The effect of fish meal replacement by soyabean products on fish growth: a meta-analysis

James Sales

doi:10.1017/S0007114509991279

The effect of fish meal replacement by soyabean products on fish growth: a meta-analysis

Published online by Cambridge University Press: 14 December 2009

James Sales

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James Sales*: Affiliation:
Research Institute of Fish Culture and Hydrobiology, University of South Bohemia, Zatisi 728, 38925Vodnany, Czech Republic
*: *Corresponding author: Dr James Sales, fax +420 383 382 396, email [email protected]

Article contents

Abstract
Materials and methods
Results and discussion
References

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Abstract

Meta-analysis was applied to quantify the effect of replacement of fish meal by soyabean products in diets on fish growth. Measurement of growth in different units among studies required the use of a standardised effect size (Hedges' d). From a total of ninety-nine studies concentrating on fish meal replacement by defatted soyabean meal, 53 % were eliminated due to, among others, absence of a fish meal control diet (n 18), or no statistical differences or measurement of dispersion (n 6) indicated. Replacement of 4 to 40 % fish meal by soyabean meal (inclusion levels of 71–366 g/kg) resulted in a mean effect size of − 0·1142 (95 % CI − 0·4665, 0·2382) obtained in forty-eight comparisons evaluated with seventeen different fish species. However, at higher fish meal replacement levels the 95 % CI calculated for combined effect sizes did not overlap with zero. With soya protein concentrate replacing 25 to 100 % of fish meal in diets for seven fish species, methionine supplementation (mean − 2·4373 (95 % CI − 3·9004, − 0·9742); n 10) did not have a substantial influence on the magnitude of cumulative effect sizes relative to no supplementation (mean − 2·7306 (95 % CI − 3·7991, − 1·6620); n 16). Information on other soyabean products (full-fat soyabeans, soya flour) used as protein sources in fish diets was found as too limited for analysis and definite conclusions. The present study contributes by putting a numerical value to the magnitude of growth differences in fish when replacing dietary fish meal by soyabean products.

Keywords

Fish meal Soyabean products Fish diets Growth Meta-analysis

Type: Full Papers
Information: British Journal of Nutrition , Volume 102 , Issue 12 , 28 December 2009 , pp. 1709 - 1722

DOI: https://doi.org/10.1017/S0007114509991279 [Opens in a new window]
Copyright: Copyright © The Author 2009

Reviews on the future of aquaculture production⁽Reference Naylor, Goldburg and Primavera¹⁾ and development of fish diets⁽Reference Hardy²^–Reference Lim, Webster and Lee⁹⁾ have centred around the replacement of fish meal, on which most fish diets are based, by economically viable and environmentally friendly plant protein alternatives. Defatted soyabean meal has received considerable attention due to a high protein content, reasonably balanced amino acid profile, consistent availability, cost effectiveness and palatability to most fish species⁽Reference Watanabe⁴^, Reference Gatlin, Barrows and Brown⁶⁾.

Soyabeans, although evaluated after heat treatment in the whole form in fish diets, are predominantly processed into defatted soyabean meal with or without hulls, but also into soya flour, soya protein concentrate and soya protein isolate. However, costs hamper the use of the latter processed products for effective replacement of fish meal in fish diets⁽Reference Gatlin, Barrows and Brown⁶⁾.

As with all potential plant protein sources, the nutrient and antinutritional profiles of soyabean meal are currently not ideal for inclusion in fish diets⁽Reference Gatlin, Barrows and Brown⁶^, Reference Francis, Makkar and Becker¹⁰⁾. Furthermore, as summarised by, among others, Chou et al. ⁽Reference Chou, Her and Su¹¹⁾ and Lim et al. ⁽Reference Lim, Choi and Wang¹²⁾, there generally appears to be large variability among fish species in the maximum dietary levels of soyabean meal tolerated, indicating different sensitivities to soyabean meal inclusion. Barrows et al. ⁽Reference Barrows, Stone and Hardy¹³⁾ concluded that the upper dietary inclusion levels of soyabean meal before fish performance or health will be deteriorated is 10–15 % (25 % fish meal replacement) for carnivorous species such as Atlantic salmon (Salmo salar), rainbow trout (Onchorynchus mykiss), sea bass (Dicentrarchus labrax) and yellowtail (Seriola quinqueradiata). However, Heikkinen et al. ⁽Reference Heikkinen, Vielma and Kemiläinen¹⁴⁾ stated upper inclusion levels of 20–30 % for carnivorous salmonids. In contrast, omnivorous and carnivorous freshwater fish such as common carp (Cyprinus carpio), tilapia (Oreochromis spp.), blue catfish (Ictalurus furcatus) and channel catfish (I. punctatus) seem to grow well on high percentages (70–100 %) of fish meal replaced by soyabean meal⁽Reference Chou, Her and Su¹¹^, Reference Kikuchi¹⁵⁾. Factors causing discrepancy among researchers on the use of soyabean meal as a protein source for fish might be related to quality, processing and inclusion levels of soyabean meal, variation in diet formulation, and differences in fish species, fish size and culture system⁽Reference El-Sayed³^, Reference Elangovan and Shim¹⁶^–Reference Romarheim, Skrede and Gao¹⁷⁾.

Although several reviews⁽Reference Hardy²^–Reference Gatlin, Barrows and Brown⁶^, Reference Lim, Webster and Lee⁹^–Reference Francis, Makkar and Becker¹⁰⁾ on feed ingredients for use in fish diets have included the replacement of fish meal by soyabean products, they were concentrated on summative descriptions of results obtained from research studies. These narrative reviews consider all studies with equal weight, without an account for measures of dispersion. Meta-analysis, the review of scientific literature with the emphasis on providing a quantitative synthesis of data, allows the evaluation and integration of results from a group of studies, even those with seemingly contradictory results⁽Reference Fernandez-Duque¹⁸⁾.

The objective of the present study was to analyse, with the use of meta-analytic techniques, available published growth results obtained in fish due to the replacement of dietary fish meal by soyabean products. The outcome would provide a numerical measurement of the extent of growth differences.

Materials and methods

Selection of studies

A comprehensive literature search was conducted on the Internet with the use of several search engines and publishers' websites. Cook et al. ⁽Reference Cook, Guyatt and Ryan¹⁹⁾ concluded that unpublished results should not be completely excluded from meta-analysis, but be subjected to the same rigorous methodological evaluation than published peer-reviewed data, and results being presented with and without inclusion of unpublished results. However, inclusion of the latter can be problematic, especially when coming from interested sources. Willingness of investigators related to outcome, with favourable results being provided more easily, and hidden unpublished results even after extensive consultation, could result in an unpresentative sample of unpublished studies. This causes doubt if the inclusion of unpublished studies increases or decreases bias in meta-analyses⁽Reference Davey Smith and Egger²⁰⁾. Taking the above into consideration, studies have been selected for evaluation in the present study that: (1) had replaced fish meal in diets by soyabean products, (2) presented a measurement of fish growth, (3) appeared in peer-reviewed journals, and (4) been published in English in order to extract all relevant information. Studies fulfilling the above were further subjected to evaluation for inclusion in meta-analyses according to criteria presented in Table 1.

Table 1 Selection of studies for inclusion in meta-analysis

Whereas some studies included only one level of fish meal replacement, others contained multiple replacements. Furthermore, different products⁽Reference Wee and Shu²¹^–Reference Hemre, Sanden and Bakke-McKellep²⁸⁾, similar products subjected to different processing treatments⁽Reference Olivia-Teles, Gouveia and Gomes²³^, Reference Nengas, Alexis and Davies²⁵^, Reference Boonyaratpalin, Suraneiranat and Tunpibal²⁷⁾, supplementation with amino acids⁽Reference Lim, Choi and Wang¹²^, Reference Brown, Twibell and Jonker²⁶^, Reference Shiau, Chuang and Sun²⁹^–Reference Tibaldi, Hakim and Uni⁴¹⁾, effects at different dietary protein levels⁽Reference Shiau, Chuang and Sun²⁹^, Reference Shiau, Pan and Chen⁴²⁾, and the influence on different fish species⁽Reference Refstie, Korsoen and Storebakken⁴³⁾ and fish sizes⁽Reference Brown, Twibell and Jonker²⁶^, Reference Khan, Jafri and Chadra³⁷^–Reference Choi, Wang and Park³⁸^, Reference Gallagher⁴⁴^–Reference Hernández, Martínez and Jover⁴⁶⁾, were often evaluated in the same study. Due to the apparent effect of all of the above variables, data were not pooled for individual studies, but used in individual comparisons. Although this might caused dependence on one another for some effect sizes, exclusion of non-independent comparisons may bias results more than their inclusion⁽Reference Hedges and Olkin⁴⁷^, Reference Gurevitch, Morrow and Wallace⁴⁸⁾. The above resulted in a coding system based on trial identification numbers.

Data analysis

Fish growth in studies selected for inclusion in the meta-analysis has been presented in different units: total weight gain (g), weight gain (%), specific growth rate (%), and daily and thermal growth coefficients. This necessitated the use of a common metric independent of differences in unit measurements. Effect size was measured with Hedges' d ⁽Reference Hedges and Olkin⁴⁷⁾, based on the difference between the means ( $\overline{ X }$ ) for treatment (T) and control (C) groups, standardised by dividing by the pooled standard deviation (s _p), and corrected for bias (J) for small sample sizes (n):

$\begin{eqnarray} d = \frac {\overline{ X }_{T} - \overline{ X }_{C}}{ s _{p}} J \end{eqnarray}$

with

$\begin{eqnarray} J = 1 - \frac {3}{4( n _{T} + n _{C}) - 9} \end{eqnarray}$

and

$\begin{eqnarray} s _{p} = \sqrt {\frac {( n _{T} - 1) s _{T}^{2} + ( n _{C} - 1) s _{C}^{2}}{ n _{T} + n _{C} - 2}}. \end{eqnarray}$

The asymptotic se of the effect size was estimated by Hedges⁽Reference Hedges⁴⁹⁾:

$\begin{eqnarray} se = \sqrt {\frac { n _{T} + n _{C}}{ n _{T} n _{C}} + \frac { d ^{2}}{2( n _{T} + n _{C} - 2)}}. \end{eqnarray}$

Precision of d was illustrated with the 95 % CI:

$\begin{eqnarray} d - 1\cdot 96\,se\,to\, d + 1\cdot 96\,se. \end{eqnarray}$

Summary statistics were calculated using a random-effects model⁽Reference Hedges and Vevea⁵⁰⁾, which takes into account between-trial variability (true heterogeneity) as well as within-trial variability (sampling error).

A fail-safe number (N_fs)⁽Reference Orwin⁵¹⁾ has been calculated to indicate the number of unpublished comparisons with null effects needed to reduce the observed d to a negligible level:

$\begin{eqnarray} N_{fs} = n \frac {\overline{ d } - \overline{ d }_{s}}{\overline{ d }_{s} - \overline{ d }_{fs}}, \end{eqnarray}$

where n is the number of treatment v. control comparisons, $\overline{ d }$ is the weighted mean d of comparisons, $\overline{ d }_{s}$ is the desired minimal mean d and $\overline{ d }_{fs}$ is the mean d of additional comparisons.

Results and discussion

Soyabean meal

Of ninety-nine studies presenting information on the influence of replacement of dietary fish meal by defatted soyabean meal on fish growth, 47 % were found suitable for inclusion in a meta-analysis (Table 1). Absence of a diet without any soyabean meal, which could serve as a true control group for calculation of an effect size, was the single factor resulting in the highest amount (n 18) of rejected studies.

Comparisons of the replacement of fish meal by soyabean meal at different levels without dietary supplementation of amino acids, extracted from different studies and coded as trials, are presented in Table 2⁽Reference Chou, Her and Su¹¹^, Reference Lim, Choi and Wang¹²^, Reference Kikuchi¹⁵^–Reference Romarheim, Skrede and Gao¹⁷^, Reference Wee and Shu²¹^–Reference Boonyaratpalin, Suraneiranat and Tunpibal²⁷^, Reference Shiau, Chuang and Sun²⁹^, Reference Shiau, Kwok and Hwang³⁰^, Reference Davies and Morris³²^, Reference Keembiyehetty and Gatlin³³^, Reference Khan, Jafri and Chadra³⁷^–Reference Ai and Xie³⁹^, Reference Tibaldi, Hakim and Uni⁴¹^, Reference Refstie, Korsoen and Storebakken⁴³^, Reference Hernández, Martínez and Jover⁴⁶^, Reference Robaina, Izquierdo and Moyano⁵²^–Reference Akiyama, Unuma and Yamamoto⁶¹⁾.

Table 2 Highest levels of defatted soyabean meal inclusion and fish meal replacement at which growth obtained did not differ from that with a fish meal control diet (P>0·05), and trials where soyabean meal inclusion could not maintain a similar growth to a fish meal control diet (P<0·05)

C, carnivorous; S, salt water; N, not indicated; WG, weight gain (%); W, warm water ( ≥ 20°C); TWG, total weight gain (g); SGR, specific growth rate (%); CO, cold water ( < 20°C); F, fresh water; O, omnivorous; TGC, thermal growth coefficient.

* Not included in meta-analysis.

A total of 67 % of trials evaluated carnivorous species, with separation according to water type (fresh v. salt) and water temperature (cold v. warm). Only one saltwater omnivorous species (sharpsnout seabream; Diplodus puntazzo)⁽Reference Hernández, Martínez and Jover⁴⁶⁾ has been included, and all omnivorous species had been reared in warm ( ≥ 20°C) water. Evaluation periods varied from 33 to 182 d, although 80 % of trial periods were between 8 and 12 weeks. Dietary crude protein levels, converted, if possible, to dry weight when presented on a wet weight basis, varied from 250 to 612 g/kg. Fish meal replaced included brown, Chilean, menhaden, Norwegian, Peruvian and white sources. However, information on the processing status of soyabean meal evaluated was extremely limited. Available data indicated the ranges of crude protein and lipid of fish meal evaluated as 614–750 and 35–152 g/kg, respectively, with 448–544 and 10–141 g/kg, respectively, reported for soyabean meal. In trials 14 and 15 replacement of fish meal by soyabean meal presented higher (P < 0·05) specific growth rate values than the fish meal control diet. This could probably be related to the quality of the fish meal used⁽Reference Wee and Shu²¹^, Reference Olivia-Teles, Gouveia and Gomes²³⁾.

In the calculation of Hedges' d, referred to as effect size hereafter, at individual replacement levels (Fig. 1), comparisons from trials 1, 5, 15, 16 and 34 (Table 2) were excluded due to the absence of a measurement of dispersion of the means. Although effect size can be calculated from P values if the direction of the finding is known, P values in the above five trials were reported as less or more than a number. Such significance levels are often treated as if they were an exact P value (0·05) if P < 0·05, with effect size set to zero if results are reported as non-significant (P>0·05). However, doing this causes poor estimates⁽Reference DeCoster⁶²⁾, and so was omitted in the present study. An additional trial⁽Reference Krogdahl, Bakke-McKellep and Baeverfjord⁶³⁾, which evaluated inclusion (76, 117, 153, 194, 270 g/kg) of toasted solvent-extracted soyabean meal as replacement (12, 18, 24, 30, 42 %) for low-temperature dried fish meal in diets (958–962 g/kg crude protein) with Atlantic salmon (fish size: 280 g) over a 60 d period, was included in the meta-analysis. Although this trial did not indicate significance levels among individual replacements, it presented a pooled sem. Estimation of an effect size failed in trial 20 due to sd values of 0·0.

Fig. 1 Effect sizes (Hedges' d, as defined in the Data analysis section) for growth with 95 % CI as influenced by level of fish meal replacement by defatted soyabean meal for carnivorous (○; n 52) and omnivorous (●; n 25) fish species.

Limited values and overlapping of 95 % CI demonstrated no gain in separation of species according to feeding habits (Fig. 1). Furthermore, dietary crude protein levels, which could be categorised accordance to feeding habit (carnivorous, 360–612 g/kg; omnivorous, 225–433 g/kg; Table 2) in the present study, were not linearly related to effect size (Fig. 2), as illustrated by a weighted Pearson correlation coefficient (r) of 0·1334 (95 % CI − 0·0934, 0·3471; P = 0·2474). This eliminated the suggestion⁽Reference El-Sayed³⁾ that dietary crude protein level, despite some contradictory results, might have an influence on the effect of replacement of fish meal by soyabean meal.

Fig. 2 Effect sizes (Hedges' d, as defined in the Data analysis section) for growth with 95 % CI when replacing fish meal by defatted soyabean meal as influenced by dietary crude protein levels (n 77).

Figure 1 illustrates that the influence of fish meal replacement level prevented the calculation of a cumulative mean effect size across all levels. In addition, effect sizes did not follow a distinct trend with increasing replacement levels. The absence of a strong linear relationship was displayed by a weighted Pearson r of − 0·4271 (95 % CI − 0·5943, − 0·2246; P = 0·0001). This presented an R ² value of 0·1824, with little of the variation explained by a linear model, and little predictive value.

However, according to their distribution (Fig. 1), effect sizes tended to be grouped into three replacement level categories: 4–40 %, with several mean effect sizes higher than 0 and most 95 % CI overlapping with zero; 42–83 %, with all mean values less than 0 and limited overlapping of 95 % CI with zero; and 100 % with values, although limited (n 5), including extremes. Trials presenting effect sizes that deviated to a large extent from zero in the 4–40 % replacement category included: 37 % fish meal replacement evaluated with hybrid striped bass in trial 7 ( − 4·8717; 95 % CI − 7·6320, − 2·1115), and 40 % replacement with rainbow trout in trial 36 ( − 8·8314; 95 % CI − 14·0782, − 3·5847).

As mentioned above, factors related to ingredients, diet, fish species and rearing might have an influence on the outcome of dietary fish meal replacement by soyabean meal. With information on these sources of variability seldom reported, and all sources of variation most often unidentified, the logic of the analysis in the present study was that effect sizes have been sampled from a distribution of effect sizes with a true effect that could vary from study to study. Therefore a random-effects model was the appropriate model to compute the mean of the effect sizes⁽Reference Borenstein, Hedges and Rothstein⁶⁴⁾. Mean effect sizes for different fish meal replacement categories are presented in Table 3. To be compatible with further comparisons, categories were classified as 4–40, 41–95 and 100 %. This strategy should not be confounded with subgroup analysis, which can be described as an analogue of the ANOVA⁽Reference Lipsey and Wilson⁶⁵⁾, and is used to identify heterogeneity among studies when fitting a fixed-effects model.

Table 3 Mean effect sizes* for fish meal replacement by defatted soyabean meal at different levels

* Hedges' d (as defined in the Data analysis section).

Interpretation of effect sizes is controversial, but the most accepted opinion is that of Cohen⁽Reference Cohen⁶⁶⁾, who proposed values of 0·2, 0·5 and 0·8 to be considered as indicative of small, medium and large standardised effect sizes, respectively, in social sciences. However, biological importance is more objective than practical or clinical importance in which subjective judgements are needed, and biologists should evaluate effect sizes according to their hypotheses⁽Reference Nakagawa and Cuthill⁶⁷⁾. In the present study an effect size was considered as statistically significant from no effect (0) at the the 5 % level (two-tailed) if the the 95 % CI did not overlap with zero⁽Reference Steidl, Thomas, Scheiner and Gurevitch⁶⁸⁾. According to the above, growth obtained with diets in which 4–40 % of fish meal (inclusion levels of 150 to 756 g/kg) was replaced by soyabean meal (inclusion levels of 71 to 366 g/kg) did not differ from growth when feeding a fish meal control diet (Table 3). However, with an upper 95 % CI of − 1·1625, fish meal replacement at 41–95 % caused a cumulative effect size substantially different from zero. The effect size calculated for 100 % fish meal replacement should be treated with caution, as it becomes impossible to estimate the between-trials variance with any precision when sample sizes become limited⁽Reference Borenstein, Hedges and Rothstein⁶⁴⁾.

Due to most studies evaluating the effect of soyabean meal inclusion at several fish meal replacement levels, the occurrence of the tendency to only publish positive results causing publication bias, the so-called ‘file drawer problem’⁽Reference Rosenthal⁶⁹⁾, is unlikely to have had any importance in the present study. However, a N_fs was calculated to estimate the robustness of each cumulative effect size, with $\overline{ d }_{s}$ chosen as − 0·2000 and $\overline{ d }_{fs}$ as 0⁽Reference Rosenberg⁷⁰⁾. With a mean effect size of − 0·1142, calculation of the number of unpublished comparisons with null effects to reduce the observed effect size to − 0·2000 was irrelevant for replacement of fish meal at 4–40 %. However, with replacement of 41–95 % fish meal, 183 additional studies with an effect size of 0 would reduce the mean effect size to − 0·2000. With N_fs considered as strong if greater than 5n+10, with n the original number of studies⁽Reference Rosenthal⁷¹⁾, the above value illustrates the stability of the latter calculated mean effect size. Although seventy-four null effects would be needed to reduce the effect size to − 0·2000 at 100 % fish meal replacement, care should be practised with the interpretation of this calculated mean effect size, as described above.

Supplementation with amino acids

With defatted soyabean meal limiting in total sulfur amino acids when used in animal feeds, diets with high dietary inclusion levels of soyabean meal are often supplemented with methionine and other amino acids⁽Reference Gatlin, Barrows and Brown⁶⁾. Trials that have evaluated this concept are summarised in Table 4⁽Reference Lim, Choi and Wang¹²^, Reference Brown, Twibell and Jonker²⁶^, Reference Shiau, Chuang and Sun²⁹^, Reference Shiau, Kwok and Hwang³⁰^, Reference Davies and Morris³²^, Reference Keembiyehetty and Gatlin³³^, Reference Khan, Jafri and Chadra³⁷^–Reference Ai and Xie³⁹^, Reference Tibaldi, Hakim and Uni⁴¹^, Reference Shiau, Pan and Chen⁴²^, Reference Gallagher⁴⁴^, Reference McGoogan and Gatlin⁴⁵^, Reference Refstie, Førde-Skjærvik and Rosenlund⁷²^–Reference Storebakken, Kvien and Shearer⁷⁸⁾.

Table 4 Highest levels of defatted soyabean meal inclusion and fish meal replacement, with dietary supplementation of methionine, at which growth obtained did not differ from that with a fish meal control diet (P >0·05), and trials where soyabean meal inclusion together with supplemented methionine could not maintain a similar growth to a fish meal control diet (P<0·05)

C, carnivorous; S, salt water; CO, cold water ( < 20°C); SGR, specific growth rate (%); F, fresh water; TWG, total weight gain (g); O, omnivorous; W, warm water ( ≥ 20°C); WG, weight gain (%).

* Fish meal control diet supplemented with 1·2 % dl-methionine.

† Fish meal control diet supplemented with 0·1 % dl-methionine.

‡ Plus l-lysine.

§ Fish meal control diet supplemented with 0·2 % l-methionine.

∥ Not included in meta-analysis.

¶ Plus arginine, histidine, l-lysine, threonine, tryptophan.

In general, methionine supplementation, varying from 0·12 to 2·70 %, has been applied at higher fish meal replacement levels (Table 4) than used when only soyabean meal was included. Five trials (trials 45, 48, 49, 54, 64) evaluated replacements with methionine supplementation together with lower replacement levels without supplementation (Table 2). Few trials included supplementation of lysine (trials 48, 49, 65) and other essential amino acids (trial 65). Methionine was included either in the dl (trials 40, 41, 42, 44, 46, 47, 56, 61, 62, 63) or l form (trials 45, 52, 53, 54, 55, 60, 64, 65), with some studies not reporting the form of methionine.

With the calculation of combined effect sizes, additional studies that did not present statistically significant differences, but supplied data suitable for meta-analysis, were included. Refstie et al. ⁽Reference Refstie, Helland and Storebakken⁷⁹⁾ replaced 68 % of fish meal by soyabean meal (inclusion level: 600 g/kg) in diets (447–467 g/kg crude protein) supplemented with 0·5 % dl-methionine to evaluate growth of 33·5 g rainbow trout over 56 d. Refstie et al. ⁽Reference Refstie, Storebakken and Roem⁸⁰⁾ included 339 g/kg hulled toasted soyabean meal together with 2·30 % dl-methionine to replace 39 % fish meal in diets (388–433 g/kg crude protein) for Atlantic salmon (fish size: 107 g) over a 55 d period The above two studies presented growth parameters over different subperiods of the trial. However, variability associated with the dividing factor removed from standard deviations could be regained to get a pooled standard deviation over the entire period⁽Reference DeCoster⁶²⁾. Venou et al. ⁽Reference Venou, Alexis and Fountoulaki⁸¹⁾ presented data on the replacement (20, 30, 45 %) of fish meal by hulled soyabean meal (before and after extrusion) at inclusion levels ranging from 231–485 g/kg, with dl-methionine supplementation at 0·20–0·30 %. These diets (470 g/kg crude protein) were evaluated with 9 and 50 g gilthead seabream over periods of 60 and 66 d, respectively.

Amino acid supplementation did not substantially change effect sizes in the 0–40 and 100 % fish meal replacement categories, compared with those obtained without supplementation. However, it caused a decrease in the mean effect size and 95 % CI in the 41–95 % group (Table 3). Trial 42, with an evaluation of growth in Atlantic salmon over a 300 d period, presented effect sizes of 1·9352 (95 % CI − 0·4396, 4·3100) and − 6·3832 (95 % CI − 11·2212, − 1·5452) at 18 and 38 % fish meal replacement levels, respectively.

Effect sizes obtained with and without amino acid supplementation in the same study are illustrated in Fig. 3. In trials 49, 56 and 57, with 30, 52 and 75 % fish meal replaced, respectively, methionine supplementation caused overlapping of 95 % CI with zero, compared with no overlapping without supplementation. Although 95 % CI still intersected with zero, methionine supplementation decreased the positive effect size found without supplementation in trial 56 at 39 % fish meal replacement, and to a lesser extent in trial 60 at 33 % replacement.

Fig. 3 Effect sizes (Hedges' d, as defined in the Data analysis section) for growth with 95 % CI when replacing fish meal by defatted soyabean meal for amino acid supplementation (□; n 17) compared with non-supplementation (▒; n 12) evaluated in the same study.

Different supplementation levels of dl-methionine at a constant fish meal replacement level presented similar results with Southern catfish (trial 56). However, supplementation with multiple amino acids resulted in a significantly higher growth than supplementation of only methionine and lysine in rainbow trout (trial 65). In trial 57, Keembiyehetty & Gatlin⁽Reference Keembiyehetty and Gatlin³³⁾ evaluated different forms (l-, dl-, acetyl-, dl-hydroxyl analogues) of methionine at the same fish meal replacement level with sunshine bass, but did not find any significant growth differences among l-, dl- and acetylmethionine, and a fish meal control diet.

The 95 % CI ( − 2·7177, − 0·3164) of the cumulative mean effect size ( − 1·5171) with non-supplementated diets (n 12) of trials indicated in Fig. 3 did not include zero. However, when amino acids were supplemented, the 95 % CI moved to − 1·2308 to 0·0015, with a mean effect size of − 0·6146. It should be stressed that supplemented crystalline amino acids are suggested to be prone to faster uptake and catabolism⁽Reference Cowey and Walton⁸²⁾, and to leaching in aquatic environments⁽Reference Zarate and Lovell⁸³⁾, compared with those in intact protein.

Soya protein concentrate

Trials that replaced dietary fish meal by soya protein concentrate, produced through aqueous ethanol or methanol extraction of defatted soya flakes, with a typical crude protein content of 650–700 g/kg⁽Reference Lusas and Riaz⁸⁴⁾, are presented in Table 5⁽Reference Rumsey, Siwicki and Anderson²⁴^, Reference Nengas, Alexis and Davies²⁵^, Reference Kaushik, Cravedi and Lalles³¹^, Reference Médale, Boujard and Vallée³⁴^–Reference Day and Plascencia González³⁶^, Reference Deng, Mai and Ai⁴⁰^, Reference Kissil, Lupatsch and Higgs⁸⁵^–Reference Stickney, Hardy and Koch⁸⁹⁾. However, crude protein content of the product used in trial 74⁽Reference Stuart and Hung⁸⁶⁾ was indicated as approximately 900 g/kg. Soya protein concentrate has been evaluated with only seven fish species, of which two (Atlantic halibut, white sturgeon) were omnivorous, and twenty-nine from thirty-six comparisons used it to replace ≥ 50 % of fish meal.

Table 5 Highest levels of soya protein concentrate (SPC) inclusion and fish meal replacement, with and without dietary supplementation of methionine, at which growth obtained did not differ from that with a fish meal control diet (P>0·05), and trials where soya protein concentrate could not maintain a similar growth than a fish meal control diet (P<0·05)

C, carnivorous; F, fresh water; CO, cold water ( < 20°C); DGC, daily growth coefficient; N, not indicated; SGR, specific growth rate (%); S, salt water; W, warm water ( ≥ 20°C); TWG, total weight gain (g); O, omnivorous; WG, weight gain (%).

* Not included in meta-analysis.

† Plus l-lysine and l-threonine.

‡ Plus mixture of l-leucine, l-lysine, dl-methionine, l-threonine, l-valine as crystalline amino acids.

§ Plus mixture of l-leucine, l-lysine, dl-methionine, l-threonine, l-valine as cellulose acetate-encapsulated amino acids.

∥ Supplemented with 0·22 % dl-methionine.

¶ Supplemented with 0·42 % dl-methionine.

Replacement of fish meal by soya protein concentrate caused a significant growth decrease in most trials. However, its value as a fish meal substitute was substantially increased when supplemented with amino acids (Table 5). Deng et al. ⁽Reference Deng, Mai and Ai⁴⁰⁾ evaluated a mixture of amino acids, included as either a crystalline amino acid mixture (trial 80) or encapsulated by cellulose acetate phthalate (trial 81), at a similar fish meal replacement level, but did not find any significant differences in the growth of Japanese flounder between treatments. Methionine supplementation at 100 % fish meal replacement decreased (P < 0·05) growth compared with a fish meal control diet in rainbow trout (trials 82, 83, 84). However, at lower replacement levels in the latter studies soya protein concentrate without amino acid supplementation resulted in similar growth between diets (trials 67, 68).

The absence of a measurement of variance eliminated trials 66, 67, 77, 78 and 82 (Table 5) from the calculation of effect sizes (Fig. 4). An additional trial⁽Reference Storebakken, Shearer and Roem⁹⁰⁾, which indicated statistical significance for differences in specific growth rate of Atlantic salmon (fish size: 106–111 g) over different phases of a 84 d period, was included in the calculation of effect sizes. In the latter study soya protein concentrate (inclusion level: 480 g/kg) replaced 75 % of low temperature dried fish meal in diets with crude protein levels of 430–457 g/kg.

Fig. 4 Effect sizes (Hedges' d, as defined in the Data analysis section) for growth with 95 % CI as influenced by level of fish meal replacement by soya protein concentrate without (○; n 16) and with (●; n 10) amino acid supplementation.

Limited values and non-significant weighted Pearson r's between effect sizes and replacement levels found without (r − 0·1055; 95 % CI − 0·5714, 0·4118; P = 0·6973; n 16) and with (r − 0·4541; 95 % CI − 0·8428, 0·2459; P = 0·1874; n 10) amino acid supplementation eliminated any further evaluation of relationships. Cumulative mean effect sizes did not differ substantially between trials without ( − 2·7306; 95 % CI − 3·7991, − 1·6620) and with ( − 2·4373; 95 % CI − 3·9004, − 0·9742) amino acid supplementation, and 95 % CI did not overlap with zero in either.

The evaluation of effect sizes obtained with fish meal replacement by other soyabean products, for example, full-fat soyabeans and soya flour, was prevented by a lack of studies presenting appropriate values, as illustrated in Table 1.

Conclusions

The present study quantified the magnitude and precision of the effect caused by the replacement of dietary fish meal by soyabean products on fish growth. The absence of standardisation in units for measurement of growth in fish resulted in the application of Glassian meta-analysis, based on standardised effect sizes calculated between a control (fish meal) and treatment (fish meal replacement) diet. An important contribution from the study could be ascribed to the identification of deficiencies in reporting of results. Failure to report a measurement of variation, as found with numerous studies evaluated for inclusion, rendered results unsuitable for meta-analysis. Standardising in experimental protocol regarding, among others, replacement levels, evaluation period, measurement units and reporting of variance, are of utmost importance for evaluation of trends with information supplied by different studies.

Data used in the current study presented evidence that the effect of the replacement of fish meal by defatted soyabean meal did not display a definite trend with replacement level. However, replacement of up to 40 % fish meal caused similar growth to that obtained with diets based solely on fish meal as a protein source, irrespective of dietary protein content, in a wide range of fish species. Amino acid supplementation of diets, mostly as crystalline methionine, aided in decreasing the negative effect caused by the replacement of fish meal at levels higher than 40 %. Despite the fact that the above has been indicated by narrative reviews, it was based on summative results obtained with null hypothesis significance testing in individual studies. With limited replicates, as often is encountered in fish nutrition studies, the latter testing technique has low statistical power to detect differences, and gives no indication of the size of differences. The present study is the first to put numerical values to the above differences, and to indicate the direction of effects as obtained across studies.

Evaluation of the influence of fish species, and the influence of stratification of fish species according to feeding habit, water type and water temperature on growth differences due to the replacement of fish meal by soyabean products, are hampered by a lack of suitable values for analysis. A similar lack of values prevented searching of trends at replacement levels higher than 40 %. Further research in order to provide results suitable for meta-analysis is urgently needed.

Baseline values are presented in the currrent study for the magnitude of effect sizes due to replacement of fish meal with soya products, which could be utilised not only in further meta-analyses, but also for comparative purposes in research on individual fish species. Furthermore, the present study illustrates the use of Glassian-based meta-analytic techniques to quantify responses in studies on fish nutrition.

Acknowledgements

The present study was financially supported, including the salary of J. S., by research plan no. MSM 6007665809 of the University of South Bohemia Ceske Budejovice, Research Institute of Fish Culture and Hydrobiology (Vodnany, Czech Republic). It received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.

J. S. was the only contributor to all (research, analysis, writing, etc) of the paper.

There are no conflicts of interest involved in this paper.

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