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Phytogenic pigments in animal nutrition: Potentials and risks

Article  in  Journal of the Science of Food and Agriculture · September 2015

DOI: 10.1002/jsfa.7478

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Received: 27 January 2015 Revised: 23 July 2015 Accepted article published: 29 September 2015 Published online in Wiley Online Library: 5 November 2015

(wileyonlinelibrary.com) DOI 10.1002/jsfa.7478

Phytogenic pigments in animal nutrition:

potentials and risks
Bettina Faehnrich,* Brigitte Lukas, Elke Humer and Qendrim Zebeli

Abstract
Phytogenic pigments are secondary plant compounds responsible for coloring effects in plant tissues. In particular, phenolic
flavonoids and terpenoid carotenoids, but also rare compounds like curcumin and betalain, form this group of biochemical
agents used in animal nutrition. From the perspective of ecological mutuality between plants and animals, these compounds are
of crucial importance because they serve as visual attraction for herbivores but also signal nutritional and/or health-promoting
values. This review focuses on the properties of phytogenic pigments which are likely to impact feed intake and preferences
of livestock. Also natural prophylactic and/or therapeutic properties and, in particular, the potential of pigments to enhance
quality and health value of animal products for human consumption are important issues. Nevertheless, reasonable limits of use
due to possible adverse indications have been suggested recently. Pathways of digestion, metabolism and excretion in animals
play a crucial role not only in the evaluation of effectiveness but also in the prediction of potential risks for human consumption.
The popularity of natural feed additives is growing; therefore, more research work is needed to better understand metabolic
pathways in the animal’s body and to better estimate the potentials and risks of pigmenting plant compounds used in animal
nutrition.
© 2015 Society of Chemical Industry

Keywords: plant pigments; phytogenic; animal nutrition; feed additives

INTRODUCTION PHYTOGENIC PIGMENTS IN ANIMAL

Phytogenic pigments may be defined as natural compounds
apparent in plants reflecting a part of the light spectrum, vis-
ible as color. Plant-derived pigments may be differentiated by
forming groups with similar chemical structures. According to this
approach, Bertram (1989) treats carotenoids, chinones, indigoids,
melamines, oxacine and phenacine colorants, pteridines, flavonoids,
anthocyans and tetrapyrrolic pigments as distinct groups.1 From
a different point of view, allocations can be set according to
the localization in plant structures. Plasmochromic pigments are
hydrophobic and located in plastids; chymochromic pigments are
hydrophilic and will be found in vacuoles; membranous pigments
are present in cell walls.2,3
Intentional use of plant pigments in animal nutrition is mainly
known for the huge group of phenolic compounds called
flavonoids and of the tetra-terpenoid carotenoids.3 Little doc-
umentation exists of the use of betalain, the red color of beetroot,
or of curcumin, the yellow color of turmeric.4,5 This review will
focus on phytogenic pigments used in animal nutrition and
will therefore exclude groups without documented use in feed,
like chinones or chlorophyll. On the other hand, it will also
exclude secondary compounds chemically and functionally sim-
ilar to colorants but with colorless appearance like phenolic
acids or hydrolyzable tannins. However, in some cases effects
cannot be distinguished between humans and animals and
will therefore be treated equally. Moreover, in some cases an
exact border cannot be defined between feed additives with
health-promoting effects and therapeutic, plant pigment-derived
agents. Thus the latter will also be mentioned as examples for
1420
NUTRITION
Flavonoids
Biosynthesis of flavonoids in plants starts from the amino acid
phenylalanine and ends in three main sinks of the metabolic
flux: flavones, anthocyanins and proanthocyanidins or condensed
tannins.6 The basic chemical structure consists of a C15 -frame with
two aromatic rings connected by a third O-including ring (I).7 The
biosynthetic pathway includes various branches, intermediates
and side products. The apparent color of the respective compound
depends on various factors like primary and secondary structures,
pH value, co-pigmentation and metal complexation.8 To provide
color to plant regions (e.g. flowers, fruits or stems) flavonoids
accumulate in vacuoles of plant cells or in cell walls, like the
membranochromic quercetin.3,9 However, the color is only one of
the favorable characteristics of these secondary plant compounds
applied in animal nutrition.
Yellow flavonoid pigments: in particular, chalcones, aurones,
flavones and flavonols
Chalcones, aurones, flavones and flavonols (II, III, IV, V) are pale yel-
low to orange pigments of plant tissues hardly visible to humans
∗ Correspondence to: Bettina Faehnrich, Institute of Animal Nutrition and Func-
tional Plant Compounds, Department for Farm Animals and Veterinary Pub-
lic Health, University of Veterinary Medicine Vienna, Veterinaerplatz 1, 1210
Vienna, Austria. E-mail: bettina.faehnrich@vetmeduni.ac.at
Institute of Animal Nutrition and Functional Plant Compounds, Department for
Farm Animals and Veterinary Public Health, University of Veterinary Medicine

effects. Vienna, 1210, Vienna, Austria

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Phytogenic pigments in animal nutrition www.soci.org

Table 1. Scientific documentation of flavonoid use in animal nutritiona

Flavonoid source Animal category Intended effect Source Year

Polyphenolic tannins Ruminants Amelioration of bloat Davies14 2004

Quercetin–aglycon Pigs Prevention of chronic Bieger et al.86 2008
diseases
Parsley, buckthorn, mint, n.s. n.s. Misan et al.122 2010
caraway, birch
Pineapple rind meal Etawah dairy goats Enhancing milk quality Mardalena et al.72 2011
Matricaria chamomilla Japanese quails Protection against negative Skalicka et al.15 2011
cadmium effects
Soybean n.s. Regulation of immune and Zhang et al.123 2011
endocrine system
Quercetin–aglycon, rutin Non-lactating cows Enhancing, stabilizing Berger et al.42 2012
animal performance
Asteracantha longifolia n.s. n.s. Dash et al.113 2012
Pseudolachnostylis n.s. n.s. Motlhanka114 2012
maprouneifolia
‘Bioflavex’ supplement Cattle Stabilizing rumen Serra et al.60 2013
fermentation, reducing
acidosis
Propolis Nellore heifers Greater idleness during the Geron et al.16 2014
day
Phenolic herb components Cattle Decrease of ruminal Leiber22 2014
methane production
a Excluding animal experimental models for human medicine.

but nevertheless playing an important ecological role for pol-
linating insects.10,11 Moreover, their contribution to flower pig-
mentation can be of importance as they are able to modu-
late anthocyanin color due to interactive co-pigmentation or in
co-occurrence with carotenoids.9 Yellow flavonoid pigments are
also mentioned as a UV absorbent and therefore are important for
insects attracted by colors visible in UV light. The most widespread
flavonol is probably quercetin and its derivatives, present not only
in the inner bark of Quercus tinctoria (black oak) but also in many
edible fruits and herbs.7,12 – 14 Also, the yellow flavone apigenin
is used for numerous protective and health-promoting effects in
farm animals (Table 1).15,16
Red to blue flavonoid pigments or anthocyanins
Anthocyanins (VI) are the most variable flavonoid pigments in
plant material. Slight chemical differences cause the variability in
color. The degree of oxygenation and the absence/presence of
different functional groups at distinct positions of the aromatic
rings affect the color characteristics. Even the pH of the surround-
ing solution plays a crucial role in color expression: the higher
the pH, the bluer is the plant material.13 Nevertheless, this blue
anthocyanic color would be rather instable unless stabilized by
co-pigmentation or complexation with metals.8,9,17 Health ben-
efits arising from anthocyanins are known in human and ani-
mal nutrition, including antioxidant and anti-inflammatory prop-
erties. Moreover, their utility as a natural food colorant is becoming
increasingly important.18
Dark flavonoid pigments or condensed tannins
Pigments causing the dark color in woody plant material or in
seed coats are flavonoid polymers and called proanthocyanidins,
because they can be hydrolyzed to anthocyanidins. These con-
densed tannins are colorless in living plant material, but turn dark
their ability to act as an antimicrobial and antifungal agent and
their affinity to bind proteins and consequently alter their biolog-
ical effects, they are of high economic importance in animal nutri-
tion, in particular in ruminants.19 They are polymers of catechin
(VII) or epicatechin and should not be confused with hydrolyz-
able tannins, which are esters of phenolic acids and sugars. Both
kinds of tannins show the special protein-complexing properties,
but hydrolyzable tannins are not colored and therefore will not be
treated in this review.3,6,18
Carotenoids
Providing distinctive and intensive yellow to red colors in plant
tissues and aromas, and owing to their function as a protector
from photo-damage by an excess of UV light, the tetra-terpenoid
carotenoids (e.g. 𝛼-carotene, VIII) play an important role in human
and animal nutrition. The hydrophobic molecules are located in
lipid globules of the plastids or in cell walls and can be transported
into different tissues of herbivores.17,20 – 22 Table 2 provides an
overview of reports of carotenoid sources and effects in animals
after their supplementation in the diet.
Rare colorants (betalains, curcumin)
Betalains
Deriving from betalaminic acid (IX), two different forms of
water-soluble betalains exist: (i) betacyanins, as reddish forms
(in beetroot, Beta vulgaris); and (ii) betaxanthins, as yellow forms
(in Opuntia ficus-indica). Like the anthocyanins, betalains are
hydrophilic and located in the vacuoles, but in contrast to them
they are alkaloid-like and contain nitrogen.2,17 Betalains are
known to have antioxidant properties, but are also known to
cause beeturia (excretion of betalains in the urine and feces).23
The designated use as a feed additive is very limited. Studies of
their use in ornamental fish displayed no effect on skin color or
1421

upon oxidation and desiccation. Because of their astringent taste, lightness, but suggested a certain color maintenance property.4

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Table 2. Scientific documentation of carotenoid use in animal nutritiona

Carotenoid source Animal category Intended effect Source Year

Bixa orellana Poultry Increase in pigmentation of egg Reggianini et al.124 1978

yolk and skin
Tagetes flowers n.s. Not defined Czygan and Kruger125 1981
Cassava residue Laying hens Intensity of yolk color decreased Garcia et al.65 1994
Paprika Goldfish, Koi carp Increase in red color intensity Hancz et al.66 2003
Plant-derived carotenoids Birds and fish Coloring egg yolks and fish flesh Davies14 2004a
Plant-derived carotenoids Marine invertebrates Generating vivid colors, Davies14 2004a
including blues and greens
Synthetic astaxanthin Dwarf gourami Increase in red coloration Baron et al.4 2008
Natural carotenoids Fish Intensifying color of flesh and Yesilayer et al.68 2008
skin
Annatto seed Laying hens Increase in yolk pigmentation Carvalho et al.126 2009
‘Carophyll Red 10%’, Ross 308 chickens Red: carcass and shank skin Hamelin et al.69 2013
‘Xamacol 30 g’, (broiler) color increase
‘Carophyll Yellow 10%’ Yellow: no differences
Spirulina platensis, synthetic Rainbow trout Increase in skin and fillet Teimouri et al.127 2013
astaxanthin pigmentation
Pure canthaxanthin Reproductive poultry, Increase in pigmenting egg EFSA67 2014
ornamental fish and yolk, skin, plumage
birds
a Excluding animal experimental models for human medicine.

Curcumin of polyphenols.32 This effect was seen as a consequence of an

The curcumin biosynthetic pathway in plants is similar to that
of flavonoids. Both derive from phenylalanine, but the curcumin
pathway includes diarylheptanoids as intermediates. Crucial is the
difference from flavonoids due to the water insolubility of cur-
cumin (X).24 Various effects of curcumin in mammals are known:
in particular, anti-inflammatory, antioxidant and anticancer
properties.5 The increased ability in eliminating infectious agents
is proven for broilers fed with curcumin–Zn supplements.25
increased palatability of feed.
An interesting aspect of polyphenols such as flavonoids and
condensed tannins is their cross-reaction with enzymes. While
polyphenols can produce a kind of bitterness in taste that is
believed to be appetite quickening, it is also known that they affect
gastric enzymes which might result in a reduction of uptake rate
of nutrients. Saliva proteins should balance this effect by forming
indigestible complexes with polyphenols.18,22,33,34

EFFECTS OF USE IN ANIMAL NUTRITION
Feed intake
There is an obvious relation between selection of certain roughage
plants and the well-being of ruminants. Leiber describes the ability
of ruminants – led by the taste (which is directly associated with
secondary plant metabolites) – to choose herbs suitable to con-
trol and regulate ruminal processes.22 This is particularly true for
condensed tannins, which are taste-relevant and astringent. It is
known that ruminants prefer tannin-rich fodder in case of parasitic
infection.26 Additionally there is an influence of the sequence of
offered feed with different functional components on the duration
and amount of feed intake.27
Besides the taste connected to certain plant pigments, the
color itself might be the stimulus to increase intake. Color pref-
erences are known to be relevant in birds. The lipophilic char-
acter of carotenoids makes them more stable to food and feed
processing and therefore can serve to quicken the appetite of
visually oriented animals, e.g. poultry.21 In particular, in hens this
context has been proven.28,29 However, the simple addition of
plant-derived colorants will not always foster intake. In the paper
by Kraemer investigations are listed which show no increase in
intake of broilers after addition of flavonoid phytogenics.30,31 Blank
and Wolffram observed an increased feed intake and improved
1422
Antioxidative effects
In many herbs and spices used in animal nutrition, antioxidants
are found as biologically active compounds. Hashemi and Davoodi
(2011) give an overview of a range of spices in this context,
listing the number of identified antioxidants per plant species,
without working out the names of the single compounds.35
Active compounds in this context could be diverse polyphe-
nols, carotenoids, betalains, curcumin and certain vitamins. At the
same time, coloring agents are only found within the flavonoids,
betalains, curcumin and the carotenoids. Antioxidants help to
prevent oxidative stress by removing free radical intermediates
and are therefore an effective agent against a number of dis-
eases, in particular coronary heart disease and tumor develop-
ment, among many others (Tables 1 and 2).18,23,36 – 41 In animal
nutrition antioxidant properties are appreciated to act mainly
as health stabilizers. In early-lactating cows flavonoids such as
quercetin might prevent metabolic disorders like fatty liver dis-
ease or ketosis.42 Similar effects were found for supplementation of
flavonoid-rich mixtures with high antioxidative properties to cows,
improving their health status and alleviating the consequences of
mastitis.43,44
Curcumin is a natural antioxidant, resulting in positive per-
formance effects such as body weight gain, increased feed
efficiency and decreased mortality rates after administration to

growth rates in weaning pigs fed elder pomace as a known source poultry.45,46

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Phytogenic pigments in animal nutrition
Oxidative stability of the meat of broilers fed with antioxidant
rosemary supplement, concentrating on the total phenolic con-
tent without separating different sources of phenols, is revealed in
a study by Loetscher et al. (2013).47 The oxidative stability of pork
could be increased by feeding a polyphenolic-rich herb mixture.48
The approach to measuring the antioxidant properties of food
and feed without separation of coloring agents is followed in var-
ious publications.49 – 52 Besides that, the use of tocopherols in ani-
mal nutrition in the context of antioxidant properties should be
mentioned, although tocopherols – as yellow components color-
ing plant-derived fatty oils but not essentially plant tissues them-
selves – are not listed as plant pigments.32
Not only the occurrence of antioxidative compounds but also
their specific availability due to certain chemical compositions
(e.g. in human consumption the connection of anthocyanins and
tannins in red wine) is a limiting factor for a positive effect.18,49
Some authors appeal explicitly against a generalization of the
overall positive effects of antioxidant supplements.53 – 55
Other health-promoting effects
In the course of these antioxidant properties of plant pigments,
and owing to their ability to trap free radicals that could damage
other molecules, health-promoting side effects are often listed
(Tables 1 and 2). Certain carotenoids (e.g. crocin) are tested in
animal experiments for their effect in inhibiting inflammation,
colon carcinogenesis and colitis.56 Other effects occur due to the
influence of secondary plant compounds such as flavonoids on
saliva and gastric secretions, on the intake of feed (as mentioned
above), on the immune system and owing to their antibacterial
and antiviral properties.49 Lila gives a comprehensive overview of
human health-promoting effects of plant pigments, which could
in many ways also be useful in farm animals.57
Some dietary carotenoids, e.g. 𝛼-carotene or 𝛽-carotene, can
be split by mammals into molecules of vitamin A, a crucial
health-promoting agent. These carotenoids are therefore referred
to as provitamin A.21,58 Carotenoid precursors of vitamin A can
prevent visual disorders of animals – an approach that has
already been followed with the development of ‘golden rice’ in
human nutrition.57 Also anthocyanins of bilberries (Vaccinium
myrtillus) are used to improve visual acuity.18 owing to the
photo-protective role pigments play in plants, they could also
be useful as UV-protecting agents in herbivores.14,35 Besides
certain flavonoids, carotenoids have the ability to protect from
light-mediated damage. These protective effects can be deduced
from their ability to filter blue light and to scavenge reactive
oxygen species involved in photo-oxidative processes.57
Polyphenolic components of herbs, especially condensed
tannins, have great potential to modify ruminal fermenta-
tion rate and/or methane production.59 Diverse papers have
reported about these effects under normal and acidosis condi-
tions (Table 1).14,16,60 As fermentation rate is strongly correlated
with methane fermentation, feeding elevated levels of condensed
tannins may reduce CH4 emissions at the expense of nutrient
utilization.61 Thus one challenge might be the detection of plants
or plant combinations that mitigate CH4 without a correspond-
ing and extensive reduction of ruminal nutrient degradation
(Table 1).22,59
In ruminants, condensed tannins can bind proteins in the rumen
and therefore foster the forwarding of proteins to later stages of
digestion. In general, decreasing the rate of ruminal degradation
and subsequently increasing the flow of nutrients for digestion in
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the lower gut may beneficially affect rumen health by maintaining
an optimal ruminal pH.
Although condensed tannins are well-known as antinutritive
substances in monogastric livestock, due to their negative effect
on protein digestibility,62 when applied in small amounts proan-
thocyanidins may exert positive effects. As an example, apples
and red wine have high polyphenolic content, primarily con-
sisting of plant pigments such as catechin and proanthocyani-
dins, and to a lesser extent chalcones and anthocyanins.62,63
In vivo experiments with pigs showed positive effects on villi mor-
phology, gut-associated lymphoid tissue-activation and pig health
after feeding diets with apple or red wine pomace.64 Furthermore,
Kraemer30 observed increased digestibility of several amino acids
in piglets receiving a polyphenol-rich apple extract.30
Effects on the animal product
In humans, carotenoids are accumulated in various tissues, includ-
ing breast milk, adipose tissue and skin.57 An obviously similar
effect is found in many animal species, where carotenoids often
influence the color of flesh, skin or plumage. Thus certain stabil-
ity during digestion and uptake into somatic cells can be assumed
(Table 2).21 The yellow to red coloring effect of carotenoids is of
interest in egg yolk, skin and plumage of ornamental fish and
birds.65 – 67 Sometimes also the flesh color is of economic interest,
e.g. in fish.14,68 Hamelin et al. found a significant increase in carcass
and shank skin pigmentation of broiler chickens after carotenoid
supplementation.69 Theoretically also betalains or curcumin could
serve as coloring agents in animal products, but only one study
is available on this matter, solely assessing a color maintenance
effect of betalain in periods of social interaction in ornamental
fish.4
A second aspect is the possible increase of oxidative defense, sta-
bility and shelf life of meat and animal fat used for human nutrition.
These valuable effects result from antioxidative properties of plant
pigments in feed and could derive from flavonoids, carotenoids,
betalains or curcumin. Comprehensive reports are only known in
the field of polyphenolic flavonoids.47,48
Condensed tannins and other phenols such as flavonoids can
protect unsaturated fatty acids to be bio-hydrogenated and there-
fore are responsible for higher transfer rates of unsaturated fatty
acids into milk or tissues.70,71 This can affect the quality and health
value of animal products (e.g. in Mardalena et al.; Table 1).72 With-
out describing the metabolic pathway in digestion, reports of a
quality improvement in milk of dairy goats due to a higher ratio of
unsaturated fatty acids after curcumin supplement exist.73 Experi-
ments with quails showed a decreased lipid content of eggs after
curcumin supplementation.74
Possible negative effects
Most secondary plant compounds, in particular plant pigments,
in food and feed are mentioned in a positive context. Never-
theless, there are some comments pointing out reasonable lim-
its for use. For instance, Bjelakovic et al. highlighted negative
effects on health after intake of antioxidant supplements.53 – 55
Even increased mortality may appear, in particular with fat-soluble
antioxidants, including the plant pigment 𝛽-carotene or the vita-
mins A and E (tocopherol). Bjelakovic’s group stress that the opti-
mal source of antioxidants probably comes from diet and not from
concentrated supplements.55 Moreover, they oppose the opinion
of antioxidants being helpful against cancer as well as against car-
1423
diovascular diseases and for prevention of several diseases.53,54
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An underlined limitation of therapeutic effects is also found in

other publications, which describe the effect of dietary antho-
cyanin pigments and polyphenolics in lowering the rate of coro-
nary heart diseases but admit the controversial opinions of their
effects regarding tumors.18 An increase in carcinogenesis in rela-
tion to high doses of 𝛽-carotene was outlined by Schubert.49
A completely different approach is mentioned by Girardi et al.,
who describe methods of oxidizing the phenolic substances in
olive residues (pomace) to improve the processing quality of this
by-product in an ingredient of livestock feed.75 In this connection
unwanted phenols can inhibit the biochemical pathways involved
in the converting process. A similar aspect is found in papers con-
cerning potato processing to dehydrated products. Phenolic com-
pounds lead to a higher susceptibility to enzymatic and chemical
discoloration.76
Some colored flavonoids are mentioned to have mutagenic
properties, in particular the yellow flavonol quercetin. Various
publications state the genotoxic and cytotoxic effect of quercetin
in bacteria as well as in human cells.77 – 79 Desired effects of
quercetin based on its high antioxidant potential therefore are
linked to a certain risk for unwanted damage.
Some publications describe tannins to explore antinutritional
effects by negatively affecting the appetite and being inversely
related to organic matter and protein digestibility in ruminants as
well as in monogastric livestock. Moreover, a delay in the entire
gastrointestinal passage can be a consequence of high tannin rates
in feed.34,80 Other papers modify this message by realizing that, in
ruminants, the binding of proteins by tannins can affect protein
digestion positively or negatively. Piluzza et al. reviewed that the
assumption that condensed tannins at dietary concentrations of
<50 g kg−1 are beneficial can be attributed to Lotus species, but
may not be applicable to other feeds.70
In monogastric livestock condensed tannins are well known as
antinutritive substances, owing to their negative effect on protein
digestibility, which is related to binding dietary and endogenous
proteins like digestive enzymes.62 Hence diverse feed-processing
techniques aim at reducing tannin content, to enable higher inclu-
sion levels of protein sources in monogastric livestock nutrition.80
Figure 1. Pathways of phytogenic pigments in animal nutrition.

PHYSIOLOGICAL PATHWAYS OF PHYTOGENIC
PIGMENTS IN METABOLISM OF ANIMALS
As the pharmaceutical value of different phytogenic pigments is
primarily of interest in human applications, there are far more
investigations for human use than for animal use. A general
overview of pathways of plant-derived pigments with regard to
animal nutrition is given in Fig. 1. An overview of physiological
pathways of phytogenic colorants in different animal categories is
given in Table 3.
Flavonoids like the flavonol quercetin are typically present as
their glycoside forms.81 Because of the difficulties in methodology,
contradictory results have been reported as to the ratio of detected
undegraded and resorbed quercetin ranging from undetectable
(in humans and in rats) up to 20% (in rats).36 It is generally accepted
today that quercetin metabolites rather than quercetin glycosides
can be found in body compartments or excretion products.82
Studies in humans suggest that quercetin glycosides are efficiently
deglycosylated in the small intestine by 𝛽-glucosidase to liberate
aglycone, which can then be absorbed passively.83 Additionally,
quercetin glycosides are deglycosylated by enterobacteria and
absorbed in the large intestine.82 Even then, additional metabolic
1424
the fact that intact quercetin or its glycoside rutin could not be
detected in the urine or in the blood, neither in humans nor in
animal tests with rodents. However, the generated phenolic (and
antioxidant) metabolites could be identified in urine and intestine
of humans and animals (Table 3).36 In this context, Bieger et al.
(see Table 3) demonstrated a broad distribution of quercetin and
its methylated metabolites in pigs fed a high quercetin diet.86 In
particular, the high concentrations in the intestinal wall, liver and
kidneys indicate that these flavonoids are extensively metabolized
and eliminated by these organs. Accumulation within skeletal
muscle and adipose tissue was suggested to be unlikely, due to the
considerably lower concentrations found within these tissues even
after long-term application. In contrast to monogastric species,
knowledge regarding the bioavailability of quercetin in ruminants
is scarce. Similar to studies in monogastric species, Berger et al.
(see Table 3) demonstrated that after intraruminal application of
flavonols mainly their conjugated forms are present in plasma.42
Nevertheless, lower bioavailability of quercetin can be assumed
due to rapid and extensive microbial degradation in the rumen.42
A further striking contrast to monogastric species is the higher
bioavailability of quercetin after administration of rutin compared

processes take place, mainly in the liver.84,85 This is supported by with quercetin aglycon (Table 3).42,87

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Table 3. Physiological pathways of phytogenic pigments in animalsa

Phytogenic Animal
pigment category Metabolized via Accumulation Excreted via Source Year

Quercetin Rats Enterobacteria, liver n.s. Urine, bile Heilmann and Merfort36 1998a
Quercetin Pigs Intestinal wall, liver, No accumulation in Urine, feces Bieger et al.86 2008
kidneys skeletal muscle,
adipose tissue
Quercetin Cattle Rumen microbiome, n.s. n.s. Berger et al.42 2012
liver
Apigenin Rats Liver Possible due to slow Urine, feces Gradolatto et al.89 2005
elimination
Anthocyanins Pigs Liver Accumulation in tissues n.s. Kalt et al.91 2008
Anthocyanins Rats Liver, intestine, n.s. Bile, urine Fernandes et al.90 2014
kidney
Catechin Rats Gastrointestinal n.s. Bile, urine Heilmann and Merfort37 1998b
microbiome
Carotenoids Pigs n.s. No accumulation n.s. Bertram1 1989
Carotenoids Newborn calves Intestine, other Accumulation in serum n.s. Poor et al.95 1992
tissues and various tissues
Carotenoids Birds Liver Accumulation e.g. in fat, n.s. (absent in McGraw et al.128 2002
yolk bile, feces)
Carotenoids Fish n.s. Accumulation n.s. McGraw et al.128 2002
Betalain Rats Gastrointestinal tract n.s. Urine Reynoso et al.97 1999
Curcumin Rats Colon mucosa, liver n.s. Not determined Sharma et al.98 2001
Curcumin Rats Intestine, liver n.s. Bile Dempe100 2009
a Including animal experimental models for human medicine.

Flavones like apigenin are metabolized in a completely different
way. Tests in rodents and in humans showed that the hydroxylation
is done only to a very small extent by the microbiome of the
digestive system and rather by metabolism in the liver and other
organs.88 No resorption of flavone glycosides is assumed, whereas
flavone aglycones are resorbed intact (Table 3).37 Gradolatto et al.
(see Table 3) suggested a slow but high absorption of apigenin in
rats; excretion occurred mainly via urine.89 Owing to the observed
slow metabolism and elimination, possible accumulation in the
body was hypothesized.
Anthocyanins appear to be rapidly absorbed. Studies in rats
showed high contents of intact anthocyanins (20–25%) in plasma
a few minutes after intake. They seem to be quickly metabolized
and eliminated via bile and urine as both intact and metabolized
forms (Table 3).90 Kalt et al. (see Table 3) detected intact anthoy-
canins in the liver, eye, cortex and cerebellum in pigs fed diets
supplemented with blueberries, although they were not able to
detect anthocyanins in plasma or urine.91
In humans, proanthocyanidins or condensed tannins are first
broken down to the monomer catechin, which can be detected at
the highest level in blood after 1–2 h. The renal elimination of con-
jugates with an intact main aromatic ring was at 25% of the appli-
cation rate. Catechin is metabolized via the gastrointestinal micro-
biome, resulting in wide variations between species. Knowledge
regarding the metabolic pathways of proanthocyanidins is scarce.
It remains unclear to what extent metabolites or intact compounds
are resorbed and via which organs elimination occurs. However,
studies in rodents showed elimination of radioactively labeled cat-
echin via bile and urine (Table 3).37,92
Resorption, accumulation and metabolism of carotenoids differ
widely in different animal species. Humans are somewhat unique
in that they can absorb a whole variety of carotenoids intact,
in contrast to most species, pre-ruminant calves absorb intact
carotenoids (Table 3).95 Generally, the absorption and transport
of carotenoids are influenced by numerous events, impeding the
predictability of the actual absorbability of carotenoids.93 Lipids
serve as transport vehicles and carotenoids are primarily stored
in lipid tissues but also in cell membranes and lipoproteins. They
can be found in almost all tissues in humans.94,96 The accumu-
lation of carotenoids in cells of different organs is a reversible
process. Whereas poultry accumulate xanthophylls, an oxidation
product of carotenes, horses are known rather to accumulate
carotenes, humans store both carotenoid versions and pigs none
of them.1
Little is known about pathways of digestion of betalains in
livestock. One can only assume that in the case of livestock the
body reaction to betalains is similar to that of humans, where
at least 15% of consumers absorb large amounts of unchanged
betalains in the body. Red urine and feces are a consequence
of betalain intake; betalains are metabolized only to a minimal
extent. Nevertheless, betalains can be enriched in lipoproteins,
resulting in an increased defense against oxidation.57 Digestibility
studies in rats showed an almost complete degradation of the
pigments in the gastrointestinal tract within 24 h. The absorbed
betalains were eliminated via urine without being metabolized
in the liver (Table 3).97 Baron et al. suggested that, owing to the
hydrophilic nature of betalains, they may not be transported in the
way carotenoids are transported to skin cells, explaining their poor
pigmentation efficiency.4
According to studies in humans and rats it is assumed that
curcumin is poorly absorbed (Table 3).98,99 Additional to poor
gastrointestinal absorption, efficient first-pass metabolism, rapid
elimination and poor aqueous solubility contribute to low bioavail-
ability of oral curcumin. Excretion of conjugated metabolites is
1425

whereby absorption does not exceed 50–70%.93,94 Additionally, largely via bile (Table 3).5,100

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 www.soci.org
PHYTOGENIC PIGMENTS IN ECOLOGY IN THE
CONTEXT OF ANIMAL NUTRITION
Pigments play a primary role in plant metabolism and fulfill diverse
functions in the interactions of plants with their abiotic and biotic
environment. The reproductive success of many plant species is
strongly dependent on color-sensitive pollinators and seed dis-
persers, and the adaptive significance of pigment accumulation in
plant reproductive structures (flowers and fleshy fruits) is gener-
ally attributed to the attraction of animal vectors. For herbivores,
conspicuous colored plant structures are informative signals that
help to identify nutritive plants or plant parts and allow an assess-
ment of ripeness, nutritional gain or overall senescence state. With
respect to fruits, loss of green color and accumulation of antho-
cyanins, carotenoids and betalains are associated with fruit ripen-
ing. Chroma and brightness of fleshy fruits can reliably advertise
specific contents such as carbohydrates (often dark-colored fruits
like black, purple black or blue ones) or proteins (often bright col-
ored fruits like orange, yellow or white ones) to mutualists.101,102
Plant pigments not only indicate nutritive reward but might
themselves constitute rewards as they induce positive health
effects by reducing antioxidative stress, affecting inflammatory
processes or improving immune functions.103 – 106 Schaefer et al.
and Catoni et al. demonstrated that a wild frugivorous bird species
actively selects food enriched with flavonoids and that antiox-
idative agents such as anthocyanins and quercetin are absorbed
and circulate in the bird’s blood at relevant concentrations.106,107
Moreover, daily flavonoid supplementation increased the ability of
birds to mount a primary immune response to a novel antigen.106
These results indicate that frugivores may attend to plant signals to
increase their intake of antioxidants for self-medication. Thus the
color of ripe fruits might also be determined by pigments that are
physiologically important to seed dispersers.108 – 110
Plants may increase their reproductive success by colorfully
advertising the nutritional and antioxidant properties of their
fruits. However, apart from their role in animal attraction pigments
might have different tasks such as defending or protecting against
pathogens, fungi, predator insects or abiotic factors (e g. radia-
tion). The accumulation of pigments during the process of fruit
ripening may thus be at least partly explained by their defen-
sive properties.107,109 According to an alternative hypothesis, color
could also be simply an expression of fruit biochemistry and thus
indicative of its content.102 It was shown that sugars upregulate
the anthocyanin biosynthesis by inducing the expression of key
enzymes in the anthocyanin biosynthetic pathway.111 Dark fruit
colors that were found to be indicative for high sugar contents
could thus also be explained by plant biochemistry and may not
necessarily represent a signal that evolved for communication.102
DISCUSSION AND CONCLUSIONS
Because nature-oriented feed additives are gain increasing impor-
tance in the market, a close look at the potential and risks of
diverse plant-derived compounds is highly desirable. Exploring
and imitating the use and effects of plant pigments in ecol-
ogy, multiple promising applications have already been put into
practice in animal nutrition or can be utilized in the future. In
nature, color in herbal tissues acts as a signal, either for attract-
ing and enhancing feed intake or as a sign for nutritional and/or
health-promoting value. Therefore, as a special and highly effec-
tive group of plant-derived feed additives, coloring agents are the
1426
focus of this review.
wileyonlinelibrary.com/jsfa © 2015 Society of Chemical Industry
B Faehnrich et al.
In fact, there is an economic potential to foster the use of
plant pigments as natural antioxidants to enhance the quality
and extend the shelf life of animal products.47,48 Because of an
increased environmental conscience and an increasing market for
natural feed/food additives in developed countries and the chance
for developing countries to use sound knowledge of effective
plant-derived feed additives, available without high costs, the
topic of plant pigments in animal nutrition should be given high
priority.14,35,112 – 117
Various effects of plant pigments in animal nutrition are already
widely known, e.g. polyphenolic flavones and flavonols providing
antioxidant properties, anthocyanins providing appetite quicken-
ing colors and carotenoids – due to their fat solubility – providing
stable colors in animal products.14,18,68,69,77 – 79 It was observed that
ruminants having the opportunity to choose their fodder plants
balance the selection according to secondary plant metabolites
and their health-related needs. This is a behavior described as
‘self-medication’.26 Thus a high share of desired benefits of fed
plant pigments is not yet fully exploited yet, e.g. potential antiox-
idative properties of betalains and carotenoids or coloring effects
of curcumin.
As in all natural plant products, a high variability of compo-
sition of compounds occurs in the plant source. Not only the
genetic background of plant species, but also impacts due to
the plant’s environment and growing conditions, as well as
the harvesting season, the used plant part or the processing
technology are influencing factors. Even the pure compounds
themselves – due to their complexity – often follow contradic-
tory roles in the animal’s body. For instance, condensed tannins
decrease methane production in ruminants (desired), but at
the same time also decrease fermentation rate (undesired)
(Scharenberg and Arrigo (http://www.agroscope.admin.ch/)).118
Quercetin, for example, provides a high antioxidative value
(desired), but has at the same time mutagenic and cytotoxic
properties (undesired).77 – 79 Effects might change with duration
of application, but long-term studies are mostly missing.5 Also
interactions with other feed ingredients and the general nutri-
tional status of the animal might alter the expected effects in a
positive or negative direction.18,49,119,120
Considering these conclusions, it is clear that physiological path-
ways of metabolism in animals are still widely unknown, leav-
ing an uncertainty of accumulation or excretion of certain com-
pounds which would be of crucial importance regarding the
desired effects on the animal’s health, welfare and performance
as well as regarding the quality of the animal products (Table 3).
Moreover, detection methods vary from study to study, leaving a
mess of data instead of compiled information.36
As plant pigments are natural compounds, no negative impact
on the environment after excretion is expected, but enrichment
of the compounds or involvement in processes of manure conver-
sion and therefore in water cycles is still possible.121 Similar to this
aspect, phenolic compounds are rather undesired in feed process-
ing technologies.75
Limits of reasonable application therefore are to be considered.
As far as is known up to now, risks mainly derive from an excessive
use of plant pigments in animal nutrition, starting from stagna-
tion of desired effects (e.g. enhancing color and brightness of skin
and plumage by carotenoid additives) up to health deterioration
and tumorigenic or mutagenic effects (known, for example, for
quercetin and curcumin).5,65 – 67,77 – 79 In particular, highly antiox-
idative properties of feedstuff might not be a guarantee for an
overall disease-protecting effect.53 – 55
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Phytogenic pigments in animal nutrition www.soci.org

An overall conclusion generating a comprehensive overview of

useful pigmenting plant compounds, with advice on product qual-
ity control, application and dosage, defined for certain animal
species, would be a desirable goal. Therefore, further investiga-
tions to provide comparable data are necessary to be able to use
the natural potential of plant pigments in an optimal way.

CHEMICAL STRUCTURES

Structure V. Basic structure of flavonols.

Structure I. Flavan, the basic structure of flavonoids.

Structure VI. Basic structure of anthocyanins.

Structure II. Basic structure of chalcones.

Structure VII. Catechin, as a monomer of condensed tannins.

Structure III. Basic structure of aurones.

Structure VIII. 𝛼-Carotene, a typical carotenoid.

Structure IV. Basic structure of flavones.

1427

Structure IX. Betalaminic acid, the basic structure of betalains.

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 www.soci.org
Structure X. Curcumin, keto-form.
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