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The effects of food pellet dimensions on feeding responses by Atlantic salmon (Salmo salar L.) in a marine net pen
ELSEVIER
Aquaculture 130 (1995) 167-175
The effects of food pellet dimensions on feeding responses by Atlantic salmon (S&w salar L.) in a marine net pen I.P. Smith*, N.B. Metcalfe, F.A. Huntingford Fish Behaviour and Ecology Group, Department of Zoology, University of Glasgow, Glasgow Gl2 8QQ, UK
Accepted 2 August 1994
Abstract The effects of the diameter and length of cylindroid food pellets on the feeding responses of onesea-winter Atlantic salmon in a marine net pen have been investigated. Pellets of different shapes and sizes were dropped into the pen in a random sequence and the responses of salmon were recorded with a video system. Both the diameter and length of pellets affected the time until first capture, with salmon taking longer to capture small pellets. The probability of a pellet being rejected after having been grasped was related to its length, but not its diameter: shorter pellets were rejected least often. Thus, the larger pellets that appeared to be initially most attractive to salmon were not the sizes that they ingested most readily once grasped. Acceptability (as indicated by rejection rate) varied over the range of pellet lengths that occurs within the size class of commercial feed recommended for these fish, and the optimum length (in terms of the number of pellets eaten rapidly) was shorter than the mean length of commercial pellets. The possible interaction of the effects of pellet size and hardness on palatability should be investigated. Kevwords: Salmo salar; Feeding and nutrition -
fish - behaviour; Feeding and nutrition - Pellet dimensions
1. Introduction
Efforts to maximise feed utilisation in salmonid aquaculture should take account of fish feeding behaviour. The proportion of administered feed consumed is partly determined by the responses of fish to individual food particles. Ingestion of food involves a sequence of events starting with detection of a potential food item, continuing through orientation, *Corresponding author. Present address: Scottish Office Agricultureand Fisheries Department, Marine Laboratory, PO Box 101, Victoria Road, Aberdeen AB9 SDB, UK 0044-8486/95/$09.50 0 1995 Elsevier Science B.V. All rights reserved SsDIOO44-8486(94)00207-X
168
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approach and capture, leading ultimately to the item being swallowed (Stradmeyer, 1989). This sequence may terminate at any stage prior to swallowing. For example, having approached a food item, a fish may proceed to capture it or leave it; having captured a food item, the fish may either swallow or eject it (Wahkowski, 1979; Knights, 1985). Completion of the feeding sequence depends both on the motivational state of the fish and the characteristics of the food particle (Huntingford and Thorpe, 1992). Physical attributes of the particle not only affect the ability of the fish to eat it (a food item may be too large to capture, for example), but also influence whether the fish is stimulated to eat it (a pellet may not be perceived as a desirable food item). Food particle design is therefore an important consideration when processed feedstuffs, such as pelleted fish meal, are used. Studies of juvenile salmonids indicate that some forms of dry pelleted food are less likely to elicit feeding responses than wild prey (Paszkowski and Olla, 1985; Stradmeyer and Thorpe, 1987) and several characteristics of artificial food items have been found to influence the probability of ingestion by juvenile salmonids (Mearns, 1990; Stradmeyer, 1992). The size and shape of food items are likely to be important at each stage of the feeding sequence, by influencing their detectability, attractiveness, ease of capture and probability of ingestion once captured (acceptability) (Stradmeyer et al., 1988). Size and shape of food items may have contrasting effects on attractiveness and acceptability (Metcalfe et al., 1987; Stradmeyer et al., 1988). Wankowski and Thorpe ( 1979) found that the growth rate of Atlantic salmon parr was influenced by food particle size. At most times of year, parr grew fastest on food particles of a width equivalent to 2.2-2.6% of the fishes’ mean body length, similar to the optimum size indicated by behavioural observations (Wahkowski, 1979). The feeding responses of post-smolt Atlantic salmon in relation to pellet characteristics have received less attention than those of fry and parr. Commercially supplied pellets for marine phase salmon tend to be approximate cylinders of relatively precise diameter, but variable length (Stradmeyer, 1992). Atlantic salmon in marine net pens are known to capture and then eject commercially produced pellets (Juell, 1991; Smith et al., 1993). Consequently, the present study was designed to investigate the influence of food pellet dimensions on the feeding responses of one-sea-winter Atlantic salmon in a marine net pen.
2. Materials and methods Study site and$sh The study was carried out at a commercial production site in Dunstaffnage Bay, Argyll, W. Scotland in April 1991. Atlantic salmon were stocked in a net pen (net depth 5 m; wooden collar 7 X9 m) as l-year-old smolts in May 1989. During the study the pen contained approximately 860 fish with an average weight of 3.4 kg. During non-observational periods, the fish were fed commercially produced pellets of the manufacturer’s recommended size ( ‘Mainstream’ Grower 6, BP Nutrition (UK) Ltd., Northwich), which were dispensed to the centre of the pen at 5-min intervals during daylight by an automatic feeder (Tessomat lOOL.B-12, Tess Aquaculture Ltd., Newport). In addition, fish farm staff dispensed a small quantity of the same type of pellets by hand at approximately 08.00 h
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each day. We had access to only one net pen, but our study fish appeared typical of salmon of the same age at the site. Experimental pellets Commercially produced pellets were approximate cylinders with a diameter of 8 f 0.2 mm and length of 13 + 3.5 mm (X + s.d.) , a 1ength:diameter ratio of 1.625. Experimental pellets were prepared in four diameters (5,6,8, 10 mm) and three lengths (6, 13,20 mm). The lengths corresponded to the mean length + 2 s.d. of commercial pellets (i.e. they were within the range of lengths found in commercial feed). Experimental pellets of diameter 8 mm were also manufactured in lengths of 8, 10 and 16 mm, which corresponded to 1.625 times the other experimental pellet diameters (5, 6 and 10 mm). Experimental pellets were prepared by grinding commercially produced pellets (BP Mainstream) with a pestle and mortar and mixing the resulting powder with water at room temperature. This paste was extruded from a rigid PVC tube (diameter 8 cm) through an appropriately sized hole drilled in a flat end-plate (thickness 0.5 cm) attached to the tube, with a pressure of approximately 2OAO kPa. The cylinders of paste thus formed were allowed to dry at room temperature and were then cut to the required lengths. Observation of feeding responses The responses of salmon to experimental pellets were observed with a video system. The video camera (charge coupled device, 12.7 mm format, lens focal length 3.5 mm) was encased in a cylindrical, waterproof housing (diameter 12 cm, length 18 cm) (C-Technics, Oban), mounted on a scaffold gantry so that the lens was positioned just below the water surface, 2 m from one side of the pen, viewing directly downwards. The angle of view was approximately 65” and the depth of view (which depended on water transparency and ambient light level) was approximately 4 m. The camera was connected by a waterproof cable to a video recorder (Video Walkman, Sony Corporation, Tokyo). Recordings were made in daylight and no artificial light was used. Single pellets of each size were dispensed into the pen in a random order at 30-s intervals, between actuations of the automatic feeder. Pellets were dropped into a plastic pipe that guided them into the water next to the video camera. It was not possible to determine the fate of all pellets presented, since some drifted laterally out of the camera’s field of view, or were obscured by fish. The fate of 357 pellets was recorded. Sample sizes for each pellet type are given in Table 1. Statistical analysis Four measures of the behavioural responses of salmon to experimental pellets were made from the video recordings: the time between pellets appearing in the field of view and the first grasp by salmon (response time) ; the proportion of pellets ejected from the mouth after having been grasped (rejections) ; the proportion of pellets eaten rapidly (within 5 s of appearing in the field of view); and the time taken for pellets to be eaten. Pellets that sank out of sight were deemed to be uneaten (27.2% of pellets whose fate was recorded). Uneaten pellets took approximately 30 s to sink out of sight and were excluded from analysis of the time taken for pellets to be eaten. Response time was determined for the first 215
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Table 1 Sample sizes for observations lengths
of feeding responses
I30 (1995) 167-175
of salmon to experimental
pellets of different diameters and
Diameter
Length
(mm)
(mm)
Number of pellets of known fate
Number of grasps’
Sample sizes for response times’
Number of pellets uneaten3
5 5 5 6 6 6 8 8 8 8 8 8 10 10 10
6 13 20 6 13 20 6 8 10 13 16 20 6 13 20
33 35 38 26 35 35 14 16 30 15 16 18 17 14 15
34 34 34 22 37 37 18 17 35 17 24 22 16 22 28
16 14 12 12 13 18 10 7 17 8 10 8 5 9 10
8 11 19 9 10 9 1 5 2 5 1 5 5 3 4
‘The number of times salmon rejected pellets was analysed in relation to the number of grasps. ‘Response time was determined for the first 215 pellets presented, ignoring those to which there was no response. ‘The number of pellets that sank out of sight, including those that had been grasped and rejected by salmon.
pellets only, but since pellets were presented in a random order, this should not bias comparisons of this measure among pellet sizes. Response time and time to eat pellets were analysed in relation to pellet diameter and length by analysis of variance (ANOVA), followed by Scheffe’s test for multiple comparisons (Zar, 1984). Measurements of time were normalised by square root transformation. Pellet length
6 mm 14
-
12
-
10
-
8
-
6
-
4
-
2
-
20 mm
13 mm
I
O-
31 II 8 5
Pellet diameter (mm)
B
10
Fig. 1. Mean response time of Atlantic salmon to cylindroid food pellets of different lengths and diameters, Error bars represent standard errors; sample sizes are given in Table 1.
1-P. Smith et al. /Aquaculture
130 (1995) 167-175
The proportion of grasps resulting in rejection and the proportion were analysed by log-linear analysis (Wilkinson, 1990).
171
of pellets eaten rapidly
3. Results The mean response time of salmon to experimental pellets varied significantly among diameters and lengths of pellet (Fig. 1; two-factor ANOVA, F,,,,, =5.64, P< 0.01, F 2.,23 = 9.98, P < 0.001 and F6,rz3 = 0.56, P > 0.50 for diameter, length and interaction term, respectively). Response times did not differ significantly between pellet diameters 5 mm and 6 mm (Scheffe’s test, S =0.682, P> 0.05) or between diameters 8 mm and 10 mm (S = 0.482, P > 0.05)) but salmon took significantly longer to respond to the two smaller (a)
Pellet length 13 mm
6 mm
2 6 I.= P CL .c P e z F “a 62
7o
r
60
-
50
-
40
-
30
-
l-l
20 10
0
(b)
w
2
n
10
a” 0
0 ton5
6
I
0
8 10
8
Pellet
diameter
(mm)
Fig. 2. Feeding responses of salmon to pellets of different sizes: (a) percentage of grasps that resulted in rejection of the pellet; (b) percentage of pellets eaten within 5 s. Sample sizes are given in Table 1.
I.P. Smith et al. /Aquaculture
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130 (1995) 167-175
Pellet length
-
12
-
20 mm
13 mm
6 mm 14
z? ?% $ B
86-
z F
4
0 5
IO0AIlI
-
5
6
a
IIII 10
5
6
a
I 10
:
Pellet diameter (mm)
!lili 6
6
10
Fig. 3. Mean time for salmon to eat food pellets of different sizes. Error bars are standard errors; sample sizes are given in Table 1 as the number of pellets of known fate minus the number uneaten.
pellet diameters than the two larger (S = 4.267, P < 0.001). With regard to pellet length, salmon took longest to respond to short (6 mm) pellets (S =4.206, PCO.001). Mean response times for intermediate ( 13 mm) and long (20 mm) pellets were not significantly different (S = 1.903, P> 0.05). The proportion of grasps that were followed by pellet rejection varied significantly among pellet lengths (G = 6.57, df = 2, P < 0.05)) but not diameters (G = 7.06, df = 3, P > 0.05)) although there was an indication that pellets of large diameter were more likely to be rejected
(b) 8 80 v)
r
phi,,I,,, a”
6
8
10
13
16
20
Pellet length (mm)
Fig. 4. Feeding responses of salmon in relation to pellet length (diameter 8 mm) : (a) mean response time with standard errors; (b) percentage of pellets eaten within 5 s. Sample sizes are given in Table 1.
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173
when they were long (Fig. 2a). Shorter pellets tended to be rejected least often. The proportion of pellets eaten rapidly did not differ significantly among diameters (G = 5.5 1, df=3, P> 0.10) or lengths of pellet (G=4.75, df=2, P> 0.05), although few of the extreme sizes of pellets (short and narrow or long and wide) were eaten within 5 s (Fig. 2b). The mean time for pellets to be eaten (Fig. 3) varied significantly with length (FUN = 3.04, P < 0.05)) but not diameter (F,.,,, = 1.04, P > 0.25), There was no indication of an interaction between the effects of length and diameter ( F6,rg4 = 1.27, P > 0.25). Pellets of intermediate length were eaten quicker than short pellets (S = 2.485, P < 0.05)) but there was no significant difference between long and short pellets (S = 1.096, P > 0.05)) or between intermediate and long pellets (S = 1.395, P > 0.05). Pellets of diameter 8 mm (the same as the commercial pellets fed routinely) were presented in a greater number of lengths (Table 1) to allow the effects of pellet length to be examined in more detail. The time taken by salmon to respond to g-mm diameter pellets varied significantly with pellet length (Fig. 4a; F,,,,= 3.05, P < 0.025). The salmon took longest to respond to short pellets. The proportion of grasps of g-mm diameter pellets that resulted in rejections did not differ significantly among pellet lengths (G = 4.47, df = 5, P> 0.25), ranging from 20% for lo-mm-long pellets to 41% for 20-mm-long pellets. However, the proportion of &mm diameter pellets eaten in less than 5 s did vary significantly in relation to pellet length (G = 11.34, df = 5, P < 0.05) and approximately mirrored the pattern of response time (Fig. 4b). A greater proportion of lo-mm-long pellets were eaten rapidly than either extremely long or short pellets. The mean time for g-mm-diameter pellets to be eaten varied in a similar way, ranging from 4.9 s for lo-mm-long pellets to 8.6 s for 6-mm-long pellets, but differences were not significant ( F5,s9 = 1.68, P > 0.10).
4. Discussion The feeding responses of salmon recorded in this study reflect the effects of pellet characteristics on different stages in the feeding sequence. Response time represents a combination of the detectability and attractiveness of pellets and the percentage of grasps followed by rejection indicates pellet acceptability. The time taken for a pellet to be eaten depended both on the speed of response by fish and on how often the pellet was rejected. Length and diameter of pellets affected their detectability and/or attractiveness: salmon took longer, on average, to respond to small pellets. However, as found with juvenile salmon (Stradmeyer et al., 1988), the pellet sizes that appeared to be initially most attractive to salmon were not the sizes that they ingested most readily once grasped. Pellets of long and intermediate length tended to elicit a more rapid response (Fig. 1)) but were more likely to be rejected than short pellets (Fig. 2a) _ Within the range of sizes tested, pellet diameter seemed not to influence acceptability significantly. This may be because diameter was not greater than the length for most of the experimental pellets. The conflicting trends in response time and rejections in relation to pellet length affected the time taken for pellets to be eaten (Fig. 3). Over the range of diameters tested, pellets of intermediate length were eaten quickest. More detailed examination of the effects of variation in the length of g-mm-diameter pellets (the same diameter as the commercial pellets)
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suggested that the optimum length, as indicated by the number of pellets eaten rapidly, was somewhat shorter than the mean length of commercial pellets (Fig. 4b). The lengths of pellet tested were within the range of variation found in commercial pellets. The differences apparent in attractiveness and acceptability among these lengths suggest that feed utilisation might be improved if variation in the length of commercial feed pellets was reduced. Some variation in pellet size may be desirable to cater for individual variation in fish size, particularly to avoid depressing further the growth rate of the smallest fish. However, this might be more precisely controlled by using different size classes of feed, rather than relying on random variation in pellet length within size classes. The texture and hardness of the experimental pellets, while similar between sizes, were not necessarily the same as the commercial pellets from which they were constituted. Soft pellets of a given size are more acceptable to juvenile salmon than hard (Stradmeyer et al., 1988)) but there may also be an interaction between the effects of pellet size and hardness, such that fish can handle larger food particles when they are soft (e.g. Knights, 1985; Mearns, 1990). The relationship between pellet hardness, size and acceptability should be investigated in post-smolt salmon to assess the scope for improving feeding responses and feed utilisation by using pellets that combine attractiveness and acceptability. Under ideal conditions, Atlantic salmon may consume a wide variety of pellet types, so making it unnecessary to incur the expense and inconvenience of optimising pellet size precisely. However, studies of other species of fish have shown that prey size selectivity increases as feeding motivation declines (e.g. Beukema, 1968; Bence and Murdoch, 1986; Croy and Hughes, 1991; Gill and Hart, 1994). In aquaculture, there are times when it is desirable that fish continue to feed despite low feeding motivation, such as following transfer of smolts to seawater ( Stradmeyer, 1994)) or during episodes of disease, when medication may need to be administered in the food. The variation in feeding responses described here allows optimisation of pellet characteristics that may significantly affect feed utilisation and food intake at times of low feeding motivation.
Acknowledgements We are grateful to Howietoun Fish Farms Ltd. for allowing us to study their fish and to Dunstaffnage Marine Laboratory for logistical support. This study was funded by the Scottish Salmon Growers Association and the Highland and Islands Development Board.
References Bence, J.R. and Murdoch, W.W., 1986. Prey size selection by the mosquitotish: relation to optimal diet theory. Ecology, 67: 324-336. Beukema, J.J., 1968. Predation by the three-spined stickleback (Gasterosteus aculeatus L.): the influence of hunger and experience. Behaviour, 31: 1-126. Croy, M.I. and Hughes, R.N., 1991. The influence of hunger on feeding behaviour and on the acquisition of learned foraging skills by the fifteen-spined stickleback, Spinachia spinachia L. Anim. Behav., 41: 161-170. Gill, A.B. and Hart, P.J.B., 1994. Feeding behaviour and prey choice of the threespine stickleback: the interacting effects of prey size, fish size and stomach fullness. Anim. Behav., 47: 921-932.
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Huntingford, F.A. and Thorpe, J.E., 1992. Behavioural concepts in aquaculture. In: J.E. Thorpe and F.A. Huntingford (Editors), The Importance of Feeding Behavior for the Efficient Culture of Salmonid Fishes. World Aquaculture Society, Baton Rouge, LA, pp. 1-4. Juell, J.E., 1991. Hydroacoustic detection of food waste - a method to estimate maximum food intake of fish populations in sea cages. Aquacult. Eng., 10: 207-217. Knights, B., 1985. Feeding behaviour and fish culture. In: C.B. Cowey, A.M. Mackie and J.G. Bell (Editors), Nutrition and Feeding in Fish. Academic Press, London, pp. 223-24 1. Mearns, K.J., 1990. The behavioural approach in identifying feeding stimulants for fish and its application in aquaculture. In: E. Kjorsvik (Editor), Application of Behavioural Studies in Aquaculture. Proceedings from the Minisymposium on Ethology in Aquaculture, Trondheim, 22 October 1989. Norwegian Society for Aquacultural Research, Bergen, pp. 69-74. Metcalfe, N.B., Huntingford, F.A. and Thorpe, J.E., 1987. Predation risk impairs diet selection in juvenile salmon, Anim. Behav., 35: 931-933. Paszkowski, C.A. and Olla, B.L., 1985. Foraging behavior of hatchery-produced coho salmon (Oncorh.ynchus kisutch) smolts on live prey. Can. J. Fish. Aquat. Sci., 42: 1915-1921. Smith, I.P., Metcalfe, N.B., Huntingford, F.A. and Kadri, S., 1993. Daily and seasonal patterns in the feeding behaviour of Atlantic salmon (Salmo salar L.) in a sea cage. Aquaculture, 117: 165-178. Stradmeyer, L., 1989. A behavioural method to test feeding responses of fish to pelleted diets. Aquaculture, 79: 303-310. Stradmeyer, L., 1992. Appearance and taste of pellets influence feeding behaviour of Atlantic salmon. In: J.E. Thorpe and F.A. Huntingford (Editors), The Importance of Feeding Behavior for the Efficient Culture of Salmonid Fishes. World Aquaculture Society. Baton Rouge, LA, pp. 21-28. Stradmeyer, L., 1994. Survival, growth and feeding of Atlantic salmon, Salmo salar L., smolts after transfer to sea water in relation to the failed smolt syndrome. Aquacult. Fish. Manage., 25: 103-l 12. Stradmeyer, L. and Thorpe, J.E., 1987. The responses of hatchery-reared Atlantic salmon, Salmo salar L., parr to pelleted and wild prey. Aquacult. Fish. Manage., 18: 51-61. Stradmeyer, L., Metcalfe, N.B. and Thorpe, J.E., 1988. Effect of food pellet shape and texture on the feeding response of juvenile Atlantic salmon. Aquaculture, 73: 217-228. Wahkowski, J.W.J., 1979. Morphological limitations, prey size selectivity, and growth response of juvenile Atlantic salmon, Salmo salar. J. Fish Biol., 14: 89-100. Waiikowski, J.W.J. and Thorpe, J.E., 1979. The role of food particle size in the growth of juvenile Atlantic salmon (Salmo salarL.). J. Fish Biol., 14: 351-370. Wilkinson, L., 1990. SYSTAT: The System For Statistics. SYSTAT, Inc., Evanston, IL, 677 pp. Zar, J.H., 1984. Biostatistical Analysis. Prentice Hall International, Inc., Englewood Cliffs, NJ, 718 pp.
Aquaculture 130 (1995) 167-175
The effects of food pellet dimensions on feeding responses by Atlantic salmon (S&w salar L.) in a marine net pen I.P. Smith*, N.B. Metcalfe, F.A. Huntingford Fish Behaviour and Ecology Group, Department of Zoology, University of Glasgow, Glasgow Gl2 8QQ, UK
Accepted 2 August 1994
Abstract The effects of the diameter and length of cylindroid food pellets on the feeding responses of onesea-winter Atlantic salmon in a marine net pen have been investigated. Pellets of different shapes and sizes were dropped into the pen in a random sequence and the responses of salmon were recorded with a video system. Both the diameter and length of pellets affected the time until first capture, with salmon taking longer to capture small pellets. The probability of a pellet being rejected after having been grasped was related to its length, but not its diameter: shorter pellets were rejected least often. Thus, the larger pellets that appeared to be initially most attractive to salmon were not the sizes that they ingested most readily once grasped. Acceptability (as indicated by rejection rate) varied over the range of pellet lengths that occurs within the size class of commercial feed recommended for these fish, and the optimum length (in terms of the number of pellets eaten rapidly) was shorter than the mean length of commercial pellets. The possible interaction of the effects of pellet size and hardness on palatability should be investigated. Kevwords: Salmo salar; Feeding and nutrition -
fish - behaviour; Feeding and nutrition - Pellet dimensions
1. Introduction
Efforts to maximise feed utilisation in salmonid aquaculture should take account of fish feeding behaviour. The proportion of administered feed consumed is partly determined by the responses of fish to individual food particles. Ingestion of food involves a sequence of events starting with detection of a potential food item, continuing through orientation, *Corresponding author. Present address: Scottish Office Agricultureand Fisheries Department, Marine Laboratory, PO Box 101, Victoria Road, Aberdeen AB9 SDB, UK 0044-8486/95/$09.50 0 1995 Elsevier Science B.V. All rights reserved SsDIOO44-8486(94)00207-X
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approach and capture, leading ultimately to the item being swallowed (Stradmeyer, 1989). This sequence may terminate at any stage prior to swallowing. For example, having approached a food item, a fish may proceed to capture it or leave it; having captured a food item, the fish may either swallow or eject it (Wahkowski, 1979; Knights, 1985). Completion of the feeding sequence depends both on the motivational state of the fish and the characteristics of the food particle (Huntingford and Thorpe, 1992). Physical attributes of the particle not only affect the ability of the fish to eat it (a food item may be too large to capture, for example), but also influence whether the fish is stimulated to eat it (a pellet may not be perceived as a desirable food item). Food particle design is therefore an important consideration when processed feedstuffs, such as pelleted fish meal, are used. Studies of juvenile salmonids indicate that some forms of dry pelleted food are less likely to elicit feeding responses than wild prey (Paszkowski and Olla, 1985; Stradmeyer and Thorpe, 1987) and several characteristics of artificial food items have been found to influence the probability of ingestion by juvenile salmonids (Mearns, 1990; Stradmeyer, 1992). The size and shape of food items are likely to be important at each stage of the feeding sequence, by influencing their detectability, attractiveness, ease of capture and probability of ingestion once captured (acceptability) (Stradmeyer et al., 1988). Size and shape of food items may have contrasting effects on attractiveness and acceptability (Metcalfe et al., 1987; Stradmeyer et al., 1988). Wankowski and Thorpe ( 1979) found that the growth rate of Atlantic salmon parr was influenced by food particle size. At most times of year, parr grew fastest on food particles of a width equivalent to 2.2-2.6% of the fishes’ mean body length, similar to the optimum size indicated by behavioural observations (Wahkowski, 1979). The feeding responses of post-smolt Atlantic salmon in relation to pellet characteristics have received less attention than those of fry and parr. Commercially supplied pellets for marine phase salmon tend to be approximate cylinders of relatively precise diameter, but variable length (Stradmeyer, 1992). Atlantic salmon in marine net pens are known to capture and then eject commercially produced pellets (Juell, 1991; Smith et al., 1993). Consequently, the present study was designed to investigate the influence of food pellet dimensions on the feeding responses of one-sea-winter Atlantic salmon in a marine net pen.
2. Materials and methods Study site and$sh The study was carried out at a commercial production site in Dunstaffnage Bay, Argyll, W. Scotland in April 1991. Atlantic salmon were stocked in a net pen (net depth 5 m; wooden collar 7 X9 m) as l-year-old smolts in May 1989. During the study the pen contained approximately 860 fish with an average weight of 3.4 kg. During non-observational periods, the fish were fed commercially produced pellets of the manufacturer’s recommended size ( ‘Mainstream’ Grower 6, BP Nutrition (UK) Ltd., Northwich), which were dispensed to the centre of the pen at 5-min intervals during daylight by an automatic feeder (Tessomat lOOL.B-12, Tess Aquaculture Ltd., Newport). In addition, fish farm staff dispensed a small quantity of the same type of pellets by hand at approximately 08.00 h
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169
each day. We had access to only one net pen, but our study fish appeared typical of salmon of the same age at the site. Experimental pellets Commercially produced pellets were approximate cylinders with a diameter of 8 f 0.2 mm and length of 13 + 3.5 mm (X + s.d.) , a 1ength:diameter ratio of 1.625. Experimental pellets were prepared in four diameters (5,6,8, 10 mm) and three lengths (6, 13,20 mm). The lengths corresponded to the mean length + 2 s.d. of commercial pellets (i.e. they were within the range of lengths found in commercial feed). Experimental pellets of diameter 8 mm were also manufactured in lengths of 8, 10 and 16 mm, which corresponded to 1.625 times the other experimental pellet diameters (5, 6 and 10 mm). Experimental pellets were prepared by grinding commercially produced pellets (BP Mainstream) with a pestle and mortar and mixing the resulting powder with water at room temperature. This paste was extruded from a rigid PVC tube (diameter 8 cm) through an appropriately sized hole drilled in a flat end-plate (thickness 0.5 cm) attached to the tube, with a pressure of approximately 2OAO kPa. The cylinders of paste thus formed were allowed to dry at room temperature and were then cut to the required lengths. Observation of feeding responses The responses of salmon to experimental pellets were observed with a video system. The video camera (charge coupled device, 12.7 mm format, lens focal length 3.5 mm) was encased in a cylindrical, waterproof housing (diameter 12 cm, length 18 cm) (C-Technics, Oban), mounted on a scaffold gantry so that the lens was positioned just below the water surface, 2 m from one side of the pen, viewing directly downwards. The angle of view was approximately 65” and the depth of view (which depended on water transparency and ambient light level) was approximately 4 m. The camera was connected by a waterproof cable to a video recorder (Video Walkman, Sony Corporation, Tokyo). Recordings were made in daylight and no artificial light was used. Single pellets of each size were dispensed into the pen in a random order at 30-s intervals, between actuations of the automatic feeder. Pellets were dropped into a plastic pipe that guided them into the water next to the video camera. It was not possible to determine the fate of all pellets presented, since some drifted laterally out of the camera’s field of view, or were obscured by fish. The fate of 357 pellets was recorded. Sample sizes for each pellet type are given in Table 1. Statistical analysis Four measures of the behavioural responses of salmon to experimental pellets were made from the video recordings: the time between pellets appearing in the field of view and the first grasp by salmon (response time) ; the proportion of pellets ejected from the mouth after having been grasped (rejections) ; the proportion of pellets eaten rapidly (within 5 s of appearing in the field of view); and the time taken for pellets to be eaten. Pellets that sank out of sight were deemed to be uneaten (27.2% of pellets whose fate was recorded). Uneaten pellets took approximately 30 s to sink out of sight and were excluded from analysis of the time taken for pellets to be eaten. Response time was determined for the first 215
170
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Table 1 Sample sizes for observations lengths
of feeding responses
I30 (1995) 167-175
of salmon to experimental
pellets of different diameters and
Diameter
Length
(mm)
(mm)
Number of pellets of known fate
Number of grasps’
Sample sizes for response times’
Number of pellets uneaten3
5 5 5 6 6 6 8 8 8 8 8 8 10 10 10
6 13 20 6 13 20 6 8 10 13 16 20 6 13 20
33 35 38 26 35 35 14 16 30 15 16 18 17 14 15
34 34 34 22 37 37 18 17 35 17 24 22 16 22 28
16 14 12 12 13 18 10 7 17 8 10 8 5 9 10
8 11 19 9 10 9 1 5 2 5 1 5 5 3 4
‘The number of times salmon rejected pellets was analysed in relation to the number of grasps. ‘Response time was determined for the first 215 pellets presented, ignoring those to which there was no response. ‘The number of pellets that sank out of sight, including those that had been grasped and rejected by salmon.
pellets only, but since pellets were presented in a random order, this should not bias comparisons of this measure among pellet sizes. Response time and time to eat pellets were analysed in relation to pellet diameter and length by analysis of variance (ANOVA), followed by Scheffe’s test for multiple comparisons (Zar, 1984). Measurements of time were normalised by square root transformation. Pellet length
6 mm 14
-
12
-
10
-
8
-
6
-
4
-
2
-
20 mm
13 mm
I
O-
31 II 8 5
Pellet diameter (mm)
B
10
Fig. 1. Mean response time of Atlantic salmon to cylindroid food pellets of different lengths and diameters, Error bars represent standard errors; sample sizes are given in Table 1.
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The proportion of grasps resulting in rejection and the proportion were analysed by log-linear analysis (Wilkinson, 1990).
171
of pellets eaten rapidly
3. Results The mean response time of salmon to experimental pellets varied significantly among diameters and lengths of pellet (Fig. 1; two-factor ANOVA, F,,,,, =5.64, P< 0.01, F 2.,23 = 9.98, P < 0.001 and F6,rz3 = 0.56, P > 0.50 for diameter, length and interaction term, respectively). Response times did not differ significantly between pellet diameters 5 mm and 6 mm (Scheffe’s test, S =0.682, P> 0.05) or between diameters 8 mm and 10 mm (S = 0.482, P > 0.05)) but salmon took significantly longer to respond to the two smaller (a)
Pellet length 13 mm
6 mm
2 6 I.= P CL .c P e z F “a 62
7o
r
60
-
50
-
40
-
30
-
l-l
20 10
0
(b)
w
2
n
10
a” 0
0 ton5
6
I
0
8 10
8
Pellet
diameter
(mm)
Fig. 2. Feeding responses of salmon to pellets of different sizes: (a) percentage of grasps that resulted in rejection of the pellet; (b) percentage of pellets eaten within 5 s. Sample sizes are given in Table 1.
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130 (1995) 167-175
Pellet length
-
12
-
20 mm
13 mm
6 mm 14
z? ?% $ B
86-
z F
4
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-
5
6
a
IIII 10
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6
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I 10
:
Pellet diameter (mm)
!lili 6
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Fig. 3. Mean time for salmon to eat food pellets of different sizes. Error bars are standard errors; sample sizes are given in Table 1 as the number of pellets of known fate minus the number uneaten.
pellet diameters than the two larger (S = 4.267, P < 0.001). With regard to pellet length, salmon took longest to respond to short (6 mm) pellets (S =4.206, PCO.001). Mean response times for intermediate ( 13 mm) and long (20 mm) pellets were not significantly different (S = 1.903, P> 0.05). The proportion of grasps that were followed by pellet rejection varied significantly among pellet lengths (G = 6.57, df = 2, P < 0.05)) but not diameters (G = 7.06, df = 3, P > 0.05)) although there was an indication that pellets of large diameter were more likely to be rejected
(b) 8 80 v)
r
phi,,I,,, a”
6
8
10
13
16
20
Pellet length (mm)
Fig. 4. Feeding responses of salmon in relation to pellet length (diameter 8 mm) : (a) mean response time with standard errors; (b) percentage of pellets eaten within 5 s. Sample sizes are given in Table 1.
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when they were long (Fig. 2a). Shorter pellets tended to be rejected least often. The proportion of pellets eaten rapidly did not differ significantly among diameters (G = 5.5 1, df=3, P> 0.10) or lengths of pellet (G=4.75, df=2, P> 0.05), although few of the extreme sizes of pellets (short and narrow or long and wide) were eaten within 5 s (Fig. 2b). The mean time for pellets to be eaten (Fig. 3) varied significantly with length (FUN = 3.04, P < 0.05)) but not diameter (F,.,,, = 1.04, P > 0.25), There was no indication of an interaction between the effects of length and diameter ( F6,rg4 = 1.27, P > 0.25). Pellets of intermediate length were eaten quicker than short pellets (S = 2.485, P < 0.05)) but there was no significant difference between long and short pellets (S = 1.096, P > 0.05)) or between intermediate and long pellets (S = 1.395, P > 0.05). Pellets of diameter 8 mm (the same as the commercial pellets fed routinely) were presented in a greater number of lengths (Table 1) to allow the effects of pellet length to be examined in more detail. The time taken by salmon to respond to g-mm diameter pellets varied significantly with pellet length (Fig. 4a; F,,,,= 3.05, P < 0.025). The salmon took longest to respond to short pellets. The proportion of grasps of g-mm diameter pellets that resulted in rejections did not differ significantly among pellet lengths (G = 4.47, df = 5, P> 0.25), ranging from 20% for lo-mm-long pellets to 41% for 20-mm-long pellets. However, the proportion of &mm diameter pellets eaten in less than 5 s did vary significantly in relation to pellet length (G = 11.34, df = 5, P < 0.05) and approximately mirrored the pattern of response time (Fig. 4b). A greater proportion of lo-mm-long pellets were eaten rapidly than either extremely long or short pellets. The mean time for g-mm-diameter pellets to be eaten varied in a similar way, ranging from 4.9 s for lo-mm-long pellets to 8.6 s for 6-mm-long pellets, but differences were not significant ( F5,s9 = 1.68, P > 0.10).
4. Discussion The feeding responses of salmon recorded in this study reflect the effects of pellet characteristics on different stages in the feeding sequence. Response time represents a combination of the detectability and attractiveness of pellets and the percentage of grasps followed by rejection indicates pellet acceptability. The time taken for a pellet to be eaten depended both on the speed of response by fish and on how often the pellet was rejected. Length and diameter of pellets affected their detectability and/or attractiveness: salmon took longer, on average, to respond to small pellets. However, as found with juvenile salmon (Stradmeyer et al., 1988), the pellet sizes that appeared to be initially most attractive to salmon were not the sizes that they ingested most readily once grasped. Pellets of long and intermediate length tended to elicit a more rapid response (Fig. 1)) but were more likely to be rejected than short pellets (Fig. 2a) _ Within the range of sizes tested, pellet diameter seemed not to influence acceptability significantly. This may be because diameter was not greater than the length for most of the experimental pellets. The conflicting trends in response time and rejections in relation to pellet length affected the time taken for pellets to be eaten (Fig. 3). Over the range of diameters tested, pellets of intermediate length were eaten quickest. More detailed examination of the effects of variation in the length of g-mm-diameter pellets (the same diameter as the commercial pellets)
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suggested that the optimum length, as indicated by the number of pellets eaten rapidly, was somewhat shorter than the mean length of commercial pellets (Fig. 4b). The lengths of pellet tested were within the range of variation found in commercial pellets. The differences apparent in attractiveness and acceptability among these lengths suggest that feed utilisation might be improved if variation in the length of commercial feed pellets was reduced. Some variation in pellet size may be desirable to cater for individual variation in fish size, particularly to avoid depressing further the growth rate of the smallest fish. However, this might be more precisely controlled by using different size classes of feed, rather than relying on random variation in pellet length within size classes. The texture and hardness of the experimental pellets, while similar between sizes, were not necessarily the same as the commercial pellets from which they were constituted. Soft pellets of a given size are more acceptable to juvenile salmon than hard (Stradmeyer et al., 1988)) but there may also be an interaction between the effects of pellet size and hardness, such that fish can handle larger food particles when they are soft (e.g. Knights, 1985; Mearns, 1990). The relationship between pellet hardness, size and acceptability should be investigated in post-smolt salmon to assess the scope for improving feeding responses and feed utilisation by using pellets that combine attractiveness and acceptability. Under ideal conditions, Atlantic salmon may consume a wide variety of pellet types, so making it unnecessary to incur the expense and inconvenience of optimising pellet size precisely. However, studies of other species of fish have shown that prey size selectivity increases as feeding motivation declines (e.g. Beukema, 1968; Bence and Murdoch, 1986; Croy and Hughes, 1991; Gill and Hart, 1994). In aquaculture, there are times when it is desirable that fish continue to feed despite low feeding motivation, such as following transfer of smolts to seawater ( Stradmeyer, 1994)) or during episodes of disease, when medication may need to be administered in the food. The variation in feeding responses described here allows optimisation of pellet characteristics that may significantly affect feed utilisation and food intake at times of low feeding motivation.
Acknowledgements We are grateful to Howietoun Fish Farms Ltd. for allowing us to study their fish and to Dunstaffnage Marine Laboratory for logistical support. This study was funded by the Scottish Salmon Growers Association and the Highland and Islands Development Board.
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