1. Introduction
Tannins are plant secondary metabolites and represent the fourth most abundant group of secondary compounds of the plant kingdom, after cellulose, hemicellulose, and lignin [
1]. Tannins are polyphenolic compounds, located mainly in vacuoles of the vegetal cell or in waxes, where they do not interfere with plant metabolism. They are found in many parts of the plant, such as fruits, leaves, bark, and wood [
2], and in common foodstuffs, for example grapes, strawberries, blackberries, hazelnuts, cocoa, guarana. Feed such as sorghum grains, peas, fava beans, or legume trees like
Acacia sp.,
Sesbania sp. also contain tannins [
2,
3], as well as acorns (
Quercus spp.) and chestnuts (
Castanea sativa), as spontaneous fruits of wood forest, chiefly for wild mammals and birds, but also domestic species [
4,
5,
6]. Tannins exert various beneficial functions for the plant, depending on the tissue where they are found, such as regulating dormancy of seeds, contrasting pathogens acting as chemical barriers in roots and seeds, opposing predation of unripe fruits and leaves or preservation of the heartwood of conifers [
2,
3]. In some cases, tannins also attract insects towards flowers, thus helping in cross-pollination [
7,
8].
Tannins belong to a heterogenous group of phenolic compounds, with different chemical structures but with a high affinity to bind and precipitate proteins. Tannins are mainly classified into three major groups: hydrolysable tannins, condensed tannins or proanthocyanidins, and phlorotannins. The first two groups are found in terrestrial plants, whilst phlorotannins are found in marine brown algae [
9,
10]. Hydrolysable tannins are susceptible to hydrolysis by acids, bases or esterases, being easily degraded and absorbed in the digestive tract of mammals and birds [
11,
12]. Condensed tannins are oligomeric or polymeric flavonoids with complex structures and high molecular weights. In contrast to hydrolysable tannins, only strong oxidative and acidic hydrolysis can depolymerize the condensed tannin structures that are also not susceptible to anaerobic enzyme degradation [
13]. Among the condensed tannin sources tested in poultry diets, we can find grape seed extract [
14,
15,
16], grape pomace [
16,
17], mimosa [
18] and Quebracho [
19,
20,
21].
The phenolic structure of tannins is responsible for the antioxidant activity, which finds application in different fields, such as food industry and animal feeding, medical and pharmaceutical sectors [
22]. In view of such technological and biological properties, tannins are considered an attractive family of chemicals, due to their various application potentials in different fields. Nevertheless, the study of the nutritional effects of tannins is complicated by the large chemical diversity [
23], and consequently the bird’s responses may vary greatly. For instance, tannins were reported to act as anti-nutritional compounds in poultry diets, affecting productive performance due to a decrease in the feed intake and the digestibility of organic matter [
24,
25]. In contrast, it has been shown that depending on the bird’s age, health and physiological status, beneficial effects might be obtained by combining a specific tannin group in the diet. In this regard, a positive influence on chicken growth performance [
26], improved final body weight and feed efficiency in broilers [
27], reduced cholesterol level in Leghorn hens eggs [
28], potential anticoccidial agent in broilers [
19] and anthelmintic activity in pheasants [
20] were reported in the reference literature.
Between the period 1998 and 2018, the global duck meat production expanded significantly, from 2.62 to 4.46 million tons, respectively [
29]. Asia is the main global producer, accounting for 83.0% of the total duck meat output, followed by Europe, with 11.7% in 2018 [
29]. The rearing of ducks follows different production systems. In developed countries for example, they are mainly reared intensively, while in Asia extensive production is largely applied [
30]. Within duck species, the Muscovy duck (
Cairina moschata domestica, Linnaeus, 1758.) represents an important economic resource. Central and South America represent the origin of this species, but currently Muscovy duck production is located mainly in Europe, with France as the first producer, together with southeast Asia and Taiwan [
31]. Muscovy ducks are omnivorous birds, and the natural diet is based on worms, insects, fish, amphibians, reptiles, plants, and fruits [
32]. For this reason, tannins, being widely distributed in the plant kingdom, might reasonably be part of their natural diet. Quebracho tannin (
Schinopsis sp.) as a biologically active compound has been documented in pheasants and chickens [
20,
21], but limited information is available about the effects in the diet of Muscovy ducks. Therefore, the aim of the present study was to evaluate the effect of two inclusion levels of purified Quebracho tannin (QT) in the diet of slow-growing male Muscovy ducks on growth and production performance.
4. Discussion
The increasing interest in the use of some plant-derived molecules with biological properties offers the chance to exploit several beneficial effects due to their numerous properties [
9,
42]. Against this background, more information seems to be needed about their safe use in different species, to achieve the desired effects. From this perspective, and due to previous experiences in pheasant [
20] and pullets [
21], the maximum safe QT level to be used in diets for 42 to 84-d old Muscovy ducks was set to 2.5%, on an as-fed basis. At this QT amount, no adverse effects were observed in birds of this trial, as supported by the TBP levels and liver weight. On the contrary, in a previous study involving slow-growing pullets [
21], adverse effects were observed in 35-d old birds fed 3% dietary tannins supplementation, resulting in 2% of QT as the safe inclusion level. It is widely known that tannins bind and precipitate proteins, which compromises absorption at intestinal level. This situation might lead to protein deficiency in the bloodstream [
9]. Ducks in this study fed on QT diets did not exhibit a decrease in TBP circulating value. Additionally, our results agree with those obtained by Gariglio et al. [
43] in 50-d old female Muscovy ducks.
As to liver, weight variations can be useful signs of the presence of hepatic injuries [
44]. In this trial, liver weights in QT birds were similar across birds from all experimental groups, at each QT inclusion rate tested. Furthermore, at the end of the experimental period, birds of QT1.5 and QT2.5 groups reached a similar LBW at slaughter. As demonstrated also by the growth curve trends, which were almost identical, it can be stated that the tested amounts of QT included in the diet did not negatively impact the production performance of slow-growing male Muscovy ducks. In agreement with other authors, who reported duck’s growth curves using Gompertz model [
45,
46], we also found this model as the best fitting in our trials (R
2 = 0.98–0.99).
According to the QT inclusion levels tested, a different reaction in birds was noted regarding feed intake. Birds of the QT1.5 group needed a longer time to get used to the change in diet, as demonstrated during the first days after dietary QT inclusion with an evident decrease in the ADWG and ADFI. Birds of the QT2.5 group, instead, seemed to cope with the QT by increasing the ADFI, which was higher during the whole experimental period. Such differences in response to different levels of dietary QT inclusion might be explained by the natural feeding behavior of the Muscovy duck, for which a large part of foraging activity takes place in fresh water [
32]. In captivity, when ducks find a hard, unusual or an unknown tasty food, they use to soak it into water in order to render it “eatable”. It could be argued that such behavior of soaking feeds was performed with the purpose of expressing the innate feeding behavior. With the increasing QT, the feed taste becomes reasonably astringent and birds tended to put the feed into the water with a consistent higher consumption. In QT1.5 group, instead, astringency perception presumably following a lower QT inclusion amount, might have not led birds to adopt coping solutions, for which a lower feed intake was also observed. Elkin et al. [
47] reported no growth depression in ducks fed sorghum rich in tannins. Same authors also suggested that the innate feeding behavior of ducks could be a key factor in the interpretation of such a response.
In this trial, the FCR calculated throughout the experimental period and the final LBW were not affected by dietary QT at both tested levels. However, in QT1.5 birds, an initial retarded growth occurred, with a successive compensatory growth, evident especially during the last 15 days (70–84). This compensatory growth trend was also reported by other authors in broilers reared under feeding restriction, followed by ad libitum feed provision [
48]. A decrease in growth rate, lower LBW, lower ADFI and higher FCR were reported in male Muscovy ducks fed low- or high-tannin-sorghum diets [
49]. These authors also reported no differences in these parameters in Muscovy males fed on diets 50/50 high/low tannin-sorghum enriched with L-Methionine, attributing the reduction in the negative effect of tannin on protein availability to this amino acid.
Unexpectedly, the use of dietary QT did not lead birds to excrete dryer droppings as observed in other bird species, namely chickens [
21] and pheasants [
20], but rather the opposite effect could be observed. This result might be attributed to the high daily water intake in ducks, which did not allow the QT to have a “drying” effect. As some authors reported, 800 ml/d was the water intake in 14 to 42-d old Pekin ducks [
50], while in 20-week old White Leghorn hens the intake was 228 ml/d [
51], thus, threefold lower than the intake in ducks.
The dietary QT did not negatively affect carcass traits in 84-d old male ducks, rather, it led to improved yields in both the hot and chilled RCC of QT birds, which was heavier than QT0. Higher RCC yields were also reported in male Muscovy ducks of the same strain [
52], fed on diets with 50/50 high/low tannin-sorghum [
48]. In slow-growing chickens, instead, the RCC yield pointed out no differences [
21], as well as in broiler chickens [
26] and in female pheasants [
20].
Wild birds feeding on diets rich in tannins developed larger intestines and caeca, and heavier gizzards [
53], however, this could be also induced by a different physical form of natural feeding sources, rich also in more fibrous nutrient content [
54]. In this trial, small intestine length was influenced by the diet. Nevertheless, this influence resulted in the opposite to what we would have expected, with QT1.5 birds having a shorter small intestine. In contrast, no effect was observed in growing female pheasants after a 60-d QT diet [
20], and longer small intestine length after a 4-week trial in adult grey partridges was observed by Liukkonen-Anttila et al. [
53]. Further research is needed to clarify this result.