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Effects of temperature and feeding rate on postprandial metabolic response in juvenile Percocypris pingi

  • Corresponding author: WANG Zhijian, wangzj@swu.edu.cn
  • Received Date: 2020-09-03
    Accepted Date: 2021-04-16
    Available Online: 2021-08-12
  • The marked increase in the metabolic rate that occurs following feeding is commonly referred to as specific dynamic action (SDA). Previous studies on SDA in animals have found that the meal type, temperature, body size, feeding frequency, fasting and feeding rate all have significant effects on SDA. The study of postprandial metabolic response in Percocypris pingi has not been reported. To investigate the effects of temperature and feeding rate on postprandial metabolic traits in juvenile P. pingi, the experimental fish [body weight: (38.35±0.49) g, body length: (14.22±0.10) cm] were fed with loach (Misgurnus anguillicaudatus) (feeding rates: 1%, 2%, 4% body mass at 15 °C; 1%, 2%, 4% and 6% body mass at 25 °C) for 4 weeks as diet acclimation at 15 °C and 25 °C in indoor recirculating aquaculture systems. After that, the oxygen consumption rate was detected and parameters related to postprandial metabolic response were calculated. Results showed that at the same feeding rate, resting metabolic rate, peak metabolic rate, total energy expenditure on SDA and SDA coefficient of 25 °C acclimation group were significantly higher than those of 15 °C acclimation group. The SDA duration of 25 °C acclimation group at 2% and 4% feeding rate was significantly shorter than that of 15 °C acclimation group. At the 25 °C, fish of higher feeding rates (4% and 6%) presented significantly higher peak metabolic rate, factorial metabolic scope, SDA duration and total energy expenditure on SDA than those of lower feeding rates (1% and 2%) at 25 °C, and times to peak metabolic rate of 4% and 6% feeding rates were significantly earlier than that of 1% and 2% feeding rates as well. However, the SDA coefficient showed an opposite situation: higher feeding rate presented significantly lower values. At the 15 °C, peak metabolic rate, factorial metabolic scope, SDA duration and energy expended on SDA of 4% feeding rate group were significantly higher than those of 1% and 2% feeding rates. Nevertheless, no significant difference in the time to peak metabolic rate and the SDA coefficient among all feeding rates were observed at 15 °C. All the above information suggested that the water temperature of 25 °C is more beneficial to the rapid food digestion and absorption by juvenile P. pingi; and the fish may meet the increased energy demand during digestive process by means of increasing peak metabolic rate and prolonging SDA duration with the increase of feeding rate. The results of this study may provide important reference data for the breeding practice and species protection of P. pingi.
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Effects of temperature and feeding rate on postprandial metabolic response in juvenile Percocypris pingi

    Corresponding author: WANG Zhijian, wangzj@swu.edu.cn
  • 1. Key Laboratory of Freshwater Fish Reproduction and Development, Education of Ministry, Key Laboratory of Aquatic Science of Chongqing, Southwest University, Chongqing    400715, China
  • 2. Sichuan Lubei Biotechnology Co., Ltd., Heima Rare Fish Breeding and Releasing Station, Chengdu    610065, China

Abstract: The marked increase in the metabolic rate that occurs following feeding is commonly referred to as specific dynamic action (SDA). Previous studies on SDA in animals have found that the meal type, temperature, body size, feeding frequency, fasting and feeding rate all have significant effects on SDA. The study of postprandial metabolic response in Percocypris pingi has not been reported. To investigate the effects of temperature and feeding rate on postprandial metabolic traits in juvenile P. pingi, the experimental fish [body weight: (38.35±0.49) g, body length: (14.22±0.10) cm] were fed with loach (Misgurnus anguillicaudatus) (feeding rates: 1%, 2%, 4% body mass at 15 °C; 1%, 2%, 4% and 6% body mass at 25 °C) for 4 weeks as diet acclimation at 15 °C and 25 °C in indoor recirculating aquaculture systems. After that, the oxygen consumption rate was detected and parameters related to postprandial metabolic response were calculated. Results showed that at the same feeding rate, resting metabolic rate, peak metabolic rate, total energy expenditure on SDA and SDA coefficient of 25 °C acclimation group were significantly higher than those of 15 °C acclimation group. The SDA duration of 25 °C acclimation group at 2% and 4% feeding rate was significantly shorter than that of 15 °C acclimation group. At the 25 °C, fish of higher feeding rates (4% and 6%) presented significantly higher peak metabolic rate, factorial metabolic scope, SDA duration and total energy expenditure on SDA than those of lower feeding rates (1% and 2%) at 25 °C, and times to peak metabolic rate of 4% and 6% feeding rates were significantly earlier than that of 1% and 2% feeding rates as well. However, the SDA coefficient showed an opposite situation: higher feeding rate presented significantly lower values. At the 15 °C, peak metabolic rate, factorial metabolic scope, SDA duration and energy expended on SDA of 4% feeding rate group were significantly higher than those of 1% and 2% feeding rates. Nevertheless, no significant difference in the time to peak metabolic rate and the SDA coefficient among all feeding rates were observed at 15 °C. All the above information suggested that the water temperature of 25 °C is more beneficial to the rapid food digestion and absorption by juvenile P. pingi; and the fish may meet the increased energy demand during digestive process by means of increasing peak metabolic rate and prolonging SDA duration with the increase of feeding rate. The results of this study may provide important reference data for the breeding practice and species protection of P. pingi.

  • 摄食是动物基本的生理行为之一,为其生存、生长、发育及繁殖提供了物质基础。动物在摄食后的消化过程中代谢耗能增加的现象被称为特殊动力作用(specific dynamic action,SDA),包括所有与营养代谢有关的食物的消化、吸收、代谢的转换以及生长等过程中能量的消耗[1]。动物摄食代谢特征的评价指标主要包括摄食代谢峰值(peak metabolic rate)、峰值时间(time to peak metabolic rate)、峰值比率(factorial metabolic scope)、SDA时间(duration)和SDA系数(SDA coefficient)等[1-2]。鱼类的摄食代谢特征不仅与其种类和营养状况相关,还受到食物组成、温度、溶解氧、光照强度、摄食率和摄食频率等各种环境因素的影响[3-4]

    温度是最重要的环境生态因素之一,直接或间接影响着动物生长、发育、形态、行为和分布,特别是对鱼类等外温动物的生存和繁衍起着决定性作用[5-6]。以往研究发现,在适宜的温度范围内,鱼类的摄食后代谢峰值通常会随着温度的升高而上升,而SDA时间则会随温度升高而缩短[7-10]。此外,由于自然界中食物资源分布的时空异质性,动物不可能随时获得足够的饵料供其利用,因此动物在不同摄食率下的生理反应一直受到研究者的广泛关注[1-2]。已有研究表明,鱼类的摄食代谢峰值、SDA时间和SDA总耗能等特征都会随着摄食率的增加而增大,但其影响程度存在显著的种间差异[11-16]

    鲈鲤(Percocypris pingi),俗称江鲤、青脖、花鲤,属鲤形目(Cypriniformes)鲤科(Cyprinidae)鲃亚科(Barbinae)鲈鲤属(Percocypris),主要分布于金沙江、雅砻江及大渡河等长江上游水系,是当地特有的经济鱼类[17]。近年来,由于其自然栖息地生态环境遭受破坏以及过度捕捞等原因,野生鲈鲤的数量大幅下降,现其濒危等级已达濒危级别,同时被多个省市列为重点保护的水生野生动物,已被列为国家二级保护动物[17-18]。目前,有关鲈鲤的研究主要涉及基础生物学特征、生长能力、运动功能、组织形态、营养品质、疾病防治和养殖技术等方面[18-24],而有关温度和摄食率对其消化生理功能的研究还未见报道。本研究以鲈鲤幼鱼为实验对象,考察温度和摄食率对其摄食代谢特征的影响,分析其消化代谢生理特征,为其养殖实践提供重要的参考资料,此外通过探讨其消化代谢在不同温度下的适应性策略,为其种群保护提供重要的理论支撑数据。

1.   材料与方法
  • 本实验所用的1龄鲈鲤幼鱼(30~50 g)购于四川省西昌市冷水鱼养殖基地,在重庆市西南大学水产科学重点实验室室内循环水养殖系统中驯养4周。本研究中采用同一批次相同规格的鲜活泥鳅(Misgurnus anguillicaudatus)作为饵料,去头尾和内脏后切片冷冻保存,投喂前解冻。驯养期间以泥鳅细块作为饵料投喂,每天饱食投喂1次(09:00),投喂1 h后用虹吸管清理残饵和粪便。驯养的水温控制在(20±1) °C,养殖用水为充分曝气的自来水,利用充气泵向水体中持续充入空气,溶解氧含量大于6 mg/L,光照周期为12L∶12D。

  • 根据对长江上游水温的监测数据可知,鲈鲤分布水域冬季水温约为12 °C,夏季水温约为23 °C[25]。因此,为了探讨不同温度下鲈鲤摄食代谢的适应性策略,本实验模拟其生境冬季和夏季水温,设置15和25 °C两个温度组进行实验。驯养期结束后,随机挑选大小相似的实验鱼80尾[体质量(38.35±0.49) g,体长(14.22±0.10) cm]并平均分为15 °C驯化组和25 °C驯化组,转移到相应的养殖水槽后以1 °C/d的变温速率将水温分别调整至驯化温度(15或25 °C),驯化水温变幅为±0.5 °C。当温度达到驯化温度后,进行4周的温度驯化处理。温度驯化期间的其他养殖条件与驯养期间一致。

    温度驯化期结束后,将单尾实验鱼禁食24 h后测量其体质量和体长,随后转移到鱼类流水式呼吸仪的单独呼吸室内适应24 h。在投喂前8 h内,每隔2 h测量1次耗氧率,共4次,以平均值作为实验鱼的静止代谢率。随后从呼吸室入水口上方可开启的投喂孔用泥鳅块[(4.85± 0.32) kJ/g]对其进行投喂,30 min后关闭呼吸室的投喂孔。根据预备实验,发现实验鱼在代谢仪的呼吸管中能够主动摄食,且在15 °C下单次最大摄食率约为体质量的4%,在25 °C下单次最大摄食率约为体质量的6%。因此,15 °C驯化组设置3个摄食率(1%、2%和4%体质量)的处理,25 °C驯化组设置4个摄食率(1%、2%、4%和6%体质量)的处理。投喂结束后每隔2 h测定1次耗氧率,直至实验鱼的耗氧率恢复到摄食前水平。15 °C驯化组的耗氧率测定至摄食后30 h,25 °C驯化组的耗氧率测定至摄食后34 h。不同驯化温度组每个摄食率的样本量均为9尾。

  • 以实验鱼的耗氧率作为其代谢率衡量指标。采用鱼类流水式呼吸仪测定实验鱼的耗氧率[13]。鱼类流水式呼吸仪主要由上位水槽(105 cm×65 cm×32 cm)和下位水槽(95 cm×95 cm×75 cm)组成,上位水槽中放置15个呼吸室(400 mL),每个呼吸室流速都通过一个单独的阀门控制。实验鱼被分别放置于独立的呼吸室中,每次测定包括1个空白呼吸室(无实验鱼)和14个测定呼吸室(有实验鱼)。溶解氧含量用溶氧仪(HQ30d,Hach Company,Loveland,CO,USA)测定,测量范围0~20 mg O2/L,精确度0.01 mg O2/L,使用前按照说明书校正。每尾实验鱼的耗氧率用以下公式计算:

    式中,M为每尾鱼的耗氧率(mg O2/h),ΔO2为空白呼吸室与测定呼吸室之间的溶解氧含量差值(mg O2/L),f为测定呼吸室的水流量(L/h),通过测定1 min内呼吸室出水口处流水的体积得到。为了消除体质量的差异对耗氧率造成的影响,使用体质量校正系数0.75将上式中的耗氧率M校正为1 kg体质量的标准耗氧率:

    式中,M′为每尾鱼的标准耗氧率[mg O2/(kg·h)],m为每尾鱼的体质量(kg),M为通过公式(1)计算得到的每尾鱼的耗氧率。

  • 本实验主要采用静止代谢率[mg O2/(kg·h)]、代谢率峰值[mg O2/(kg·h)]、峰值时间(h)、峰值比率、SDA时间(h)、SDA总耗能(kJ/kg)和SDA系数(%)等参数来描述实验鱼摄食代谢特征。各参数计算方法参见相关文献[12]

    利用Excel 2007软件对得到的实验数据进行常规性的计算后,用SPSS 17.0软件进行统计分析。温度和摄食率对SDA参数的影响采用双因素方差分析(ANOVA)。温度对SDA参数的影响采用t-test分析。摄食率对所有参数的影响采用单因素方差分析,若差异显著则进行多重比较(LSD法)。统计值用平均值±标准误(mean±SE)表示,显著差异性水平定为P<0.05。

2.   结果
  • 本实验中各处理组实验鱼摄食后代谢率均显著增加,在摄食后的2~8 h达到峰值,随后逐步下降到摄食前水平(图1)。在相同的摄食率下,25 °C驯化组静止代谢率、代谢率峰值、SDA总耗能和SDA系数都显著高于15 °C驯化组(P<0.001)(表1)。25 °C驯化组在1%和2%摄食率下的峰值时间显著小于15 °C驯化组对应摄食率(P=0.008),但是在4%摄食率下,两个温度组的峰值时间无显著差异(表1)。在相同的摄食率下,25 °C驯化组的峰值比率与15 °C驯化组之间都无显著差异(表1)。25 °C驯化组在1%摄食率下的SDA时间与15 °C驯化组之间无显著差异,2%和4%摄食率下的SDA时间显著小于15 °C驯化组对应摄食率(P<0.001)(表1)。

    Figure 1.  Changes of postprandial metabolic rate in juvenile P. pingi at different temperatures and feeding rates

           指标
           index
    摄食率/%
    feeding rate
    双因素方差分析
    results of Two-Way ANOVA
    1246温度影响
    temperature
    effect
    摄食率影响
    feeding
    rate effect
    交互影响
    interaction
    effect
    体质量/g
    body weight
    25 °C 37.37±1.40 38.83±1.20 38.53±1.52 39.07±1.24 F1,62=0.003
    P=0.954
    F3, 62=0.125
    P=0.945
    F2,62=0.694
    P=0.504
    15 °C 39.12±1.57 37.94±1.11 37.47±1.02
    体长/cm
    body length
    25 °C 14.14±0.23 14.74±0.24 14.18±0.28 14.46±0.31 F1,62=1.120
    P=0.294
    F3, 62=0.527
    P=0.665
    F2,62=0.170
    P=0.844
    15 °C 13.94±0.34 14.14±0.27 14.09±0.23
    摄食率/%
    feeding rate
    25 °C 1.00±0.00d 2.00±0.00c 3.92±0.06b 5.95±0.05a F1,62=1.291
    P=0.260
    F3, 62=6819.793
    P< 0.001
    F2,62=1.322
    P=0.274
    15 °C 1.00±0.00c 2.00±0.00b 4.00±0.00a
    能量摄食率/(kJ/kg)
    energy ingested
    25 °C 49.70±0.00d 99.40±0.00c 194.65±2.97b 295.91±6.88a F1,62=1.291
    P=0.260
    F3, 62=6819.793
    P< 0.001
    F2,62=1.322
    P=0.274
    15 °C 49.70±0.00c 99.40±0.00b 198.80±0.00a
    静止代谢率/[mgO2/(kg·h)]
    resting metabolic rate
    25 °C 69.95±2.63 68.47±2.36 64.58±3.86 64.81±3.02 F1,62=278.392
    P<0.001
    F3,62=1.144
    P=0.339
    F2,62=0.206
    P=0.814
    15 °C 34.69±1.37* 33.12±0.84* 32.05±0.95*
    代谢率峰值/[mgO2/(kg·h)]
    peak metabolic rate
    25 °C 110.39±4.11c 114.11±3.24c 131.18±4.38b 157.84±8.32a F1,62=317.875
    P<0.001
    F3, 62=24.929
    P<0.001
    F2,62=1.096
    P=0.341
    15 °C 53.09±1.16b* 53.84±2.31b* 61.84±2.34a*
    峰值时间/h
    time to peak metabolic rate
    25 °C 2.44±0.29b 3.60±0.58b 7.47±0.72a 8.66±0.82a F1,62=7.528
    P=0.008
    F3,62=21.843
    P<0.001
    F2,62=7.877
    P=0.001
    15 °C 5.55±0.44* 5.56±0.55* 6.22±0.22
    峰值比率
    factorial metabolic scope
    25 °C 1.58±0.03c 1.68±0.05c 2.07±0.07b 2.43±0.06a F1,62=2.337
    P<0.132
    F3,62=49.421
    P< 0.001
    F2,62=0.390
    P=0.679
    15 °C 1.54±0.05b 1.63±0.06b 1.93±0.07a
    SDA时间/h
    duration
    25 °C 16.44±1.19c 16.80±0.61c 20.72±0.62b 25.11±0.89a F1,62=28.201
    P<0.001
    F3,62=21.413
    P<0.001
    F2,62=3.631
    P=0.033
    15 °C 18.89±2.29b 21.56±1.59b* 29.77±1.02a*
    SDA总耗能/[(kJ/kg)
    energy expended on SDA
    25 °C 11.59±1.17c 14.14±1.09c 26.22±1.33b 40.13±2.00a F1,62=52.228
    P<0.001
    F3,62=117.506
    P< 0.001
    F2,62=1.289
    P=0.283
    15 °C 5.61±1.05b* 7.57±0.71b* 16.52±0.99a*
    SDA系数/%
    SDA coefficient
    25 °C 23.33±2.36a 14.23±1.10b 13.45±0.61b 13.58±0.71b F1,62=54.333
    P<0.001
    F3,62=11.717
    P<0.001
    F2,62=3.736
    P=0.030
    15 °C 11.29±2.12* 7.62±0.71* 8.31±0.50*
    注:上标小写字母不同的同一行数值差异显著(P<0.05)。* 表示相同摄食率不同温度驯化组之间差异显著(P<0.05)
    Notes: values in each row without a common lowercase letter indicate a significant difference(P<0.05). The asterisk (*) denotes a significant difference in values between different temperature groups in the same feeding rate (P<0.05)

    Table 1.  Postprandial metabolic characteristics in juvenile P. pingi at different temperatures and feeding rates

  • 15和25 °C驯化组的不同摄食率之间的静止代谢率都没有显著差异。在25 °C驯化组中,4%摄食率的代谢率峰值、峰值比率、SDA时间和SDA总耗能都显著高于1%和2%摄食率,但是却显著低于6%摄食率(P<0.001)(表1)。在25 °C驯化组中,4%和6%摄食率的峰值时间显著高于1%和2%摄食率(P<0.001)(表1),2%、4%和6%摄食率的SDA系数显著低于1%摄食率(P<0.001)(表1)。在15 °C驯化组中,4%摄食率代谢峰值、峰值比率、SDA时间和SDA总耗能都显著高于1%和2%摄食率组(P<0.001)(表1)。在15 °C驯化组中,各摄食率的峰值时间和SDA系数没有显著差异(表1)。

3.   讨论
  • 静止代谢是指鱼类在禁食和相对静止状态下的氧气消耗量,主要反映其维持体液循环、蛋白质合成和渗透压调节等基本生命活动的最低能量需求[26]。本研究发现,在25 °C时,鲈鲤幼鱼的静止代谢率显著高于15 °C,表明其高温下的基础能量消耗明显增加,这将有利于其摄食、消化和运动等生理活动的进行。这种结果在其他鱼类研究中也被发现[7-8, 27]。摄食后代谢峰值往往代表着鱼类最大的消化代谢能力[28]。与以往的研究相似,本研究发现鲈鲤幼鱼的摄食代谢峰值也随着温度的升高而增加,这表明其在25 °C下对食物的消化能力更强,这可能与其胃肠道的蠕动增加,消化酶、胃酸和相应激素分泌量增加以及蛋白质合成与运输加快有关[8, 10, 28]。大多数鱼类的摄食代谢峰值约是其静止代谢时的1.5~2.5倍[29]。有研究发现,具有伏击捕食和躲藏消化习性的南方鲇(Silurus meridionalis)的最大峰值比率能够达到4,并且随着温度的升高而增加[30]。这一特征可能更有利于其在高温下对食物的快速消化和吸收。本研究发现,鲈鲤幼鱼的摄食代谢峰值比率约为1.54~2.43,随着温度的升高并无显著变化。这可能是因为其静止代谢和代谢峰值随着温度的增加而同比例增加导致的。这一现象在鲤(Cyprinus carpio)、中华倒刺鲃(Spinibarbus sinensis)[8]和刺鲈(Sander lucioperca)[9]等鱼类中也有发现。

    SDA时间代表着动物对一餐食物总的消化时间,直接影响着动物对下一次摄食时间的选择。有研究发现,温度并不会对鱼类的SDA时间产生显著性的影响,如短角魟(Myoxocephalus scorpius)[31]、双棘裸南极鱼(Harpagifer bispinis)和扁头澳绵鳚(Austrolycus depressiceps)[32]等。本研究发现,相同的摄食率下,鲈鲤幼鱼的SDA时间会随着温度的升高而明显缩短。由此表明,高温条件下鲈鲤幼鱼能够更快地对食物进行消化和吸收,进而提高其摄食频率。这与南方鲇[30]、日本黄姑鱼(Argyrosomus japonicus) [7]、黄鳍金枪鱼(Thunnus albacares) [10]、刺鲈[9]的研究结果相似。此外,温度对鱼类SDA系数的影响并没有一致的结论。一些鱼类的SDA系数并不会随着水体温度的增加而变化[7, 9, 31]。而另一些鱼类的SDA系数随着温度的升高而增加,如南方鲇[30]、毛利鳕(Paranotothenia magellanica)、双棘裸南极鱼、扁头澳绵鳚[32]和黄鳍金枪鱼[10]等。本研究发现,相同摄食率下,25 °C驯化组鲈鲤幼鱼SDA系数均显著高于15 °C驯化组,由此表明,高温条件下鲈鲤幼鱼用于消化和吸收食物的能量可能较低温条件下更多,进而可能促进其快速生长。

  • 由于摄食率高低所造成的动物代谢率的变化通常与食物所含的能量多少成正比[33],因此,鱼类的摄食后代谢率和能量消耗通常随着摄食率的提高而显著增加[1-3]。有研究发现,杂食性的锦鲫(Carassius auratus)摄食代谢峰值随着摄食率的增加而显著增大,而其SDA时间并无显著性变化。研究者认为,锦鲫主要通过代谢峰值的提高满足其SDA耗能增加的需求,这种消化代谢策略有利于对食物的快速消化和吸收,提高摄食频率,促进自身生长,这与其频繁的摄食习性和较低的摄食率有关[34]。不过,另外一种杂食性鱼类岩原鲤(Procypris rabaudi)的SDA时间随着摄食率的增加而显著延长,摄食代谢峰值却没有显著变化。研究者认为,岩原鲤仅通过延长消化时间来满足SDA耗能增加的需求,暗示其消化速率较慢[12]。本研究发现,不论是高温还是低温环境,鲈鲤幼鱼的代谢峰值、SDA时间和SDA总耗能都随着摄食率的提高而表现出增加的趋势。由此表明,鲈鲤幼鱼主要通过代谢峰值的提高和SDA时间的延长来满足其SDA耗能增加的需求。这种消化策略有利于更加充分地消化和利用食物资源以促进生长,可能与其营养等级较高有关。这一现象在对南方鲇[13]和鲇(S. asotus)[14]等肉食性鱼类的研究中也有发现。

    本研究发现,25 °C驯化组1%摄食率的SDA系数(达到23%)显著高于其他摄食率。这可能是因为高温下各摄食率组消化功能的启动耗能(主要是机械SDA)基本一致,而低摄食率下启动耗能占摄入能量相对比例较高所致。这种现象在对南方鲇和乌鳢(Channa argus)的研究中也有发现[14-15]。然而,15 °C驯化组各摄食率之间的SDA系数却无显著差异。这可能与低温条件下鲈鲤幼鱼消化功能的启动和维持能量相对较低有关,其内在机理有待进一步研究。

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