effects of feed composition on life history developments in feed intake, metabolism, growth and body...

2007) 175–187www.elsevier.com/locate/aqua-online

Aquaculture 267 (

Effects of feed composition on life history developments in feedintake, metabolism, growth and body composition

of European eel, Anguilla anguilla

Leon T.N. Heinsbroek a,b,⁎, Paul L.A. Van Hooff a, William Swinkels a,Michel W.T. Tanck a, Johan W. Schrama a, Johan A.J. Verreth a

a Aquaculture and Fisheries Group, Wageningen University, P.O. Box 338, 6700 AH Wageningen, The Netherlandsb Wageningen Aquafeed, Mennonietenweg 13, 6702 AB Wageningen, The Netherlands

Received 30 November 2006; received in revised form 26 March 2007; accepted 26 March 2007

Abstract

To examine the effect of feed composition on changes in feed intake and subsequent feed utilization with age, five populationsof European eel, with an average initial body weight of 5 g each fed a different diet, were monitored for 302 d. The five feedsdiffered in their content of crude protein (33–63% DM), crude fat (6–28% DM) and calculated carbohydrates (NFE; 15–42% DM)such that five levels of digestible protein/digestible energy (DP/DE) were realised: 13, 16, 21, 28 and 29 g MJ−1. At three points intime, with three size groups, nitrogen and energy balance studies were conducted in which next to feed intake and growth alsodigestibilities of dry matter, protein, fat, NFE and energy as well as O2 consumption and NH4–N excretion were measured.

Due to the distinct life history of the semelparous, in the present study predominantly male eel, a well-defined goal in terms of maturesize and composition could be inferred, presumably tomaximize their lifetime reproductive output. In order to reach this goal the animalneeds to survive and to grow and voluntary feed intake of the eels could be adequately described with the feed intake model ‘eating torequirements subject to constraints’, where voluntary feed intake is considered to originate from a requirement formaintenance (survival)and a requirement for growth. Live weight gain is almost completely based on protein deposition (PD) and eels, like other animals, striveto reach a genetically determined growth potential (PDmax) thought to be driven by the difference from themature proteinmass (Ptmax).Body lipid content increases with size and varied with diet from a minimum of 25% at high DP/DE ratios to a maximum of 33% at lowDP/DE ratios, at bodyweights of 130–140 g. Preferable allocation of dietary protein to PD (protein sparing action of non-protein energy)was confirmed as marginal efficiency of protein utilization increased with decreasing DP/DE ratio from 0.29 to 0.54.Marginal energeticefficiency of PD, kp was 0.54 and marginal energetic efficiency of LD, kf varied from 0.67, indicating de novo lipid synthesis (fromdietary protein) at high DP/DE ratios, to 0.93, indicating direct lipid synthesis (from dietary lipid) at low DP/DE ratios. Marginalefficiencies did not differ from those of other fish or other farm animals. Differences between fish species in feed intake and utilization offeeds differing in macronutrient composition, as well as life history developments in feed intake and feed utilization are therefore basedon differences in growth rate, in turn with mature weight (Ptmax), and body composition (LD/PD ratio).© 2007 Elsevier B.V. All rights reserved.

Keywords: Anguilla anguilla; Life history; Feed intake model; Growth; Oxygen consumption; Nitrogen excretion

⁎ Corresponding author. Wageningen Aquafeed, Mennonietenweg 13, 6702 ABWageningen, The Netherlands. Tel.: +31 646 408813; fax: +31 317419001.

E-mail address: [email protected] (L.T.N. Heinsbroek).

0044-8486/$ - see front matter © 2007 Elsevier B.V. All rights reserved.doi:10.1016/j.aquaculture.2007.03.028

mailto:[email protected]

http://dx.doi.org/10.1016/j.aquaculture.2007.03.028

176 L.T.N. Heinsbroek et al. / Aquaculture 267 (2007) 175–187

1. Introduction

Farm animals, including fish, are mostly fed tosatiation to maximize growth and profitability (Forbes,2000, 2003; Yearsley et al., 2001). Feed intakedominates the economic performance of animal produc-tion systems through direct feed costs (feed price andfeed efficiency), which in intensive production processesare often the most important costs, and through the effecton growth, productivity and associated fixed costs.Where from the relationship between feed intake andgrowth it is shown that growth rate also influences feedefficiency (Forbes, 2000; Bureau et al., 2006), under-standing and predicting voluntary feed intake is vital foreconomic sustainability of the production system.

The relationship between feed intake and growth infish has been studied extensively using bioenergeticapproaches (Heinsbroek, 1987; Heinsbroek et al., 1993;Bureau et al., 2006). However, as bioenergetic models arefocussed on energy they do not take into account thedifferences in attributes and functions of the differentenergy containing nutrients as well as the differences intransformation efficiencies, including deposition. Ofthese energy containing nutrients it has been indicatedthat the non-protein macronutrients, lipids and carbohy-drates, are to some extend interchangeable in their effecton feed intake and growth and can be grouped as non-protein energy (NPE), provided that the level ofcarbohydrates does not exceed the limit of the fish speciesinvestigated (Ruohonen et al., 2007). Macronutrientcombinations can than be expressed in a protein/energydimension. European eel has been shown to effectivelyutilize (digestible) dietary carbohydrate levels of up to50% (Degani and Viola, 1987; Suarez et al., 2002).

A further complication is that most bioenergeticmodels imply a trade-off or competition between res-piration and production, while respiration is to a largeextend caused by and an inevitable part of the productionprocess (Jobling, 1985). To overcome these problems thebiochemical role of the macronutrients has beenmodeledmore specifically in nutrient flow models, both for fish(Machiels, 1987; Olsen, 1989; Van Dam and Pauly,1995) and other farm animals (Birkett and de Lange,2001; Green and Whittemore, 2003; Moughan, 2003;Van Milgen and Noblet, 2003).

Animals seem to a certain extend to know what theyneed and also for fish this ‘nutritional wisdom’ has beenconfirmed. When fish could self-select amount andcomposition of their diet, they consistently choose aspecies (and size?) specific combination of macronutri-ents, based on postingestive, i.e. metabolic consequences(Sanchez-Vazquez et al., 1998, 1999; Yamamoto et al.,

2003; Rubio et al., 2003). It is not clear on which criteriathis ‘target intake’ (Simpson and Raubenheimer, 2001) isbased, e.g. on maximization of growth or on optimizationof the balance between costs and benefits of growth(Tolkamp, 1999; Yearsley et al., 2004; Mangel andMunch, 2005). When not offered a choice, but offered asingle diet, animals can only vary the amount eaten andthey have to compromise between overeating somenutrients and undereating others. Where both over- andundereating are ‘off-target’, Forbes (2003) proposed thetheory that being ‘off-target’ causes the animal discomfort,and that it will eat the amount that causes the lowest levelof total (added for all nutrients separately) discomfort.

Although the criteria on which the above choices aremade are not clear, feed intake is known to vary with fishspecific factors (species, age, size, body composition),often taken together as internal or developmental state.The objective of the present study was to examine theinteraction of the effects of feed (macronutrient compo-sition) and fish (age/developmental state) on voluntaryfeed intake and associated metabolism and growth of theEuropean eel.

2. Materials and methods

2.1. Fish, experimental conditions

A sorted batch of about 8000 European eels, Anguillaanguilla L., with an average individual body weight of5 g were obtained from a commercial eel farm (Mondi-aal, Veenendaal, The Netherlands). After arrival in ourexperimental facilities, the fish were stocked in theexperimental aquaria for an acclimation period of2 weeks. The experiment was conducted in 140 Laquaria which were part of a recirculation system whichconsisted of 32 aquaria, a sedimentation unit and abiological (trickling) filter. During the experiments watertemperature was 25.2±0.4 °C, pH was 8.1±0.3, oxygencontent of the water flowing out of the aquaria remainedabove 6 g m−3 and system concentrations of NH4–N andNO2–N remained below 0.1 and 0.3 g m−3, respectively.Photoperiod was 12 h light, from 7:00–19:00 h, with15 min of artificial dawn and dusk through dimmers.

2.2. Experimental diets

Five diets were formulated with different contents ofcrude protein (33–63% DM), crude fat (6–28% DM)and calculated carbohydrates (NFE; 15–42% DM) suchthat five levels of digestible protein/digestible energy(DP/DE) were realised: 13, 16, 21, 28 and 29 g MJ−1.The diets were produced using a single-screw extruder

177L.T.N. Heinsbroek et al. / Aquaculture 267 (2007) 175–187

in the experimental feed mill of Provimi (Provimi B.V.,Rotterdam, The Netherlands) as extruded pellets of2.2 mm. For the diets with more than 20% fat, part of thefat was coated on the feed after extrusion and drying.Ingredients and analysed composition of the diets aregiven in Table 1.

2.3. Experimental procedures

After the acclimation period of 2 weeks (day 0), 15aquaria were stocked each with 500 eels (average bodyweight 5±0.2 g) A sample was taken from the commonpool, euthanised and stored at −20 °C for laterdetermination of body composition. The five diets werefed to triplicate groups. Due to increasing aggression,grading was necessary and from day 145–259 the trip-licates consisted of three size classes from the samepopulation. After day 259 small and large fish were dis-carded and from day 260–302 triplicates were groups ofaverage size per diet. Feeding was by hand till satiationduring 1 h, once daily, at 9.00 h and daily feed intake wasrecorded. Average body weight was determined approx-imately every 4 weeks and body composition of differentsize classes was determined at the beginning and after 57,145, 259 and 302 d. At three points in time, day 62(average body weight 10–20 g), day 150 (average bodyweight 40–80 g) and day 264 (average body weight 90–130 g), nitrogen and energy balance studies wereconducted in which next to feed intake and growth alsodigestibilities of dry matter, protein, fat, NFE, ash and

Table 1Ingredients and proximate composition of the experimental diets

Diet D13 D16 D21 D28 D29

Ingredients (g kg−1)Protein mix a 400 500 500 800 750Fish oil 250 250 10 70 –Extruded wheat starch 320 220 460 100 220Vitamin/mineral premix b 30 30 30 30 30Analysed compositionDry matter (DM) (%) 92.4 92.7 91.0 93.8 92.7Protein (N×6.25) (%DM) 32.2 40.3 43.5 63.2 60.7Lipid (%DM) 26.3 28.2 7.1 11.0 5.9Ash (%DM) 6.8 7.4 7.9 10.3 10.1Carbohydrates (NFE, %DM) 34.7 24.1 41.5 15.5 23.3Gross energy (kJ g DM−1) 25.3 25.5 21.0 22.5 21.1Digestible protein (%DM) c 29.4 37.6 40.2 58.8 57.0Digestible energy (kJ g DM−1) c 22.3 23.3 19.2 20.8 19.7DP/DE (mg kJ−1) 13.2 16.1 20.9 28.2 28.9

a Protein mix consisted of 760 g kg−1 Fish meal (Herring CPN700 gkg−1), 163 g kg−1 Blood meal (Spray dried CP 830 g kg−1) and 77 gkg−1 Soy protein isolate (Provimi, CP 850 g kg−1).b Provimi BV, Rotterdam, The Netherlands.c Digestibilities are given in Table 3.

energy as well as O2 consumption and NH4–N excretionwere measured. Balance studies were done in the balancerespirometer system described by Heinsbroek et al.(1993), with average weight samples of the fivepopulations and lasted for ±3 weeks.

2.4. Sampling, data collection and analysis

Initial and final bodyweight and (daily) amount of feedwere determined to the nearest 0.1 g. In the respirometersystem, a 24 h monitoring period was conducted twice aweek. Faeces were collected continuously by faecescollectors (Heinsbroek et al., 1993) and were stored at−20 °C.Water flow rates through the respirometer aquariawas measured by flow meters. Water was sampled fromthe inflowing water and from the out-flowing water ofeach of the 5 aquaria every 30 min. Oxygen concentra-tions in in- and out-flowing water were measured with anoxygen electrode andmeter (WTWTriOXmaticR 601 and160, respectively; Retsch, Ochten, The Netherlands).Nitrogen excretion was determined by analysing the in-and out-flowing water for NH4–N and NOx–N concen-trations by colorimetric methods using a continuous flowanalyzer (AlpkemRFA/2™; AlpkemCorporation, Clack-amas, Oregon, USA).

Feeds, fish and faeces were analysed for dry matter,ash, protein, fat and energy. For determination of diges-tibilities, acid insoluble ash (AIA) was determined infeeds and faeces. Whole fish bodies were crushed andhomogenised. Dry matter, ash and protein were deter-mined in this fresh homogenate. Fat and energy weredetermined in freeze-dried homogenate. Dry matter wasdetermined by drying the samples for 4 h at 103 °C. Ashcontent was determined by ashing the samples for 4 h at550 °C. For determination of AIA, the ash residue wasboiled in 0.1 N H2SO4 for 15 min, filtered over ash-freefilter paper and re-ashed for 4 h at 550 °C. Proteincontent was determined as N×6.25 by Kjeldahlprocedure after acid digestion. Fat content was deter-mined by Soxhlet extraction with petroleum–ether for4 h and gross energy was determined by bomb-calorimetry (IKA-C-7000). Carbohydrate content ofthe diets was calculated as nitrogen free extract: drymatter minus the sum of protein, fat and ash.

2.5. Data analysis

Due to the size grading the three aquaria per dietcould not be treated as genuine replicates and effect ofage (period) was not statistically tested. Instead rates offeed intake, metabolism and growth were related tobody weight and were expressed in g or kJ fish−1 d−1 or


in metabolic weight units (g or kJ kg−0.8 d−1), based onthe geometric average body weight over the experimen-tal period (ABWg=(BWi×BWf)

0.5). To test effects ofdiet and body weight on body composition the data werefirst linearized according to Ramseyer (2002) as:

LnðyÞ ¼ aþ b⁎LnðxÞ ð1Þwhere y = body constituent (g fish−1), a = intercept,amount of y for a fish of 1 g, b = effect of body weightand x = body weight (g). The effect of diet was testedwith the model:

y ¼ lþ Di þ b1⁎xþ b2⁎ðDi⁎xÞ þ e

where y = Ln [Body constituent (g fish−1)], μ = generalintercept,D = fixed effect of diet i on the intercept (i=1,5),x=Ln [Body weight(g)], β1 = regression coefficient forthe effect of body weight, β2 = regression coefficient forthe interaction between effect of diet and effect of bodyweight and ε = residual error. Non-significant (PN0.05)effects of diet were removed from the model.

Results on digestibilities of dry matter, protein, lipid,carbohydrates and energy were, after testing fornormality (Kolmogorov–Smirnov) and homogeneity ofvariances (Levene), analysed for effects of diet and sizegroup with two way ANOVAwith post hoc comparisonof means (Duncans multiple range test, Pb0.05).

Voluntary feed intake (VFI) and metabolism wereanalysed using the ‘requirements’ model (Emmans,

Table 2Initial and final body weight, feed intake, oxygen consumed, nitrogen producfive diets differing in DP/DE ratio

Period/size

Diet Duration(d)

Body weight Feed intake Oco(mfisd−

Initial(g)

Final(g)

(g DM fish−1

d−1)(g DM kg−0.8

d−1)

1 D13 23 8.2 11.1 0.12 4.9 6D16 23 9.9 13.1 0.13 4.5 7D21 23 9.9 13.7 0.12 4.3 8D28 23 11.2 14.0 0.13 4.2 8D29 23 11.2 15.1 0.15 5.0 9

2 D13 21 46.4 57.4 0.65 7.0 26D16 21 48.7 60.9 0.69 7.0 32D21 21 42.7 56.4 0.88 9.8 31D28 21 51.0 61.9 0.74 7.4 32D29 21 52.9 65.6 0.86 8.3 36

3 D13 22 96.8 107.3 0.64 4.0 42D16 22 111.4 124.5 0.68 3.8 41D21 22 102.2 114.7 0.83 4.9 44D28 22 122.0 134.4 0.74 3.8 42D29 22 116.2 126.1 0.60 3.3 44

1997; Lupatsch et al., 2001), where voluntary feedintake is considered to originate from a requirement formaintenance and a requirement for growth.

VFI ¼ FImþ ð1=kÞ⁎GR ð2ÞWhere VFI = voluntary feed intake (g or kJ), FIm =

feed intake for maintenance (g or kJ), k = constant,denoting the efficiency of utilizing feed intake abovemaintenance (–) and GR = growth (g or kJ). N.B. forVFI (and FIm) one can substitute metabolic rates (O2

consumption and NH4–N excretion). Linearity in thismodel implies that the efficiency (k) is in fact constantover the range of growth tested, which has led to a lot ofdiscussion over the past 50 years (Heinsbroek, 1987;Bureau et al., 2006). We tested for linearity and althoughwe did find some deviations, notably in energy intake asaffected by energy growth (Fig. 3b) and in NH4–Nexcretion as affected by digestible protein intake (Figs.6a and 7a), we decided to use a general linear model tocompare whether average effects of growth and intakewere affected by diet. Dietary effects on maintenance(intercept) and marginal growth efficiency (slope) weretherefore tested with the model:

y ¼ lþ Di þ b1⁎xþ b2⁎ðDi⁎xÞ þ e

where y = feed intake or metabolism (g or kJ), μ =general intercept, D = fixed effect of diet i on theintercept (i=1,5), x = growth (g or kJ), β1 = regression

ed and final body composition of three size groups of European eel fed

2

nsumedgh−11)

NH4–Nproduced(mgfish−1

d−1)

Body composition

Dry matter(%)

Protein(%)

Lipid(%)

Ash(%)

Energy(kJ g−1)

7 1 34.7 15.1 17.4 1.8 10.46 2 35.3 15.6 17.3 1.6 10.50 3 32.2 16.3 12.9 1.9 9.00 5 32.7 17.3 11.7 1.7 8.79 7 32.5 17.1 11.1 1.9 8.4

5 8 42.3 14.2 26.0 2.0 13.63 13 41.8 14.6 25.7 2.1 13.60 20 37.0 15.4 19.7 2.1 11.40 31 36.3 16.2 18.3 2.0 11.06 36 35.8 16.3 18.3 1.9 11.1

6 10 45.9 13.9 30.3 1.6 15.33 14 47.4 14.1 30.9 1.6 15.60 24 40.6 14.9 24.4 1.7 13.24 31 41.4 15.6 23.1 2.0 12.81 27 41.7 16.0 22.8 1.9 12.8


coefficient, β2 = regression coefficient for the interactionbetween effect of diet and effect of x and ε = residualerror. Non-significant (PN0.05) effects of diet wereremoved from the model.

Fig. 2. Body lipid (a) and body protein content (b) of European eel fedfive diets differing in DP/DE ratio. Whole model (after removal of non-significant effects of diet) coefficients of determination are given (n=95).Lines in (a) are: D13: y=9.6 (±0.6)⁎x0.245 (±0.018), D16: y=8.9(±0.6)⁎x0.259 (±0.018), D21: y=5.9 (±0.5)⁎x0.300 (±0.019), D28:y=5.2 (±0.4)⁎x0.304 (±0.020), D29: y=4.4 (±0.3)⁎x0.338 (±0.018).Lines in (b) are: D13: y=16.7 (±0.2)⁎x−0.040 (±0.004), D16: y=17.2(±0.3)⁎x−0.040 (±0.004), D21: y=18.2 (±0.2)⁎x−0.040 (±0.004), D28:y=19.1 (±0.2)⁎x−0.040 (±0.004), D29: y=19.3 (±0.3)⁎x−0.040 (±0.004).

Fig. 1. Feed intake (a), cumulative feed intake (b) and body weight (c) offive groups of European eel fed diets differing in DP/DE ratio. Symbolsin (a) are results for individual aquaria while lines in (a) connect theaverages per diet. Symbols in (b) and (c) are averages per diet.

All statistical analysis were executed with SPSS 12.0for Windows.

3. Results

Feed intake in g fish−1 d−1 increased for all diets to amaximum at 80–100 g body weight and declinedthereafter, such that both cumulative feed intake andbody weight of the fish increased with age in a sigmoidfashion (Fig. 1). Growth leveled off at a body weight of130–140 g, indicating that the majority of the populationwere male. During the first 4 months, up to a body weightof ca. 20 g, the fish fed diet DP/DE 28 grew fastest. After

Table 3Digestibilities of dry matter, protein, lipid, carbohydrates and energy asaffected by diet and size in European eel

Dry matter Protein Lipid Calculatedcarbohydrates

Energy

DietD13 84.9a 91.3a 85.6a 88.1a 88.1a

D16 88.3b 93.2cd 89.9b 92.0cd 91.5b

D21 87.3c 92.3b 90.3b 90.0b 91.3b

D28 87.2c 93.1c 91.8b 90.9bc 92.6c

D29 89.0b 93.9d 92.1b 93.7d 93.6d

Size10–20 g 86.6a 92.9 87.2a 89.9 90.7a

40–60 g 86.9a 92.4 89.6b 90.6 91.1a

90–130 g 88.3b 92.5 95.6c 91.3 92.8b

Total average 87.1 92.6 90.0 90.7 91.3Pooled SE 0.2 0.1 0.4 0.2 0.2

ANOVADiet ⁎⁎⁎ ⁎⁎⁎ ⁎⁎⁎ ⁎⁎⁎ ⁎⁎⁎

Size ⁎⁎⁎ ns ⁎⁎⁎ ns ⁎⁎⁎

Interaction ⁎ ns ⁎⁎⁎ ns ⁎

⁎ Pb0.05, ⁎⁎ Pb0.01, ⁎⁎⁎ Pb0.001, ns = not significant.Diets or size groups with a different superscript are significantlydifferent (Duncan, Pb0.05).

Fig. 3. Intake of digestible protein as affected by protein deposition (a)and intake of digestible energy as affected by energy deposition (b) ofEuropean eel fed five diets differing in DP/DE ratio. Whole model(after removal of non-significant effects of diet) coefficients ofdetermination are given (n=165). Lines in (a) are: D13: y=0.77(±0.12)+1.81 (±0.16)⁎x, D16: y=0.80 (±0.12)+2.10 (±0.15)⁎x,D21: y=1.24 (±0.18)+2.66 (±0.25)⁎x, D28: y=1.65 (±0.14)+3.19(±0.15)⁎x, D29: y=1.50 (±0.16)+3.25 (±0.18)⁎x. Lines in (b) are:D13: y=59 (±8)+1.34 (±0.08)⁎x, D16: y=52 (±8)+1.36 (±0.09)⁎x,D21: y=51 (±12) +1.73 (±0.18)⁎ x, D28: y=43 (±10) + 1.81(±0.15)⁎x, D29: y=35 (±11)+1.81 (±0.16)⁎x.


these 4 months the fish fed diet DP/DE 16 showed thefastest growth. These latter fish reached market size of120 g after±260 d, while fish fed diet DP/DE 21were stillca. 85 g.

Growth, feed intake, metabolism and body compo-sition of the three size groups from the balance studiesare given in Table 2. Body content of dry matter, lipidand energy were strongly related and all showed acontinuous increase with body weight (Fig. 2a). The fishfed diets DP/DE 13 and 16 reached a body lipid level of33% (of fresh body weight), at body weights of 130–140 g, while fish fed diets DP/DE 28 and 29 reached alipid level of 25% at these body weights. Body proteincontent first increased with body weight up to ca. 15 gand thereafter showed a distinct decrease. Body proteincontent was also negatively correlated with body fatcontent, as body protein content of the fish fed diets DP/DE 13 and 16 decreased to 14% at body weights of 130–140 g, while that of the fish fed diets DP/DE 28 and 29decreased to 16% at these body weights (Fig. 2b).

Digestibilities were little affected by diet composition,only diet DP/DE 13 showed a general lower digestibilityof dry matter, protein, fat, NFE, ash and energy (Table 3).Notably is the high digestibility of carbohydrates,independent of dietary level. Digestibilities of protein(92.6%) and carbohydrates (90.7%) were not affected bybody weight. Digestibility of lipid showed a significant

increase with body weight, from 87% at 10–20 g to 96%at 100–140 g.

Voluntary feed intake, either as digestible proteinintake (DPI) or digestible energy intake (DEI), showedlinear relations with both protein deposition (PD) andenergy deposition (ED) (Fig. 3), in accordance with the


requirements model (2). For DPI there was a clear effectof diet in relation to PD. The marginal efficiency of PD(kP=1 / slope) was inversely related to the DP/DE ratioof the diets, showing a decrease from 0.54 for diet D13to 0.29 for diets D28 and D29. Effects on DEI were

Fig. 4. Oxygen consumption as affected by digestible protein intake (a)and protein deposition (b) of European eel fed five diets differing in DP/DE ratio. Whole model (after removal of non-significant effects of diet)coefficients of determination are given (n=84 and n=15 respectively).Lines in (a) are: D13: y=1.51 (±0.06)+0.662 (±0.046)⁎x, D16: y=1.51(±0.06)+0.607 (±0.038)⁎x, D21: y=1.51 (±0.06)+0.490 (±0.025)⁎x,D28: y=1.51 (±0.06)+0.406 (±0.021)⁎x, D29: y=1.51 (±0.06)+0.433(±0.021)⁎x. Line in (b) is: y=1.65 (±0.19)+1.59 (±0.16)⁎x.

Fig. 5. Oxygen consumption as affected by digestible energy intake (a)and energy deposition (b) of European eel fed five diets differing in DP/DE ratio. Whole model (after removal of non-significant effects of diet)coefficients of determination are given (n=84 and n=15 respectively).Lines in (a) are: D13: y=1.50 (±0.08)+0.008 (±0.0006)⁎x, D16:y=1.50 (±0.08)+0.009 (±0.0006)⁎x, D21: y=1.50 (±0.08)+0.010(±0.0005)⁎x, D28: y=1.50 (±0.08)+0.012 (±0.0006)⁎x, D29: y=1.50(±0.08)+0.013 (±0.0006)⁎x. Lines in (b) are: D13: y=1.55 (±0.15)+0.016 (±0.004)⁎x, D16: y=1.55 (±0.15)+0.018 (±0.004)⁎x, D21:y=1.55 (±0.15)+0.020 (±0.005)⁎x, D28: y=1.55 (±0.15)+0.023(±0.004)⁎x, D29: y=1.55 (±0.15)+0.013 (±0.005)⁎x.

smaller, here it was found that the fish fed the highenergy diets (D13 and D16), which had higher bodylipid contents, showed a higher marginal energeticefficiency (kE) of 0.74 compared to 0.56 for the otherdiets.

Fig. 6. Ammonia nitrogen excretion as affected by digestible proteinintake (a) and protein deposition (b) of European eel fed five dietsdiffering in DP/DE ratio. Whole model (after removal of non-significanteffects of diet) coefficients of determination are given (n=69 and n=15respectively). Lines in (a) are: D13: y=0.01 (±0.02)+0.043 (±0.005)⁎x,D16: y=0.01 (±0.02)+0.051 (±0.004)⁎x, D21: y=0.01 (±0.02)+0.060(±0.003)⁎x, D28: y=0.01 (±0.02)+0.070 (±0.002)⁎x, D29: y=0.01(±0.02)+0.072 (±0.002)⁎x. Lines in (b) are: D13: y=0.04 (±0.03)+0.04 (±0.008)⁎x, D16: y=0.04 (±0.03)+0.08 (±0.008)⁎x, D21:y=0.04 (±0.03)+0.14 (±0.006)⁎ x, D28: y=0.04 (±0.03)+0.27(±0.008)⁎x, D29: y=0.04 (±0.03)+0.28 (±0.007)⁎x.

Fig. 7. Ammonia nitrogen excretion as affected by digestible energyintake (a) and energy deposition (b) of European eel fed five dietsdiffering in DP/DE ratio. Whole model (after removal of non-significanteffects of diet) coefficients of determination are given (n=69 and n=15respectively). Lines in (a) are: D13: y=0.01 (±0.02)+0.00048(±0.00007)⁎x, D16: y=0.01 (±0.02)+0.00072 (±0.00007)⁎x, D21:y=0.01 (±0.02)+0.0012 (±0.00006)⁎x, D28: y=0.01 (±0.02)+0.0019(±0.00007)⁎x, D29: y=0.01 (±0.02)+0.0020 (±0.00007)⁎x. Lines in(b) are: D13: y=0.02 (±0.02)+0.0007 (±0.0001)⁎x, D16: y=0.02(±0.02) + 0.0011 (±0.0001) ⁎ x, D21: y=0.02 (±0.02) + 0.0020(±0.0003)⁎x, D28: y=0.02 (±0.02)+0.0041 (±0.0004)⁎ x, D29:y=0.02 (±0.02)+0.0043 (±0.0004)⁎x.


Oxygen consumption and nitrogen excretion werelinearly related to DPI and DEI, and also to PD and ED(Figs. 4 5 6 and 7). The effect of diet on oxygen

consumption was dependent on the LD/PD ratio; were1 g PD costs 1.6 g O2 irrespective of diet (Fig. 4b), 1 MJED costs 1.6 g O2 for fish fed D13 and 2.6 g O2 for fish

Fig. 8. Intake of five different feeds by European eel as influenced by twonutrient dimensions, digestible protein intake and intake of digestiblenon-protein energy. The slopes of the lines connecting the intake points ofthe three size groups indicate the relative weight of the nutrientdimensions in the feed intake compromise. Lines for the three size groupsare: 10–15 g: y=4.2 (±0.8)–27.4 (±3.5)⁎x, 40–60 g: y=18.7 (±0.7)–23.4 (±1.8)⁎x, 80–120 g: y=21.7 (±0.7)–18.1 (±1.2)⁎x.


fed D29 (Fig. 5b). This effect of body composition wasalso found for NH4–N excretion where the effect of dietwas even stronger for ED than for PD (Figs. 6b and 7b)which indicates that the carbon chains of the deaminatedamino acids were used for lipid synthesis.

In Fig. 8 the rules of compromise of Simpson andRaubenheimer (2001) are depicted for three size groups.The slopes of the lines, representing the relative weightof the ‘nutrient’ on both axes in the compromise, aredecreasing with body weight, indicating an increasedimportance of non-protein energy (NPE).

4. Discussion

Reproduction and growth are fundamental to allanimals. The ultimate purpose of an individual is topass on its genes and they need to achieve a critical orthreshold size to be able to reproduce (Mangel, 1996;Metcalfe, 1998; Jobling, 2002;Mangel andMunch, 2005;Fraser and Rogers, 2007). Growth of the eels in this studylevelled off at a bodyweight of 130–140 g, indicating thatthemajority of the fish in the population(s) weremale. Sexdifferentiation in eels is labile and influenced byenvironmental factors (temperature, fish density, foodavailability), possibly through growth rate during thesensitive period (Helfman et al., 1987; Holmgren andMosegaard, 1996; Metcalfe, 1998), as well as by hor-monal treatment (Degani and Kushnirov, 1992). Underculture conditions the majority of the eels (80–95%)develop as phenotypic males (Egusa, 1979; Degani andKushnirov, 1992; Holmgren and Mosegaard, 1996;

Beullens et al., 1997; Davey and Jelliman, 2005). Ineels males mature at a smaller size than females. A.anguilla males mature at 30–45 cm and 80–180 g whilefemales mature at 60–80 cm and 400–1000 g (Tesch,2003). Life-history theory attempts to predict what life-history strategies, growth and resource tradeoffs in var-ious developmental stages, are adaptive, that is whichstrategies maximize (expected) lifetime reproductiveoutput (Wootton, 1985; Metcalfe and Monaghan, 2001).According toDavey and Jelliman (2005)male eelsmatureat a minimal size allowing for successful reproduction(spawning migration), following a time-minimizingstrategy, while females follow a more variable size-max-imizing strategy to optimize the trade-off between mor-tality and fecundity.

In the search for and interpretation of somatic size andsize of body (energy) stores as targets or triggers for lifehistory events (metamorphosis, smolting, migration, mat-uration, spawning), focus has almost exclusively been onbody lipid stores (Metcalfe, 1998; Silverstein et al., 1999;Jobling et al., 2002). For the eels in the present studyhowever final lipid mass varied between ca. 33 g fish−1

for eels fed the high DP/DE diets and ca. 46 g fish−1 foreels fed the low DP/DE diets. Also Kadri et al. (1995)found that the timing of anorexia in maturing Atlanticsalmon was more related to body protein mass than tobody lipid mass. As Mangel (1996) pointed out, repro-ductive success of fish, or any organism, is, apart from theenergy invested in this reproduction, largely based on thestructural components the organism is able to pass on tothe next generation. Depletion of body energy stores in eelduring prolonged (N150 d) starvation, with or withoutsustained swimming activity as in the spawning migra-tion, was shown to be about equal for protein and fat(in g), or about 30% of the energy utilized (in kJ) camefrom body protein (Boetius and Boetius, 1985; Van Gin-neken et al., 2005). This agrees with the results of Einenet al. (1998) for prolonged (86 d) starvation of Atlanticsalmon. The above results all emphasize the role of pro-tein mass as threshold indicator.

Since further live weight gain in animals is almostcompletely based on protein deposition (Jobling, 1985;Birkett and de Lange, 2001; Moughan, 2003), mostanimal feed intake and growth models view the size ofthe protein mass (Pt) and protein deposition (PD) as thecornerstones of growth but also of feed intake (Webster,1993; Milward, 1995; Emmans, 1997; Emmans andKyriazakis, 1997; Birkett and de Lange, 2001; Greenand Whittemore, 2003; Van Milgen and Noblet, 2003).Animals strive to follow an anabolic program (Milward,1995), or to achieve a genetically determined (protein)growth potential, PDmax (Webster, 1993; Birkett and de


Lange, 2001). With potential growth of protein massdescribed by a Gompertz function (a ‘relative’ of the infisheries better known von Bertallanfy growth function,VBGF), this target PDmax can be thought of as beingdriven by (the difference from) the mature size. The ideaof a distinct mature size poses no conceptual problemfor semelparous fish, like anguillid eels, anadromousOncorhynchus spp. and some populations of ayu, Ple-coglossus altivelis, and shad, Alosa sapidissima (Woot-ton, 1985). In all the five eel populations in the presentstudy, average maximum protein mass converged to 20–25 g fish−1. However, also for other (iteroparous) fish atarget size, or an ‘end condition’ (Mangel, 1996), couldbe envisaged either as size at first maturity or as theasymptotic von Bertallanfy Winfinity (Shuter et al.,2005). PDmax as first derivate of the sigmoid growthcurve reaches a maximum at the inflexion point, in thepresent study at a Pt of 11–13 g or a body weight ofabout 80 g, not by chance (see below) the same size asfor the feed intake maximum.

In order to reach the above mentioned goal in size andcomposition, the animal needs to survive and to grow.These needs are conceptualized in the feed intake model‘eating to requirements subject to constraints’ (Emmans,1997; Yearsley et al., 2001), where voluntary feed intakeis considered to originate from a requirement formaintenance (survival) and a drive and thus a requirementfor growth (2). This model addresses both the why of feedintake (requirement to reach goal) as the how of feedintake (possibilities and limits in nutrient processingcapacity) (Tolkamp, 1999; Yearsley et al., 2001). In thepresent study and in earlier studies on eel in our laboratory(Heinsbroek et al., unpublished) it is shown that feedintake of eels can be adequately described by this model,as also shown for several Mediterranean species(Lupatsch et al., 2003), for common carp, Cyprinuscarpio (Meyer-Burgdorff and Rosenow, 1995; Schwarzand Kirchgessner, 1995) and for salmonids (Rodehuts-cord and Pfeffer, 1999; Azevedo et al., 2004, 2005).

The feed intake model ‘eating to requirements subjectto constraints’ can be translated as ‘an animal eats asmuchas it needs, but not more than it can handle’. There is somediscussion about the relevance of these (physical)constraints, of which volume or capacity of the gastro-intestinal tract (GIT) has received most attention, sinceevolutionary considerations would favour a metabolicregulation cq. optimization at a level below that where theconstraint becomes effective (Ketelaars and Tolkamp,1991; Tolkamp, 1999; Yearsley et al., 2001, 2004). Inearlier work with eels we found that with practical dry, i.e.nutrient dense diets, stomach volume was not limitingmeal size (Heinsbroek et al., unpublished). Meal size was

influenced by (expected) level of metabolism, measuredas oxygen consumption and nitrogen excretion. Foraquatic animals, at low dissolved oxygen concentrationsoxygen consumption is shown to be diffusion limited, andVan Dam and Pauly (1995) could therefore relate feedintake of fish to gill surface area. At higher levels ofdissolved oxygen in the water, oxygen supply to thetissues through the cardiovascular system (heart rate,oxygen capacity of the blood) could still limit metabolismand thereby feed intake, at least in so called ‘visceral’ typeof fish (Priede, 1985). Alsop and Wood (1997) coulddemonstrate for rainbow trout a competition between thedifferent metabolic processes of feed processing andswimming activity, which have only a need for ATP(oxygen) in common. This view would be consistent withthe general power budgeting problem of survival versusgrowth, that is the reduction in feed intake whichaccompanies in increase in maintenance needs due toactivity, stress and disease. Since however oxygen con-sumption is also implicated to represent costs of growing,through accumulation of somatic damage (aging), it isagain suggested that even maximal growth (PDmax asdefined above) is regulated below its physiologicalmaximum, which in turn would be consistent with thephenomenon of compensatory growth (Ketelaars andTolkamp, 1991; Metcalfe andMonaghan, 2001; Ali et al.,2003; Yearsley et al., 2004; Mangel and Munch, 2005).Yearsley et al. (2004) did show that a plastic, submax-imumal growth strategy, which allows for variation ingrowth rate in response to the animal's environment andinternal state, was adaptive, where growth is bothassociated with fitness costs (increased mortality) andbenefits (earlier maturity).

The above mentioned drive for PD also explains theoften implied allocation ‘rule’ that dietary protein ispreferably used for PD, as indicated by the so-calledprotein sparing action (PSA) of dietary non-proteinenergy (NPE). This effect is also seen with the eels inthe present study as protein intake increases faster withincreasing PD as the DP/DE ratio is higher. The inverse ofthis slope, the marginal (e.g. above maintenance) proteinutilization efficiency (k in (2) or ep in Emmans andKyriazakis, 1997), increases with increasing NPE from0.29 at DP/DE of 28/29 to a value of 0.54 at DP/DE 13.This is in very close agreement with results of Reinitz(1987) for rainbow trout and Lupatsch et al. (2001) forgilthead seabream. Emmans and Kyriazakis (1997)proposed a similar model for pigs where ep increaseslinearly with the dietary ME/DP ratio, up to a maximumep⁎. The maximum ep⁎ found for pigs, 0.76±0.06(Sandberg et al., 2005) seems higher than maximumvalues found for fish, 0.55–0.60 (Reinitz, 1987; Lupatsch


et al., 2001), although the P/E ratio where this maximumis reached, 13–14mg kJ−1, does not differ (Reinitz, 1987;Lupatsch et al., 2001; Sandberg et al., 2005; presentresults). The fact that even at these low P/E ratios ep isbelow unity, because of inevitable protein turnover,should probably not be considered as waste, but as aprice paid for flexibility and reliability of PD. Due to thisinefficiency PD could in fact in most cases be fuelledcompletely by amino acids. In this sense NPE intake isnever limiting for PD (Eits et al., 2002; Nijhof andHeinsbroek, unpublished), unless NPE intake falls belowthat needed for (maintenance and) LD and dietary proteinis used for this. Where PSA is often interpreted as proteinspared asmetabolic fuel, i.e. spared fromoxidation, in thisview PSA stands for the sparing of dietary protein frombeing used for LD. This can also be seen in the study ofAzevedo et al. (2004) as an almost perfect negativecorrelation seems present between nitrogen retentionefficiency (NRE) and the LD/PD ratio for Atlantic salmonand rainbow trout. In the present study we further foundthat the NH4–N excretion could better be explained by thedeposition of energy than by the deposition of protein.

Protein content of most fish species increases slightlyor remains more or less stable with increasing bodyweight (Ramseyer, 2002). Although the eels in thepresent study showed a distinct decline in proteincontent with increasing size, as well as a decrease withincreasing lipid content, their body protein contentremained relatively stable within the general limits (13–18%) for animal whole body content. Lipid content ofeels showed a very marked increase with body weight.The fact that even at high DP/DE ratio LD was higherthan PD for most of the weight trajection, and dietaryprotein was used for LD, suggests that there is a minimalpreferred lipid content, the relative level depending onfish species (Schreckenbach et al., 2001; Azevedo et al.,2004), but generally increasing with fish size (Olsen,1989; Nijhof, 1993; Schreckenbach et al., 2001;Lupatsch et al., 2003). Fish fed (sub-) maintenancerations could even reach lower lipid levels as fish fedaround maintenance (for energy) still deposit protein atthe expense of body lipid (Meyer-Burgorff et al., 1989;Bureau et al., 2006). Svedang and Wickstrom (1997)described migrating female silver eels with body lipidlevels (sometimes far) below 20%, and while theseauthors questioned the capacity of these eels tosuccessfully migrate and reproduce, these results areyet another indication that lean body mass or Pt is themost important target for maturation. Our results alsosuggest that there is a maximum body lipid content,again increasing with body weight, as body lipid contentdoes not increase further between D16 and D13. Such a

maximum body lipid content might be instigated by thenegative feedback of adiposity on feed intake reportedin a number of fish species (Machiels, 1987; Silversteinet al., 1999; Jobling et al., 2002), possibly throughleptin-like factors.

From the above also follows that LD and PD are notindependent from each other, e.g. they are correlated (inthe present study r2 =0.97). Due to this multi-collinearityestimation of the marginal energetic efficiencies of PDand LD, kp and kf, respectively, through multivariateanalysis of variance can give nonsense results (Rode-hutscord and Pfeffer, 1999; Azevedo et al., 2005; Bureauet al., 2006). In the present study at low DP/DE ratios kpand kf values of 0.3–0.4 and 1.5–3.0 were found (cf.Rodehutscord and Pfeffer, 1999; Azevedo et al., 2005)and at high DP/DE ratios values of 0.54 and 0.67. Whenkp was fixed at 0.54 (Meyer-Burgdorff and Rosenow,1995; Rodehutscord and Pfeffer, 1999; Lupatsch et al.,2001, 2003; Azevedo et al., 2005) kf varied from 0.93with diet D13 to 0.67with diet D29, indicating again a lotof de novo lipid synthesis (from protein) at the higherDP/DE ratio. These results were further corroborated bythe oxygen consumption of the eels. As de novo lipidsynthesis costs more energy than LD through directincorporation of dietary lipid, we could see a significanteffect of dietary DP/DE ratio when oxygen consumptionwas related to energy deposition (ED), but not whenrelated to PD. Typical values for fish are 0.45–0.56 forkp and 0.7–0.9 for kf (Heinsbroek, 1987; Meyer-Burgorff et al., 1989; Meyer-Burgdorff and Rosenow,1995; Rodehutscord and Pfeffer, 1999; Lupatsch et al.,2001, 2003; Azevedo et al., 2005; Bureau et al., 2006)and there are therefore no indications that they differfrom those of other farm animals (Emmans, 1997).

Where potential growth and thereby the requirementsfor growth are genetically programmed, according to the‘eating to requirements’ model this follows also for feedintake, as shown in the consistency of macronutrientchoice in self-selection experiments in fish (Sanchez-Vazquez et al., 1998, 1999; Rubio et al., 2003; Yamamotoet al., 2003). Which nutrient carries the largest weight inthe compromise when comparing different unbalanceddiets can be deducted from the rule of compromise in thegeometric framework of Simpson and Raubenheimer(2001). The decreasing slope of the lines depicting thecompromise between protein and NPE eaten with in-creasing body weight in the present study suggests anincreasing importance of NPE with size. This agreeswith the well known decrease in optimal DP/DE ratiowith increasing fish size, which from the ‘eating torequirements’ model originates from a) a decreasingmaximum feed intake, expressed as multiples of


maintenance and b) an increasing L/P ratio in the gain(Heinsbroek, 1987; Lupatsch et al., 2001, 2003; Heins-broek et al., unpublished).

5. Conclusions

Due to the distinct life history of the semelparous, inthe present study predominantly male eel, a well-definedgoal in terms of mature size and composition could beinferred, presumably to maximize their lifetime reproduc-tive output. In order to reach this goal the animal needs tosurvive and to grow and voluntary feed intake of the eelscould be adequately described with the feed intake model‘eating to requirements subject to constraints’, wherevoluntary feed intake is considered to originate from arequirement for maintenance (survival) and a drive andthus a requirement for growth. Life weight gain is almostcompletely based on protein deposition (PD) and eels, likeother animals, strive to reach a genetically determinedgrowth potential (PDmax) thought to be driven by thedifference from the mature protein mass (Ptmax). Bodylipid content increases with size and seemed to beregulated between a distinct minimum and maximum.Preferable allocation of dietary protein to PD wasconfirmed through protein sparing action of NPE.Marginal efficiencies did not differ from those of otherfish or other farm animals. Differences between fishspecies in feed intake and utilization of feeds differing inmacronutrient composition, as well as life history de-velopments in feed intake and feed utilization are thereforebased on differences in growth rate, in turn with matureweight (Ptmax), and body composition (LD/PD ratio).

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effects of feed composition on life history developments in feed intake, metabolism, growth and body...

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