Effect of fasting on resting metabolic rate and postprandial metabolic ...

Journal of Fish Biology (2005) 67, 279—285 doi:10.1111/j.1095-8649.2005.00723.x, available online at http://www.blackwell-synergy.com

Effect of fasting on resting metabolic rate and postprandial metabolic response in Silurus meridionalis S. J. F U *†, X. J. X I E *‡

AND

Z. D. C A O †

*Institute

of Fisheries Sciences, Southwest China Normal University, Chongqing, 400715, China and †College of Life Sciences, Chongqing Normal University, Chongqing, 400047, China (Received 4 May 2004, Accepted 4 February 2005)

Resting metabolic rate in southern catfish of 2 and 5 day fasting groups were significantly higher than that of the 15 day fasting group (P < 005). After feeding, peak metabolic rate of specific dynamic action (SDA) of the 15 day fasting group was significantly lower than that of the 2 and 5 day fasting groups (P < 005). The duration of the SDA of the 15 day fasting group was significantly longer than that of the 2 day fasting group (P < 005) and the SDA coefficient of the 15 day fasting group was significantly lower than that of the 2 day fasting group # 2005 The Fisheries Society of the British Isles (P < 005). Key words: fasting; lie-and-wait forager; metabolic rate; specific dynamic action.

Due to the temporal and spatial patchiness of food availability, long periods of fasting are common events in the life of aquatic species. The ability to withstand and recover from periods of nutritional stress is a critical adaptation for any organism surviving in a food-limited system (Hervant & Renault, 2002). The ecophysiological effects of fasting for fishes have been studied for several decades (Jobling, 1980; Mehner & Wieser, 1994; Fu et al., 1999; Guderley et al., 2003). Such work has demonstrated that in response to fasting, fishes ‘down regulate’ their physiological functions, and thereby incur a lower maintenance cost (Me´ndez & Wieser, 1993; Mehner & Wieser, 1994). Under such conditions, metabolic capacity and swimming performance may decrease markedly (Collins & Anderson, 1997; Martinez et al., 2003), thus reducing the probability of successful hunting and predator avoidance. The southern catfish Silurus meridionalis (Chen), is a sit-and-wait forager that consumes large meals and lies motionless most of the time (Xie & Sun, 1992a). It is widely distributed in the Yangtze and Zhujiang Rivers where the abundance of its food fluctuates dramatically during the year. The southern catfish probably adopts an energy-saving strategy during extended periods of fasting. Investigations on infrequently feeding snakes suggest that fasting elicit wide ‘down-regulation’ of gut performance (Secor, 2001). Previous work on the structure of the gastrointestinal

‡Author to whom correspondence should be addressed. Tel.: þ86 2368253505; fax: þ86 2365432801; email: [email protected]

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tract and liver of juvenile southern catfish also found the digestive function to be depressed during fasting (Fu et al., 1999). Specific dynamic action (SDA) represents the energy expended on ingestion, digestion and assimilation of food, as well as protein synthesis and deposition (Jobling, 1981; Beamish & Trippel, 1990; Brown & Cameron, 1991; Wang et al., 2001). If southern catfish do experience a depression of digestive function with fasting, then the digestive organs must ‘upregulate’ their functioning when the animal feeds. The ‘upregulation’ of a quiescent gastrointestinal tract would have an impact on the magnitude of the postprandial metabolic response (i.e. SDA). Few studies have fully documented the effects of fasting on maintenance energy expenditure and the corresponding postprandial metabolic response for fishes. The southern catfish was selected to investigate the metabolic responses to fasting and refeeding. The aim of this study was to determine whether fasting in the southern catfish had profound effects on its postprandial metabolic response. Experimental fish were obtained from a local hatchery and acclimated for 15 days prior to the experiment. During this period fish were fed every other day to satiation on pieces of freshly killed loach Misgurnus anguillicaudatus (Cantor). Water temperature was maintained at 275 C, range 02 C, and oxygen content was kept >5 mg l1. The oxygen consumption rate of southern catfish using a 15-chamber (04 l), continuous-flow respirometer modified from the design of Xie & Sun (1990) and Fu et al. (2005) was measured. A feeding tube was mounted at the front of the respirometer to feed fish within the respirometer. The faeces were siphoned out by a tube mounted at the rear of the respirometer chamber. The faeces are usually egested 18—24 h after feeding. One fish was placed in each chamber, with one chamber left empty to serve as a control. The following formula was used to calculate fish metabolic rate (R, mg O2 kg1 h1): R ¼ DO2v m1, where DO2 is the difference in oxygen concentration between an experiment chamber with a fish and the control chamber, v is the velocity of water flow in a chamber, and m is the body mass of the fish. The dissolved oxygen concentration was measured at the outlet of the chamber by an oxygen probe (YSI 52, Yellow Springs Instruments, Yellow Springs, OH, U.S.A.). Water flow through the repirometer chamber was measured by collecting the water outflow from each tube in a beaker over a 2 min period (Cutts et al., 2002). The flow rate of each chamber was adjusted to assure that the outlet water had a minimum saturation of 70% dissolved oxygen in order to avoid stress on physiological processes (Beamish, 1974; Blaikie & Kerr, 1996). To enhance the accuracy of oxygen readings, a difference of at least 1 mg O2 l1 was maintained between the outflow water of experiment chamber and that of the control chamber (Tandler & Beamish, 1980). The light was left on for the duration of the whole experiment period to minimize the effect of circadian rhythms on R (Tandler & Beamish, 1980; Blaikie & Kerr, 1996). Fish were fed in the respirometer chamber every other day for 2 weeks, and then fasted for 2, 5 or 15 days (n ¼ 8 for each fasting treatment). Experimental fish had no food in the gut prior to the experiments in all treatments. Standard metabolic rate (RS) was measured for each fish four times at 2 h intervals. Fish were fed loach meals of 8% of southern catfish body mass (maximum daily ration level, Xie & Sun, 1992b). If a fish did not finish its meal within 15 min, it was removed from the study.

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2005 The Fisheries Society of the British Isles, Journal of Fish Biology 2005, 67, 279—285

EFFECT OF FAST ON METABOLIC RATE IN CATFISH

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The energy content of the loach meals was determined using bomb calorimetry (Model 1281, Parr Instrument Company, Moline, IL, U.S.A.). The mean S.E. energy content of three samples (570 022 kJ g1 wet-mass) was used to calculate the energy content of each meal. To evaluate the effects of fasting on metabolic capacity of the southern catfish, the chasing protocol was used as adopted for studies of cod Gadus morhua L. and largemouth bass Micropterus salmoides (Lacepe´de) (Cutts et al., 2002; Hunt von Herbing & White, 2002) quantifying maximum metabolic rate (Rmax) rather than critical swimming speed, because southern catfish are unable to maintain a stationary position against a current to allow determination of Rmax during critical swimming speed. Eight juvenile southern catfish were chased with a hand-net to exhaustion in a circular trough (usually for 15—30 min), and then each placed in a respirometer chamber immediately. The Rmax was quantified for each fish from the maximum measured oxygen consumption during the recovery process after the fish had been chased. The Rmax was usually observed 15—20 min after the fish were placed in the chambers. The following five variables were quantified as described by Jobling (1981) and Secor & Diamond (1997): peak metabolic rate (Rp), the observed maximum postprandial metabolic rate Rmax; factorial metabolic scope, Rp Rs1; duration, time from feeding to when R fell to within the S.E. of Rs for each fish; energy expended on SDA, calculated from the total oxygen consumed above Rs during the duration of SDA; SDA coefficient (%), energy expended on SDA quantified as a percentage of the energy content of the meal. The oxygen consumption was converted to energy by using a conversion factor of 1384 J mg O21 (Guinea & Fernandez, 1997). STATISTICA 4.5 (StatSoft Inc) was used for data analysis. ANCOVA (body mass as covariate) was used to test the effect of fasting duration on SDA variables. Body mass proved not to be a significant covariate for the effect of fasting duration on Rs (P ¼ 0136), Rp (P ¼ 0059), factorial metabolic scope (P ¼ 0484), duration (P ¼ 0111), energy expended on SDA (P ¼ 0155) and SDA coefficient (P ¼ 0187). ANOVA was used to determine the effects of fasting duration on metabolic variables and the post hoc least significant difference (LSD) was applied to distinguish mean values that differed significantly between pairs of treatments. A P-value 005). The duration of the SDA response for the 15 day fasting group was significantly longer than that of the 2 day fasting group (P < 005), but neither the duration of the 2 day fasting group nor that of the 15 day fasting group was significantly different from that of the 5 day fasting group (P > 005). The #


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TABLE I. The effect of fasting on the standard metabolic rate (Rs), maximum metabolic rate (Rmax) and postprandial metabolic response (Rp) in Silurus meridionalis Treatment Variables

2 days fasting 5 days fasting 15 days fasting

Body mass (g) Meal size (%) Rs (mg O2 kg1 h1) Rs (kJ kg1 h1) Duration (h) Rp (mg O2 kg1 h1) Rp (kJ kg1 h1) Factorial metabolic scope ðRp R1 s Þ Energy expended on SDA (mg O2 kg1) Energy expended on SDA (kJ kg1) SDA coefficient (%) Rmax (mg O2 kg1 h1) Rmax (kJ kg1 h1)

436 802 1038 144 280 3057 423 328 3891 5385 116 3996 553

06 006 46a 006a 12b 84a 012a 025 139a 192a 05a 160a 022a

516 792 1009 140 320 2989 414 298 3506 4852 105 3902 540

26 445 16 015 797 006 44a 879 78b a 006 122 011b 19ab 360 24a a 111 2639 95b a 015 365 013b 022 305 032 147ab 3394 192b 203ab 4697 266b 05ab 101 05b 121a 3252 52b 017a 450 007b

‘Cutlets’ of freshly killed Misgurnus anguillicaudatus without viscera, head and tail were used as test diet. Values in each row without a common superscript are significantly different (P < 005). Data are presented as mean S.E., (n ¼ 8). Water temperature was maintained at 275 C, range 02 C.

Metabolic rate (mg O2 kg–1 h–1)

energy expended on SDA and the SDA coefficient for the 15 day fasting group was significantly lower than that of the 2 day fasting group (P < 005), but energy expended on SDA and the SDA coefficient for the 2 and 15 day fasting group were not significantly different from those of the 5 day fasting group (P > 005).

275

225

175

125

75 0

4

8

12

16

20

24

28

32

36

40

44

48

Time postfeeding (h) FIG. 1. The effect of fasting [2 (*), 5 (n) and 15 (&) days] on postprandial mean S.E. (n ¼ 8) metabolic rate in juvenile southern catfish. Fish were fed at 0 h, water temperature was maintained at 275 C, range 02 C.

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The Rmax of southern catfish of the 2 and 5 day fasting groups were significantly higher than those of the 15 day fasting group (P < 005) (Table I). Fasting duration had significant effect on Rp, SDA duration and energy expended on SDA. The Rp expressed as multiplies of Rs (i.e. factorial metabolic scope) ranged from 298 to 305. These scopes are higher than those observed previously (Jobling, 1980; Hunt von Herbing & White, 2002; Peck et al., 2003), which usually ranged between 15 and 25 (Jobling, 1981). The SDA coefficients ranged from 101 to 116 in this study. The value is within the range calculated for other fishes (10—19%, Jobling, 1981). The SDA duration ranged from 28 to 36 h. It was a little longer than those of fishes such as Cephaloscyllium ventriosum (Garman) (Ferry-Graham & Gibb, 2001) and Sparus aurata L. (Guinea & Fernandez, 1997) and markedly longer than that of wren chick Troglodytes aedon (Chappell et al., 1997). It was much shorter, however, than that of infrequently feeding reptiles such as Python molurus (Secor & Diamond, 1997). The Rs of the 2 and 5 day fasting groups were not significantly different. The Rs of the 15 day fasting group, however, was lower than those of the 2 and 5 day fasting groups, which suggests that the ‘downregulation’ of the physiological function occurs in this fish with fasting. The metabolic capacity, Rmax; in this southern catfish also decreased with fasting duration. This suggests that aerobic performance is also ‘downregulated’ during fasting. The Rmax is set by limits for assimilation, transportation, mobilization and utilization of oxygen and aerobic substrate (Peterson et al., 1990; Hammond et al., 2000). The decrease of Rmax might suggest that the cardiovascular system’s capacity to uptake or transport oxygen or the physiological function of muscle mitochondria decreased. As for the Rp, the ‘downregulation’ of the capacity of any tissues involved in the digestive process might lead to the decrease of Rp. For example, secretion of digestive enzymes and intestinal nutrient uptake. Under conditions of fasting, southern catfish decreases energy expenditure. The decrease of metabolic capacity may partly account for the extension of the digestive period. Under such conditions, the probability of successful hunting and avoiding predation might also decrease. The regulation of physiological status occurs in the southern catfish when it faces fluctuations in food resources. When food is limited the animal saves energy by ‘downregulation’ of physiological functions When food resources are abundant, however, the fish may favour ‘upregulation’ of its metabolic performance at the cost of more energy expenditure and lower energy efficiency (Mueller & Diamond, 2001).

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