## Maternal age

Maternal age has a strong influence on broiler productivity. Effects of maternal nutrition tend to be amplified in progeny from young breeders.

## Timing of maternal nutrition

The amount of time prior to egg and chick production that a diet or nutritional management is applied has significant influence on the outcome of many studies. Factorial arrangements of maternal nutrition treatments, including diet changes from the rearing to laying phases will help to identify epigenetic effects.

## Genetic factors

The major components of hatching eggs (yolk, albumen and shell) vary in a predictable manner according to age, body composition, and maternal nutrition (Nonis and Gous, 2013), but there are strain- (Johnston and Gous, 2007) and likely hen-specific differences in egg composition that can and should be accounted for. Pedigree information should be used to account for genetic variation in broiler performance. This will allow for more precise estimation of the actual effects of maternal nutrition treatments on progeny performance.

Romero et al. (2009) characterized the efficiency of hens in terms of residual feed intake (RFI) and residual maintenance requirement ($RME_m$). $RME_m$ was particularly useful for explaining variation in egg and chick weights. Efficient hens (with low $RME_m$) partitioned more nutrients toward reproduction than inefficient hens (with high $RME_m$). Broilers from RFI-efficient hens grew at a higher rate from 21 to 28 days, and of age, and had a higher 28- and 38-day BW. Broilers from $RME_m$-efficient hens grew at a lower rate than less $RME_m$-efficient hens. In fact, the broilers with the highest BW originated from RFI-efficient and $RME_m$-inefficient hens. Breast meat yield in broilers from $RME_m$-efficient hens was lower, whereas no meaningful relationship between RFI and breast muscle yield was detected.

## Maternal body weight variation

Body weight differences due to unequal feed distribution is a growing challenge in interpreting the complex effects of maternal nutrition on progeny performance. A more strategic approach to maternal nutrition research must start with rigid BW control and high breeder flock uniformity, achieved through better control of feed distribution. Precision feeding offers promise as a research tool to manage feed intake according to individual birds according to their body weight. Combined with adequate micronutrient supplementation, consistent hatching and brooding management, and better accounting for heritable maternal and paternal contributions to broiler growth, a more clear and consistent pattern of the effects of maternal nutrition on progeny performance will be possible.

## Conclusion

The data currently available on the impact of maternal dietary ME and CP levels does not paint a simple picture of how to use maternal nutrition to optimize broiler performance and yield. More strategic experimental design, expert breeder management, control of ancillary sources of variation, and evolution of our understanding of epigenetics and nutritional programming will add resolution to our understanding of this difficult subject.

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# NUTRITIONAL SOLUTIONS TO IMPROVE BROILER UNIFORMITY

**R. M. Gous**

University of KwaZulu-Natal, Pietermaritzburg, South Africa; gous@ukzn.ac.za

## Summary

Poor uniformity in a broiler operation reduces revenue and increases waste. Uniformity in body weight at harvest is influenced by variation in genotype, environment and feed composition and form. Variation in broilers within a sex and growing at their potential is relatively small but increases markedly when a poor quality feed is given. In attempting to grow at their potential on a feed low in protein, birds will need to overconsume energy and release excessive amounts of heat to the environment and this ability will be constrained by both feather cover and the ability to faten. Consequently, as broiler genotypes have become faster growing and leaner there is an increased need to feed higher levels of balanced protein in a cooler environment as a means of improving uniformity. Separating the sexes and reducing the range in day-old body weights will assist in achieving a greater uniformity at harvest.

## Introduction

Uniformity is an important measure of performance when optimising the feed and feeding programme of a population of broilers as it relates to the spread of product yield in the processing plant. Poor uniformity reduces revenue and increases waste so broiler producers need to take account of any factors that may influence this. The potential performance of a broiler population depends largely on the inherent genotype of the population and the extent to which this varies between individuals (EMMANS & FISHER, 1986), but many factors conspire to constrain this potential performance resulting in a wider spread of body weights at harvest than would be the case if all birds grew at their potential (GOUS & BERHE, 2006).

The theory of food intake proposed by EMMANS (1981) suggests that a bird will attempt to consume sufficient of a given food to enable it to grow at its potential, thus over-consuming energy if the feed is marginally deficient in an essential nutrient such as an amino acid. It is apparent that strains of broilers and individuals within a strain over-consume energy to different extents when faced with a marginally deficient feed (GOUS et al., 1990; CORZO et al., 2004; KEMP et al., 2005; BERHE & GOUS, 2008). It is likely therefore that such feeds will reduce uniformity, as some birds will be capable of consuming more than others and would thus benefit from the extra feed intake.

But it is not only the variation between individuals in their response to a given feed or environment that contributes to the variation in the response of a population of birds to a feeding programme in a given environment. Variation also exists in the environmental conditions to which the birds are subjected, as well as the composition of the feed used. Each of these sources of variation will be addressed in the following review, but emphasis will be placed on the genotype x environment interactions that result from the feeding of marginally deficient feeds.

## Genetic variation

Individuals within a population of broilers vary in many respects, the most important in this context being their potential rates of body and feather protein growth (more specifically their rates of maturing, B), their mature body and feather protein weights (Pm) and their ability to deposit lipid when faced with a nutrient deficiency. EMMANS & FISHER (1986) have given estimates of the variation of these parameters within a population, coefficients of variation (CV) being 0.06 – 0.10 for Pm, 0.02 for the scaled rate parameter B* (=BPm<sup>0.27</sup>), and 0.04 for the rate of lipid deposition (LDR). Differences between males and females in these genetic parameters are considerably greater than the CV’s given above, the mean Pm in females being between 0.7 and 0.8 of that of males, the rates of maturing of body and feather protein of females being 0.95 – 0.98 and 1.04 – 1.06 of the male values respectively. The lipid to protein ratio in females is between 1.6 and 2.0 times that of males (HANCOCK et al., 1995; GOUS et al., 1996; 1999).

Most quantitative biological traits of commercial importance are described by a normal distribution, this being the basis on which genetic selection is made. However, the full expression of these traits is possible only if the environment (including, in this case, the feed offered) is not limiting. In practice the expression of genetic potential in the highest producers is often constrained, and the smallest birds are often culled, thereby limiting the range (CURNOW & TORENBEEK, 2007) and changing the shape of the distribution. This might result in a distribution that is positively or negatively skewed depending on the constraints applied. The trait having the greatest effect in altering the distribution of weights at harvesting is the rate of feathering (FR).
In a sensitivity analysis of the effects of variation in each of the above traits, as well as the initial body weight ($W_0$), which is not a genetic parameter, on the performance of broilers, GOUS & BERHE (2006) found that food intake, and hence body weight gain, increased almost linearly with $B^*, P_m$ and LDR. However, the effect of FR was non-linear, with higher rates of feather growth causing an increased depression of food intake and body growth which was more pronounced in females than in males, and more severe among males fed a low lysine feed in the starter period than those fed the high lysine feed. This genotype x environment interaction would therefore be a particularly important source of variation in fast-growing strains of broiler kept in hot conditions and fed poor quality food (Fig. 1).

<figure><img src="image_14.png" /><figcaption>**Figure 1.** The relative effect on simulated food intake in male and female broilers fed a lysine-limiting feed containing 9 (A, C) or 16g lysine/kg (B, D) from 7 to 21d when the means of each of five genetic parameters were increased or decreased by 0.05, 0.1, 0.15 or 0.20 whilst holding the five remaining genetic parameters constant (B = .-▼-.; FR = ..-o..-.; LPRm = ..■..; $P_m$ = __□__; and $W_0$ = __▽__/) (from GOUS & BERHE, 2006)</figcaption></figure>

## Variation in the environment within a broiler house

Controlling the physical microenvironment in a broiler house is an important element in optimising the production process (REECE & LOTT, 1982; MITCHELL, 1985; PARMAR *et al.*, 1992; AERTS *et al.*, 2000). However, depending on the system used for such control, variation in the environment within a poultry building may be considerable, impacting significantly on the performance of broilers housed in different areas of the house. Many factors contribute to this variation such as unadjusted inlet openings, unsealed cracks, dirty fan shutters, loose curtains, the amount of time the fans run, the total length of the timer cycle and the position of thermo-sensors (AL HOMIDAN *et al.*, 1997; 1998). The behaviour of the broilers themselves will also cause variations in temperature along the length of the house as a result of mass migrations and clustering in some areas (WATHES & CLARK, 1981) which will affect thermoregulation. Such variation in the environment is likely to be positively correlated with the variation in the weight of the end product of the production process, raising the question whether the optimum feeds or feeding programme should be adjusted to take account of this variation.

The vertical temperature profile in a poultry house is affected by many factors, including heat generated by heaters, the flock and solar radiation, microbial fermentation in the litter, heat fluxes between poultry house air and the soil, walls and roofs due to temperature gradients, moisture loss from the litter and natural convection around broilers (VAN BEEK & BEEKING, 1995; BOSHOUWERS *et al.*, 1996). However, of greater importance in a tunnel-ventilated house is the variation that exists in the horizontal temperature profile at bird level. Winter and summer conditions alter this profile, with differences in temperature along the length of the house being considerably greater in winter than in summer. In winter, chicks often migrate towards the air inlets, thereby increasing the stocking density in that area, and
the temperature differential in the early stages of growth can be as high as 7 - 9°C (XIN *et al.*, 1994) and remains at least 3.5°C cooler at the far end, with 7% higher relative humidity, by the end of the production cycle. In summer, because of the higher ventilation rates used, XIN *et al.* (1994) found little difference in temperature at either end of the house. Many factors interact to influence this gradient, so it would be expected that the temperature and humidity gradient would differ markedly between houses and between seasons.

Poor air quality, due to environmental contaminants such as carbon monoxide, carbon dioxide, ammonia and dust, reduces performance, increases the potential for respiratory disease and may increase mortality (WEAVER & MEIJERHOF, 1991). Conditions at the exhaust end of a tunnel-ventilated broiler house may be far more hostile than at the inlet end, especially in winter, resulting in considerable variation in the performance of the flock.

Because of the range of body weights and potential growth rates in a broiler house at any one time there may be some advantage in providing a range of temperatures in the house so that the fastest growers can move to a cooler area where their potential is more likely to be achieved. However, at high stocking rates it may be impossible for the necessary migration of birds to take place.

The effects of variation in temperature, humidity and air quality in the broiler house on the range of body weights present in the house at the end of the production cycle cannot be estimated empirically because of the expected interactions between these environmental factors and potential body protein growth rate, feathering rate and the chemical and physical composition of the feed, all of which are expected to vary also.

## Variation in the nutrient content of the feed

Variation in the nutrient content of feeds offered to broilers in a commercial operation is due mainly to three sources: variation in ingredient composition, mixer inefficiency (including weighing errors), and separation after mixing and during transportation.

Sources of variation in the physical and chemical characteristics of grains used in poultry feeds include variety, seasonal effects, growth sites (METAYER *et al.*, 1993), crop treatment and grain fumigants, post-harvest storage conditions and period of storage and processing (DALE, 1996; HUGHES & CHOCT, 1999), rainfall and environmental temperature patterns during the period of grain maturation, genetic effects, level of fertilizer usage (METAYER *et al.*, 1993; HUGHES & CHOCT, 1999) and inclusion rate (SENKOYLU & DALE, 1999). This type of variation should not be dealt with in the formulation process through the use of a margin of safety as suggested by NOTT & COMBS (1967) but through non-linear stochastic programming (ROUSH *et al.*, 1996), but the consequences of variation introduced in this way, and through mixer inefficiency, must be modelled differently from the variation brought about through separation, which is intuitively less random than the first two types of variation.

Performance is adversely affected when variation in nutrient content in feeds is increased (DUNCAN, 1989; MCCOY *et al.*, 1994). Some of the more sophisticated feed formulation programs used in the feed industry, which attempt to account for variation in nutrient content in the ingredients used in the feed, generally favour the use of ingredients that exhibit the least amount of variation, thereby potentially reducing the variation in performance of the broilers being fed such feeds. However, whereas natural variation in the composition of a feed has zero cost, a considerable cost is incurred when attempting to reduce variation, as these non-linear programs demonstrate, so there is an economic limit to the extent to which a reduction in variation in nutrient content should be attempted.

FAWCETT *et al.* (1992) attempted to determine this limit by predicting the response of broilers, in margin/m², to a range of dietary lysine and ME contents with the use of the 'Poultry Growth Model' of EMMANS (1981), and then integrating the bivariate probability distribution for different degrees of variation in nutrient content over the response surface to determine the value of reducing the variance in the feed. This approach, although interesting, does not simulate the day-to-day variation in feed nutrient content to which broilers are subjected in practice, where nutrient composition varies continuously throughout the rearing period. A more useful technique would be to predict the response of each bird in the population to random variations in feed quality on each day of the growing period, thereby obtaining a more realistic assessment of the effect of variation in feed quality. This would require a stochastic approach to the definition of the composition of the feed offered to the broilers, as well as to the broilers themselves.

Such an approach is a useful tool for determining the upper limit to the value of variance reduction, but does not address the issue of further systematic variation in nutrient content brought about by separation during road, rail, auger, blower or chain transportation. Such variation tends to separate the fine from the coarse particles, particularly when the feed is conveyed in a mash form, or when the quality of pellets is poor, resulting in a high proportion of fines.
This problem does not appear to be addressed in the literature, so the variation introduced in this way is unknown, but could be considerable. This variation is likely to be systematic, in that separation would take place along the length of the feeder lines, with fines being left behind as the coarser particles move to the end of the line. If the fines consisted predominantly of major and minor minerals and vitamins, bone development could be seen to worsen at the far end of a broiler house compared with the end at which the feed is introduced. The effect of such nutrient separation could be modelled in the same way as are the systematic changes that take place in the environment within a broiler house, the birds along the length of the house being subjected to changes in temperature, humidity and air quality. But it is not only the chemical separation of the food that takes place that influences performance along the length of a broiler house; the physical nature of the feed may also be affected.

Pelleted feeds are known to improve feed conversion efficiency when compared with mash feeds (JENSEN et al., 1962), this being due to the shorter period of time spent by the broilers consuming pellets, resulting in lower energy expenditure. The physical nature of the feed therefore has an effect on performance and, because of the abrasive nature of some feeding equipment used in broiler houses, the amount of time spent eating, and hence the energy expended in eating, may well increase as the distance of the feed trough from the hopper increases.

## Nutritional interventions

As the potential growth rate of broilers has been increased by genetic selection, so the daily amino acid and energy requirements of the bird have also been increased, but these do not increase in the same proportion: the requirement for amino acids increases proportionately faster than does the energy requirement, thus a higher amino acid to energy ratio is required in faster growing strains of broiler. Many nutritionists believe, incorrectly, that broilers will simply increase their intake of an inadequate feed in order to obtain sufficient of the limiting nutrients. Whereas broilers may attempt to do so, it is seldom that they achieve the intake required to enable them to grow at their potential. This is well illustrated by the results of an experiment by MORRIS & NJURU (1990) who fed diets of increasing protein content to broilers and to laying-type cockerels. The maximum gain in weight and in protein content in the laying-type chickens was achieved on diets with considerably lower protein contents than was needed to maximise the gain in the broilers (Table 1). Even on marginally deficient protein levels the broilers were unable to consume sufficient to grow at their potential. The inability to consume sufficient of a marginally deficient feed would be more pronounced with the broiler genotypes available at present, these having been subjected to a further 25 years of selection for feed efficiency since the above publication, which would have further reduced the ability of broilers to fatten (PYM & SOLVYNS, 1979).

<table><caption>**Table 1.** Liveweight, food intake, feed conversion efficiency (FCE) and protein content of broiler and layer-type chickens at 21 d of age (after MORRIS & NJURU, 1990)</caption><thead><tr><th>Crude protein<br>in diet<br>g/kg</th><th>Liveweight<br>g</th><th>Food<br>intake<br>g/chick</th><th>FCE<br>g gain/<br>kg food</th><th>Protein<br>content<br>g/chick</th></tr></thead><tbody><tr><td colspan="5"><strong>Broiler chickens</strong></td></tr><tr><td>167</td><td>414</td><td>938</td><td>400</td><td>53</td></tr><tr><td>188</td><td>618</td><td>1193</td><td>486</td><td>85</td></tr><tr><td>209</td><td>706</td><td>1183</td><td>564</td><td>100</td></tr><tr><td>230</td><td>786</td><td>1230</td><td>607</td><td>114</td></tr><tr><td>251</td><td>836</td><td>1320</td><td>603</td><td>123</td></tr><tr><td colspan="5"><strong>Layer chickens</strong></td></tr><tr><td>167</td><td>235</td><td>683</td><td>293</td><td>35</td></tr><tr><td>188</td><td>290</td><td>702</td><td>362</td><td>45</td></tr><tr><td>209</td><td>295</td><td>711</td><td>366</td><td>46</td></tr><tr><td>230</td><td>291</td><td>650</td><td>394</td><td>46</td></tr><tr><td>251</td><td>299</td><td>689</td><td>384</td><td>47</td></tr></tbody></table>

There is strong evidence that uniformity is increased by feeding higher levels of a limiting amino acid or protein (DUNCAN, 1984; LEMME, 2003; BERHE & GOUS, 2008). This is illustrated by the data in Table 2 where the coefficient of variation (CV %) in liveweight at 42 d was reduced by 40 % and breast meat yield by 47 % through the supplementation of DL Methionine to a basal feed (LEMME, 2003). Supplemental vitamins too have been reported to improve uniformity in a broiler flock. MCNAUGHTON (1995) reported continuing economic responses in several characteristics up
to the highest level of vitamins tested. There was little convincing evidence in his trial that the response to vitamin level depended on the level of stress applied, as performance improved with increasing vitamin doses even when no stress was applied.

<table><caption>**Table 2** The effect of graded levels of DL-Methionine on liveweight and breast meat yield in broilers (1 – 42 d) (after LEMME, 2003)</caption><thead><tr><th></th><th colspan="4">DL-Methionine supplementation (g/kg)</th></tr><tr><th></th><th>0</th><th>0.4</th><th>0.8</th><th>1.2</th></tr></thead><tbody><tr><td>Liveweight (d 42) g</td><td>1831</td><td>2452</td><td>2646</td><td>2836</td></tr><tr><td>CV %</td><td>16.8</td><td>11.1</td><td>9.5</td><td>6.7</td></tr><tr><td>Breast meat (d 42) g</td><td>362</td><td>543</td><td>630</td><td>707</td></tr><tr><td>CV%</td><td>18.5</td><td>14.3</td><td>11.7</td><td>7.8</td></tr><tr><td>Breast as % of live weight</td><td>19.8</td><td>22.1</td><td>23.8</td><td>24.9</td></tr></tbody></table>

The reason for the improved uniformity is that the requirements of a greater proportion of the population will be met as the concentration of the limiting feed resource is increased. FISHER *et al.* (1973) showed that the response of an individual (laying hen) to an increasing supply of an amino acid differs markedly from that of the population from which the individual is drawn. Whereas the response of each hen can be assumed to be linear, up to a point where output plateaus (the genetic potential), the population response is a continuous, asymptotic curve with no abrupt threshold. This population response curve, the mean response of a group of individuals at a time, is the result of the variation that exists in both body weight (maintenance requirement) and the potential egg output of the population. This so-called Reading Model (FISHER *et al.*, 1973) may be used to determine the optimum economic intake of the limiting amino acid for a flock of hens. The increased egg output of those birds with above-average requirements for maintenance and above-average maximum potential egg outputs justifies the cost of increasing the amino acid intake by all birds.

In a population of growing broilers, as with laying hens, at any point in time body weights and potential outputs (growth rates) will be normally distributed about a mean value, but in addition to this, because each bird is growing and food intake is increasing, variation in growth rate within each animal over time also needs to be considered (GOUS & MORRIS, 1985). This is not as critical in the case of laying hens as these birds are in a relatively steady state over time. To understand these interactions a mechanistic model that accurately simulates food intake and growth of an individual broiler over time is useful.

Such a model, based on the theory of food intake and growth of EMMANS (1987) has been developed (EFG SOFTWARE, 2015). This simulates the growth of a single bird, taking account of genetic parameters, diet composition and feeding programme, the environment, stocking density and other factors that may affect the outcome of production decisions in practice. The model works by calculating the desired amount of a given food the bird needs to consume each day to grow at its potential, and will predict the consequences in food intake, growth and carcass composition if this intake is constrained by feed bulk or an environment that is too hot to allow the bird to lose sufficient heat to that environment.

As mentioned above, male and female broilers have different growth characteristics which will impact on the way in which they should be fed and housed during growth. Because males have the potential to grow faster, and to a larger size, than females their amino acid requirements for potential growth would be expected to be higher. When their lysine requirements for maintenance and potential body and feather protein growth are calculated and converted to a feed concentration, these are similar for males and females at day-old, but as the growing period progresses male broilers require considerably more lysine than females, the difference increasing throughout the growing period (Fig. 2).
<figure><img src="image_15.png" /><figcaption>**Figure 2.** Feed content of lysine (g/kg) required to enable male (dashed line) and female (dotted line) broilers to grow at their potential at a feed energy content of 13 MJ ME/kg, simulated using the EFG broiler growth model (EFG SOFT-WARE, 2015)</figcaption></figure>

By growing males and females together the feed composition used is clearly a compromise between that required by each sex. Feeding a fixed protein content during each of the phases of growth is likely to result in male broilers being under-fed amino acids for long periods whereas the opposite would be the case for females. Under certain circumstances birds are capable of partially overcoming the effect of being underfed protein: to do so they would need to be capable of over-consuming energy, and they would need to be housed in cool conditions. The genetic parameter referred to above, which controls the maximum rate of lipid deposition in the short run, reflects the ability of the genotype to over-consume energy and fatten when presented with a feed in which one or more amino acids or other nutrients are marginally limiting.

Birds with a low propensity to fatten, such as turkeys, would be disadvantaged when presented with a marginally limiting feed, as they would be unable to store the excess energy as body lipid, the resultant food intake therefore being lower than desired and weight gain being below the potential. Modern broiler strains are becoming leaner through selection so they are becoming less capable of overcoming marginal dietary deficiencies than were broiler genotypes of the past, and this would explain why uniformity is increased when higher protein and vitamin levels are included in the feed.

The ability to lose heat to the environment is another factor influencing the ability of birds to overcome nutrient deficiencies. For a broiler to be able to grow at its potential it needs to be able to lose all the heat that is produced in growing at that potential, including the heat generated by maintaining itself, in growing and in digesting the feed. Clearly, the density of feather cover will play a major role in determining the extent to which heat can be lost to the environment. Feather growth differs markedly between genotypes and sexes, especially in feather-sexable strains and this variation will impact severely on food intake and hence body weight at harvesting, especially on marginally to severely deficient feeds.

Initial (day-old) body weight has an impact on final body weight, the response being almost linear, as illustrated in Fig. 1. In a simulation exercise using the EFG Broiler Growth Model, for initial body weights varying from 35 to 60 g the simulated 42-d body weights ranged from 3099 to 3373 g, a range of 274 g. This is without taking account of social stresses and difficulties experienced by smaller chicks in reaching the feeders and drinkers, which would have the effect of increasing even further the variation in final weight. Although NETO *et al*. (2013) found no improvement in uniformity at 42 d when grouping day-old chicks according to weight and rearing them in these groups, SINGH & NAGRA (2006) reported that the largest chicks at day-old retained this advantage by 35 d in both male and female broilers. Because broiler chicks of the same genotype have the same potential to grow irrespective of day-old bodyweight, smaller chicks at day-old would benefit from higher dietary protein levels as their ability to consume food is constrained by gut capacity. Broiler producers should strive to reduce the range of day-old chick weights if the objective is to improve uniformity in the end-product.
## Conclusions

The spread of product yield in the processing plant is influenced by variation in genotype, environment and feed composition and form. To increase uniformity through nutrition, broiler producers should consider rearing sexes separately, feeding high levels of balanced protein and vitamins, reducing the environmental temperature in the broiler house, minimising the range of day-old body weights, and using good quality pellets.

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# NUTRITIONAL REQUIREMENTS AND FEEDING MANAGEMENT OF MEAT TYPE DUCKS

E. Baéza

INRA, UR 83 Recherches Avicoles, F-37380 Nouzilly, France; baeza@tours.inra.fr

The introduction presents the main countries producing duck meat and the different species and rearing systems used in production. The review is then divided into four parts. The first three parts describe successively the requirements of meat type ducks only for energy, protein and amino acids and minerals, vitamins and trace-elements. The last part presents recommendations regarding feeding management (feed presentation, feed restriction, use of enzymes and feedstuffs, fatty acid composition of diets). In the world, the main ducks dedicated to meat production are Pekin, Muscovy and mule ducks. As, the growth rate, the growing performance and the body composition of these different genotypes are different, the specificities of each type of duck are indicated in each part. The review is only focussed on ducks reared under intensive production system.

**Keywords:** nutritional requirements, growing ducks, energy, proteins, amino acids, minerals

## Introduction

From 1993 to 2012, the world duck production largely increased, and meat production rose from 1.72 to 4.34 million tons (Deman, 2014). Asia is the leading production region and this is the area where the industry is expanding most rapidly. Asia accounted for 76 and 83% of duck meat output in 1993 and 2012, respectively (FAO statistics, 2014). In Asia, China's contribution (3 millions of tons) represents 86% of the total region. The next largest producers are Malaysia (128,100 tons), Myanmar (105,200 tons), Vietnam (105,000 tons), Thailand (82,000 tons), the Republic of Korea (68,900 tons) and Taïwan (67,700 tons). Europe represents the second high production region. Annual production grew from 262,736 in 1993 to 480,000 tons in 2013, France being the leading producer with 239,000 tons. Next came Hungary (77,000 tons) followed by Germany with just over 53,000 tons and the UK (30,000 tons). Production in North and Central America is dominated by the USA (54,000 tons in 2012) followed by Mexico (21,000 tons) and Canada (7,600 tons). In Africa, the industry is primarily centred on Egypt and Madagascar, producing 63,300 and 12,000 tons of duck meat, respectively. Less than 4% of duck meat production is exported. In 2011, the main exporters were China (42,616 tons), Hungary (23,670), Germany (20,129 tons) and Netherlands (17,511 tons) and the main importers in Asia and Europe were Japan (4,865 tons in 2011) and Germany (16,232 tons).

The main species used to produce duck meat are Pekin, Muscovy (mostly in France) and mule ducks (hybrid resulting from the cross between males Muscovy duck, Cairina moschata and females Pekin, Anas platyrhynchos, mostly in France for the production of fatty liver and Taïwan). Other duck species such as Jinding and Shao ducks in China, Tsaiya ducks in Taïwan, Khaki Campbell, Indian runner and Desi ducks in India, Vietnam, Cambodia and Indonesia are used mainly for egg production and meat is a by-product (Pingel, 2004).

Different production systems are used in the world. In developed countries, ducks are mainly reared intensively in total-confinement housing or with access to pasture (free-range, organic or "label rouge" systems, mule ducks reared for fatty liver production) and sometimes to water for swimming. In Asia, extensive systems such as fish-duck farming are largely used, ducks being housed above fishponds (Prinsloo et al., 1999; Syed, 2002). To decrease feed costs, ducks can also be reared in rice fields (Men et al., 2002a; 2002b).

As for other poultry species, the industry developed cut and processed duck products. The meat yield of ducks has therefore increased and carcass fatness has decreased owing to genetic selection and to improvements in duck management, particularly in nutrition. This review presents the requirements of meat type ducks only for energy, protein and amino acids and minerals, vitamins and trace-elements. It presents also recommendations regarding feeding management. As, the growth rate, the growing performance and the body composition of Pekin, Muscovy and mule ducks are different, the specificities of each genotype are indicated in each part. The review is only focussed on ducks reared under intensive production system.
## Energy

According to Leclercq (1990), the duck energy requirement in the conditions of thermal neutrality (25°C) can be estimated thanks to the following equation:

$$E = 105 BW^{0.75} + 14 Prot + 11 Lip$$

E is the daily energy requirement (kcal), BW = Body Weight (kg), Prot = amount of daily stored proteins, Lip = amount of daily stored lipids

The duck is able to regulate the amount of ingested energy. It is therefore nonresponsive in the variations of dietary energy level. The growth will be the same with high (3,000 kcal ME/kg) or low (2,500 kcal ME/kg) dietary energy levels but feed consumption and feed conversion ratio will be higher with low dietary energy level than with high dietary level. According to Scott and Dean (1991), the Pekin duck is able to regulate the amount of ingested energy when energy dietary level is comprised between 2,300 and 3,100 kcal ME/kg. For the Muscovy duck, the range of energy level variation is comprised between 2,500 and 3,000 kcal/kg (Leclercq, 1990).

Duck diets are usually formulated using ME values obtained from chickens even if a few studies showed differences between both species for some feedstuffs (for a review, see Elkin, 1987). For Pekin duck, Adeola (2006) recommended diets containing 2825-2875 kcal ME/kg for the starting period (0-2 weeks of age) and 3050-3075 kcal ME/kg for the growing period (2-6 weeks of age). The NRC (1994) recommendations are 2,900 and 3,000 kcal ME/kg for the starting and growing periods, respectively. For Muscovy duck, dietary energy levels are usually comprised between 2800 and 3000 kcal ME/kg (INRA, 1989).

Fan et al. (2008) analysed the effects of dietary energy on growth performance and carcass composition of growing Pekin ducks from 2 to six weeks of age. The dietary energy level varied between 2,600 and 3,100 kcal/kg whereas the crude protein, methionine, cystine and lysine contents were similar for all diets (180, 4.0, 3.2 and 9.0 g/kg, respectively). This study showed that the apparent metabolisable energy (AME) requirements for optimal weight gain and feed: gain ratio were 3,008 and 3,030 kcal/kg, respectively. The dietary energy level had no effect on carcass composition except the proportion of abdominal fat which was lower with diets providing 2,600 and 2,700 kcal/kg by comparison with the other diets.

Xie et al. (2010) determined the AME requirement of Pekin ducklings from hatch to 3 weeks of age. The dietary energy level varied between 2,454 and 3,050 kcal/kg whereas the crude protein, methionine, cystine, lysine, threonine and tryptophan contents were similar for all diets (205, 5.2, 3.5, 11.0, 7.8 and 2.4 g/kg, respectively). This study showed that the AME requirement for optimal feed conversion efficiency was 3,022 kcal/kg. It was not possible to determine the requirement for optimal weight gain. However, the highest body weight at 3 weeks of age was obtained with the diet providing 3,050 kcal/kg (1,319 vs. 1,194 g for diet providing 2,454 kcal/kg) The dietary level did not affect the carcass meat yield but the proportion of abdominal fat increased with the increase in dietary energy level from 0.58 to 0.94% with diets providing 2,454 and 3,050 kcal/kg, respectively.

Several studies have been conducted to determine energy utilization in a variety of grains, meals and by-products for ducks (Adeola, 2006; Hoai et al., 2011; Table 1). The hierarchy of energy values for the grains and meals is the same for ducks and broilers. Of the grains examined thus far, barley, rye and triticale have significantly lower energy values for ducks than corn, sorghum or wheat. It is generally assumed that ME value of individual feedstuffs can be added together to match the required energy supplied by the diet. This assumption was tested and verified in barley-canola meal (complete) diet (Hong et al., 2001) and corn-wheat red dog-soybean meal (complete) diet (Hong et al., 2002a). Zhao et al. (2008) and Wan et al. (2009) showed that neutral detergent fibre (NDF) content could be used as an effective indicator to predict the true metabolisable energy (TME) value of corn and wheat milling by-products, respectively, for ducks.

## Protein and amino acids

For Pekin duck, the recommendations for dietary protein and amino acid (AA) contents are indicated in table 2. For most duck diet formulations, methionine, lysine, threonine and tryptophan are likely to be the most limiting AA. Elkin et al. (1986) reported that 1-day-old male Pekin ducklings require between 3.82 and 4.22 g methionine/kg diet during the first 12 days of life. Xie et al. (2004) estimated the optimal methionine and cysteine requirements of Pekin ducklings from hatch to 21 days of age at 4.81 and 3.25 g/kg, respectively. Between 21 and 49 days of age, the optimal methionine requirement was 3.8 g/kg (Xie et al., 2006). For Bons et al. (2002), the dietary lysine concentration should be 11.7
g/kg for the starter period (until 21 days of age) and 10.0 g/kg for the grower period (from 22 days until slaughter). From 7 to 21 days of age, Xie et al. (2009) evaluated the dietary lysine requirement to 9.8 g/kg. With a diet containing 180 g crude protein/kg and 2,990 kcal/kg, Timmler and Rodehutscord (2003) estimated the optimal in dietary valine concentration at 8.0 g/kg for the first three-week post-hatching period. Zhang et al. (2014) estimated the optimal dietary threonine requirement to 8.0 g/kg from 15 to 35 days. Between 1 and 21 days of age, the dietary arginine requirements was 9.5, 11.6 and 9.9 g/kg for optimal weight gain, feed conversion ratio and breast meat yield, respectively (Wang et al., 2013).

For Muscovy ducks, the recommendations for dietary protein and AA contents are indicated in table 3. Leclercq and De Carville (1977) reported that male Muscovy ducklings required 6.0 and 5.5 g total SAA/kg for maximal growth from 3 to 6 and 6 to 10 weeks of age, respectively with diets containing 155 or 130 g CP/kg and 2,986 or 3090 kcal ME/kg, respectively. The 3 to 6 week lysine requirement was estimated to 6.0 g/kg that is 2.2 g lysine per 1,000 kcal ME representing an absolute intake of 21 g lysine over the period (Leclercq and De Carville, 1979). The 6 to 10 week lysine requirement estimation was 1.96 g lysine per 1,000 kcal ME representing an absolute intake of 30-35 g lysine over the period (Leclercq and De Carville, 1979). For threonine, Leclercq (1998) estimated the dietary requirement to 3.97 g/kg between 8 and 12 weeks of age.

For mule ducks, Baéza et al. (2012) showed that 235, 154 and 138 g CP/kg levels could represent optimal levels for growing performance in the starting (0 to 3 weeks of age), growing (3 to 7 weeks of age) and finishing (7 to 10 weeks of age) diets containing 2,900 kcal/kg, respectively. Chen and Shen (1979) reported that for maximal 9 to 21-day weight gain and feed efficiency, the minimal dietary requirements for lysine and arginine were 10.6 and 10.8 g/kg, with diets containing 2,828 kcal and 2,810 ME/kg, respectively. The minimal dietary tryptophan level required for maximal growth and feed efficiency between 8 and 20 days of age was 2.3 g/kg with a diet containing 3,013 kcal/kg and 180 g CP/kg (Wu et al., 1984). The minimal dietary requirements for leucine, isoleucine and valine between 8 to 20 days of age were 12.6, 6.3 and 7.8 g/kg, respectively (Yu and Shen, 1984). Lin and Shen (1994) showed that the minimum requirement of phenylalanine plus tyrosine was 11.1 g/kg between 0 and 3 weeks of age.

For ducks, diets are usually formulated by using the requirements for total AA or the digestibility coefficients of AA determined for broilers even if different studies showed that these coefficients were lower for ducks compared to broilers (for a review, see Helmbrecht, 2012). There are few studies reporting dataset for AA utilisation in feed ingredients for ducks. A comparison of digestibility coefficients for the indispensable AA in corn, barley, bakery meal, canola meal, soybean meal and wheat red dog revealed a considerable variation (Adeola, 2006). In general, true digestibility of the indispensable AA is lower in barley than in corn; and much lower in canola meal than in soybean meal. Digestibility coefficients for most of the indispensable AA in canola or soybean meals are greater than 80%. By comparing diets containing different threonine levels from 5.7 to 8.0 g/kg, Zhang et al. (2014) calculated the apparent ileal threonine digestibility which was comprised between 73 and 83%. The assumption of additivity of individual feed ingredients AA utilization values in complete diets was also tested for barley, canola meal, corn, wheat red dog and soybean meal (Hong et al., 2001; 2002a). While the true digestibilities were additive for most AA, significant exemption was observed for arginine, histidine, lysine, tryptophan and aspartate. Thus, true digestibilities of some AA are not additive, demonstrating some associative effects that vary with the ingredient matrix (Hong et al., 2001; 2002a).

A diet providing 3,012 kcal ME/kg and 182 g CP/kg and supplemented with 10 g L-arginine/kg between 21 and 42 days of age decreased carcass fatness and increased meat yield by comparison with Pekin ducks fed with the same diet not supplemented with L-arginine (Wu et al., 2011). The lipid and protein contents of breast muscle were also increased.

Baéza and Leclercq (1998) tested the possibility to decrease the CP concentration in finishing diets of Muscovy ducks by adding 4 essential AA in order to cover the requirement for these AA. During this period, feed consumption is economically very important as it represents nearly 50% of the total feed intake for the growth of male Muscovy ducks. Protein and AA requirements are lower. Unlike in chicks, feed conversion ratio and fattening of ducks are not modified by decreased dietary CP concentration. Finally, a reduction in dietary CP content should reduce the nitrogen content of excreta and litter, which is a source of environmental pollution. Baéza and Leclercq (1998) showed that it was possible to reduce to 12.4% the CP content of finishing diet supplemented with the 4 essential AA. There was no advantage in supplying more than 4.3 g digestible lysine/kg. When threonine was not added, breast yield decreased significantly (-4.3%), while omitting tryptophan supplementation did not influence growth performance and body composition. It will be interesting to test decreased dietary protein concentration for the starting and growing periods by supplementing diets
with essential and may be not essential AA by using the ideal protein concept developed for broilers according to Baker and Han (1994) and Mack et al. (1999).

## Minerals, vitamins and trace-elements

### Minerals

For Pekin duck, the recommendations for dietary mineral contents are indicated in table 4. Rodehutscord et al. (2003) showed that Pekin ducks require a dietary nonphytate phosphorus level of 3.4 (1 to 21 days of age) and 2.3 g/kg (21 to 49 days of age) based on phosphorus retention data.

For Muscovy duck, the recommendations for dietary mineral contents are indicated in table 5. Leclercq et al. (1990) showed that the best bone characteristics were obtained with 4.0 g nonphytate phosphorus and 8.4 g calcium/kg between 3 and 8 weeks of age and 2.6 g nonphytate phosphorus and 4.3 g calcium/kg between 8 and 12 weeks of age.

For mule duck, Bernadet et al. (2002a; 2002b) showed that the nonphytate phosphorus requirement was 3.1 and 1.4 g/kg for the starting (0-28 days of age) and growing (28-84 days of age) periods, respectively.

Wendt and Rodehutscord (2004) showed that phosphorus availability for Pekin ducks depended on the inorganic sources and ranged between 77 and 100% which should be considered in diet formulation.

The ducklings require approximately 1.4 g sodium and 1.2 g chloride/kg for maximal weight gain (Dean, 1972).

### Vitamins and trace-elements

The recommendations for these nutrients are indicated in NRC (1994), Adeola (2006), Elkin (1987) and INRA (1989). Recently, Wen et al. (2014a; 2014b) revised the choline requirements of Pekin ducks to 810 and 823 mg/kg to optimise weight gain and feed intake during the starting (0-3 weeks) period and to 980 and 950 mg/kg to optimise weight gain and feed intake during the growing (3-6 weeks) period. To prevent an excessive liver lipid deposition during the growing period, the dietary choline concentration should be 1130 mg/kg. For Halle et al. (2011), 20 µg vitamin B12/kg met the requirements of growing ducks. An additional supplementation of cobalt to feed did not have additional advantages for the ducks. The dietary riboflavin requirement from hatch to 21 days of age is around 3.3 mg/kg for Pekin ducks (Tang et al., 2013). Attia et al. (2012; 2013) showed that diet supplementation with 8 mg copper/kg and 30 ppm zinc from inorganic sources were optimal for growth performance of Pekin ducks from hatch to 56 days of age.

## Feeding management

### Feed presentation

Pelleted diets are utilized more efficiently by ducks than diets in mash form because of reduced wastage (10 to 20%) and ease of consumption (NRC, 1994). Starter diets are usually fed as pellets of 3 mm diameter and 8 mm length and for grower diets the pellets are given in 5 mm diameter and 12 mm length.

### Feed restriction

Tan et al. (1999) tested a feed restriction of Pekin ducks to 80, 60 and 40% of ad libitum intake from 7 to 14 days of age. Ducks had the same starter diet (2,900 kcal ME/kg and 230 g CP/kg) from hatch to 21 days of age and the same finisher diet (3,200 kcal ME/kg and 190 g CP/kg) up to 47 days of age. At slaughter age, the feed restriction had no effect on body weight and carcass composition but the feed conversion ratio was reduced by comparison with the ad libitum group. Leclercq and De Carville (1978) tested on male Muscovy ducks a slight (5%) and a severe feed restriction (20%) between 8 and 12 weeks of age. The slight feed restriction had no effect on the slaughter body weight and the carcass composition whereas the severe feed restriction had a negative impact on slaughter body weight and meat yield. It also decreased carcass fatness. The Muscovy duck is able to compensate an earlier feed restriction (25%) realised between 4 and 6 weeks of age with no impact on the growing performance for the whole rearing period and the carcass composition at 12 weeks of age (Baéza, 2000).

Another possibility to restrict poultry is to dilute diets with feedstuffs containing high fibre content. Wu et al. (2012) tested 40 or 60% rice hulls inclusion in the basal diet of Pekin ducks between 8 and 14 days of age. Ducks were fed with the same starter diet (2,902 kcal ME/kg and 210 g CP/kg) from hatch to 14 days of age and the same grower diet (3,002 kcal ME/kg and 180 g CP/kg) between 14 and 42 days of age. The use of 40% of rice hulls had no effect on body weight, feed conversion ratio and meat yield at 42 days of age. The carcass fatness and the lipid content of breast
muscle were decreased whereas the protein contents of carcass and breast muscle were increased. Guo et al. (2013) confirmed that diluting diet with 40% rice hull between 8 to 14 days of age might be a suitable method to improve feed efficiency and to reduce carcass fatness in the production of Pekin ducks.

## Use of enzymes

As for broilers, the use of enzymes (xylanase, β-glucanase, amylase, cellulase, protease, phytase) in diets formulated for ducks can easily improve the nutritive values and digestibility of feedstuffs by reducing digesta viscosity (Timmler and Rodehutscord, 2001; Adeola, 2006) and by consequence decrease the nitrogen and phosphorus contents of excreta (Hong et al., 2002b; Rodehutscord, 2006). For ducks, the use of enzymes is more efficient during the starting and growing periods than the finishing period. It allows also the use of feedstuffs rich in phytic phosphorus and non-starch polysaccharides and therefore decreases the use of mineral phosphorus in diets (Baéza et al., 2010). The use of a diet between 4 and 13 weeks of age containing 1.6 g nonphytate phosphorus/kg and supplemented with a phytase at 600 FTU/kg allowed a reduction of phosphorus in excreta reaching 26 g per mule duck (Bernadet et al., 2004).

## Use of feedstuffs

In practice, many duck diets closely resemble diets for chickens, in being largely corn-soybean meal type. However, worldwide, several non-traditional nutrient sources are available for formulation into the diets of ducks. In Thailand, broken rice, full fat rice bran and extracted rice bran are available. In Vietnam, duck producers can use full fat rice bran and cassava. In Malaysia, Thailand and Indonesia, palm kernel cake is available and could be used at 10-15% (Creswell, 2012). Distiller's dried grains with solubles (DDGS), imported from USA, are available in all Southeast Asian countries and could be used at 10-15% (Creswell, 2012). Inclusion of corn DDGS in amounts up to 25% in the diet of Pekin ducks between 22 to 56 days of age had no adverse effect on growth performance, carcass composition at slaughter, chemical composition, pH and colour of breast meat (Kowalczyk et al., 2012). Peillod et al. (2010) showed that it was possible to include corn DDGS in amounts up to 24% in growing and finishing diets without negative effect on growth performance of mule ducks. Wheat is available in several Asian countries (imported from Australia) and Europe. Wheat milling by-products (bran, pollard) can also be used. Copra, cottonseed and groundnut meals are suitable ingredients for ducks but testing for aflatoxins is recommended before use (Creswell, 2012). Jiang et al. (2012) showed that dietary alfalfa meal introduced in diet at 3, 6 or 9% between 14 and 49 days of age decreased carcass fatness and increased breast meat yield of Muscovy ducks, without an adverse effect on growth performance. It is possible to use industrial rapeseed meal at 7% for the starting period and 14% for the growing-finishing period without adverse effect on growing performance and carcass fatness of mule ducks (Bernadet and Lessire, 2010). Sunflower meal can be used up to 12% in growing diets without affecting growth performance and carcass composition of Pekin ducks (Attia et al., 1998). El-Deek and Brikaa (2009) showed that red seaweed Polysiphonis spp. washed, dried (72 h at 60°C) and ground can be used in starter (0-35 days of age) and fisisher (35-63 days of age) diets of Pekin ducks up to 12 and 15%, respectively, without adverse effect on growth performance, carcass composition and sensory quality of meat. The inclusion of sweet lupins at 400 g/kg in the starter and finisher diets had no deleterious effects on growth performance and carcass composition of Pekin ducks (Olver, 1997). The bitter lupins can also be used in duck diets at the same level but it is necessary beforehand to soak and micronized them (Olver and Jonker, 1998).

## Fatty acid composition of diets and nutritional quality of meat

As for all monogastric animals, it is easy to modulate the fatty acid (FA) composition of meat duck by using different fat sources in diets. Feeding Muscovy ducks with diets containing fish meal or fish oil enriched adipose and muscle tissues with n-3 FA but reduced the sensory acceptance of meat (El-Deek et al., 1997; Schiavone et al., 2004). Schiavone et al. (2007) enriched breast meat of Muscovy ducks with docosahexaenoic acid (DHA) a long chain polyunsaturated n-3 FA, interesting for health consumers, by supplementing diet with 5 g microalgae meal/kg whereas the protein and lipid contents, colour, pH, oxidative stability and sensory characteristics were not affected. Moreover, it is possible to decrease oxidative susceptibility of duck meat enriched with polyunsaturated FA by supplementing diets with vitamin E. Schiavone et al. (2010) measured 2-fold lower values of thiobarbituric acid reactive substances (an indicator of lipid peroxidation) with breast meat from ducks fed a diet containing 230 mg α-tocopheryl acetate/kg by comparison with breast meat from ducks fed a diet containing 30 mg α-tocopheryl acetate/kg.
Conclusion

The main part of duck nutrition studies only examined the effects of nutrients on growth performance, carcass com-
position at the end of the experimental period or at usual slaughter age and chemical composition of carcass or cut
parts (breast or thigh meat, abdominal fat) which will impact the nutritional quality of meat. However, diet composition
and characteristics can also affect the technological (pH, colour, water holding capacity, processing yield, oxidative
susceptibility) and sensorial (texture, flavour, juiciness) qualities of meat. In the future, these parameters also should be
taken into account. Actually, Berri et al. (2008) showed that an increase in dietary digestible lysine from 8.3 to 9.3 g/kg
between 21 and 42 days of age increased growth rate and breast yield, and improved feed conversion ratio of broilers.
Growth performance and carcass composition remained unchanged when the concentration of dietary digestible lysine
was higher than 9.3 g/kg. However, when the dietary digestible lysine increased from 8.3 up to 10.3 g/kg, the ultimate
pH of breast meat increased (6.02 vs. 5.91) and drip loss correlatively decreased (0.85 vs. 1.10%) suggesting modifica-
tions of breast muscle energy metabolism, particularly on glycogen storage, improving the technological quality of
breast meat. Dietary AA composition can also influence sensory quality of meat. Increasing dietary concentrations of
isoleucine and valine, 10 days before slaughter, increased free glutamate (a taste-active component) content and sen-
sory score of overall taste intensity of broiler breast meat (Imanari et al., 2008). In order to determine precisely the AA
requirements it will be also necessary to measure digestibility of AA for duck species during the different feeding
phases. Apart the enzymes, there are also a large variety of feed additives (probiotics, prebiotics, antioxydants, clays,
plant extracts) that can be used also for ducks in relation with their sanitary status, gut microbiota, physiological re-
sponse faced to environmental stress. These different additives need to be evaluated for duck production. Finally, con-
tinued progress in efficient worldwide duck production still requires nutritional evaluation of non-traditional nutrient
sources for the determination of optimal inclusion levels in diets formulations in order to attain safe, sustainable and
efficient production of duck meat that will contribute to satisfy human nutritional requirements for high-quality protein.

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<table><caption>Table 1. Apparent metabolisable energy (AME), nitrogen-corrected apparent metabolisable energy (AMEn), true metabolisable energy (TME) and nitrogen-corrected true metabolisable energy (TMEn), expressed as kcal/kg of feed ingredients for white Pekin ducks (Hoai et al., 2001; Adeola, 2006)</caption><thead><tr><th>Ingredients</th><th>Number of studies</th><th>AME</th><th>AMEn</th><th>TME</th><th>TMEn</th></tr></thead><tbody><tr><td>Barley</td><td>2</td><td>2,622-2,753</td><td>2,726-2,730</td><td>2,973-3,205</td><td>2,863-2,960</td></tr><tr><td>Corn</td><td>12</td><td>3,111-3,624</td><td>3,100-3,505</td><td>3,310-4,014</td><td>3,271-3,833</td></tr><tr><td>Low-phytin corn</td><td>1</td><td>3,412</td><td>2,391</td><td>4,050</td><td>3,847</td></tr><tr><td>High-oil corn</td><td>1</td><td>3,563</td><td>3,501</td><td>4,201</td><td>3,959</td></tr><tr><td>Oats dehulled</td><td>1</td><td>3,563</td><td>3,482</td><td>3,761</td><td>3,642</td></tr><tr><td>Pearl millet</td><td>1</td><td>3,392</td><td>3,350</td><td>3,612</td><td>3,484</td></tr><tr><td>Rice</td><td>2</td><td>3,421-3,622</td><td>3,452-3,500</td><td>3,740-3,653</td><td>3,612-3,526</td></tr><tr><td>Rye</td><td>1</td><td>2,633</td><td>2,691</td><td>2,952</td><td>2,851</td></tr><tr><td>Sorghum</td><td>3</td><td>3,021-3,312</td><td>3,038-3,260</td><td>3,339-3,682</td><td>3,310-3,567</td></tr><tr><td>Triticale</td><td>1</td><td>2,800</td><td>2,757</td><td>3,170</td><td>3,065</td></tr><tr><td>Wheat</td><td>1</td><td>3,262</td><td>3,144</td><td>3,461</td><td>3,300</td></tr><tr><td>Bakery meal</td><td>3</td><td>3,731-3,760</td><td>3,755-3,796</td><td>4,130-4,158</td><td>3,896-3,933</td></tr><tr><td>Canola meal</td><td>1</td><td>2,181</td><td>2,186</td><td>2,764</td><td>2,439</td></tr><tr><td>Corn gluten meal</td><td>1</td><td>4,044</td><td>3,695</td><td>4,367</td><td>3,934</td></tr><tr><td>Meat and bone meal</td><td>12</td><td>1,781-3,916</td><td>1,772-3,662</td><td>nd</td><td>nd</td></tr><tr><td>Low-phytin soybean meal</td><td>1</td><td>3,018</td><td>2,579</td><td>3,539</td><td>2,959</td></tr><tr><td>Soybean meal</td><td>1</td><td>2,938</td><td>2,691</td><td>2,969</td><td>2,720</td></tr><tr><td>Cassava meal</td><td>1</td><td>3,301</td><td>3,201</td><td>3,326</td><td>3,227</td></tr><tr><td>Fish meal</td><td>2</td><td>3,132-3,184</td><td>2,835-2,852</td><td>3,160-3,213</td><td>2,861-2,878</td></tr><tr><td>Wheat middling</td><td>2</td><td>2,208-2,478</td><td>2,149-2,385</td><td>2,711-2,859</td><td>2,502-2,673</td></tr><tr><td>Wheat red dog</td><td>4</td><td>2,385-2,571</td><td>2,519-2,592</td><td>3,117-3,213</td><td>2,900-2,948</td></tr><tr><td>Rice bran</td><td>1</td><td>3,079</td><td>2,950</td><td>3,112</td><td>2,978</td></tr><tr><td>Wheat bran</td><td>1</td><td>3,048</td><td>2,907</td><td>3,093</td><td>2,947</td></tr></tbody></table>

nd = not determined
<table><caption>Table 2. Protein and amino acid requirements of white Pekin ducks</caption><thead><tr><th rowspan="2">Nutrients (%)</th><th colspan="3">NRC (1994)</th><th colspan="3">Adeola (2006)</th></tr><tr><th>0-2 weeks</th><th>2-7 weeks</th><th>0-2 weeks</th><th>0-2 weeks</th><th>2-7 weeks</th><th>2-7 weeks</th></tr></thead><tbody><tr><td>Metabolisable energy (kcal/kg)</td><td>2,900</td><td>3,000</td><td>2,825</td><td>2,875</td><td>3,050</td><td>3,075</td></tr><tr><td>Crude protein</td><td>22</td><td>16</td><td>23.0</td><td>20.5</td><td>17.5</td><td>15.0</td></tr><tr><td>Arginine</td><td>1.1</td><td>1.0</td><td>1.20</td><td>1.04</td><td>0.94</td><td>0.85</td></tr><tr><td>Histidine</td><td></td><td></td><td>0.44</td><td>0.37</td><td>0.33</td><td>0.29</td></tr><tr><td>Isoleucine</td><td>0.63</td><td>0.46</td><td>0.84</td><td>0.69</td><td>0.63</td><td>0.56</td></tr><tr><td>Leucine</td><td>1.26</td><td>0.91</td><td>1.56</td><td>1.28</td><td>1.16</td><td>1.04</td></tr><tr><td>Lysine</td><td>0.90</td><td>0.63</td><td>1.20</td><td>0.96</td><td>0.86</td><td>0.78</td></tr><tr><td>Methionine</td><td>0.40</td><td>0.30</td><td>0.60</td><td>0.55</td><td>0.45</td><td>0.30</td></tr><tr><td>Methionine + cysteine</td><td>0.70</td><td>0.55</td><td>0.95</td><td>0.85</td><td>0.75</td><td>0.60</td></tr><tr><td>Phenylalanine</td><td></td><td></td><td>0.78</td><td>0.64</td><td>0.58</td><td>0.52</td></tr><tr><td>Phenylalanine + tyrosine</td><td></td><td></td><td>1.52</td><td>1.24</td><td>1.12</td><td>1.01</td></tr><tr><td>Threonine</td><td></td><td></td><td>0.76</td><td>0.62</td><td>0.56</td><td>0.50</td></tr><tr><td>Tryptophan</td><td>0.23</td><td>0.17</td><td>0.22</td><td>0.18</td><td>0.16</td><td>0.15</td></tr><tr><td>Valine</td><td>0.78</td><td>0.56</td><td>0.93</td><td>0.77</td><td>0.69</td><td>0.62</td></tr></tbody></table>

<table><caption>Table 3. Protein and amino acid requirements of Muscovy ducks (INRA, 1989)</caption><thead><tr><th rowspan="2">Nutrients (%)</th><th rowspan="2">Starting</th><th rowspan="2">Growing</th><th colspan="2">Finishing</th></tr><tr><th>Females</th><th>Males</th></tr></thead><tbody><tr><td>Metabolisable energy (kcal/kg)</td><td>3,000</td><td>3,000</td><td>3,000</td><td>3,000</td></tr><tr><td>Crude protein</td><td>19.0</td><td>16.0</td><td>13.5</td><td>15.0</td></tr><tr><td>Arginine</td><td>1.07</td><td>0.86</td><td>0.74</td><td>0.82</td></tr><tr><td>Histidine</td><td>0.40</td><td>0.37</td><td>0.32</td><td>0.36</td></tr><tr><td>Isoleucine</td><td>0.70</td><td>0.56</td><td>0.48</td><td>0.53</td></tr><tr><td>Leucine</td><td>1.18</td><td>0.96</td><td>0.83</td><td>0.92</td></tr><tr><td>Lysine</td><td>0.91</td><td>0.76</td><td>0.65</td><td>0.72</td></tr><tr><td>Methionine</td><td>0.36</td><td>0.33</td><td>0.27</td><td>0.30</td></tr><tr><td>Methionine + cysteine</td><td>0.76</td><td>0.65</td><td>0.56</td><td>0.62</td></tr><tr><td>Phenylalanine + tyrosine</td><td>1.23</td><td>1.02</td><td>0.87</td><td>0.97</td></tr><tr><td>Threonine</td><td>0.61</td><td>0.55</td><td>0.47</td><td>0.52</td></tr><tr><td>Tryptophan</td><td>0.17</td><td>0.16</td><td>0.14</td><td>0.15</td></tr><tr><td>Valine</td><td>0.86</td><td>0.70</td><td>0.59</td><td>0.66</td></tr></tbody></table>

Starting period = 0-3 weeks for females and 0-4 weeks for males

Growing period = 3-6 weeks for females and 4-8 weeks for males

Finishing period = 6-10 weeks for females and 8-12 weeks for males
<table><caption>Table 4. Requirements of white Pekin ducks for minerals, vitamins and trace-elements</caption><thead><tr><th rowspan="2">Nutrients</th><th colspan="3">NRC (1994)</th><th colspan="3">Adeola (2006)</th></tr><tr><th>0-2 weeks</th><th>2-7 weeks</th><th>0-2 weeks</th><th>0-2 weeks</th><th>2-7 weeks</th><th>2-7 weeks</th></tr></thead><tbody><tr><td>Metabolisable energy (kcal/kg)</td><td>2,900</td><td>3,000</td><td>2,825</td><td>2,875</td><td>3,050</td><td>3,075</td></tr><tr><td>Crude protein, %</td><td>22</td><td>16</td><td>23.0</td><td>20.5</td><td>17.5</td><td>15.0</td></tr><tr><td>Calcium, %</td><td>0.65</td><td>0.60</td><td>1.2</td><td>1.0</td><td>0.9</td><td>0.8</td></tr><tr><td>Chloride, %</td><td>0.12</td><td>0.12</td><td></td><td></td><td></td><td></td></tr><tr><td>Magnesium, mg</td><td>500</td><td>500</td><td></td><td></td><td></td><td></td></tr><tr><td>Nonphytate phosphorus, %</td><td>0.40</td><td>0.30</td><td>0.60</td><td>0.55</td><td>0.45</td><td>0.30</td></tr><tr><td>Sodium, %</td><td>0.15</td><td>0.15</td><td>0.22</td><td>0.18</td><td>0.16</td><td>0.15</td></tr></tbody></table>

<table><caption>Table 5. Requirements of Muscovy ducks for minerals, vitamins and trace-elements (INRA, 1989)</caption><thead><tr><th rowspan="2">Nutrients, %</th><th rowspan="2">Starting</th><th rowspan="2">Growing</th><th colspan="2">Finishing</th></tr><tr><th>Females</th><th>Males</th></tr></thead><tbody><tr><td>Metabolisable energy (kcal/kg)</td><td>3,000</td><td>3,000</td><td>3,000</td><td>3,000</td></tr><tr><td>Crude protein</td><td>19.0</td><td>16.0</td><td>13.5</td><td>15.0</td></tr><tr><td>Calcium</td><td>0.90</td><td>0.80</td><td>0.64</td><td>0.64</td></tr><tr><td>Nonphytate phosphorus</td><td>0.40</td><td>0.35</td><td>0.26</td><td>0.26</td></tr><tr><td>Sodium</td><td>0.16</td><td>0.16</td><td>0.16</td><td>0.16</td></tr><tr><td>Chloride</td><td>0.14</td><td>0.14</td><td>0.14</td><td>0.14</td></tr></tbody></table>

Starting period = 0-3 weeks for females and 0-4 weeks for males

Growing period = 3-6 weeks for females and 4-8 weeks for males

Finishing period = 6-10 weeks for females and 8-12 weeks for males
# NUTRITIONAL DETERMINANTS FOR GUT HEALTH AND LITTER CHARACTERISTICS IN TURKEYS

**Jesse L. Grimes**

Prestage Department of Poultry Science, North Carolina State University, Raleigh, NC 27695-7608, USA;
[jesse_grimes@ncsu.edu](mailto:jesse_grimes@ncsu.edu)

## Summary

Turkey intestinal health is directly related to growth, performance, and productivity. When intestinal health is sub-optimal, we usually think of some disease or parasite as the main reason for the intestinal dis-order. In many cases this is, of course, very true. However, the relationship between nutrition and gut health can be very direct even though the cause and effect may be indirect. Understanding and appreciating underlying relationships between physiology, nutrition, and health are important but many times are over looked, under estimated, or under appreciated. One can make the argument that some intestinal disorders are not first caused by disease but are initiated by intestinal insults caused by suboptimal nutrition, suboptimal environment, or some combination of the two understanding that both of these cover a great many factors. Intestinal disorder can easily, if not usually, lead to loose feces if not diarrhea. This, in turn, can lead to wet litter which provides more direct insult to the animal through a number of pathways including pathogen production in the litter, ammonia production, breast blisters, and food pad dermatitis. The skin disorders can then lead to more insults directed to the bird. Therefore, we can start to appreciate the holistic system affecting turkeys, especially those in confinement, which is greatly dependent upon gut health.

## Post Hatch

Turkey poults post hatch are very sensitive to their environment. The first hours and days post hatch are critical to proper intestinal health. The poults intestinal tract is immature and rapidly developing. The microbiota of bacteria, protozoa, viruses, etc. are in the process of developing and are affected by the environment of both the hatchery and brooding facilities. Avoiding as much stress as practically possible while providing the environmental and nutritional resources for a good start in life are critical to the future health and productivity of any poult. Optimal incubation and hatching profiles yield a short hatch window. Limiting the amount of time in the hatcher while optimizing development produces healthier poults that can transition better to intestinal nutrition and precocial behavior.

## Brooding

In order for turkey poults to get off to the best start, avoid stress, and be a good performing flock, the brooding facilities must be prepared and set up properly. When the brooding area is not properly prepared in a timely manner, we introduce unwanted and unnecessary stress to our birds leading to poor growth and performance. If conditions are not optimum during brooding, then initial growth is lost, and either the birds will not be as heavy or efficient at slaughter or days to market age will be increased. Less than optimum brooding can also lead to health problems or disease further slowing growth and increasing cost of production. When birds are placed into suboptimal environments, it is difficult to expect any type of nutritional regime to yield maximum results. Bio-security is absolutely a part of all turkey rearing activities especially brooding. While bio-security is not the topic of this discussion, its importance is fully recognized. Reviews on bio-security are available and their applications are encouraged herein.

Proper brooding conditions are critical to provide. Young poults need proper temperature, feed, water, and ventilation in a disease and pest free environment. Litter and proper litter management are also critical to the poults' welfare. Correct temperatures for our poults are critical. Turkey poults are especially sensitive to improper temperature. Poults seem to have a more difficult time in establishing their body temperature regulation process compared to chicks. They seem to perform better when they can move back and forth and into and out of different temperature zones so that they can regulate and maintain their optimal body temperature. Improper or sub-optimal brooding conditions may result in sub-optimal intestinal development. This, in turn, yields less than optimal results from even the best nutritional regime. During the brooding period, especially the first few days, it is extremely important to maximize poulт physiology in order to maximize the provided nutrition.

## Stress

Stress is in every life including that of poults. It is unavoidable as only in death is there absence of stress. However, too much stress in a poults early life can be very counterproductive. Seyle (1973) defined stress as the non-specific response of the body to any demand placed upon it. Each stressor results in specific behavior and physiological
response: cold results in huddling and shivering, hot results in panting and wing drooping, etc. However, in any case of a response to any stressor, there is a general physiological response. This non-specific response has been defined as the “general adaption syndrome (GAS). This general response can be grouped into three categories: alarm, resistance, and exhaustion. The alarm stage includes the classic “fight” or “flight” response and includes immediate physiological actions such as rapid heart rate and redistribution of blood. More long term changes include actions by the glucocorticoid hormones. A cascade of events ensues including the production of corticosterone (the stress hormone). Corticosterone results in both the inhibition of protein synthesis and degradation of proteins. Therefore, in cases of stressful events and environments, we have a difficult time providing a nutritional regime that yields maximum or optimal growth. Usually, in these conditions the requirement of all nutrients is increased and the digestibility of the feed stuffs becomes more critical. Poor digestion of feed and nutrients also leads to more nutrients entering the lower gut which in turn feeds pathogenic bacteria such as some of the clostridia which we want to avoid. In this regard management directly affects the poult’s holistic health which, in turn, affects our ability to provide optimal nutrition.

There are numerous reports in the literature describing the effects of stress on turkey physiology and performance (Grimes, 1995). We have conducted several trials on young turkeys simulating the effects of management events on the stress response in turkeys and subsequent performance. We have observed that simple events such as a one-time, over-night feed and water restriction can yield a short term, corticosterone defined stress response with long term reduction in performance. We also observed that this negative response to stress can be mitigated to some degree by dietary fermentation products. Therefore, while the birds were receiving the same nutrition, their response was different because of environmental factors; and, these environmental factors can be mitigated through nutritional changes or supplementations.

## Feed

Feed and feed quality are especially critical during the brooding period. There are any number of reasons why young poults might refuse feed, limit their feeding, or have a negative response to their feed. Some of those reasons would include aspects of feed quality such as crumble or pellet size, the amount of fat (or lack of fat) in the feed, the amount of fines in the feed, dustiness of the feed, etc. While this article is not about feed quality per se, it is important for producers to be in tune with their flocks’ eating behavior and report any problems, even subtle ones, to the appropriate personnel such as their flock supervisor, veterinarian, nutritionist, or feed mill manager. Numerous disease agents can be associated with intestinal enteritis of poultry. Therefore, any problems with feed quality or abnormal acceptance of feed by the birds should be addressed immediately. The producer should be the first to notice any such change in behavior allowing for a short response time for corrective action. In addition, growers can help their poults get off to a better start by having adequate numbers of supplemental feeders for the first week. Poults should not have to go far to feed. The supplemental feeders or trays should have feed added on a regular basis to stimulate poults to eat.

Poult diets should be simple but highly digestible. Alternative feed ingredients can be challenging to include while maintaining optimal poult performance. It may be worth considering to maintain the highest quality in the first feed even if feed costs are increased. Savings by use of alternative ingredients may be better used when the birds are older with a more mature gut and better able to deal with different feed ingredients.

Even with older birds there are ways to maintain or improve turkey performance with respect to feed ingredients. Using least cost feed formulation, we should consider the final cost of the performance. This final performance may be live weight, breast meat yield, or final product yield and should include the costs of producing this final product. All of these final products may yield, or be based on, differing “least cost” formulas which may or may not be actually least cost diets.

Soybean meal deserves special mention. It is by far the most used protein meal for poultry diets. It is a good source of protein with good amino acid balance except for methionine. When properly processed, the amino acids have good digestibility. However, soybean meal has high levels of indigestible carbohydrates (oligosaccharides) which are difficult for monogastrics to digest. The metabolizable energy level for monogastrics is low compared to corn and other grains. The natural soybean contains high levels of trypsin inhibitors which reduce the protein digestibility. These inhibitors must be heated treated to denature them. When over-heated; however, soybean meal amino acid digestibility is decreased. The phosphorus in soybean meal can also be poorly digested. Therefore, for these and other reasons, high inclusion of soybean meal, above 35%, in turkey diets can lead to increased litter moisture. Many turkey nutritionists utilize other protein sources to limit soybean meal to 35% or less in the diet. These can include animal and animal by-product meals, corn gluten meal, canola meal, limited amounts of DDGS, and other meals. Peanut meal can be good
but can also contain aflatoxin and other mycotoxins. Turkeys are very sensitive to aflatoxin; therefore, peanut meal is usually not used in turkey diets. Diets can be formulated with lower CP levels and increased levels of synthetic amino acids. This helps limit soybean meal inclusion. New varieties of soybeans contain lower levels of trypsin inhibitors, increased protein, and lower levels of oligosaccharides. As these new varieties become more available, there use in turkey diets will increase. Enzymes such as phytases, proteases, and mannanases also help increase the digestibility of soybean meal. (For reviews see Araba and Dale, 1990; Mitchell; Stein et al.; Thakur and Hurlburgh, 2007)

Enzymes can be very beneficial in utilizing many types of feed ingredients, some traditional and some considered "alternative". While wheat is a common feed ingredient, it can be variable with respect to nutrient and indigestible fiber content. Research demonstrating variations in bird performance when birds are fed different wheats and the improvements in bird performance when fed enzymes to improve wheat digestibility is well represented in the literature (Crouch et al., 1997). There are various feed ingredient sources that serve as alternative protein ingredients such as shrimp meal, crab meal, low quality poultry meal, feather meal, and others. Protein enzymes are in development to make better use of these chitin based protein meals. These proteinases may also have usefulness in more traditional corn/wheat/soy diets. DDGS from various grains but mostly from corn and wheat are becoming common place in turkey diets. Enzymes, including xylanases and proteases, can be beneficial supplements in such diets. DDGS, however, can be quite variable in their quality and energy (oil) content. Direct and open communication with ingredient suppliers detailing feed ingredient quality requirements is most helpful in avoiding sub-optimal nutrient specifications and poor quality ingredients. Neither of these can be overcome by enzyme supplementation.

Mycotoxins represent a special challenge for rearing turkeys. There are ample reports in the literature on the effects of dietary mycotoxins on turkey physiology, health, and performance. The effects from naturally occurring mycotoxins may be more meaningful than from the effects of feed spiked with cultured mycotoxins. Turkeys are very sensitive to aflatoxins and probably more sensitive than realized to other mycotoxins. In our work we have observed that physiology, growth, and performance of young turkeys are inhibited by low levels of naturally occurring mycotoxins (Grimes et al., 2010). In addition, we observed little protection was provided by "mycotoxin binders". Mycotoxins in feed will be a continuing challenge for turkey production. A persistent quality control program in which pertinent mycotoxins are continually monitored is time and effort worthy.

## Antibiotics

Traditionally and historically, antibiotics have been provided to poults in the feed to help the bird through critical stages, maintain good health, and improve performance. The use of AGP became widespread for rearing livestock and poultry because of the benefits they afford to the producer, the animal, and the environment, as well as the consumer (Gadd, 1997). These feed borne antibiotic growth promoters (AGP) have been fed to livestock for about 50 years as an aid to improve growth performance (Dibner and Richards, 2005). Specific benefits of feeding AGP to poultry by producers include improved feed efficiency and increased body weight gain. Poultry have been fed AGP during the rearing period to protect them from pathogenic organisms, maintain health, improve growth efficiency and improve meat quality and wholesomeness. However, controversy over the feeding of antibiotics as growth promotants in many countries has increased because of the fears concerning the development of antibiotic resistant microbes from the use of AGP in food animals. Therefore, dietary antibiotics have come under increasing scrutiny by some scientists, consumers, activists, politicians, and bureaucrats because of the potential development of antibiotic-resistant bacteria (including pathogenic strains) in livestock and poultry. Poultry companies are now either required or more dedicated to eliminate or reduce dietary AGP depending on their location and/or customer base.

## Probiotics

Although the antibiotic debate continues, there is interest and need in developing alternatives to AGP. Two candidates are prebiotocs and probiotics. In addition to the term "probiotic", the Association of American Feed Control Officials (AAFCO, 1999) and the US Food and Drug Administration (FDA, 2003) have recommended the term "direct-fed microbials" (DFM) be used to describe live culture feed additives (Elam et al., 2003). Other types of probiotics that are not live cultures have been referred to as "prebiotics" (Patterson and Burkhold, 2003). Probiotics have been developed to counter the growth depressing effects that certain strains of bacteria elicit in poultry. There are numerous reports and reviews of these supplements being fed to livestock and poultry, including turkeys (Blair et al. 2004; Damron et al. 1981; Gustafson and Bowen 1997; Fuller, 1989; Owings, 1992).
The use of DFM supplements in diets changes and stabilizes the microflora environment of the avian digestive tract (Jin et al., 1998; Knarreborg, et al., 2002; Patterson and Burkholder, 2003; Smirnov et al., 2005). There are numerous reports describing competitive exclusion including the significant reduction of intestinal levels of *Salmonella spp* in turkeys or other livestock by use of DFM (Bailey, 1987; Casas et al. 1998; Juven et al., 1991; Nurmi and Rantala, 1973; Vicente et al., 2005). In addition to colonizing the intestinal tract, the use of *L. reuteri* resulted in shorter, lighter intestines and smaller relative intestinal weight in turkeys; similar results have been observed and reported in other studies with broilers (England et al., 1996).

We have conducted several studies and reported the positive effects of dietary prebiotocs, probiotics, and DFM on poultry including turkeys (Grimes et al., 2008; Parks et al., 2001; Rahimi et al., 2008; Russell and Grimes, 2009). Using these supplements, we have observed improved poult performance, improved performance to market age, and reductions in bacterial intestinal colonizations of birds induced by gavage. One study included both university and field trials. In the field, the water borne probiotic resulted in more weight harvested from the farm representing improved efficiency of production. Therefore, it is apparent that DFM, probiotic organisms, and prebiotics can improve the nutrition of poultry without necessarily changing the nutritional makeup of the feed.

## Water

Water is the least appreciated nutrient. Turkeys should be provided with as clean and fresh water supply as possible. Poor quality water laced with bacteria and protozoa can undermine any management and nutritional regimen. This is especially true for the poults during the brooding period when poults are most sensitive to intestinal insults. Cleanliness of water equipment, including water lines, is a major component of providing clean water. Cleaning and sanitation of all water equipment should be accomplished before the poults arrive on the farm. During cold weather it is also important that water lines and extra poult waterers be filled the day before arrival so that the birds do not have to drink cold water. Water samples should be collected periodically to assess the water for contaminants and high mineral levels. Nipple drinkers are becoming popular for brooding turkeys. However, it is advised that only nipple drinkers designed for and tested with turkey poults be used to brood turkeys. Some broiler nipple drinkers will not support proper poult growth and this growth may not be recovered after switching to adult or rearing type drinkers (Russell et al. 2009). In addition, some of the broiler type nipple drinkers may be high flow systems which might lead to wetter litter which is not desirable (Quilumba et al. 2015).

## Litter Moisture

As is the case with any poultry flock reared on litter, producers should monitor litter quality closely so that when conditions change, managerial changes can be put into place. At thermo-neutral temperatures, birds consume twice as water by weight as they do feed. Most (80%) of this water leaves the bird and enters the house either through respired air or by feces. Only about 20% is retained in the bird. Furthermore, when the temperature is increased 10 C (20 F), feed intake decreases while water intake can double. Most turkey houses are equipped with water meters – are we paying attention to these meters and the bird’s water usage? Even without a meter we can do some math. A flock of 5000 tom turkeys at 20 kg/tom with a FCR of 2.5 equates to 50 kg of feed and 100 kg of water per bird under ideal conditions. This is about 100 L of water per bird or 500,000 L (125,000 gal) of water into the turkeys with 400,000 L (100,000 gal) into the house itself. That is a lot of water! While many turkey producers till their litter, the only way to really handle this water is through forced air ventilation. Some brooder facilities are equipped with forced air systems; however, many, if not most, grow-out houses are not. This places turkey facilities at a disadvantage compared to broiler houses. This is further disadvantaged when turkey houses are cooled using foggers. Much of the water used to cool the air actually ends up in the litter. Wet litter is directly associated with foot pad dermatitis. Most turkeys, especially toms, by market age have foot pad dermatitis to some degree (da Costa et al. 2014; Liesner, 2007). Many of these cases are severe. Litter under turkeys reared in houses equipped with tunnel ventilation with cool cell pads seem to have less foot pad dermatitis. This is advantageous for bird welfare. It also reduces insults to the birds’ skin thereby reducing potentially reducing pathogen entry into the bird. Healthier birds have better intestinal health and utilize their nutrition better.

Changes in water usage can be, and usually are, noticed ahead of any feed use changes. We can take advantage of this physiology and begin intervention strategies before the situation deteriorates further. As the poults grow, their air and oxygen requirements grow accordingly, if not exponentially. The birds are producing more manure and the litter can get wetter producing the perfect conditions for increased ammonia production. During cold weather, poult barns may be closed up tight, as they should be. However, just because there is no, or little, ammonia being produced in the litter does not mean there is no need for air exchange. Brooders and poults share one requirement and that is
oxygen. As the brooders and poults use up the oxygen in the house, moisture and carbon dioxide are produced. In some cases, carbon monoxide is also produced, especially with poorly working heaters. None of these are desired in the poult barn. Increased air moisture may lead to increased litter moisture. Increased litter moisture will eventually lead to more ammonia production and foot pad dermatitis. In addition, many turkey veterinarians, turkey health researchers, managers, service people, and producers have noticed and associated increased litter moisture in the turkey brooder barn with increased turkey health issues such as poult enteritis and other diseases. This increase in brooder house litter moisture has been observed in the U.S. especially during spring when weather conditions are changing from cool and dry to warm and humid. As stated above, many turkey poult barns are not equipped with the ventilation systems found in broiler houses and in many cases, even when systems are in place, are not used as optimally as they could be. Most turkey barns are also not equipped with vents, which when present can aid in proper movement and mixing. It has been mentioned in a number of reports that commercial turkeys are not maximizing their genetic potential. Ventilation systems in turkey facilities, both brooding and growing, should be closely examined to align optimal ventilation with maximum bird performance.

## Conclusion

While much is studied and written about turkey nutrition, much of this subject is viewed from the reverse perspective. Of course we want optimal nutritional regimens provided to our birds. However, only through optimal intestinal health can any nutritional package provided to the bird be fully appreciated and utilized. Certainly veterinarian care is critical to our cause. However, turkey intestinal health and overall turkey health and welfare can only be fully maximized when we provide the best environment and daily care for our birds. This the first and most important element of turkey production. Unfortunately, this will not always guarantee success as we have seen lately and historically with severe disease outbreaks. However, this is where we must begin our journey in successful turkey production.

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# DIFFERENCES IN AMINO ACID AND PHOSPHORUS DIGESTIBILITY BETWEEN BROILER CHICKENS, TURKEYS AND DUCKS

## Markus Rodehutscord

Institute of Animal Science, University of Hohenheim, 70599, Stuttgart, Germany; inst450@uni-hohenheim.de

### Summary

Digestibility of amino acids and phosphorus became highly relevant in feed formulation for poultry. In recent years, digestibility measurements were increasingly done using growing birds and on the precaecal level. More data are available for broiler chickens than turkeys and ducks. Literature evaluated in this contribution does not support the assumption of broiler chicken digestibility data being applicable in feed formulation for turkeys and ducks. Species differences in amino acid digestibility appeared to be dependent on the type of feedstuff investigated. Species differences in phosphorus digestibility were hypothesised to be mainly related to differences in gastrointestinal phytate breakdown. However, conclusions from the comparisons could be drawn only with care because the database is small and differences in assay conditions applied in different institutions affect the studies outcome. Science and industry joint research activities should be initiated to fill the knowledge gap and better understand species-specific metabolism and digestibility. This will support achieving more precise feed formulation through avoidance of safety margins which are needed more when the database of raw material digestibility is less precise.

### Introduction

Different raw materials contribute to the energy and nutrient supply of birds to a variable extent. Chemical analysis is the primary step of characterization of raw materials. However, characteristics other than those chemically analysed contribute to the "value" that a raw material has when considered in diet formulation. Determination of digestibility in animal studies thus is a very important tool to characterize the feeding value with the target animal species.

Determination of digestibility is, in its simplest definition, the "balance of the digestive tract". However, in order to make digestibility values comparable in feeding systems and tables, certain standards in the trial protocols need to be agreed on. Such standards must consider the metabolic situation and adaptation of an animal. Therefore, they are specific for individual nutrients or fractions of the feed, meaning that a "digestibility of a feed" does not exist. This leads to considerable effort being necessary before digestibility values can be implemented in practical feed formulation and explains why the consideration of digestibility is primarily aimed for nutrients of high economic or environmental relevance. Next to energy, which will not be considered in this contribution because addressed in another session, amino acids (AA) and phosphorus (P) received most attention in recent years in digestibility studies.

In poultry, the distinct species focus of digestibility studies has been on the domestic fowl using different types of rooster assays and, more recently, broiler chickens. Feed formulation for ducks and turkeys can also benefit from consideration of digestibility values, but data are more scarce than for broilers. As differences in anatomic and physiological characteristics of the digestive tract between the species are known, nutritionist are interested in whether data obtained with broiler chickens can be used to fill the gap that exists in duck and turkey nutrition in regard to digestibility values. Hence the objective of this presentation is to compare on the basis of the scientific literature and to draw conclusions for both the scientific community and the feed industry.

### Amino acid digestibility

Different assays were used in the past to study AA digestibility. Many studies involved differently standardized rooster assays and excreta collection. Other approaches used broiler chickens as the target category to feed, and more recent studies with broiler chickens in the vast majority had a special focus on precaecal (or ileal) AA digestibility. This technique implies collection of digesta from the ileum rather than excreta collection. Both approaches (rooster-based and broiler-based) found their entry in commercially driven databases and Tahir and Pesti (2012) described differences in the relative ranking of groups of feedstuffs between the two databases. This can be taken as a descriptive example of the relevance that assay conditions have in AA digestibility studies. In broiler studies of precaecal AA digestibility specific assay conditions (section of ileum sampled, procedure of asphyxiation, age of birds, level of feed intake, etc.) and consideration of basal endogenous AA flow in the ileum are also relevant for the determined digestibility values (Kluth and Rodehutscord, 2009). Taking all this into consideration unravels some difficulty when evaluating species differences in AA digestibility based on literature. This is because possibly existing species differences can be masked by
differences in assay conditions used in different studies. In consequence, this contribution will focus on the (few) studies that made comparisons using the same assays conditions for the species considered and will focus on precaecal digestibility studied in growing birds.

## COMPARISONS OF TURKEYS AND BROILER CHICKENS

When viewed on a high level of integration of the available literature, the first indication is that precaecal Lys and Met digestibility is very similar in turkeys and broiler chickens (Figure 1) (these AA will be exemplarily focused on in this contribution). However, the range of values was very high. This range was to a large extent caused by the types of feed that were used in the studies. However, against the impression given with Fig. 1, differences between turkeys and broiler chickens were found in some studies and differences were not always in the same direction. Kluth and Rodehutscord (2006) used the regression approach and found that precaecal digestibility of Lys and Met was not different between turkeys and broiler chickens for soybean meal, but lower in turkeys than broiler chickens for rapeseed meal. A similar difference between turkeys and broiler chickens was found by Jia et al. (2012) who used different qualities of rapeseed in studying apparent AA digestibility. In diets that included 70% wheat-DDGS Lys digestibility was around zero and Met digestibility was substantially lower in turkeys than broiler chickens, irrespective of whether a protease supplement was included or not (Adebiyi and Olukosi, 2015b). Extensive comparative work was also done by the colleagues at Purdue University and their collaborators. While Lys digestibility of maize was lower in turkeys than broiler chickens at 5 days of age, Lys digestibility of different types of DDGS, canola meal, and soybean meal was similar or higher in turkeys than broilers (Adedokun et al., 2008). In this study similar trends were seen when turkeys and broilers were 21 days old. When investigating AA digestibility of meat and bone meal, Lys and Met digestibility was either higher or lower in broiler chickens than turkeys, depending on the source of meat and bone meal used (Adedokun et al., 2007b).

<figure><img src="image_16.png" /><figcaption>**Figure 1.** Mean and range of Lys and Met digestibility for different raw materials and diets as investigated in different studies with broiler chickens and turkeys (25 obser-vations) using similar methods (Adebiyi and Olukosi, 2015b, Adedokun et al., 2007b, Adedokun et al., 2008, Jia et al., 2012, Kluth and Rodehutscord, 2006)</figcaption></figure>

It has been debated whether differences in the level of ileal endogenous AA flow between poultry species may be a reason for differences seen in apparent AA digestibility values in some studies. However, species differences remain to persist, at least in part, when digestibility is determined by regression analysis, thus eliminating the effect of basal endogenous AA flow (Kluth and Rodehutscord, 2006).

Knowledge about the ileal flow of endogenous AA becomes relevant when the regression approach is not applied but apparent digestibility values are transferred to standardised values. Some studies systematically compared the ileal flow of endogenous AA between broiler chickens and turkeys. Ileal flow of endogenous AA as studied by using a N free diet and expressed in relation to dry matter intake was higher in turkeys than broilers at the age of 5, 15 and 21 days, the difference being statistically significant only at 5 days of age (Adedokun et al., 2007a) (Table 1). In contrast, ileal flow of endogenous essential AA at the age of 4 weeks was on average one third higher in broilers than turkeys (Adebiyi and Olukosi, 2015b). Adedokun et al. (2008) compared AA digestibility in broilers and turkeys in the age of 5 and 21 days. They also measured endogenous AA flow and concluded that age-specific values for endogenous AA flow should be considered when apparent digestibility values are corrected. Differences in the ileal flow of endogenous AA reported here did not contribute to the range of values shown in Fig. 1 because values were expressed on a standardized basis when possible.
Palander et al. (2006) found significantly lower AA digestibility in 10-wk old turkeys compared to 5-wk old when using diets that contained 50% of peas, faba beans or lupins. In another study of this group using diets containing rapeseed and soybean products, crude protein digestibility was also reduced when turkeys were 12 wk old compared to 4 wk or 8 wk (Palander et al., 2004). The authors hypothesised this age effect to be caused by changes in passage rate and endogenous secretions becoming more relevant with age (Palander et al., 2006). They also suggested, in reference to chicken data reported by Gonzalez and Vinardell (1993) and Gonzalez et al. (1996) that intestinal AA transport systems may become less active with increase in age. The quantitative relevance of such differences seen in processes and mechanisms however still needs to be elucidated before it can be better evaluated whether or not they affect digestibility.

<table><caption>**Table 1:** Estimates of ileal endogenous amino acid flow based on the use of N free diets (mg/kg of dry matter intake)</caption><thead><tr><th rowspan="3"></th><th colspan="8">Age (days)</th></tr><tr><th colspan="2">5<sup>1)</sup></th><th colspan="2">15</th><th colspan="2">21</th><th colspan="2">28<sup>2)</sup></th></tr><tr><th>Broiler</th><th>Turkey</th><th>Broiler</th><th>Turkey</th><th>Broiler</th><th>Turkey</th><th>Broiler</th><th>Turkey</th></tr></thead><tbody><tr><td>Lysine</td><td>522</td><td>1168</td><td>209</td><td>276</td><td>182</td><td>287</td><td>308</td><td>216</td></tr><tr><td>Methionine</td><td>153</td><td>391</td><td>56</td><td>86</td><td>44</td><td>85</td><td>91</td><td>121</td></tr><tr><td>Reference</td><td colspan="8">Adedokun et al. (2007a) Adebiyi and Olukosi (2015b)</td></tr><tr><th rowspan="3"></th><th colspan="4">Age (days)</th></tr><tr><th colspan="2">19<sup>3)</sup></th><th colspan="2">26<sup>3)</sup></th></tr><tr><th>Broiler</th><th>Duck</th><th>Broiler</th><th>Duck</th></tr><tr><td>Lysine</td><td>374</td><td>965</td><td>382</td><td>1402</td></tr><tr><td>Methionine</td><td>86</td><td>333</td><td>100</td><td>413</td></tr><tr><td>Reference</td><td colspan="4">Kong and Adeola (2013b) Kong and Adeola (2013a)</td></tr></tbody></table>

## COMPARISON OF DUCKS AND BROILER CHICKENS

Pioneering comparative work on waterfowl and broiler chickens was done by Dorota Jamroz and her colleagues. When feeding mixed diets based on barley, wheat and soybean meal, digestibilities were different between chicken and waterfowl (Jamroz et al., 2001, Jamroz et al., 2002). Mean digestibility for all AA at the age of 14, 28 and 42 days was 70, 73, and 73% in chickens, respectively, and 44, 62 and 60% in ducks (Jamroz et al., 2002). As mentioned before, differences in the level of endogenous AA losses between species may have contributed to these differences. This was a motivation to use the regression approach for further comparative work (Kluth and Rodehutscord, 2006). In their study, the mean AA digestibility of soybean meal and rapeseed meal was investigated in 3-wk old birds and it also was lower in ducks (72% for soybean meal and 68% for rapeseed meal) than broiler chickens (79% for soybean meal and 80% for rapeseed meal). Kluth and Rodehutscord (2006) thus concluded that basal endogenous AA losses were not the primary reason for differences found between ducks and broiler chickens in earlier studies. It is important to mention that in another study on soybean meal and canola meal apparent digestibility values were slightly lower in ducks than broiler chickens at 19 days of age (Kong and Adeola, 2013b). However, following regression analysis of the data thus excluding differences in basal endogenous losses significant species differences no longer existed for most of the AA studied. In both studies (Kluth and Rodehutscord, 2006, Kong and Adeola, 2013b) and irrespective of the level of digestibility the ranking of individual AA digestibility was similar in ducks and broiler chickens.

Estimates of ileal flow of endogenous AA when using a N free diet were much higher in ducks than broilers (on average approximately threefold to fourfold higher) at the age of 19 or 26 days (Kong and Adeola, 2013b, Kong and Adeola, 2013a) (Table 1).

The studies by Jamroz et al. (2004) indicate that differences in the development of the digestive tract might be a partial cause of species differences in digestibility. They found that the relative length of the small intestine (in relation to BW<sup>0.67</sup>) was higher in broiler chickens than in ducks. Similarly, estimates made from Figure 2 and Table 2 of Applegate

<footnote n="1">1) Differences between species were statistically significant at 5 days of age.</footnote>

<footnote n="2">2) Statistical analysis of species difference was not reported.</footnote>

<footnote n="3">3) Differences between species were statistically significant.</footnote>
et al. (2005) indicate that the length of jejunum + ileum in relation to BW, measured 7 days posthatch, is greater in turkeys than in ducks.

## CONCLUSIONS FOR AMINO ACIDS

Based on current scientific evidence, no clear statement can be made regarding species differences. There are indications that precaecal AA digestibility can be lower in turkeys than in broiler chickens and again lower in ducks. However, literature is not consistent regarding these differences and likewise the magnitude of difference depends on the feed raw material. However, comparisons between species so far can only be made on a small database because only few studies were performed under *ceteris paribus* conditions. Both the scientific community and industry are encouraged to consider this a challenge. Feeding costs are affected by safety margins needed as long as uncertainties about digestibility values exist. Scientists are encouraged to clarify possible reasons for species differences and to continue in standardising assay conditions. Only on the basis of a standardized methodology all the data that are urgently needed can be generated and used to compile feeding tables.

## Phosphorus digestibility

The digestibility of P is affected by different factors related to both the feed and the bird's physiology. In plant-based raw materials, most of the P is contained as phytic acid (myo-inositol 1,2,3,4,5,6-hexakis (dihydrogen phosphate); $InsP_6$) and phytate (any salt of $InsP_6$), but the proportion is variable in different raw materials. Plant seeds also differ in intrinsic phytase activity (Eeckhout and De Paepe, 1994). Mineral feed phosphates and animal by-products differ in their solubility. All these differences affect the availability of P. The animals have physiological mechanisms that allow an adaptation to different levels of P supply and this leads, in contrast to what has been mentioned above for AA, to the need for specification of upper levels of P and optimal Ca:P ratio in diets used in P availability studies. This, together with the specification of other assay details, is considered in the standard protocol for the determination of P availability published by the Working Group 2 -Nutrition- of the European Federation (WPSA, 2013). This protocol defines precaecal P digestibility as the criterion to measure. It was also mentioned that P retention equals precaecal P digestibility under the condition of marginal P supply because in such condition the urinary loss of P is negligibly low (Rodehutscord et al., 2012). The complexity of feed- and animal-related factors influencing P metabolism explains why, as for AA digestibility, a comparison of P digestibility between poultry species can only be made when experimental conditions are well standardised.

When using a low-P basal diet and further diets containing graded levels of monobasic calcium phosphate, P utilisation of the basal diet was higher in broiler chickens than in turkeys and ducks, but utilisation of supplemented mineral P was highest in ducks, followed by turkeys and broiler chickens, respectively (Rodehutscord and Dieckmann, 2005). In other experiments that investigated the utilisation of different feed phosphates for Pekin ducks values also were very high (Wendt and Rodehutscord, 2004). Adebiyi and Olukosi (2015a) studied precaecal P digestibility and P retention of wheat-DDGS using the regression approach. Estimated digestibility and retention values were very high in broiler chickens (94 and 92%) and were lower in turkeys (76 and 71%).

Differences in $InsP_6$ degradation in the digestive tract and release of phosphate may have contributed to the differences between species. Endogenous mucosal phytase activity was detected in the small intestine of broiler chickens (Huber et al., 2015, Maenz and Classen, 1998) and it cannot be ruled out that this is different in turkeys or ducks, thus leading to differences in phosphate release from $InsP_6$. However, gastrointestinal $InsP_6$ hydrolysis still is a black box in regard to the origin of contributing enzymes and likewise phytase producing microbes resident in the digestive tract are involved (Zeller et al., 2015a). The crop plays some role in microbial enzyme production in broiler chickens and it may be speculated whether the absence of a fully functioning crop in ducks is a reason for lower P utilisation in ducks compared to broiler chickens.

Hydrolysis of $InsP_6$ is also relevant when the digestibility of mineral or animal P sources is determined. This can only be done when the P source under test is supplemented to a low-P basal diet and the basal diet often contains $InsP_6$ if it is not a purified diet. Supplements of Ca and/or P sources, however, can reduce intestinal degradation of $InsP_6$ thus leading to interactions between $InsP_6$ breakdown, mineral supplements and phytase supplements in the digestive tract of broiler chickens (Zeller et al., 2015b, Tamim and Angel, 2003). These interactions can cause a considerable underestimation of digestibility of a mineral P source (Shastak et al., 2014). If $InsP_6$ hydrolysis is lower in ducks than in broiler chickens this might mean that the diminishing effects of mineral P supplements on $InsP_6$ hydrolysis are less pronounced in ducks than in broiler chickens. Such effects may be suitable to explain the differences in calculated digestibility
of mineral P sources between poultry species. However, the hypotheses presented here still need to be tested in ex-
periments that involve measurements of InsP₆ degradation, mucosal phytase activity and microbiota composition in
different sections of the gastrointestinal tract.

Conclusions

Differences exist in the digestibility of amino acids and phosphorus between growing broiler chickens, turkeys and ducks. The database for the comparison of species is small because the results of digestibility studies are influenced by assay conditions and methodological details, especially when measured on the precaecal level. In regard to amino acid digestibility, species differences appear to depend on the type of feed studied. In regard to phosphorus digestibility, species differences are probably caused mainly by differences in gastrointestinal InsP₆ breakdown. Among the three species, most data are available for broiler chickens and databases including digestibility values already exist for broiler chickens. If these data are used for formulating diets for turkeys and ducks, this should be done with care and using safety margins unless species differences are better understood and quantified. Research is needed in different regard: better standardisation of assay protocols; increasing linkage of quantitative digestibility data with functional studies on tissue, metabolism and microbiota level; poultry species comparisons using *ceteris paribus* experimental conditions. The applied nature and economic relevance of this research should make the industry feel invited contributing to the research questions to be answered.

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SHORT ORAL PRESENTATIONS

ID 156

PHYTATE DEGRADATION IN BROILERS AS AFFECTED BY DIETARY PHYTATE AND NON-PHYTATE PHOS-
PHORUS CONTENT

M.M. van Krimpen, J. van Harn, R.A. van Emous, and P. Bikker

Wageningen UR Livestock Research, PO Box 338, NL-6700 AH Wageningen, the Netherlands

**Corresponding author:** marinus.vankrimpen@wur.nl

**Abstract**

Broilers have the intrinsic capacity to degrade dietary phytate, thereby increasing precaecal phosphorus digestibility (pcdP). Insight in the extent and mechanism of phytate-P (PP) degradation is necessary to evaluate the contribution to the P-supply of the birds. An experiment was performed to determine the interaction of dietary PP and non-phytate P (nPP) content on pcdP in broilers, using the WPSA (2013) protocol for determination of P availability in poultry. A total of 756 day-old Ross 308 male broilers were obtained from a commercial hatchery and at d14 randomly allocated to 72 floor pens (0.96 m²). All birds received a commercial starter diet between d0 and 14. Experimental diets were provided from d14 onwards, and ileal digesta were collected on d23 and 24. Phosphorus (P)In total 12 different diets were pro- vided, varying in dietary PP and nPP content. In low PP diets, pcdP of monocalcium phosphate (MCP) was 88% and remained constant over a large range of dietary P contents (2-6 g/kg). In soybean meal (SBM) based high PP diets, pcdP of MCP was 47% over a large range of inclusion levels (total P 3-7 g/kg). In SBM-based high PP diets, PP degra- dation linearly decreased from 96 to 68% with increasing dietary nPP content. It was concluded that broilers are highly capable to regulate pcdP by increasing PP degradation under conditions of low nPP supply. These findings have to be taken into account in studies that determine pcdP of dietary ingredients.

**Keywords:** poultry, nutrition, broiler, phosphorus, phytate degradation

**Introduction**

Among other minerals, phosphorus (P) has been extensively investigated as an essential nutrient in poultry diets, and its major role in chick's growth performance and bone mineralisation cannot be over-emphasized (Underwood and Suttle, 1999). The availability of P in feedstuffs of plant origin is of considerable importance. Poultry diets consist primarily of feedstuffs of plant origin, and a large but variable portion of P in these products is found in phytate (PP) form, which is usually considered to be unavailable for birds (Van Der Klis and Versteegh, 1999). There is, however, some evidence in literature that broilers, when fed P deficient diets, have the intrinsic capacity to partly degrade PP (Marounek et al., 2010), thereby increasing precaecal P digestibility (pcdP). The level of PP degradation depends among others on the dietary available P and the PP content (Van Der Klis and Blok, 1997). The aim of the current study was to investigate the extent and mechanism of PP degradation, which would be of importance for application in protocols for determination of pcdP of feed ingredients.

**Material and Methods**

An experiment was performed to determine the interaction of dietary PP and non-phytate P (nPP) content on pcdP in broilers using the WPSA (2013) protocol for determination of P availability in poultry. A total of 756 day-old Ross 308 male broilers were obtained from a commercial hatchery and at d14 randomly allocated to 72 floor pens (0.96 m²). All birds received a commercial starter diet between d0 and 14. Experimental diets were provided from d14 onwards, and ileal digesta was collected on d23 and 24. In total 12 different diets were provided, varying in dietary PP and nPP con- tent. The results of 9 out of the 12 tested diets were included here. To determine pcdP in low PP diets, a semi-synthetic basal diet, low in total P (2.1 g/kg) and PP (0.85 g/kg) was supplemented with 3 graded levels of MCP, resulting in a total P content of 8.6 g/kg in the 4th diet. To determine pcdP and ileal PP degradation in high PP diets, a high PP basal diet containing 40% of soybean meal (SBM) (P = 3.15 g/kg, PP = 1.5 g/kg) was supplemented with 2 levels of MCP, resulting in a total P content of 7.3 g/kg in the 3rd diet. In two more treatments, the high PP basal diet was supple- mented with 11% and 22% SBM as PP source, resulting in total P content of 4.7 g/kg and a PP diet of 2.2 g/kg in the 3rd diet. All experimental diets were free of phytase and contained SBM as the only PP source. Titanium oxide was used as indigestible marker and pcdP was determined as the slope of the relationship between total and digestible P content.
At d23 and 24, birds were weighed and thereafter killed with ± 0.5 ml of T61 via the wing artery. A pooled sample of the ileal digesta from the posterior 1/3 (10-15 cm) of the part between Meckel's diverticulum and 2 cm before the junction to the caeca of the birds was collected. The ileal content was collected by flushing the gut segment with distilled water without squeezing the gut. After the collection, the samples were immediately frozen and stored at -20°C until further analysis. Both the experimental diets and the digesta samples were analysed for dry matter, Ca, P, marker (titanium oxide) and PP.

## Results

In low PP diets, the pcdP of MCP was constant (88.0% ± 0.05) over a large range of dietary P content (2.1 to 6.0 g P per kg), whereas from 6.0 to 8.6 g/kg, pcdP of MCP was estimated as 15.7% (± 0.07). The pcdP of 88% was in line with the table value (85%) of CVB (2011).

Addition of MCP to a PP rich basal diet resulted over the tested range of 3.2 to 7.3 g P per kg in a constant (46.8% ± 0.02) pcdP of MCP, which was significantly lower than 88% as determined in the low PP diets. These findings indicate an interaction between the dietary PP content diet (0.85 vs. 1.50 g/kg) and the pcdP of MCP, which may be related to the level of PP degradation. PP degradation in the birds fed the basal diet was almost complete (96.9%), but significantly reduced in birds fed the diets containing 5.3 or 7.3 g/kg P by adding MCP (82.6 and 68.2%, respectively). The birds regulated the extend of PP degradation in dependence of the amount of nPP supplemented via MCP. The expected increase in digestible P with increasing MCP levels is partly negated by the decrease in PP degradation, thus reducing the estimate of pcdP.

Adding SBM as PP rich ingredient to the high PP basal diet resulted in a small decrease in PP degradation at the highest SBM inclusion compared to the basal diet (from 96.9 to 91.3%). As a consequence, pcdP of SBM decreased with an increasing SBM inclusion level, indicating an interaction between the dietary P and/or PP content and the level of PP degradation. Over the whole test range, in which the dietary SBM inclusion level varied from 40 to 62%, pcdP of SBM was 42.4%, which is in line with the table value (41.5%) of CVB (2011).

PP degradation in the high PP diets, containing at least 40% of SBM as only PP source, showed a wide variation, ranging from 68.2 to 96.9%. As shown in Figure 1, a significant linear relationship was observed between the dietary nPP content and the PP degradation, thereby explaining 84% of the variation in PP degradation. In the tested nPP range in this experiment (1.5 – 5.5 g/kg), the level of PP degradation decreased with 7.4% for each g increase in dietary nPP content. Based on these findings it is suggested that broilers degrade more PP if less easily absorbable nPP is available in gut.

<figure><img src="image_17.png" /><figcaption>**Figure 1** Relationship between the dietary nPP content and the level of PP degradation</figcaption></figure>
Conclusions

In low PP diets, estimated pcdP of MCP was constant at a high level (88.0%) over a large range of dietary P content from MCP. Therefore, the P content of a low PP diet seems not very critical for testing pcdP of feed phosphates. In PP rich diets, pcdP of MCP was constant at a low level (46.8%) over a large range of MCP inclusion level. A significant linear relationship was derived between the dietary nPP content and the level of PP degradation. In the tested nPP range in this experiment (1.5 – 5.5 g/kg), the PP degradation decreased with 7.4% for each g increase in dietary nPP content. Based on the findings of this experiment, it is recommended to use low PP diets to determine P absorbability of feed phosphates, whereas the dietary P content may not be very critical in such studies. Moreover, low nPP diets should be used for testing P absorbability of PP rich ingredients.

Literature

CVB, 2011: Veevoedertabel 2011, Centraal Veevoederbureau. Lelystad, the Netherlands

MAROUNEK, M., M. SKRIVAN, O. ROSERO, O. ROP, 2010: Intestinal and total tract phytate digestibility and phytase activity in the digestive tract of hens fed a wheat-maize-soyabean diet. J. Anim. Feed Sci. **19** (3), 430-439.

UNDERWOOD, E. J., N.F. SUTTLE, N. F., 1999. The mineral nutrition of livestock, 3rd ed. New York: CABI Publishing, 598p.

VAN DER KLIS, J. D., M.C. BLOK, 1997. Definitief systeem opneembaar fosfor pluimvee, CVB documentatierapport nr. 20, September 1997, Centraal Veevoeder Bureau, Lelystad.

VAN DER KLIS, J. D., H.A.J. VERSTEEGH, 1999. Phosphorus nutrition of poultry. pp 309-320 in: Garnsworthy, P.C. and Wiseman, J. (eds.) Recent Developments in Poultry Nutrition 2. Nottingham University Press., Nottingham.

WPSA, M. Rodehudscord, 2013. Determination of phosphorus availability in poultry. Worlds Poult. Sci. J. **69**, 687-698.
GUANIDINOACETIC ACID AS AN ADDITIVE TO BROILER DIETS

*J. Zelenka<fnref n="1" />, J. Heger<fnref n="1" />, C. de la Cruz<fnref n="2" />, V. Machander<fnref n="3" />, D. Hampel<fnref n="1" />*

**Abstract**

Guanidinoacetic acid (GAA) is the biochemical precursor of creatine, which, in its phosphorylated form, plays an impor-
tant role as a high-energy carrier in the muscle. An experiment was conducted to determine the response of broiler
chickens to GAA added to diets with different energy levels during fattening to 35 days of age. Ross 308 male chicks
were allotted to 10 treatments, each consisting of six replicates of 140 birds/pen. Five maize-soyabean meal isonitroge-
nous diets with decreasing AME<sub>n</sub> levels (100, 99, 98, 97 and 96 % of requirement) with or without supplements of 0.6
g/kg GAA were formulated. The criteria of response were feed intake, body weight gains, feed conversion ratio and
carcass, breast meat, leg meat and abdominal fat yields. Supplementation of broiler diets with 0.06 % GAA resulted in a
significant (P<0.05) decrease in voluntary feed intake. With decreasing AME<sub>n</sub> level, voluntary feed intake and conse-
quently amino acid intakes increased which was manifested by improved growth performance (P<0.01). GAA supple-
ments significantly (P<0.001) improved feed conversion ratio and efficiency of AME<sub>n</sub> utilization and significantly
(P<0.01) increased breast meat yield. With decreasing AME<sub>n</sub> level, the effects of GAA supplementation tended to dimin-
ish.

**Introduction**

Guanidinoacetic acid is formed from the amino acids glycine and arginine in the kidney or absorbed from the gut. It is transformed to creatine in the liver. Phosphocreatine serves as a dynamic reservoir of high energy phosphate. The phosphocreatine/creatinine system buffers ATP/ADP ratio for all energy consuming functions of the cell. The degradation of creatine results in creatinine, which is excreted in the urine. Therefore creatine must be continually replaced from dietary sources or synthesized de novo from GAA. In contrast to animal proteins, creatine is not found in plant feed-stuffs and may thus be deficient in all-vegetable diets. GAA as a creatine source is more stable and less expensive than creatine itself (BAKER, 2009).

The objective of the present experiment was to determine the response of broiler chickens to GAA (trade name CreAMINO®, Evonik Industries) added to all-vegetable diets ranging in AME<sub>n</sub> levels from 100 % to 96 % of requirement.

**Materials and Methods**

The experiment was conducted at the International Poultry Testing Station Ústrašice. A total of 8400 one-day-old male Ross 308 broiler chicks were randomly assigned to 10 dietary treatments. There were six replicates per treatment (140 chicks per pen). On days 10, 24 and 35, the chickens were weighed individually. At the same time, feed consumption per pen was recorded. On the last day of experiment, ten birds of each pen were slaughtered and carcass, breast meat (boneless and without skin), leg meat (without bone, with skin) and abdominal fat yields were determined.

Maize-soyabean meal starter (d 1 to 10), grower (d 11 to 24) and finisher (d 25 to 35) basal diets with different levels of metabolizable energy (100, 99, 98, 97 and 96 % of AME<sub>n</sub> requirement as suggested by Ross Nutrition Supplement, 2009) were formulated. To the basal diets serving as controls (Treatments 1 to 5), 0.6 g/kg of CreAMINO® containing a minimum of 96 % GAA was added thus forming five experimental diets (Treatments 6 to 10). The diets for each growing period were formulated to be isonitrogenous. Crumbled starter and pelleted grower and finisher diets were supplied ad libitum.

<footnote n="1">¹ Mendel University in Brno, Brno, Czech Republic</footnote>

<footnote n="2">² Evonik Industries AG, Hanau-Wolfgang, Germany</footnote>

<footnote n="3">³ International Poultry Testing Station, Ustrasice, Czech Republic</footnote>

<footnote>*Corresponding author: zelenka@mendelu.cz</footnote>
## Results and Discussion

The response of broiler chickens to guanidinoacetic acid is summarized in Table 1. As dietary AME<sub>n</sub> density decreased, feed intake in both control and GAA-treated chickens increased.

<table><caption>**Table 1.** Response of broiler chickens to guanidinoacetic acid</caption><thead><tr><th>Treatment</th><th></th><th>AME<sub>n</sub> level</th><th>Feed intake (g/day)</th><th>Weight gain (g)</th><th>Feed conversion ratio</th><th>Energy efficiency (kJ AME<sub>n</sub>/g WG)</th><th>Breast meat yield (% LW)</th></tr></thead><tbody><tr><td rowspan="5">Control</td><td>T1</td><td>100</td><td>98.72 <sup>a</sup></td><td>2055 <sup>a</sup></td><td>1.692 <sup>a</sup></td><td>22.31 <sup>a</sup></td><td>19.84 <sup>a</sup></td></tr><tr><td>T2</td><td>99</td><td>98.70 <sup>a</sup></td><td>2099 <sup>ab</sup></td><td>1.654 <sup>ab</sup></td><td>21.64 <sup>ab</sup></td><td>20.23 <sup>bc</sup></td></tr><tr><td>T3</td><td>98</td><td>100.12 <sup>a</sup></td><td>2125 <sup>bc</sup></td><td>1.658 <sup>ab</sup></td><td>21.46 <sup>bcd</sup></td><td>20.47 <sup>de</sup></td></tr><tr><td>T4</td><td>97</td><td>99.25 <sup>a</sup></td><td>2135 <sup>bc</sup></td><td>1.640 <sup>ab</sup></td><td>20.97 <sup>bcde</sup></td><td>20.67 <sup>ef</sup></td></tr><tr><td>T5</td><td>96</td><td>99.45 <sup>a</sup></td><td>2129 <sup>bc</sup></td><td>1.652 <sup>ab</sup></td><td>20.86 <sup>cde</sup></td><td>20.73 <sup>ef</sup></td></tr><tr><td rowspan="5">Guanidino-acetic acid</td><td>T6</td><td>100</td><td>96.90 <sup>a</sup></td><td>2088 <sup>ab</sup></td><td>1.630 <sup>c</sup></td><td>21.55 <sup>bc</sup></td><td>20.48 <sup>b</sup></td></tr><tr><td>T7</td><td>99</td><td>97.22 <sup>a</sup></td><td>2116 <sup>bc</sup></td><td>1.622 <sup>c</sup></td><td>21.13 <sup>bcde</sup></td><td>20.78 <sup>cd</sup></td></tr><tr><td>T8</td><td>98</td><td>98.03 <sup>a</sup></td><td>2132 <sup>bc</sup></td><td>1.618 <sup>c</sup></td><td>20.95 <sup>bcde</sup></td><td>20.61 <sup>de</sup></td></tr><tr><td>T9</td><td>97</td><td>99.60 <sup>a</sup></td><td>2157 <sup>c</sup></td><td>1.624 <sup>c</sup></td><td>20.83 <sup>de</sup></td><td>20.93 <sup>ef</sup></td></tr><tr><td>T10</td><td>96</td><td>97.27 <sup>a</sup></td><td>2121 <sup>bc</sup></td><td>1.617 <sup>c</sup></td><td>20.48 <sup>e</sup></td><td>20.69 <sup>f</sup></td></tr><tr><td colspan="2">Pooled SEM</td><td></td><td>0.890</td><td>18.4</td><td>0.0120</td><td>0.153</td><td>0.243</td></tr><tr><td colspan="2">Significance A<sup>1)</sup></td><td></td><td>0.012</td><td>0.218</td><td>&lt;0.001</td><td>&lt;0.001</td><td>0.003</td></tr><tr><td colspan="2">Significance B<sup>1)</sup></td><td></td><td>0.288</td><td>0.002</td><td>0.122</td><td>&lt;0.001</td><td>0.002</td></tr></tbody></table>

This response has been frequently observed in *ad libitum*-fed chickens (LEESON *et al.*, 1996). Except for the starting period, the effect of AME<sub>n</sub> level on feed intake in the present experiment was rather small and insignificant, possibly due to a narrow range of dietary AME<sub>n</sub> concentrations studied. On the other hand, the multiple linear regression analysis relating feed intake (FI, g/d) to AME<sub>n</sub> level (MEL, %) and AME<sub>n</sub> intake (MEI, kJ/d) for the whole experimental period yielded the following regression equation:

$$FI = 98.43 - 1.0038 \text{ MEL} + 0.0769 \text{ MEI}; P<0.001, R^2 = 0.999$$

All the model parameters were highly significant (P<0.001) and the R-squared statistic indicated that there was a close relationship between the variables. This finding suggests that the chickens were able, at least partly, to adjust their feed intake to meet their AME<sub>n</sub> needs. Furthermore, the GAA-treated chickens consumed less feed than their control counterparts, the differences being significant in all growing periods except for the first one. This response might have been due to the better energy utilization in chickens receiving the GAA-supplemented diets or a negative effect of GAA on voluntary feed intake. A similar effect was reported by MOUSAVI *et al.* (2013), even though the differences between GAA-treated and control groups were not significant (P = 0.09) in their study. GAA supplements also reduced feed intake in turkeys (LEMME *et al.*, 2010). In contrast, MICHIELS *et al.* (2012) found slightly higher feed intakes in chickens receiving supplements of 0.6 or 1.2 g/kg GAA as compared with the control birds. No effect of GAA on feed intake of broilers was observed by RINGEL *et al.* (2007).

The effect of GAA supplementation on body weights or weight gains was small and, except for the finishing period, the differences as compared to the control group were not significant. A greater response to GAA was observed at higher AME<sub>n</sub> levels. Growth rate increased quadratically with decreasing AME<sub>n</sub> level and reached maximum around 97 % of

<footnote><sup>a,b</sup> Means within a column not sharing a common superscript were significantly different. Tukey HSD test, P<0.05</footnote>

<footnote n="1">¹) A = GAA vs. control; B = AME<sub>n</sub> levels</footnote>
AME<sub>n</sub> requirement. Better growth performance at lower AME<sub>n</sub> intakes may be explained by higher feed consumption and consequently by higher intake of protein, amino acids and other nutrients. The response of control chickens to AME<sub>n</sub> level tended to be greater than that of GAA-treated chickens, but the difference between the linear slopes fitted to experimental data was not significant (P = 0.35).

Feed conversion ratio was not significantly affected by dietary AME<sub>n</sub> level, but it responded positively to GAA supplementation. Significant differences were found in the finishing period and for the whole experiment, but numerical improvements were also observed in the starting and growing periods. This is in line with the report by MICHIELS *et al.* (2012) who concluded that the GAA effect was most apparent in the finisher period, when weight gains were maximized. There are other studies demonstrating a positive effect of GAA on feed conversion (LEMME *et al.*, 2007, RINGEL *et al.*, 2008). Similarly to growth rate, the effect of GAA on FCR diminished with decreasing AME<sub>n</sub> level, but the slope of regression line was significantly different from zero only in the control group. In contrast to FCR, efficiency of AME<sub>n</sub> conversion was significantly improved by both GAA supplementation and AME<sub>n</sub> level. The effect was most apparent in the finishing period and at the highest AME<sub>n</sub> intake (Figure 1). In both groups, energy utilization significantly improved with decreasing AME<sub>n</sub> level (and consequently increasing feed and amino acid intakes). These results suggest that the ratio of amino acids to AME<sub>n</sub> in the present diets might have been underestimated.

Of the carcass analysis parameters, only breast meat yield was significantly affected by GAA supplementation. However, the magnitude of response was small. On average, the difference between control and GAA-treated groups was 0.4 % (20.4 vs. 20.7 %). RINGEL *et al.* (2007) and MICHIELS *et al.* (2012) reported a more pronounced effect of GAA on breast meat yield, which tended to increase with increasing dietary GAA level (RINGEL *et al.*, 2007). In contrast, no effect of GAA on carcass parameters was found in the study by MOUSAVI *et al.* (2013). As dietary concentration of AME<sub>n</sub> in the present experiment decreased, the percentage of breast meat increased, particularly in the control birds. The response pattern coincided with that of body weight which corroborates the well-known fact that breast meat yield is closely related to body or carcass weight (Ross 308 Broiler Performance Objectives, 2012).

The mechanism by which GAA affects broiler performance is not fully understood. Guanidinoacetic acid is a natural precursor of creatine, which is involved in cell energy metabolism, particularly in tissues with high and varying energy demand such as skeletal muscle (MICHIELS *et al.*, 2012). In fast-growing animals fed all-vegetable diets lacking creatine, GAA may restore creatine reserves, thus improving tissue energy metabolism and body growth. Another mode of action of GAA may be associated with amino acid metabolism. *In vivo*, GAA is synthesized from glycine and arginine and GAA supplementation may thus spare arginine, one of the potentially limiting amino acids in low-protein broiler diets (BAKER, 2009). Indeed, DILGER *et al.* (2013) showed that GAA supplementation markedly improved growth of chickens fed arginine-deficient casein-based diets.

<figure><img src="image_18.png" /><figcaption>**Figure 1.** Effect of GAA supplementation on AME<sub>n</sub> efficiency in chickens at five dietary AME<sub>n</sub> levels. Plotted from the equations y = -14.82 + 0.370x, R<sup>2</sup> = 0.62 (Control) and y = -3.878 + 0.253x, R<sup>2</sup> = 0.53 (GAA)</figcaption></figure>
In practical-type diets with moderate arginine deficiency, there was no growth response to GAA, but feed conversion was significantly improved. In accordance with the present study, these results suggest that feed conversion ratio is a more sensitive indicator of nutrient adequacy than growth rate in broilers.

References

BAKER D.H. (2009) Amino Acids, 37: 29–41.

DILGER R.N. et al. (2013) Poultry Science, 92: 171–177.

LEESON S. et al. (1996) Poultry Science, 75: 529–535.

LEMME A. et al. (2007) Proceedings of the 16th European Symposium on Poultry Nutrition, 335–338.

LEMME A. et al. (2010) Proceedings of the 4th Turkey Science Production Conference, 57–61.

MICHIELS J. et al. (2012) Poultry Science, 91: 402–412.

MOUSAVI S.N. et al. (2013) Journal of Applied Poultry Research, 22: 47–54.

RINGEL J. et al. (2007) Proceedings of the 16th European Symposium on Poultry Nutrition, 387–390.

RINGEL J. et al. (2008) Poultry Science, 87 (Suppl. 1): 72.

ROSS (2009) Nutrition Supplement, 23 pp.

ROSS (2012) 308 Broiler: Performance Objectives, 23 pp.
# EFFECTS OF DIFFERENT FEEDING STRATEGIES DURING REAR AND LAY ON INCUBATION TRAITS IN BROILER BREEDER FEMALES

R.A. van Emous<fnref n="1" />, R.P. Kwakkel<fnref n="2" />, and M.M. van Krimpen<fnref n="1" />

**Corresponding author:** rick.vanemous@wur.nl

## Summary

An experiment was conducted to investigate the effects of different dietary protein levels during rearing and dietary energy levels during lay on incubation traits of broiler breeders (BB). A 2 x 3 x 2 factorial design was used with 2 crude protein (CP) levels (high = CPh; low = CPI) during rearing; high, standard and low dietary energy levels (3,000 = MEh1; 2,800 = MEs1; 2,600 = MEI1) during the first phase of lay; and standard and high dietary energy levels (2,800 = MEs2; 3,000 = MEh2) during the second phase of lay. A total of 2,880 one-day old Ross 308 BB female chicks (36 pens) were followed until 60 wk of age. Starting at 28 wk of age, at a 5-wk interval, 150 eggs per pen were collected to determine incubation traits. Hatchability of set and fertile eggs (first phase) from CPI birds was increased compared to CPh birds due to a decreased embryonic mortality. No effects of energy level on incubation traits were found for the treatments during the first phase of lay. Birds fed the MEh2 diet showed, during the second phase of lay, an increased hatchability of fertile eggs, a decreased embryonic mortality, and a lower portion of second grade chicks compared to birds fed the MEs2 diet. It was concluded that a low CP diet during rearing positively affected incubation traits during the first phase of lay. An altered energy level during the first phase did not affect, whereas a higher energy diet during the second phase of lay showed positive effects on incubation traits.

**Keywords:** broiler breeder, rearing, laying, feeding strategies, incubation traits

## Introduction

An important factor for profitability in broiler breeder production is fertility and hatchability of hatching eggs. Fertility of hatching eggs declined from 88.8% in 2000 to 84.7% in 2005 (VAN EMOUS, 2010). As reviewed by YASSIN et al. (2008), this decrease in fertility may be caused by a wide range of factors such as strain, health status of the flock, egg size, egg weight, egg quality, egg storage duration and conditions, egg sanitation, season of the year, and age of the breeders. Besides these factors, nutrition plays a very important role on fertility and hatchability. A negative effect of a high daily crude protein intake (> 25 g/day) during the laying period on fertility or hatchability of eggs has been reported (PEARSON and HERRON, 1982; WHITEHEAD et al., 1985; LOPEZ and LEESON, 1995). A decreased hatchability of fertile eggs could be explained by an increased embryonic mortality (PEARSON and HERRON, 1982; WHITEHEAD et al., 1985). The objective of this study was to evaluate the effects of different dietary protein levels during rear and different dietary energy levels during lay on incubation traits of Ross 308 broiler breeder hens.

## Materials and methods

The effects of different dietary protein levels during rearing and different dietary energy levels during lay on body composition and reproduction were studied using a 2 x 3 x 2 factorial design with 2 CP levels (CPh = high protein; or CPI = low protein) during rearing between 2 and 22 wk of age; high, standard and low dietary energy levels during the first phase of lay between 22 and 45 wk of age (3,000, MEh1; 2,800, MEs1; and 2,600, MEI1, kcal/kg AME<sub>n</sub>, respectively); and standard and high dietary energy levels during the second phase of lay between 45 and 60 wk of age (2,800, MEs2; and 3,000, MEh2, kcal/kg AME<sub>n</sub>, respectively).

A flock of 3,000 Ross 308 female broiler breeder day-old chicks was allotted to 36 floor pens (4.5 x 2.5 m) in two identical climate controlled rooms. The experiment started at d 14 with 80 pullets per pen. Due to mortality, sex errors and culling (removing the smallest), the number of pullets was gradually reduced to 70 at 22 wk of age. Males were reared elsewhere and introduced into the pens at 22 wk of age. Starting at 28 wk of age, at a 5-wk interval, 150 eggs per pen from a 3 to 4 d production period were transported and set, after a 5 d storage period, in an incubator at a commercial hatchery. Eggs were candled on d 10 of incubation and clear eggs and dead in shell were opened to determine infertility.

<footnote n="1">¹Wageningen UR Livestock Research, PO Box 338, NL-6700 AH Wageningen, the Netherlands</footnote>

<footnote n="2">²Animal Nutrition Group, Department of Animal Sciences, Wageningen University, PO Box 338, NL-6700 AH Wageningen, the Netherlands</footnote>
and the timing of embryonic mortality by visual inspection (categorized in d 1 to 2 and d 3 to 9). At d 18, eggs were transferred to hatcher baskets and placed in a hatcher. At d 21 of incubation, unhatched eggs were calculated and scored as d 10 to 21 embryonic mortality. All chicks were graded as first or second grade chicks. Fertility was calculated as the percentage of fertile eggs of the set eggs. Hatchability of set and fertile eggs was calculated as the percentage of first grade chicks hatched of set and fertile eggs, respectively. Embryonic mortality was calculated as a percentage of fertile eggs. Second grade chicks were calculated as a percentage of total hatched chicks.

## Results and discussion

Fertility during the first phase of lay was not affected by the CP diets during rearing (Table 1). However, hatchability of set eggs and fertile eggs from CPI birds were increased compared to CPh birds due to a decreased embryonic mortality between d 10 to 21 of incubation. The portion of second grade chicks during the first phase of lay was not affected by the dietary protein level during rearing.

<table><caption>**Table 1.** Incubation traits during the first phase of lay (22 to 45 wk of age) as affected by dietary protein level during rear and dietary energy level during the first phase of lay.</caption><thead><tr><th rowspan="2">Source</th><th rowspan="2">Fertility (%)</th><th rowspan="2">Hatch of set eggs (%)</th><th rowspan="2">Hatch of fertile eggs (%)</th><th colspan="3">Embryonic mortality (%)</th><th rowspan="2">2<sup>nd</sup> grade chicks (%)</th></tr><tr><th>1 to 2 d</th><th>3 to 9 d</th><th>10 to 21 d</th></tr></thead><tbody><tr><td colspan="8"><strong>Protein rear</strong></td></tr><tr><td>CPh</td><td>96.5</td><td>87.7<sup>b</sup></td><td>91.1<sup>b</sup></td><td>1.1</td><td>2.2</td><td>5.1<sup>a</sup></td><td>0.5</td></tr><tr><td>CPI</td><td>96.7</td><td>89.0<sup>a</sup></td><td>92.2<sup>a</sup></td><td>1.1</td><td>2.0</td><td>4.2<sup>b</sup></td><td>0.7</td></tr><tr><td>SEM</td><td>0.3</td><td>0.5</td><td>0.3</td><td>0.1</td><td>0.2</td><td>0.2</td><td>0.1</td></tr><tr><td colspan="8"><strong>Energy lay 1</strong></td></tr><tr><td>MEh1</td><td>96.9</td><td>88.7</td><td>91.7</td><td>1.1</td><td>2.0</td><td>4.7</td><td>0.6</td></tr><tr><td>MEs1</td><td>96.6</td><td>88.4</td><td>91.6</td><td>1.1</td><td>2.2</td><td>4.4</td><td>0.8</td></tr><tr><td>MEI1</td><td>96.3</td><td>88.0</td><td>91.6</td><td>1.1</td><td>2.0</td><td>5.0</td><td>0.5</td></tr><tr><td>SEM</td><td>0.4</td><td>0.6</td><td>0.4</td><td>0.1</td><td>0.2</td><td>0.3</td><td>0.1</td></tr><tr><td colspan="8"><strong>P-value</strong></td></tr><tr><td>CP</td><td>0.54</td><td>0.05</td><td>0.02</td><td>0.82</td><td>0.57</td><td>0.01</td><td>0.37</td></tr><tr><td>ME1</td><td>0.56</td><td>0.62</td><td>0.93</td><td>0.94</td><td>0.83</td><td>0.38</td><td>0.34</td></tr><tr><td>CP x ME1</td><td>0.12</td><td>0.10</td><td>0.54</td><td>0.08</td><td>0.31</td><td>0.09</td><td>0.61</td></tr></tbody></table>

It was hypothesised that the positive effects on incubation traits were caused by the different body compositions at the end of the rearing period. The increased abdominal fat pad (1.3 vs. 0.7%) and decreased breast muscle (17.4 vs. 20.2%) of the pullets at 22 wk of age fed the CPI diet decreased embryonic mortality of the offspring between d 10 and 21 of incubation of 0.9% during the first phase of lay. HOCKING et al. (2002) and VAN EMOUS et al. (2013) did not find any effects on incubation traits when pullets received different dietary protein levels during rearing. The explanation of the positive effects of changed body composition (more abdominal fat and less breast muscle) of the CPI birds on lower embryonic mortality in the current study is unclear.

No effects of different dietary energy levels during the first phase of lay were found on incubation traits during the first phase of lay (Table 1).

During the second phase of lay, birds fed the MEh2 diet showed an increased hatchability of fertile eggs (90.0 vs. 88.5%), a decreased embryonic mortality (8.4 vs. 9.7%) and a lower portion of second grade chicks (1.7 vs. 2.3%) compared to birds fed the MEs2 diet. No effects on fertility and hatchability of set eggs were found for the treatments during the second phase of lay. A high energy diet (and as a consequence a 10% lower daily CP/AA intake) resulted in no effects on fertility but improved hatchability of fertile eggs, which in turn was caused by decreased embryonic mortality between d 3 to 21 of incubation. This is in agreement with the studies of PEARSON and HERRON (1982) and WHITEHEAD et al. (1985). LOPEZ and LEESON (1995) observed an increased fertility and hatchability of set eggs and

<footnote><sup>a-b</sup> Means within a column and within a source without a common superscript differ significantly (P < 0.05)</footnote>
lower embryonic mortality when birds received a lower daily CP intake during the entire laying period. The improved incubation traits in the current study probably also positively affected the quality of the embryos resulting in a lower number of second grade chicks. This was previously underlined by PEARSON and HERRON (1982) who found that the portion of dead and malpositioned embryos could be reduced if daily protein intake was decreased from 27.0 to 21.3 g protein per animal per day.

## Conclusions

A low-protein diet fed to breeder pullets during the rearing period resulted in positive effects on incubation traits during the first phase of lay. Changing the dietary energy level compared to the standard (2,800 Kcal/kg) during the first phase of lay did not affect incubation traits whereas a high-energy diet (3,000 vs. 2,800 Kcal/kg) during the second phase of lay resulted in positive effects on incubation traits.

## Literature

HOCKING, P.M., R. BERNARD, G.W. ROBERTSON, 2002: Effects of low dietary protein and different allocations of food during rearing and restricted feeding after peak rate of lay on egg production, fertility and hatchability in female broiler breeders. Br. Poult. Sci. **43**, 94-103.

LOPEZ, G., S. LEESON, 1995: Response of broiler breeders to low-protein diets. 1. Adult breeder performance. Poult. Sci. **74**, 685-695.

PEARSON, R.A., K.M. HERRON, 1982: Effects of maternal energy and protein intakes on the incidence of malformations and malpositions of the embryo and time of death during incubation. Br. Poult. Sci. **23**, 71-77.

VAN EMOUS, R.A., 2010: Innovative housing in broiler breeder production. Pages 37-44 in Proc. 2nd Int. Symp. Highlights in Nutr. and Welf. in Poult. Production, Wageningen, the Netherlands. Animal Science Group, Lelystad, the Netherlands.

VAN EMOUS, R.A., R.P. KWAKKEL, M.M. VAN KRIMPEN, W.H. HENDRIKS, 2013: Effects of growth patterns and dietary crude protein levels during rearing on body composition and performance in broiler breeder females during the rearing and laying period. Poult. Sci. **92**, 2091-2100.

WHITEHEAD, C.C., R.A. PEARSON, K.M. HERRON, 1985: Protein requirements of broiler breeders fed diets of different protein content and effect of insufficient protein on the viability of progeny. Br. Poult. Sci. **26**, 73-82.

YASSIN, H., A.G.J. VELTHUIS, M. BOERJAN, J.W. VAN RIEL, R.B.M. HUIRNE, 2008: Field study on broiler eggs hatchability. Poult. Sci. **87**, 2408-2417.
# SOLID-STATE FERMENTED CEREALS PROMISES A GROWTH PROMOTING EFFECT IN BROILER CHICKEN

S. Yasar

Dept. of Animal Science, Suleyman Demirel University, Isparta Turkey

Corresponding author: sulhattinyasar@sdu.edu.tr

## Abstract

Effects of 40-50% dried wheat, barley and oats grains fermented with liquid whey and citrus pomace at 35 °C and 60-70% moisture for 8 h were tested from day 1 to day 42 on bird's performance, carcass yield, digestive organ development, intestinal viscosity and pH. In comparison to the control diets, feed intake (FI) increased with all fermented grain-based diets by 0.3%, weight gain (WG) by 5.6% and feed conversion ratio (FCR) by 4.7%. Significant improvements in WG (9%) and FCR (8.2%) were obtained from fermented barley based diet. Carcass yield was significantly higher in fermented wheat and oats diets than their control diets. Marked reductions in both digesta viscosity and in number of birds with sticky droppings were seen with all fermented grain based diets; this effect was more pronounced for the fermented barley. Birds fed on the diets with fermented feeds had lighter and shorter digestive tract than those on the unfermented feeds. Duodenum length significantly reduced, and liver weight increased by fermented feeds. In short, this fermentation method improved nutritive value of cereals for broiler chicken. The improved FCR and WG as well as marked reduction in viscosity by fermentation indicate a growth stimulating effect in broilers.

**Keywords:** broilers, fermented cereals, solid-state, whey, citrus pomace

## Introduction

Performance impairments are inevitable in poultry species fed with the diets of high levels of cereal grains (YASAR and FORBES, 1999). Wetting (YASAR and FORBES 1999) or fermenting (ENGBERG et al., 2009; UCHEWA and ONU, 2012) cereal grains or their diets improved FCR, increased WG, reduced viscosity, degraded non-starch polysaccharides (NSP), increased concentration of DL-lactic acid and lactic acid bacteria counts in the gut, increased digestibility of nutrients, improved activities of exogenous NSP-degrading enzymes. Feeding moisturised diets after several hours of fermentation with or without microbial inoculant or simply soaking in water are not considered as practical feeding tool in commercial poultry production. A suitable (cost-effective) drying process is required after fermentation in order to yield a sustainable beneficial effect in poultry nutrition. Furthermore, an appropriate (easy-made) and suitable (cost-effective) fermentation method needs to be developed. Therefore, a short period of fermentation (maximum 8 hours) with the use of non-microbial inoculants and some agricultural wastes (whey and citrus pomace), followed by a drying process below 30 °C were tested in this study.

## Material and Methods

An in-house solid state fermentation (SSF) system was used to produce the fermented grains. 1 part of ground (3 mm) wheat, barley and oats grains were soaked in 1.1, 1.1 and 1.2 parts of fresh liquid whey, respectively; to provide a 60 to 70% of moisture. Temperature was set at 35 °C, and pH of material was set under a pH of 5.0 by addition of citrus pomace (inhibition of pathogens). A pH of 4.2 for wheat grain and 4.5 for both oats and barley grains were achieved by the addition of 1 (w/w) and 2.3 % citrus pomace, respectively. The final product at the end of 8 h was dried out at room temperature for 2 days and ground (5 mm). Isocaloric and isonitrogenous diets were formulated with 45-50% of unfermented and fermented grains. A 378 of 1 d-old Ross chicks were equally distributed to 18 floor pens. Each of the 6 diets was offered to the chicks of 3 pens for 42 days. FI, BW (body weight), WG and FCR were recorded weekly. Three birds from each pen at 21 d and all birds at 42 d were killed to collect the data for digestive organ developments, digesta viscosity and carcass quality. A factorial model of analysis of variance, 3x2 (grains by fermentation), was used to statistically analyse all the data. Significant differences between the means of groups were properly separated.

## Results

Inclusion of high level of unfermented wheat in broiler diet increased FI and caused a high FCR as compared to the diet with fermented wheat with which significantly reduced FI and improved FCR with the same final BW were achieved (Table 1).
<table><caption>**Table 1.** Performance of broiler chickens at 42 days on the diets based on fermented (F) and unfermented (U) wheat, barley and oats grain (means with SEM).</caption><thead><tr><th rowspan="2">Diet</th><th colspan="2">Wheat</th><th colspan="2">Barley</th><th colspan="2">Oats</th><th rowspan="2">SEM</th></tr><tr><th>U</th><th>F</th><th>U</th><th>F</th><th>U</th><th>F</th></tr></thead><tbody><tr><td>BW (day 1) 1d, g/b</td><td>56.0</td><td>55.9</td><td>55.9</td><td>56.6</td><td>56.6</td><td>55.2</td><td>0.50</td></tr><tr><td>BW (day 42) 42d, g/b</td><td>2856.0a</td><td>2884.0a</td><td>2675.0b</td><td>2916.6a</td><td>2274.5c</td><td>2435.0d</td><td>52.0</td></tr><tr><td>FI (day 42), g/b</td><td>4715.5a</td><td>4446.2b</td><td>4481.9b</td><td>4485.3b</td><td>3856.2c</td><td>4140.4d</td><td>75.0</td></tr><tr><td>FCR (day 42)</td><td>1.68a</td><td>1.58b</td><td>1.71a</td><td>1.57b</td><td>1.74a</td><td>1.74a</td><td>0.03</td></tr><tr><td>Carcass yield, %</td><td>70.1a</td><td>72.5b</td><td>70.3a</td><td>69.6ad</td><td>66.0c</td><td>68.5d</td><td>0.5</td></tr></tbody></table>

The use of fermented barley did not influence FI as compared to the unfermented barley. But, a significant increase in BW and improvement in FCR was obtained from the diet of fermented barley. The use of unfermented oats significantly reduced FI, BW and FCR, whereas the fermented oats increased FI and BW with no change in FCR. Carcass yield was significantly high with the diet of fermented wheat and worse with the diet of unfermented oats.

A viscous gel-forming constitute is present in the intestine of young broiler chicken when fed with high levels of unfermented cereal grains (Figure 1). A marked reduction both in viscosity of ileal contents and in the number of birds with sticky droppings was observed with the fermented grain-based diets both at 21 and 42 days (Figure 1). Reduction in viscosity was better with fermented barley. Weight (227 vs 193 g/b) and length (200 vs 187 cm/b) of digestive tract were reduced by the use of fermented cereal grains. Liver weight was high with the use of fermented barley and oats based diet. All changes were well correlated with the WG and FCR values under the effect of fermentation.

## Conclusions

The results indicated that a SSF process (35°C of substrate temperature, pH of between 4.0 and 5.0, with the use of whey and citrus pomace and no microbial inoculants) of cereal grains followed by drying at room temperature provided an effectual functional property. In a similar study, CARLSON and POULSEN (1999) reported significant degradation of phytic acid, increased enzyme activities, nutrients enrichment (crude protein), increased lactic acid bacteria and lactic acids with fermentation. Reduced digesta viscosity and an efficient gut function by fermentation of cereals were parallel to improvements in FCR and WG in broilers in the present case. All these were good indicators of effectual functional properties gained under a SSF.

<figure><img src="image_19.png" /><figcaption>**Figure 1.** Changes in viscosity (cPs) of ileal contents in broilers at 21 and 42 d old.</figcaption></figure>

Using whey, instead of water, during SSF in the presence of citrus pomace and in the absence of any microbial inoculants had an added value for a valuable end product (FORBES and SHARIATMADARI, 2005; ALBORES et al., 2009; YASAR and GOK, 2014). Due to a suitable drying process (room temperature) it can be speculated that the end product may still have an appreciable amount of living microbes beneficial to the animals, as several other researchers reported such enrichment.