The behavioural, digestive and metabolic characteristics of fishes with different foraging strategies

Animals can be classified as ambush (i.e. sit-and-wait) foragers, active foragers or herbivores according to their foraging mode(Cooper, 1995). Researchers have suggested that foraging mode might be closely related to an animal's morphological, physiological and ecological characteristics and life-history traits (Huey and Pianka, 1981; Webb et al., 2003). Swimming performance, metabolic characteristics and digestive capacity may also change according to foraging behaviour in fishes and other animals(Perry, 1999; Newland et al., 2004). For example, Secor (Secor, 2001)suggested that the maximum feeding level and feeding metabolism were much higher in some sedentary ambush predators than in active foragers. Others reported that the maximum oxygen consumption rate after feeding(V̇_O2peak) of some ambush fishes was similar to (or even higher than) maximum aerobic V̇_O2(V̇_O2max) during maximum sustainable swimming (Priede,1985; Armstrong et al.,1992; Fu et al.,2005a). However, little has been done to compare the swimming performance, metabolic characteristics and digestive capacity of fishes with different foraging modes. Previous studies on the foraging mode of fishes have focused on swimming efficiency and prey encounter rate of pelagic fishes(Miyasaka and Nakano, 1999; Asaeda et al., 2001), while the sit-and-wait foraging fishes have received little attention. Thus, the first aim of this study was to determine whether significant differences in routine activity level, swimming performance, metabolic characteristics and digestive capacity exist among fishes with different foraging modes.

Feeding (hence digestion) and locomotion are the two most closely related activities involved in foraging behaviour. Although they differ in many aspects, they share the cardio-respiratory system required to obtain and supply oxygen and substrate (Hicks and Bennett, 2004). The outcome of the competition between these two activities might be different in fishes with distinct foraging modes because postprandial swimming has a different ecological relevance. Sedentary ambush fishes usually consume a large meal and then remain motionlessness for a long time while digesting, whereas active fishes must continue foraging for prey during digestion. Thus, the capacity for postprandial locomotion should be maintained in active foraging fishes. However, no comparative work exists examining the effect of feeding on locomotion in fishes with different foraging modes. Thus, the second aim of this study was to test whether digestion has different effects on the postprandial locomotory capacity in fishes with distinct foraging modes.

Newlands and colleagues (Newlands et al., 2004) suggested that the energy expenditure and return of various types of foraging behaviour are of importance in determining foraging mode in fishes. Theoretically, the differences in routine activity or locomotory capacity among fishes with different foraging modes must closely relate to their energetic profiles. The positive relationship between locomotory capacity and metabolism (either resting or maximum metabolism) has long been accepted (Wieser,1985). However, there is an apparent gap in the understanding of the energy expenditure for maintenance and the metabolic constraints on locomotory and digestive performance in different foraging fishes. Hence, our third aim was to study the metabolic strategy (i.e. metabolic ceiling, energy expenditure for maintenance and relative magnitude of the metabolic scope of digestion and locomotion) used by fishes with different foraging modes.

To address our research objectives, we selected four species of juvenile fish with distinctly different foraging modes: a sit-and-wait carnivorous southern catfish (Silurus meridionalis), an active grazing herbivorous grass carp (Ctenopharyngodon idellus), a sluggish omnivorous darkbarbel catfish (Pelteobagrus vachelli) and an active omnivorous crucian carp (Carassius auratus). The first three species are the most abundant species with their respective foraging mode in the Yangtze River (Ding, 1994). The crucian carp is a highly adaptable species with a wide distribution throughout the world, including the Yangtze River. We measured the number of movements per minute (MPM) and the per cent time spent moving (PTM) to identify foraging mode and demonstrate activity levels; the resting V̇_O2(V̇_O2rest) to represent maintenance energy expenditure; V̇_O2max to represent the metabolic ceiling; and the critical swimming speed (maximum sustainable swimming speed, U_crit) and stamina (duration at a fixed swimming speed) to represent the aerobic and anaerobic swimming capacity, respectively; and the maximum feeding level and the postprandial metabolic response to represent the digestive capacity.

Juvenile southern catfish (S. meridionalis Chen; 17.72±0.39 g, N=100), crucian carp (C. auratus Linnaeus;6.01±0.15 g, N=100), grass carp (C. idellusValenciennes 1844; 8.77±0.17 g, N=100) and darkbarbel catfish(P. vachelli Richardson 1846; 7.06±0.18 g, N=100)were obtained from local fisheries and acclimated in a rearing system for at least 30 days before the experiment. The body size of southern catfish was larger than that of the other three species because of its fast growth rate. Therefore, it was difficult to find experimental animals with a body size similar to that of the other tested species. The dechlorinated fresh water temperature was maintained at 25.0±0.5°C, and the oxygen content was kept above 7 mg l^–1. During the acclimation period, the crucian carp and the grass carp were fed to satiation with a formulated diet,and the southern catfish and the darkbarbel catfish were fed fillets of freshly killed loach (Misgurnus anguillicaudatus) once daily. The chemical composition of the formulated diet was 61.45% moisture, 14.91%protein, 1.62% lipid and 8.70% digestible carbohydrate, resulting in 5.02 kJ g^–1 of bio-available energy. The loach flesh was 78.20%moisture, 15.71% protein, 3.17% lipid and 0.07% digestible carbohydrate,resulting in 4.97 kJ g^–1 of bio-available energy. The dietary bio-available energy was calculated as 23.6 kJ g^–1 protein,39.5 kJ g^–1 lipid and 17.2 kJ g^–1 starch. Analyses of chemical composition were conducted following standard methods(Association of Official Analytical Chemists, 1995).

To measure PTM and MPM, 12 fish from each species were transferred to 48 individual observation chambers (120 l) and acclimatised for 3 days. The chambers were cylindrical unplasticised polyvinyl chloride (UPVC) tanks with lids. Because of the relatively low biomass-to-water volume ratio in the observation chamber (3.95–10.36 g/120 l), the water was partially replenished daily (20%) with slight aeration. Fish were observed through a window on the lid at 09:00, 15:00 and 21:00 h on the fourth day after they were transferred to the observation chamber. Individual fish were observed continuously for 15 min. To compensate for the disturbance of fish by the observer's presence, the first 5 min of each observation was omitted from further analyses. We defined movement as motion of the tail fin. Movement was considered to cease when the tail fin rested for more than 1 s. The tail fin was selected because it concurrently shows motion with any kind of body activity (other than opercular activity) in these four species, and its motion is easy to measure precisely. The following data were recorded: whether the fish showed movement during the whole observation period, total number of movements, and the duration of movement. The total number of movements was recorded by a hand tally counter, and the duration of the movement was recorded by a stopwatch. The PTM (%) and MPM (times min^–1)were calculated over the entire 10 min observation period.

Each fish (see Table 2 for sample size) was placed in the respirometer chamber and allowed to acclimate for 1 week before the experiment was conducted. After the fish had been fasted for 48 h, the V̇_O2was measured four times at 2 h intervals and used as V̇_O2rest(Fu et al., 2005a). The V̇_O2max was measured using the chasing method as described previously(Fu et al., 2006). Briefly,the experimental fish were chased to exhaustion with a hand net in a circular trough (the process usually lasted 3–5 min) and then immediately placed into a respirometer chamber. The water flow rate was about 0.6 l min^–1, and 99% of the water was replaced within 1 min in the 0.1 l chamber (Steffensen,1989). The first measurement of oxygen consumption was made 1 min after the fish was placed in the chamber. Maximal oxygen consumption was usually observed immediately (1–4 min) after the fish was placed in the chamber, but the measurement was continued for 30 min.

The postprandial V̇_O2 responses were measured using the continuous-flow respirometer at relative feeding levels of 0, 0.5, 1, 2, 4 and 8% body mass in the darkbarbel catfish and 0,0.5, 1, 2 and 4% body mass in the crucian carp and the grass carp with either fish fillets or the formulated diet. The maximum feeding level was 8% body mass for the darkbarbel catfish and 4% body mass for both carp species. Because in each treatment group only the fish that finished their food in 30 min during the trial were used for the experiment, the number of fish was 6,7, 7, 6 and 5 in the control, 0.5, 1, 2 and 4% body mass crucian carp groups,respectively, and 8 in all the grass carp and the darkbarbel catfish groups. The effects of feeding level (Fu et al.,2005a), temperature (Luo and Xie, 2008a) and body size (Luo and Xie, 2008b) on postprandial V̇_O2 response in southern catfish were studied extensively in our previous research; therefore,we did not repeat those parts of the experiments in the current study.

The fish were placed in the respirometer chamber and allowed to acclimate for 1 week before the experiment. V̇_O2 was measured after a 48 h fasting period. A prescribed quantity of fish fillet or formulated diet was then offered. Immediately after the fish had completed feeding, the chambers were closed, and the V̇_O2 was measured at 2 h intervals for 12 h for the crucian carp and grass carp, and 36 h for the darkbarbel catfish. The maximum feeding level and duration of the experiment were determined in a pilot experiment. A sample of each diet was collected and dried to a constant mass at 70°C for composition analysis.

U_crit and stamina were measured using gravity-driven swimming tunnels (Zhang et al.,2007). In brief, a hydraulic pressure was established between the upper holding reservoir and lower receiving tank. The hydraulic pressure was maintained by a fixed vertical height difference between the water levels of the two tanks. The water flow velocity in the swimming tunnels was dictated by parallel variable valves that could independently adjust the resistance and flow of the water entering the swimming tunnels. The inner diameter and the length of the swimming tunnel were 10 cm and 60 cm, respectively. The maximum velocity of the water flow was about 42 cm s^–1. A honeycomb plate was fixed to either side of the swimming tunnel, helping to reduce turbulence and eddies. The swimming tunnel was situated in a thermally controlled water bath, and the experimental water temperature in the swim chamber was maintained at 25.0±0.5°C in this study.

After 48 h of fasting, the experimental fish were offered the prescribed diets. Because some fish did not consume their food during the given 30 min or vomited during the experimental process, the sample number in each treatment varied from 4 to 10 (Table 3). U_crit was measured for each fish at a prescribed hour after feeding when the fish had achieved its peak postprandial V̇_O2 at a given feeding level (according to postprandial V̇_O2 response data in this study or previous work) (Fu et al., 2005a; Luo and Xie,2008a; Luo and Xie,2008b). The grass carp, crucian carp and darkbarbel catfish were transferred to the swimming tunnel 1 h after feeding. The southern catfish,however, was transferred to a swimming chamber at 3, 5, 10, 12 and 12 h after feeding for the 2, 4, 8, 12 and 20% body mass groups, respectively. U_crit of fasting fish was measured as the control group.

Before stamina was measured, the fish were acclimated at 1 BLs^–1 water flow for 1 h. Then, water velocity gradually increased to 9 BL s^–1 for crucian carp and 6 BL s^–1 for southern catfish at increments of 1 BL s^–1. The velocity of water flow was determined in a pilot experiment. The stamina test was terminated when the fish failed to move off the rear grid. The stamina was determined as the duration of time between the point when the specific velocity (9 BLs^–1 for the crucian carp and 6 BLs^–1 for the southern catfish) was achieved and the point when the fish ceased swimming. Feeding metabolism is generally considered to be an aerobic process. Thus, anaerobic locomotory capacity, indicated by variables such as anaerobic stamina, is unlikely to be affected by feeding metabolic processes such as digestion. We chose to measure only the stamina in the two extreme species in fasting status and after a maximum meal: the sedentary southern catfish and the active crucian carp were chosen because they have the lowest and highest U_crit, respectively. We predicted that postprandial digestion would have little effect on their anaerobic stamina.

We used STATISTICA 4.5 (StatSoft, Singapore) for the data analysis. The hypotheses were tested using ANOVA, followed by post-hocmultiple comparisons (least significant difference). P values<0.05 were considered statistically significant, and all the data are presented as means ± 1 s.e.m.

Some experimental fish did not show any defined movement during the entire 10 min observation period. Among the 36 observations, in all four tested species, 36/36 crucian carp, 28/36 grass carp, 29/36 darkbarbel catfish and 2/36 southern catfish showed movement. Table 1 shows the PTM and the MPM for the four fish species. Both PTM and MPM showed significant differences among all the fishes tested (P<0.05).

The V̇_O2rest of the crucian carp was 24% higher than that of the grass carp(P<0.05; Table 2),and the latter was about 30% higher than the values for the darkbarbel catfish and the southern catfish (P<0.05). The V̇_O2max values of the crucian carp and the grass carp were about 80% higher than that of the darkbarbel catfish (P<0.05), and the latter was 67% higher than that of the southern catfish (P<0.05).

The maximum feeding levels were about 4% body mass for the crucian carp and the grass carp and about 8% body mass for the darkbarbel catfish. The postprandial V̇_O2response was most notable in the crucian carp, which showed the highest V̇_O2peak (173.2 mg O₂ kg^–1 h^–1, 148% higher than that of V̇_O2rest)and shortest duration (2–8 h depending on feeding levels; Fig. 1). The postprandial V̇_O2 response was lowest in the grass carp, which also exhibited the lowest V̇_O2peak (83.6 mg O₂ kg^–1 h^–1, 49% higher than that of V̇_O2rest) and a relatively short duration (8–10 h). The V̇_O2 response in the darkbarbel catfish was lower than that of the crucian carp, but it exhibited a long duration at the higher feeding level (such as the 4% and 8%body mass, respectively).

Feeding level had a profound effect on V̇_O2 response in all the fishes tested in this study. In the crucian carp, V̇_O2 peaked significantly (P<0.05) at 2 h after feeding and returned to the pre-fed level within 6–8 h after feeding depending on feeding level. For the darkbarbel catfish, the postprandial V̇_O2 responses to lower feeding levels (0.5, 1 and 2% body mass) were low and hard to detect. However, both the 4 and 8% body mass groups showed prolonged postprandial V̇_O2 elevation,which was about 70–80% higher than the control level and lasted for about 20 h. The V̇_O2 of all the grass carp groups peaked at 2 h after feeding. The 0.5% body mass and control groups did not return to the pre-fed level. However, the 1, 2 and 4% feeding level groups returned to the pre-fed level within 6–8 h after feeding.

U_crit of the fasting crucian carp was more than 60%higher than the levels found in the grass carp and the darkbarbel catfish, and U_crit of the darkbarbel catfish was more than 50% higher than that of the southern catfish (P<0.05, Table 3). U_crit had a tendency to decrease with increased feeding level in all the fish species studied. However, there was no significant change in U_crit in both the grass carp and the darkbarbel catfish. In the southern catfish, U_crit decreased 34%after consumption of the maximum meal, and U_crit values at the maximum feeding level (20%) and the 12% body mass feeding level groups were significantly lower than those of all the other groups(P<0.05). There was no significant difference among the other groups of southern catfish. In the crucian carp, U_critdecreased significantly even after consuming at 0.5% feed level(P<0.05), but there was no significant difference among the 0.5, 1 and 2% feeding level groups. The maximum meal (4%) elicited a 12% decrease in U_crit compared with the fasting group, which was significantly lower than the U_crit of the control and the 1% feeding levels.

The effect of maximum feeding level on stamina was investigated only in the southern catfish and the crucian carp. The velocity of the water flow was 9 BL s^–1 for the crucian carp (body mass 6.08±0.10 g) and 6BLs^–1 for the southern catfish (body mass 18.73±0.42 g). The maximum feeding levels were 21.33±1.33% for southern catfish and 4.44±0.00% for the crucian carp. The stamina values of crucian carp fed at the maximum feeding level and without food were 40.77±13.01 s (N=9) and 36.27±6.54 s(N=7), respectively. The stamina values of the southern catfish fed at the maximum feeding level and without food were 51.00±3.61 s(N=9) and 36.13±4.65 s (N=6), respectively. There was no significant difference in the stamina of fish between the maximum feeding level and control groups in both the southern catfish and the crucian carp.

The main aims of this study were to test whether digestion has a different effect on the capacity for postprandial locomotion in fishes with different foraging modes, and whether the different effect related to the differences in behavioural, digestive and metabolic strategies that exist among fishes with distinct foraging modes. Fishes selected in this study showed significant differences in routine activity level, swimming performance, metabolic characteristics and digestive capacity. The active omnivorous (crucian carp)and the herbivorous (grass carp) fishes showed higher levels of activity and locomotory capacity, a higher metabolic ceiling and energy expenditure, and a lower feeding level compared with the sluggish (darkbarbel catfish) and the ambush (southern catfish) fishes. The locomotory capacity in the sedentary fish decreased profoundly after feeding, whereas it decreased little or not at all for active fishes. The effect of feeding on locomotory capacity was related not only to the change of postprandial V̇_O2 but also to the special metabolic strategy, in accordance with the competition between digestive and locomotory metabolism (an increase in V̇_O2max and metabolic scope after eating; see below).

Digestion and locomotion are two primary physiological activities that organisms in nature must, to some extent, conduct simultaneously(Bennett and Hicks, 2001). Research on postprandial locomotion has been popular in recent years in both fishes and reptiles (Blaikie and Kerr,1996; Alsop and Wood,1997; Bennett and Hicks,2001). The present study is the first attempt to explain the change in locomotory capacity that occurs after an animal eats in an ecological context. Theoretically speaking, maintaining the capacity for locomotion is more important in active fishes than in sit-and-wait foragers because the former are more likely to encounter predators and need to be able to avoid capture, and they continue to hunt or graze while still digesting. However, typical active foraging fishes such as rainbow trout(Oncorhynchus mykiss) and chinook salmon (Oncorhynchus tshawytscha) always appear to prioritise oxygen delivery to meet the needs of digestion over oxygen delivery for postprandial locomotion, as demonstrated by a decrease of U_crit by 9–15% after a meal (Alsop and Wood, 1997; Thorarensen and Farrell,2006). On the other hand, in the Atlantic cod (Gadus morhua), when swimming at a low speed after a moderate size meal, the V̇_O2 of postprandial swimming fish was larger than the sum of V̇_O2 elicited by feeding and swimming alone; i.e. the locomotion and digestion activity can process independently. However, because feeding levels had a significant effect on postprandial V̇_O2(Jobling 1981; Fu et al., 2005a), whether the additivity model adopted by cod can be maintained after a huge meal needs to be investigated further.

In the present study, U_crit of the sit-and-wait southern catfish did not decrease significantly when it was fed a meal under 8% body mass compared with the fasting fish. However, when the feeding level increased to 20%, U_crit showed a 34% decrease. The value was much larger than all published data about the effect of feeding on U_crit (Alsop and Wood,1997; Thorarensen and Farrell,2006). The low U_crit of fasting fish, the trapezoid-shaped postprandial V̇_O2 profile of fish after a large meal and the higher maximum feeding level suggest that the aerobic locomotory capacity was almost totally lost for a substantial period of time after the consumption of a large meal in the southern catfish. Because the southern catfish has a habit of digesting food while lying motionless at the bottom of a river and it belongs to the highest trophic level in its habitat, it is unlikely that it needs a large locomotory capacity, whereas digestion is necessary. The allocation of most of the metabolic capacity for digestion in the sit-and-wait southern catfish might favour fast digestion and growth (Priede 1985; Fu et al., 2005a; McGraw, 2007). However,regarding the question of whether digestion has a more profound effect on the capacity for postprandial locomotion in sit-and-wait fishes than it does in other fishes, more comparative work on species with different foraging modes using a full range of feeding levels needs to be conducted before a satisfactory conclusion can be made (Blaike and Kerr, 1996; Thorarensen and Farrell,2006). Sit-and-wait fishes, such as the pike (Esox lucius) and other kinds of sedentary catfish, might be a suitable model for future study.

In the grass carp, it was not surprising to find that U_crit showed no significant change after a meal because maximum feeding level (4% body mass) only elicited a 50%V̇_O2 increase compared with V̇_O2rest (i.e. it only accounted for 10% of total metabolic scope, as calculated by the difference between V̇_O2max and V̇_O2rest). This finding makes sense because the grass carp, with a small maximum feeding level, must graze for low-energy plant tissue with some food in the gut (i.e. in digestive status) throughout the day to meet its energy and nutrient requirements. U_crit of the fasting grass carp was greater than that of the sedentary southern catfish, but it was similar to that of the sluggish darkbarbel catfish, possibly due to the fact that the herbivorous grass carp does not require a high U_crit to chase prey. Researchers have suggested that animals with a higher locomotory performance usually have a higher metabolic capacity and maintain a higher metabolic cost when at rest (Reinhold 1999; Chappell et al., 2007). However, the V̇_O2rest of the grass carp was significantly higher than that of the darkbarbel catfish despite their similar U_crit, which is partly due to their levels of routine activity (higher MPM and PTM in grass carp). Furthermore,other locomotory performance (in addition to U_crit) such as the fast-start performance may be involved in the metabolic strategy. The fast-start performance was considered to be closely related to escape manoeuvres. Hence, the grass carp has a metabolic strategy that expends the most energy to maintain the locomotory performance involved in avoiding predators, some energy to maintain the locomotory performance related to grazing, and little energy for digestive performance.

In the crucian carp, the unanticipated profound postprandial V̇_O2 increase was even larger than that in southern catfish if we take the feeding level into account. However, the U_crit only showed a 12% decrease,even though the metabolic scope exhibited a 45% decrease as calculated by V̇_O2peak, V̇_O2max and V̇_O2rest. The reason for this discrepancy lies in the high flexibility of the crucian carp's cardio-respiratory system. Fu and colleagues(Fu et al., 2009) found that the V̇_O2maxincreased from about 300 mg O₂ kg^–1h^–1 in fasting fish to 400 mg O₂kg^–1 h^–1 in feeding fish. Hence, the metabolic scope for locomotion changed little after feeding in the crucian carp. This means that the metabolic strategy of the crucian carp is to maintain a high metabolic capacity, which can support high activity in both feeding and locomotion. The cost of such a strategy is illustrated by the V̇_O2rest data: the V̇_O2rest of the crucian carp was 25–60% higher than those of the other three fishes studied. With such a strategy and the short duration of the digestive process,feeding activity actually had little effect on locomotion from an ecological perspective.

In the darkbarbel catfish, the cellular metabolic capacity of the digestive organs is lower compared with that of the crucian carp and the southern catfish (Fig. 1), as suggested by the lower postprandial V̇_O2 curve and the prolonged trapeziform profile that occurs after a large meal. Such a digestive strategy guarantees a high capacity for locomotion after feeding, which might be critical for searching for food while still digesting. The activity, U_crit and V̇_O2rest of the darkbarbel catfish were lower than those of the active crucian carp. The explanation for this difference can be found in the traits of the darkbarbel catfish. With its venomous pectoral fin, the darkbarbel catfish can catch prey(it usually searches for small prey at night) without having to swim fast, and with its yellow aposematic colouration, it does not require the higher locomotory capacity involved in avoiding predators and thus does not have to expend energy to avoid being eaten. The darkbarbel catfish, which has the protection of venom, uses some energy for foraging and uses less energy for both digestion and predator avoidance activities.

McLaughlin (McLaughlin,1989) suggested that foraging modes are species-specific strategies that are correlated with a suite of behavioural, ecological,physiological and morphological characteristics. This premise was exhibited in the sit-and-wait southern catfish in the present study. It had a large feeding level and a high digestive capacity (suggested by the large postprandial V̇_O2peak), a low activity level (as suggested by the low PTM and MPM), and a low swimming performance (as suggested by the U_crit), and hence a lower energy expenditure (as suggested by the lower V̇_O2rest). It also had great flexibility in its digestive physiological response to nutritional status (Fu et al., 2005b). All of these characteristics are highly adaptive to its sedentary ambush life style (Priede 1985; Armstrong et al., 1992) and ensure high energy efficiency (more than 60% of ingested energy is channelled into growth) and fast growth rate (they can reach 3–4 kg in the first year when food is abundant and usually reach maturation at about 5–7 years in the wild). It is not surprising that the southern catfish is the most successful ambush forager in its habitat. The crucian carp's higher metabolic cost strategy and additivity metabolic model ensure that it can cope with the physiological issues of digestion, locomotion and postprandial locomotion. For the grass carp and the darkbarbel catfish, the lower digestive capacity strategy allows them to maintain their locomotory capacity to forage for food.