Gastrointestinal overload — A problem with formulated feeds?

51 (1986) 257-263 Elsevier Science Publishers B.V., Amsterdam - Printed in The Netherlands

Aquaculture,

GASTROINTESTINAL OVERLOAD FORMULATED FEEDS?

257

- A PROBLEM WITH

MALCOLM JOBLING Institutt

for Fiskerifag,

Universitetet

i Tromsb,

Boks

3083,

Guleng,

9001

Tromsb

(Norway)

(Accepted 12 November 1985)

ABSTRACT Jobling, M., 1986. Gastrointestinal culture, 51: 257-263.

overload - a problem with formulated feeds? Aqua-

Mechanisms regulating gastric emptying are briefly discussed and predictions are made about how differences between the emptying of natural and formulated feeds could affect intestinal digestive and absorptive efficiency. The digestibility coefficients of processed, formulated feeds are 5-10% lower than those of natural food organisms. The results support the hypothesis that high energy, small particles are emptied overrapidly from the stomach, leading to an overloading of the intestinal digestive capacity and a reduction in absorption efficiency.

INTRODUCTION

Much of the work carried out on the nutritional physiology of farmed fish species has been concerned with defining the nutritional requirements, with the aim of preparing formulated feeds of high nutritional value. Little research effort has been directed towards the examination of how well the gastrointestinal tract and digestive capacities of fish adapt to these novel food sources (Windell et al., 1969; Windell and Norris, 1969; From and Rasmussen, 1984). In this paper, the properties of natural and formulated feeds are described and compared, and predictions are made as to how well these different food types are digested and absorbed by fish. The predictions are tested by comparing digestibility coefficients for natural and for processed, formulated feeds. PHYSIOLOGICAL

BACKGROUND

AND HYPOTHESIS

Most carnivorous fish species feed on crustaceans, insects, worms or fish. All of these prey organisms have a relatively low organic content, with dry matter constituting only 15-25s of the total weight (Windell, 1966; Beamish, 1972; Elliott, 1972). Consequently, the energy contents of natural animal 0044-8486/86/$03.50

0 1986 Elsevier Science Publishers B.V.

258

prey species are also low and normally range between 4 and 8.5 kJ g wet wt-‘. Such prey items are usually consumed whole and enter the stomach as comparatively large discrete particles, and this has important consequences for the way in which the prey is digested and evacuated from the stomach (Jobling, 1986). Non-nutrient bulk is emptied rapidly and inert solids and indigestible food remains may be passed from the stomach as relatively large particles(Molnaret al., 1967; Pandian, 196’7; Kelly, 1980; Meyer, 1980; Mojaverian et al., 1985). Liquid meals are emptied from the stomach much more rapidly than are digestible solids, even when the liquids are rich in nutrients (Heading et al., 1976; Kelly, 1980; Meyer, 1980; Moore et al., 1984). Thus, both large particle size and nutrient content appear to be prerequisites for retention of food in the stomach. It has been suggested that regulation of gastric emptying based upon these characteristics would prevent the dumping of large food particles into the upper intestine and would also ensure that amounts of food energy reaching the small intestine remain relatively constant over time (Jobling, 1986). Formulated feeds used in fish farming differ markedly from natural foods and can be divided into three types: wet feeds, moist pellets and dry pellets. Wet feeds usually consist of finely minced trash fish and/or slaughterhouse wastes with added vitamins and binders, so that the finished product is a relatively low energy paste containing approximately 30% dry matter. Moist pellets usually contain 60-65s dry matter and have an energy content of 15-20 kJ g wet wt-‘, whereas in dry feed formulations the percentage dry matter is approximately 90% and energy content often exceeds 20 kJ g-l (Windell et al., 1969; Garber, 1983; From and Rasmussen, 1984). In addition to having a higher energy content than natural feed organisms, formulated feeds have different physical properties in that they are either pastes or friable pellets that disintegrate into particles of small size when subjected to gastric secretions and motor activity (Windell et al., 1969; Windell and Norris, 1969). Thus, moist and dry pellet feeds can be considered as being composed of small particles of high energy content and they may, therefore, lack one of the properties required for prolonged gastric retention. Increases in dietary energy levels do result in a slowing of gastric emptying in some fish species, which implies that nutrient concentration of the food may play an important role in the regulation of gastric emptying, even when food consists of small particles (Windell and Norris, 1969; Grove et al., 1978; Flowerdew and Grove, 1979; Jobling, 1980). This nutrientdependent compensatory mechanism does not appear to be completely effective and is probably not precise enough to ensure a constant rate of emptying of nutrients from the stomach to the intestine. Thus, natural prey, such as fish, and dry pellet formulated feeds are at opposite ends of a particle size--energy content continuum and it is questionable whether the gastrointestinal tracts of fish are capable of processing these different food types with equal efficiency. It is hypothesised that the consumption of high energy, small particle

259

size diets may lead to the rapid entry of partially digested food into the intestine, resulting in an overloading of the digestive and absorptive capacities and a reduction in absorption efficiency. Thus, it is predicted that the digestibilities of food organisms should be higher when they are consumed in their natural state than when they have been processed and are included in high energy formulated feeds. MATERIALS

AND METHODS

The data analysed were mostly taken from the literature on nutritional physiology and energy balance in fish, but also include results from my own digestibility studies conducted with plaice, Pleuronectes platessa, and turbot, Scoph thalmus maximus. There are many published digestibility studies, but the majority give values for complete formulated feeds rather than for individual feed ingredients. The majority of the complete feeds for which digestibility values are available were formulated to include material of plant origin, and these had to be excluded from the current analysis. Digestibility values were collected for food organisms consumed in a natural state and for processed ingredients of animal origin. Natural foods for which data were available consisted largely of crustaceans and fish, but also included insects, polychaetes and oligochaetes. Fish fillets were classified as natural foods since they represent food presented as large particles. Finely minced fish, meals, silages and concentrates were classified as processed foods (Table 2). For each food type (invertebrates, fish and animal products) the digestibility coefficients of natural and processed feeds were compared statistically using Student’s t test. Methods follow those outlined by Sokal and Rohlf (1969). RESULTS

AND DISCUSSION

The efficiency with which fish digest and absorb food has been shown to be influenced by a number of factors, the most important of which appear to be temperature and feeding level (Brocksen and Bugge, 1974; Elliott, 1976; Targett, 1979; From and Rasmussen, 1984). Estimates of digestibility coefficients may also vary depending upon the methodology used in collecting and analysing faecal samples (Windell et al., 1978; Smith et al., 1980; Vens-Cappell, 1985). In addition, there are probably interspecific differences in the abilities of fish to digest and absorb particular foodstuffs (Birkett, 1969; Jobling, 1983; Table 1). All of these factors would tend to mask, rather than highlight, differences in digestibility between natural and processed foods. The digestibility data for the different food types are summarised in Table 2, and the first impression is that processed foods are digested and absorbed more poorly than feedstuffs presented in their natural form. More detailed analysis (t test) showed that the majority of these differences were signifi-

260 TABLE 1 Abilities of plaice, Pleuronectes platessa, and absorb formulated feeds at 10” C Food

and turbot, Scophthalmus

Digestibility coefficient Energy

Basic mix + 20% + 20% + 20% + 20% + 20% + 20%

(80% by weight) kaolin (control) casein albumen fishmeal ‘Pruteen’ raw starch

maximus,

to digest

(W) Nitrogen

Plaice

Turbot

Plaice

Turbot

75 85 66 82 82 44

71 81 41 77 72 39

82 93 77 84 90 68

81 88 63 77 79 61

Basic mix consisted of: minced sprat 68%, vitamin binder lo%, chromic oxide 2%.

TABLE 2 Digestibilities of natural and processed foodstuffs Values given are mean + S.D. (n) Food type

Invertebrates Natural prey Processed Fish Natural prey Minced fish Fishmeal Silage/concentrate Animal products (offal, etc.) Unprocessed Processed

in fish species.

Digestibility coefficient (%) Energy

Nitrogen

84.9 i 6.3 (14) 82.7 f 3.4 (2)

93.0 2 5.2 (14) 84.1 + 7.6 (5)

93.5 + (11) 79.6 f (6) 87.0 * (6) 86.3 * (2)

5.6

95.2 ? 1.2

5.0

(4) 84.2 + 5.7

4.9 10.8

94.8 77.5 + 8.5 (5)

(6) 84.2 ? 7.3 (35) 80.9 ?r 9.8 (8) 91.8 * 2.7 (7) 78.6 + 9.1 (6)

261

cant. The exceptions were: digestible energy unprocessed vs. processed animal products, and digestible energy natural invertebrate prey vs. processed invertebrates. In the first case the sample sizes are small, and in the case of invertebrate prey the levels of indigestible exoskeletal material present in both natural and processed prey probably played a large role in determining the value of the digestibility coefficients. Thus, food organisms appear to be better digested and absorbed when consumed in their natural state than when presented in the form of pastes, meals or other processed products. The results presented in Table 2 are data gathered from experiments conducted using different species under different conditions, but the same general trends are revealed when the limited data for individual species are examined. Rainbow trout, Salmo guirdneri, digest and absorb the nitrogen content of fish fillets with approximately 95% efficiency whereas the feeding of other fish products usually results in a lowered efficiency (range 72-95s) (Mann, 1969; Hastings, 1969; Smith et al., 1980; Cho et al., 1982; Watanabe et al., 1983; Hardy et al., 1984). Fish fillets are digested and absorbed by cod, Gadus morhua, better than are processed feeds (digestible energy: 98% vs. 83% (Edwards et al., 1972; Holdway and Beamish, 1984), and plaice appear to be more efficient at digesting natural prey than fish products presented in a variety of forms (digestible nitrogen: 92% vs. 82-93s) (Birkett, 1969; Cowey et al., 1974; own observations). The feeding of processed foods of animal origin appears to lead to a decline in digestibility of 5-lo%, which gives support to the hypothesis that the high energy small particles of formulated feeds are emptied overrapidly from the stomach and overload the digestive and absorptive capacities of the intestine.

REFERENCES Beamish, F.W.H., 1972. Ration size and digestion in largemouth bass, Micropterus salmoides Lacepede. Can. J. Zool., 50: 153-164. Birkett, L., 1969. The nitrogen balance in plaice, sole and perch. J. Exp. Biol., 50: 375-306. Preliminary investigations on the influence of Brocksen, R.W. and Bugge, J.P., 1974. temperature on food assimilation by rainbow trout, Salmo gairdneri Richardson. J. Fish Biol., 6: 93-97. Cho, C.Y., Slinger, S.J. and Bayley, H.S., 1982. Bioenergetics of salmonid fishes: energy intake, expenditure and productivity. Comp. Biochem. Physiol., 73B: 25-41. Cowey, C.B., Adron, J., Blair, A. and Shanks, A.M., 1974. Studies on the nutrition of marine flatfish. Utilization of various dietary proteins by plaice (Pleuronectes platessa). Br. J. Nutr., 31: 297-306. Edwards, R.R.C., Finlayson, D.M. and Steele, J.H., 1972. An experimental study of the oxygen consumption, growth and metabolism of the cod (Gadus morhua L.). J. Exp. Mar. Biol. Ecol., 8: 299-309. Elliott, J.M., 1972. Rates of gastric evacuation in brown trout, Salmo truth L. Freshwater Biol., 2: l-18.

262 Elliott, J.M., 1976. Energy losses in the waste products of brown trout (Salmo trutta L.) J. Anim. Ecol., 45: 561-580. Flowerdew, M.W. and Grove, D.J., 1979. Some observations of the effects of body weight, meal size and quality on gastric emptying time in the turbot, Scophthalmus maximus (L.), using radiography. J. Fish Biol., 14: 229-238. From, J. and Rasmussen, G., 1984. A growth model, gastric evacuation and body composition in rainbow trout, Salmo gairdneri Richardson, 1836. Dana, 3: 61-139. Garber, K.J., 1983. Effect of fish size, meal size and dietary moisture on gastric evacuation of pelleted diets by yellow perch, Perca flavescens. Aquaculture, 34: 4149. Grove, D.J., Loizides, L.G. and Nott, J., 1978. Satiation amount, frequency of feeding and gastric emptying rate in Salmo gairdneri. J. Fish Biol., 12: 507-516. Hardy, R.W., Shearer, K.D. and Spinelli, J., 1984. The nutritional properties of co-dried fish silage in rainbow trout (Salmo gairdneri) dry diets. Aquaculture, 38: 35-44. Hastings, W.H., 1969. Nutritional score. In: O.W. Neuhaus and J.E. Halver (Editors), Fish in Research. Academic Press, New York, London, pp. 263-292. Heading, R.C., Tothill, P., McLaughlin, G.P. and Shearman, D.J.C., 1976. Gastric emptying rate measurement in man. A double isotope scanning technique for simultaneous study of liquid and solid components of a meal. Gastroenterology, 71: 45-50. Holdway, D.A. and Beamish, F.W.H., 1984. Specific growth rate and proximate body composition of Atlantic cod (Gadus morhua L.). J. Exp. Mar. Biol. Ecol., 81: 147170. Jobling, M., 1980. Gastric evacuation in plaice, Pleuronecfesplatessa L.: effects of dietary energy level and food composition. J. Fish Biol., 17: 187-196. Jobling, M., 1983. A short review and critique of methodology used in fish growth and nutrition studies. J. Fish Biol., 23: 685-703. Jobling, M., 1986. Mythical models of gastric emptying and implications for food consumption studies. Gutshop ‘84, Env. Biol. Fish., Kelly, K.A., 1980. Gastric emptying of liquids and solids: roles of proximal and distal stomach. Am. J. Physiol., 239: G71-G76. Mann, H., 1969. Difference in the digestibility of plant and animal protein by various kinds of fish. E.I.F.A.C. Tech, Paper 1969,9: 194-196. Meyer, J.H., 1980. Gastric emptying of ordinary food: effect of antrum on particle size. Am. J. Physiol., 239: G133-Gl35. Mojaverian, P., Ferguson, R.K., Vlasses, P.H., Rocci, M.L., Jr., Oren, A., Fix, J.A., Caldwell, L.J. and Gardner, C., 1985. Estimation of gastric residence time of the Heidelberg capsule in humans: effect of varying food composition. Gastroenterology, 89: 392-397. Molnar, G., Tamassy, E. and Tolg, I., 1967. The gastric digestion of living predatory fish. In: S.D. Gerking (Editor), The Biological Basis of Freshwater Fish Production. Blackwell Scientific, Oxford, Edinburgh, pp. 135-149. Moore, J.G., Christian, P.E., Brown, J.A., Brophy, C., Datz, F., Taylor, A. and Alazraki, N., 1984. Influence of meal weight and caloric content on gastric emptying of meals in man. Digestive Dis. Sci., 29: 513-519. Pandian, T.J., 1967. Transformation of food in the fish Megatops cyprinoides. I. Influence of quality of food. Mar. Biol., 1: 60-64. Smith, R.R., Peterson, M.C. and Allred, A.C., 1980. Effect of leaching on apparent digestion coefficients of feedstuffs for salmonids. Prog. Fish Cult., 42: 195-199. Sokal, R.R. and Rohlf, F.J., 1969. Biometry: the Principles and Practice of Statistics in Biological Research. W.H. Freeman & Company, San Francisco, CA, 776 pp. Targett, T.E., 1979. The effect of temperature and body size on digestive efficiency in Fundulus heteroclitus L. J. Exp. Mar. Biol. Ecol., 38: 179-186. Vens-Cappell, B., 1985. Methodicalstudiesondigestion in trout. 1. Reliability of digestion coefficients in relation to methods for faeces collection. Aquacult. Eng., 4: 33-49.

263 Watanabe, T., Nanri, H., Satoh, S., Takeuchi, M. and Nose, T., 1983. Nutritional evaluation of brown meals as a protein source in diets for rainbow trout. Bull. Jpn. SOC. Sci. Fish., 49: 1083-1087. Windell, J.T., 1966. Rate of digestion in the bluegill sunfish. Invest. Indiana Lakes Streams, 7: 185-214. Windell, J.T. and Norris, D.D., 1969. Gastric digestion and evacuation in rainbow trout. Prog. Fish Cult., 31: 20-26. Windell, J.T., Norris, D.O., Kitchell, J.F. and Norris, J.S., 1969. Digestive response of rainbow trout, Salmo gairdneri, to pellet diets. J. Fish. Res. Board Can., 26: 18011812. Windell, J.T., Foltz, J.W. and Saroken, J.A., 1978. Methods of fecal collection and nutrient leaching in digestibility studies. Prog. Fish Cult., 40: 51-55.