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Aquaculture 253 (2006) 512–522 www.elsevier.com/locate/aqua-online The influence of the dietary inclusion of the alkaloid gramine, on rainbow trout (Oncorhynchus mykiss) growth, feed utilisation and gastrointestinal histology Brett Glencross a,d,*, David Evans a,d, Neil Rutherford a,d, Wayne Hawkins b,d, Peter McCafferty c,d, Ken Dods c,d, Brian Jones a, David Harris c,d, Lincoln Morton c,d, Mark Sweetingham b,d, Sofie Sipsas b,d a Department of Fisheries-Research Division, PO Box 20, North Beach, WA 6020, Australia b Department of Agriculture-Government of Western Australia, Baron Hay Court, South Perth, WA 6150, Australia c Chemistry Centre (WA), 125 Hay St, East Perth, WA 6004, Australia d Centre for Legumes in Mediterranean Agriculture (CLIMA), Aquaculture Feed Grains Program, University of Western Australia, Crawley, WA 6909, Australia Received 9 March 2005; received in revised form 30 June 2005; accepted 1 July 2005 Abstract This study examined the influence of the alkaloid gramine, when included in diets for rainbow trout. Quinolizidine alkaloids have been suggested as a potential anti-nutritional problem with the use of lupin (Lupinus sp.) meals in aquaculture diets. The findings from the present study show that above a critical threshold, the alkaloid gramine does have a strong anti-palatability effect. The effect is noted at a minimum gramine concentration of 500 mg/kg of diet, though not at 100 mg/kg. A continuing strong anti-palatability response is noted at higher inclusion levels and at the highest gramine inclusion concentration examined in this study (10,000 mg/kg), insufficient feed was consumed to even supply maintenance protein and energy demands. No adaptation to concentrations of gramine was observed throughout the 6-week study. No effects on nitrogen, energy or phosphorus digestibility were seen at the 500 mg/kg inclusion concentration of gramine relative to the reference diet, although the inclusion of the yellow lupin kernel meals (both Wodjil and Teo varieties) in the diet did improve the digestibility of phosphorus. Growth, as assessed using a range of parameters including weight gain, growth rate, nutrient and energy retention of fish fed the experiment treatments was largely consistent with feed intake. Survival of fish was significantly reduced at gramine inclusion levels above 1000 mg/kg. Feed conversion ratio (FCR) and feed conversion efficiency (FCE) were also reflective of feed intake and growth levels observed of each treatment. The concentrations of the plasma thyroid hormones tri-iodothyronine (T3) and thyroxine (T4) of fish from each of the treatments were consistent with feed intake (including the controls) suggesting that the concentrations of these hormones are in response to feed intake, not specifically the gramine levels in the diets. However, the inclusion of the Lupinus luteus kernel meals resulted in a significant change in T4 levels, with a degree of independence of the * Corresponding author. Department of Fisheries-Research Division, PO Box 20, North Beach, WA 6020, Australia. Tel.: +61 8 9239 8103; fax: +61 8 9239 8105. E-mail address: [email protected] (B. Glencross). 0044-8486/$ - see front matter D 2005 Published by Elsevier B.V. doi:10.1016/j.aquaculture.2005.07.009 B. Glencross et al. / Aquaculture 253 (2006) 512–522 513 feed intake, suggesting that there may be another mechanism by which these meals are influencing the concentrations of this hormone. In this study, there was an increase in the density of melano-macrophage centres (MMC) with high dietary levels of gramine. However, in the absence of any histological evidence for a toxic effect, it is likely that the increased MMC densities observed in the fish fed high concentrations of gramine are associated with starvation. This study demonstrated that the lupin alkaloid gramine, can have a strong anti-nutritional effect on fish at inclusion concentrations greater than 100 mg/kg, but that its mode of action is primarily through an anti-palatability effect. It is therefore considered unlikely that alkaloid effects would be observed in diets even with 50% inclusion of kernel meals from Australian commercial L. luteus varieties. D 2005 Published by Elsevier B.V. Keywords: Plant proteins; Fish meal replacement; Anti-nutritional factors; Alkaloids 1. Introduction Consumption of gramine at toxic levels in mice has been noted to lead to psychotropic levels of excite- It is well recognized in the aquaculture feeds indus- ment and seizure. The mode of action for gramine as try that there is a need to reduce reliance on fish meal an ANF, or toxicity data on this compound is limited. in aquaculture feeds (Naylor et al., 2000). Increasing However, mammalian effects include changes in the actual or prospective utilization of other protein tubules and glomeruli in the kidney, ureter and blad- meals in diets for aquatic species, substantial risk der, endocrine changes in spleen weight, and bio- reduction is achieved. The use of plant protein chemical changes such as enzyme inhibition, meals as alternative protein resources has been well induction via changes in blood or tissue levels of studied and many viable options including soybean, phosphatases (TXCYAC, 1980), although no specific glutens and lupin meals have been adopted indust- data is available for any fish species. Tolerance con- rially (Carter and Hauler, 2000; Storebakken et al., centrations to the inclusion of dietary gramine in other 2000; Glencross et al., 2004). However, the introduc- vertebrate species (rats, pigs and poultry) have been tion of anti-nutritional factors and other biologically determined at; about 300 mg/kg for rats, N500 mg/kg active compounds can accompany the use of plant diet for pigs and about 650 mg/kg diet for poultry protein meals (Francis et al., 2001). (Pastuszewska et al., 2001). The effects of concentra- Anti-nutritional factors (ANF) can affect the uti- tions as low as 250 mg/kg of Lupinus angustifolius lization of food by an animal through several ave- alkaloids have been reported in rats (Butler et al., nues, including the metabolic axis, nutrient 1996), although concentrations of alkaloids from L. digestibility or ingredient palatability (Refstie et al., albus were only reported to have an adverse effect at 1998, 1999; Glencross et al., 2003a,b). Alkaloids are 320 mg/kg (Zdunczyk et al., 1998). heterocyclic amino acid derivatives produced by The current Australian commercial L. luteus vari- plants as a chemical defence mechanism. While ety (Wodjil) has very low gramine concentration alkaloids are found in most legume species, they compared to European varieties such as Teo. How- have traditionally been found in high concentrations ever, Wodjil has proven agronomically costly to in the seeds of plants from the Lupinus genus (Pet- produce because of the high levels of insecticide terson et al., 1997; Wasilewko and Buraczewska, use required to deal with substantial insect infesta- 1999). Notably, a variety of alkaloids are found in tion problems (Perry et al., 1998; Berlandier and these seeds. In some varieties of the species Lupinus Sweetingham, 2003). There is evidence that aphid luteus, a major alkaloid component is gramine (Pet- infestation is directly related to the low inherent terson, 2000). Feeding studies with kernel meals from concentration of gramine (Risdall-Smith et al., the seeds of L. luteus have shown good prospect for 2004). Higher alkaloid varieties of L. luteus, such their use in aquaculture feeds because of their high as Teo, have better resistance to insect infestation, digestible protein content, although some deteriora- but it is unclear whether the higher alkaloids will tion in growth performance at high inclusion levels influence the usefulness of the kernel meal as an has been noted (Glencross et al., 2004). aquaculture feed ingredient. 514 B. Glencross et al. / Aquaculture 253 (2006) 512–522 This study reports on the nutritional influence of Table 1 gramine on the feed intake, growth, some biochemical Composition of the ingredients (all values are g/kg DM unless otherwise stated) parameters and tissue histology of rainbow trout. This c d e was examined over a range of inclusion concentra- Nutrient Fish Pregelled Cellulose Wodjil Teo meala wheat tions above and below naturally occurring concentra- starchb tions found in domesticated varieties of L. luteus. Dry matter 917 906 933 924 920 content (g/kg) Crude protein 770 7 3 512 541 2. Materials and methods Crude fat 68 11 2 79 79 Ash 142 3 2 54 73 2.1. Ingredients and diet preparation Crude fibre 0 10 660 33 35 Phosphorus 22 0 0 6 7 Organic matter 858 997 998 946 927 Purified gramine was purchased (Aldrich catalogue Gross energy 21.3 17.2 17.3 20.9 20.9 No. 1080-6, 99% purity). The gramine was dissolved (MJ/kg DM) in methanol and was added to a methanol-saturated Alkaloids 0 0 0 32 4087 cellulose slurry and the mixture was thoroughly (mg/kg DM) Arginine 43 0 0 47 61 mixed. The solvent was removed in vacuo and the Histidine 25 0 0 14 14 gramine/cellulose mixture was dried under vacuum. Isoleucine 28 2 0 17 20 Cellulose was used as a carrier for the gramine allow- Leucine 55 0 0 35 43 ing for easy dispersion of the gramine in the indivi- Lysine 46 1 0 23 17 dual diets. The gramine/cellulose mixture was added Methionine 21 0 0 4 3 Phenylalanine 29 0 0 18 21 to the experimental diets according to the formula- Threonine 32 2 0 16 19 tions in Table 1. All ingredients were ground such that Valine 34 0 0 17 19 they passed through a 600-Am screen. All experiment a Chilean Anchovy meal supplied by Skretting Australia, Cam- diets were formulated to be isonitrogenous (400 g/kg) bridge, Tasmania, Australia.

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