36(19): 6062-6070.

    Fu S J, Nie L J, Wu H, et al. The effect of group size on school structure in juvenile black carp [J]. Acta Ecologica Sinica, 2016, 36(19): 6062-6070.
    [39]
    王蕾, 唐金玉, 覃英莲, 等. 饥饿对中华倒刺鲃幼鱼代谢、个性和集群的影响 [J]. 生态学报, 2019, 39(3): 1095-1104.

    Wang L, Tang J Y, Qin Y L, et al. Effect of starvation on energy metabolism, fish behavior, and schooling behavior of Spinibarbus sinensis [J]. Atca Ecologica Sinica, 2019, 39(3): 1095-1104.
    [40]
    Zhou L Y, LI X M, Fu C, et al. Effects of acclimation temperature on the thermal tolerance, hypoxia tolerance and swimming performance of two endangered fish species in China [J]. Journal of Comparative Physiology B, 2019, 189(2): 237-247. doi: 10.1007/s00360-018-01201-9
    [41]
    Pang X, Shao F, Ding S, et al. Interspecific differences and ecological correlations of energy metabolism traits in freshwater fishes [J]. Functional Ecology, 2020, 34(3): 616-630. doi: 10.1111/1365-2435.13505
    [42]
    Yan G J, He X K, Cao Z D, et al. An interspecific comparison between morphology and swimming performance in cyprinids [J]. Journal of Evolutionary Biology, 2013, 26(8): 1802-1815. doi: 10.1111/jeb.12182
    [43]
    Wahl D H, Einfalt L M, Wojcieszak D B. Effect of experience with predators on the behavior and survival of muskellunge and tiger muskellunge [J]. Transactions of the American Fisheries Society, 2012, 141(1): 139-146. doi: 10.1080/00028487.2011.652011
    [44]
    Tettweiler G, Miron M, Jenkins M, et al. Starvation and oxidative stress resistance in Drosophila are mediated through the eIF4E-binding protein, d4E-BP [J]. Genes and Development, 2005, 19(16): 1840-1843. doi: 10.1101/gad.1311805
    [45]
    Raffaghello L, Lee C, Safdie FM, et al. Starvation-dependent differential stress resistance protects normal but not cancer cells against high-dose chemotherapy [J]. Proceedings of the National Academy of Sciences of the United States of America, 2008, 105(24): 8215-8220. doi: 10.1073/pnas.0708100105
    [46]
    Xia J H, Lin G, Fu G H, et al. The intestinal microbiome of fish under starvation [J]. BMC Genomics, 2014, 15: 266-271. doi: 10.1186/1471-2164-15-266
    [47]
    Liu G Y, Wu Y J, Qin X H, et al. The effect of aerobic exercise training on growth performance, innate immune response and disease resistance in juvenile Schizothorax prenanti [J]. Aquaculture, 2017, 486(3): 18-25.
    [48]
    Choi C Y, Shin H S, Choi Y J, et al. Effect of LED lightspectra on starvation-induced oxidative stress in the cinnamon clownfish Amphiprion melanopus [J]. Comparative Biochemistry and Physiology A, 2012, 163(3-4): 357-363. doi: 10.1016/j.cbpa.2012.07.005
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