Agroforest Syst (2007) 71:77–87
DOI 10.1007/s10457-007-9089-y
Nutrient composition of mistletoe (Viscum album) and its
nutritive value for ruminant animals
H. Derya Umucalılar Æ N. Gülşen Æ B. Coşkun Æ
A. Hayirli Æ H. Dural
Received: 8 November 2005 / Accepted: 16 July 2007 / Published online: 11 August 2007
Springer Science+Business Media B.V. 2007
Abstract Mistletoe (Viscum album L. subsp.
album) is known as an obligatory hemiparasite of
trees and is consumed by herbivores in some places,
especially during periods of forage shortage and
drought. This experiment was conducted to determine
nutrient composition and nutritive value of mistletoe
with respect to vegetation stage. Mistletoe samples
were collected from three different tree species
[almond (Amygdalus communis L.), plum (Prunus
domestica L.), and willow (Salix alba L.)] at three
different vegetation stages (April, July, October)
naturally growing in Central Turkey. Five samples
were taken at each vegetation stage for each tree
species. The samples were incubated in rumens of
two 2-year old fistulated Holstein cows. Nutrient data
This experiment was funded by Selçuk University Scientific
Research Coordination Office.
H. Derya Umucalılar (&) N. Gülşen B. Coşkun
Department of Animal Nutrition and Nutritional
Disorders, Faculty of Veterinary Medicine, Selçuk
University, Konya 42031, Turkey
e-mail: hderya@selcuk.edu.tr
A. Hayirli
Department of Animal Nutrition and Nutritional
Disorders, Faculty of Veterinary Medicine, Atatürk
University, Erzurum 25700, Turkey
H. Dural
Department of Biology, Faculty of Science and Art,
Selçuk University, Konya 42031, Turkey
and nutritive value indices were subjected to 2-way
ANOVA using the GLM procedure. Crude protein
and NDF concentrations and metabolisable energy
level of the samples were in the ranges of 52.5–68.6,
291–330, and 7.8–8.4 MJ kg1 DM, respectively.
There were also significant differences in DM, crude
ash, Fe, Cu, and Zn levels among trees. As the
vegetation progressed, there were linear decreases in
DM, CP, and NDF and linear increases in ADF, Ca,
Cu, and Zn levels. There were significant interaction
effects for tree species by vegetation stage in terms of
DM, ADF, and Zn. In vitro dry matter and organic
matter digestibility coefficients were between 0.84
and 0.87 and between 0.52 and 0.55, respectively. It
was also observed that degradation of V. album was
almost completed after the first 48 h. The soluble and
readily degraded portion of DM (fraction ‘‘a’’)
increased, whereas the insoluble but degradable
portion of DM (fraction ‘‘b’’) decreased with advancing vegetation stage. Effective degradability of dry
matter (EDDM) also increased significantly as the
vegetation progressed. Gas production from fraction
‘‘b’’ varied by tree species and the stage of vegetation. A significant interaction of tree species by
vegetation effects on EDDM and gas production was
also noted. After 48 h, cumulative gas production and
fraction ‘‘b’’ ranged from 52.71 ml to 58.85 ml and
from 48.8 ml to 75.4 ml, respectively. In general, the
mistletoe was low in protein, moderate in fibre, and
high in minerals. In conclusion, as long as a lack of
deleterious effects on health and performance is
123
78
shown in feeding trials, mistletoe has potential to be
used as a dietary component in ruminant feeding.
Keywords Gas production Kinetics parameters
Mistletoe Nutrient digestibility Nutritive value
Agroforest Syst (2007) 71:77–87
sources for ruminant feeding (Madibela et al.
2000). To date, little research is available on
nutritive value of the mistletoes. Thus, the objective of this experiment was to determine nutrient
composition and nutritive value of the European
mistletoe with respect to the vegetation stage and
host tree species.
Introduction
Mistletoe (Viscum album L. subsp. album), is a
member of the Santalaceae and one of many species
in three families within the order Santalales that are
referred to as mistletoe. Mistletoes have a widespread global distribution, occurring as evergreen
plants, growing up to 80 cm on the branches of
many trees in tropical, temperate, and semi-arid
regions at altitudes ranging from 300 m to 2,000 m
(Davis 1982). Due to having low amounts of
chlorophyll–protein complexes, the mistletoes have
a low capacity for photosynthesis, which partially
explains their ability to adapt to drought conditions
(Turquet and Salle 1996). The mistletoes are
considered as hemiparasites of forest and fruit trees
(Baykal 1995), because they obtain nutrients from
the trees on which they grow as well as photosynthesising themselves. Therefore, mistletoes can be
economically deleterious due to causing reduced
growth and seed production and death of host trees
(Bhattacharyya and Johri 1998; Hawksworth and
Geils 1990; Hawksworth and Wiens 1996). On the
other hand, mistletoe, as a part of an ecosystem,
attracts avian frugivores and exotic animals (de
Buen and Ornelas 2001; Garnett et al. 2006) and
provide for their nourishment (protein, 6%; lipids,
44%; and sugars, 12%) (Godschalk 1983) as well as
hiding and nesting sites (Parks et al. 1999).
In some Mediterranean regions, leaves of shrubs
and bushes become important feed sources for the
ruminant animal, particularly during the periods of
shortage of feedstuffs and drought conditions.
Therefore, animals may consume some plants that
have thorns and contain toxic compounds, such as
Astragalus spp. and Quercus spp. (Sarı 1976).
Producers often seek for alternative feedstuffs to
meet the demand for forage. It is known that
animals also consume the mistletoes during the
feedstuff shortage in regions where conventional
animal production is predominant. Viscum species
can therefore be alternative mineral and forage
123
Materials and methods
Animals and management
Two 2-years old Holstein cows weighing an average
of 450 kg were fistulated 3 months prior to the
experiment. Diets were formulated to meet the
nutrient requirements for maintenance plus 500 g
daily live weight gain (NRC 1989). Diet consisted of
3.5 kg of grass hay (80.5 g kg1 CP), 3.0 kg of
wheat straw (36.0 g kg1 CP) and 4.0 kg of concentrate mixture (Table 1). Animals were fed twice daily
at 06:00 and 16:00 h. The experimental diets were
offered 2 weeks prior to data collection for the
adaptation period. Animals were kept in individual
pens and water was available ad libitum during the
experimental period.
Table 1 Ingredient and chemical composition of the concentrate mixture
Ingredients
g kg1 DM
Barley
572
Wheat bran
200
Cotton seed meal
190
Limestone
23
NaCl
Vitamin-Mineral Premix
5
*
10
Chemical analyses
Crude protein
183
Crude fibre
106
Ether extract
52
Ash
65
N-free extract
595
* Each kg contained: 12.500 IU vitamin A, 2.500 IU vitamin
D3, 30 mg vitamin E, 10 mg niacin, 1.600 mg Ca, 1.300 mg P,
0.4 mg Mg, 3.2 mg Zn, 3.0 mg Mn, 8 mg Cu, 0.4 mg I, 0.1 mg
Co, 0.1 mg Se, 500 mg NaCl, and 300 mg NaHCO3
Agroforest Syst (2007) 71:77–87
79
Plants
Chemical analyses
The mistletoe samples were obtained from three
different tree species [almond (Amygdalus communis
L.), plum (Prunus domestica L.) and willow (Salix
alba L.)]) at three different stages of vegetation
(April, July, and October) in Konya vicinity (38 010
565@ N, 32 300 415@ E, 1,160 m altitude). Five
representative subsamples were taken for each tree
species during each vegetation stage. Samples were
dried in oven at 65C for 48 h and then ground to
pass 1 mm-screen for chemical analyses and in vitro
assays and 3-mm-screen for the nylon bag technique.
The mistletoe samples before and after incubations
were analysed for DM, crude protein (CP), ether
extract (EE), and crude ash (CA) contents (AOAC
1984). Neutral detergent fibre (NDF) and acid
detergent fibre (ADF) contents were analysed as
described by Goering and Van Soest (1970) using
fibre analyser (Ankom 220 Fiber Analyzer, Ankom
Co., USA). Mineral contents including Ca, P, Fe, Cu,
and Zn were also determined using inductively
coupled plasma-atomic emission spectrometry (ICPAES, Varian-Vista, Australia).
Experimental procedure for in situ degradability
In situ degradability was conducted according the
protocol outlined by the Agricultural and Feed
Research Council (AFRC 1992). Bags were made
from a Dacron material (7 · 14 cm) with an average
pore size of 45 lm. Approximately 2.5 g of dried
plant samples were weighed accurately into each bag
of duplicates. After tying bags separately with a
nylon string, samples were incubated in the rumen for
8, 16, 24, 48 and 72 h from the morning feeding. At
the end of each incubation period, the bags were
removed from the rumen and washed thoroughly
under running tap water until the rinsing water was
colourless. They were washed again in a washing
machine with cold water (3 · 5 min) until all ruminal
colours disappeared. Samples were then oven dried to
constant weight at 55C for 48 h. The washing losses
of dry matter (DM) were determined by washing bags
with samples prior to incubation. The in situ DM
degradation kinetics was fitted to the following
exponential equation (McDonald 1981):
Degradability, % ¼ (a þ b) (1 ect )
where a = soluble fraction of dry matter, %;
b = insoluble but degradable fraction of dry matter,
%; c = fractional rumen degradation rate per hour of
b; and k = rumen outflow rate. Effective degradability of dry matter (EDDM) was calculated using
Neway software (Version 5.0, Rowett Research
Institute, Aberdeen, UK), assuming that ruminal
outflow rate is 5% per hour (EDDM, % = (a + b ·
c)/(c + k)).
Calculations of in vitro gas production,
metabolisable energy, and in vitro organic matter
and dry matter digestibilities
After incubation for 6, 12, 24, and 48 h, in vitro gas
production from samples was determined in ruminal
fluid collected through the rumen fistula as
described by Menke and Steingass (1988). Duplicates of each sample were used in five runs for
correcting the volume of gas production according
to a standard. Gas kinetics parameters were generated using an exponential model described by
Ørskov and McDonald (1979) in Neway software,
which is as follows:
P ¼ (a þ b) (1 ect )
where P = the amount of gas produced at time t;
a = the amount gas produced from soluble portion of
the feedstuff, ml; b = the amount gas produced from
insoluble but slowly fermentable portion of the
feedstuff, c = rate of gas production, ml h1; and
t = time relative to incubation, h.
Metabolisable energy (ME) level and in vitro
organic matter digestibility (IVOMD) were calculated using equations presented by Close and Menke
(1986), which are as follows:
ME (Mcal kg1 DM) ¼ (2.20 þ 0.136 GP þ 0.0057
CP þ 0.00029 EE2 )/4.186
IVOMD (%) ¼ 14.88 þ 0.889 GP þ 0.045
CP þ 0.065 CA
123
80
where GP = gas production, ml 48 h1; CP = crude
protein, g kg1; EE = ether extract, g kg1; CA =
crude ash, g kg1.
In vitro dry matter digestibility (IVDMD) was
determined with two-stage method outlined by Tilley
and Terry (1963) using NDF procedure (Goering and
Van Soest 1970) in in vitro incubator (Daisy II,
ANKOM Technology, Fairport, NY) according to the
following formula:
IVDMD (% ) ¼ 100 - NDFR
where, NDFR = proportion of neutral detergent residue in dry matter.
Statistics
Data were subjected to 2-way ANOVA using the
General Linear Model Procedure of SAS (SAS 1998).
The general linear model to test the main effects of
the mistletoe source and the vegetative stage and their
interaction is as follows:
Yijk ¼ l þ MSi þ VSj þ (MS VS)ij þ eijk
where Yijk = response variable, l = population
mean, MSi = ith mistletoe source, VSj = jth vegetation stage, (MS · VS)ij = ith mistletoe source by jth
vegetation stage interaction, and eijk = residual error.
Differences among means were attained by the LSD
option. The effects were considered to be significant
at probability less than 0.05.
Agroforest Syst (2007) 71:77–87
differences in NDF and ADF concentrations, ME
value, IVDMD, and IVOMD across the trees.
As the vegetation advanced from April to October
with a 3-month interval, there were linear decreases in
DM (from 409 g kg1 to 336 g kg1, P < 0.001), CP
(from 65 g kg1 to 55 g kg1 DM, P < 0.01), NDF
(from 321 g kg1 to 296 g kg1 DM, P < 0.001) and
linear increases in CA (from 86 g kg1 to 100 g kg1
DM, P < 0.001) and ADF (from 177 g kg1 to 196 g
kg1 DM, P < 0.001). Ether extract concentration, ME
value, IVDMD, and IVOMD remained constant during
the vegetation stages. There was no pattern in alterations in DM content (Fig. 1A, P < 0.0001), ADF
concentration (Fig. 1B, P < 0.05), ME value (Fig. 1C,
P < 0.0001), and IVOMD coefficient (Fig. 1D,
P < 0.0001) as the vegetation advanced.
Inorganic nutrient contents of mistletoe on different host species are shown in Table 3. Almond, plum,
and willow had similar Ca and P concentrations.
Almond and willow had the highest and lowest Fe
(P < 0.05) and lowest and highest Cu contents
(P < 0.001), respectively. Plum had slightly higher
Zn content than almond, whereas willow had about a
4.5-fold greater Zn content than plum and almond
(P < 0.001).
There were linear increases in Ca (from 12.77 g
kg1 to 14.33 g kg1, P < 0.001), Cu (from 9.47 mg
kg1 to 11.40 mg kg1, P < 0.01) and Zn (from
37.73 mg kg1 to 40.54 mg kg1, P < 0.01) contents
with advancing vegetation stage. Increase in Zn
concentration was linear for almond and plum,
whereas quadratic for willow as the vegetation
advanced (Fig. 2, P < 0.05).
Results
Dry matter degradability and degradation kinetics
Nutrient composition
Table 2 summarizes dry matter and nutrient composition as well as IVDMD and IVOMD of mistletoe on
different host species collected at different vegetation
stages. Dry matter concentration was the highest and
lowest for plum and willow, respectively (P < 0.01).
Ash concentration for plum and willow was similar,
and both were lower than almond (P < 0.05).
Almond and willow had also similar CP and EE
concentrations. Crude protein (P < 0.05) and EE
(P < 0.05) concentrations were the highest and
lowest in plum, respectively. There were no
123
Ruminal DM degradability and degradation kinetics
parameters of mistletoe on different host species
during incubation are summarized in Table 4. Soluble fraction ‘‘a’’ and insoluble but slowly fermentable
fraction ‘‘b’’ of DM differed by the type of tree and
the stage of vegetation. Fraction ‘‘a’’ was the highest
and lowest for almond and plum, respectively. It also
increased linearly from 33.3% to 37.9% with advancing vegetation stage. Fraction ‘‘b’’ was the highest
and lowest for willow and almond, respectively. In
contrast to fraction ‘‘a’’, there was a linear decrease in
fraction ‘‘b’’ from 49.3% to 41.8% as the vegetation
Agroforest Syst (2007) 71:77–87
81
Table 2 The effect of mistletoe (Viscum album) host tree species and vegetation stage on nutrient composition and in vitro
digestibility coefficients
Variableb
Mistletoe source
Almond
SEM
Plum
Willow
Apr
Jul
Oct
Apr
Jul
Oct
Apr
Jul
Oct
DM, g kg1
415
328
345
416
347
352
395
356
310
CA, g kg1 DM
93
100
107
78
102
96
86
91
98
CP, g kg1 DM
66
57
53
68
69
58
60
61
EE, g kg1 DM
73
74
69
58
66
61
67
NDF, g kg1 DM
310
304
292
324
297
304
330
ADF, g kg DM
ME, MJ kg1 DM
184
78
198
79
184
82
171
83
184
80
202
79
IVDMD
0.85
0.85
0.85
0.87
0.86
IVOMD
0.52
0.53
0.55
0.55
0.53
1
a
Statistical significance, P<a
Tree (T)
Stage (S)
TxS
0.6
**
***
***
0.2
*
***
NS
53
0.1
*
**
NS
77
68
0.2
**
NS
NS
324
291
0.3
NS
***
NS
177
82
186
84
201
79
0.2
0.04
NS
NS
***
NS
*
***
0.84
0.86
0.86
0.86
0.3
NS
NS
NS
0.53
0.55
0.56
0.53
0.3
NS
NS
***
* = P < 0.05; ** = P < 0.01; *** = P < 0.001; NS = nonsignificant
b
A
Dry Matter, g kg-1
400
350
300
Almond
250
Plum
200
150
Willow
100
50
0
Metabolisable Energy, MJ kg-1 DM
Apr
90
Jul
Vegetation Stage
210
B
180
150
Almond
120
Plum
90
Willow
60
30
0
Oct
Apr
C
0.6
75
60
Almond
45
Plum
Willow
30
15
0
In Vitro OM Dig. Coeff.
450
Acid Detergent Fibre, g kg-1 DM
DM = dry matter; CA = crude ash; CP = crude protein; EE = ether extract; NDF = neutral detergent fibre; ADF = acid detergent
fibre; ME = metabolisable energy; IVDMD = in vitro dry matter digestibility coefficient; IVOMD = in vitro organic matter
digestibility coefficient
Jul
Vegetation Stage
Oct
D
0.5
0.4
Almond
0.3
Plum
Willow
0.2
0.1
0
Apr
Jul
Oct
Vegetation Stage
Apr
Jul
Oct
Vegetation Stage
Fig. 1 Mistletoe (Viscum album) host tree species by vegetation stage interaction effects on dry matter content (A), acid detergent
fibre content (B), metabolisable energy (C), and in vitro organic matter digestibility coefficient (D)
stage advanced. Moreover, alterations in fractions
‘‘a’’ and ‘‘b’’ (P < 0.05 for both) for the mistletoe of
different host species were different as the vegetation
progressed. The stage of vegetation, but not the host
tree species, affected EDDM (P < 0.001). Interestingly, EDDM values increased linearly from 55.6%
123
82
Agroforest Syst (2007) 71:77–87
Table 3 The effect of the mistletoe (Viscum album) host tree species and vegetation stage on mineral contents
Variable
Mistletoe source
SEM
Almond
Apr
b
Plum
Jul
Oct
Apr
Statistical significance, P <a
Willow
Jul
Oct
Apr
Jul
Oct
Tree (T)
Stage (S)
TxS
13.3
14.3
13.7
12.1
14.6
14.7
12.9
13.7
14.6
1.8
NS
***
NS
3.0
3.0
3.3
2.8
3.3
3.3
3.4
3.3
3.4
0.6
NS
NS
NS
c
124.2
154.7
112.9
93.1
100.2
106.9
90.7
82.9
118.7
5.4
*
NS
NS
Cuc
6.9
8.1
8.3
8.5
11.6
11.3
13.0
14.1
14.6
0.5
***
**
NS
Znc
15.2
17.6
14.6
22.2
23.6
20.8
75.8
95.2
86.2
4.9
***
**
*
Ca
Pb
a
* = P < 0.05; ** = P < 0.01; *** = P < 0.001; NS = nonsignificant
b
g kg1
c
mg kg1
Zinc, mg kg-1
Fe
100
90
80
70
60
50
40
30
20
10
0
linearly from 0.106 ml h1 to 0.099 ml h1 as the
vegetation stage advanced.
Almond
Plum
Willow
Apr
Jul
Vegetation Stage
Oct
Fig. 2 Mistletoe (Viscum album) host tree species by vegetation stage interaction effects on Zn concentration
to 58.2% with advancing vegetation stage. However,
this increase was the dependent on tree species,
decreasing quadratically for almond and willow, but
increasing quadratically for plum (Fig. 3A,
P < 0.001).
Gas production and kinetics parameters
Cumulative gas production and corresponding gas
kinetics parameters are shown in Table 5. The host
tree species affected gas production from the insoluble but slowly fermentable portion (fraction ‘‘b’’)
(P < 0.001), which was the highest for willow and
lowest for almond. Fraction ‘‘b’’ also decreased
linearly from 70.2 ml to 49.6 ml with advancing
vegetation stage (P < 0.001). Moreover, this decrease
was less dramatic for almond than for plum and
willow (Fig. 3B, P < 0.001). Gas production rate (c)
was independent of host tree species, but was affected
by the stage of vegetation (P < 0.001), decreasing
123
Discussion
Much research dealing with mistletoes has focused on
extracting some antinutritional factors such as lectin,
agglutinin, viscotoxin, and thionin for human medicine. Among these, lectin (Pryme et al. 2006) and
agglutinin (Hajto et al. 1999) are shown to have
cytostatic and immunmodulatory properties via suppressing tumour growth at the transcriptional level as
well as potentiating the activity of tumour necrosis
factor alpha to induce apoptosis and stabilize DNA in
cancer therapy. Viscotoxin (Giudici et al. 2006; Liu
et al. 2006) and thionin (Stec 2006) have cytotoxic
properties to protect plant tissue. Other effects of the
mistletoe extracts have also been shown, which may
broadly include immunostimulant effects through
enhancing phagositosis and extracellular burst activity of leukocytes (Dugenci et al. 2003),
neurophysiolgical action to increase intestinal contractility through activating muscarinic receptors
(Radenkovic et al. 2006), and hypoglycaemic properties through an unknown mechanism (Ohiri et al.
2003).
Mistletoe is abundant in forest regions and
orchards as a hemiparasite and has long been used
for animal nutrition especially during drought and
winter. However, little research has been conducted
to evaluate its nutritive value (Madibela et al. 2000,
2002, 2003). The effects of the antinutritional
substances mentioned above on feeding behaviour
Agroforest Syst (2007) 71:77–87
83
Table 4 The effect of mistletoe (Viscum album) host tree species and vegetation stage on dry matter degradability and kinetic
parameters
Statistical significance, P <1
Mistletoe source
Almond
Apr
Plum
Jul
Oct
Willow
Apr
Jul
Oct
Apr
Jul
Oct
SEM
Tree (T)
Stage (S)
TxS
Time, h
Degraded dry matter, %
8
44.2
48.0
49.9
41.1
48.4
48.7
43.0
45.2
51.0
0.5
NS
***
**
16
61.4
61.4
61.1
59.8
62.8
60.7
58.4
59.0
62.4
0.3
NS
NS
*
24
70.2
69.4
68.0
69.5
71.1
67.7
68.0
67.7
69.2
0.3
NS
NS
NS
48
78.8
79.2
76.8
79.4
80.8
76.1
80.1
79.4
77.4
0.3
NS
***
NS
72
Variable2
80.3
81.6
79.3
81.4
Degradation kinetics parameters
83.1
78.1
83.4
82.8
79.3
0.4
NS
***
NS
A, %
35.0
36.7
38.8
31.5
36.5
36.3
33.4
34.5
38.6
0.4
**
***
*
B, %
45.8
45.7
41.7
50.7
47.4
42.6
51.4
49.9
41.3
0.6
***
***
*
C, % h1
0.0814 0.0632 0.0578 0.0785 0.0679 0.0639 0.0593 0.0557 0.0631 0.002 *
**
NS
A+b
80.7
82.4
80.7
82.2
83.9
78.9
84.8
84.4
79.9
0.4
*
***
NS
EDDM, % 56.6
58.0
58.3
54.9
58.8
57.2
55.3
56.1
59.1
0.3
NS
***
*
1
* = P < 0.05; ** = P < 0.01; *** = P < 0.001; NS = nonsignificant
2
a = soluble fraction; b = insoluble but degradable fraction; c = fractional rumen degradation rate per hour of b; EDDM = effective
degradability of dry matter ([(a + b · c)/(c + k)], with rumen outflow rate (k) of 5% h1)
Effective Degradability of Dry
Matter, %
A
60
55
50
45
40
35
30
25
20
15
10
5
0
Almond
Plum
Willow
Apr
Jul
Oct
Vegetation Stage
B
80
Gas Production, ml
70
60
50
Almond
40
Plum
Willow
30
20
10
0
Apr
Jul
Oct
Vegetation Stage
Fig. 3 Mistletoe (Viscum album) host tree by vegetation stage
interaction effects on effective degradability of dry matter (A)
and gas production from the insoluble but slowly fermentable
portion (B)
(e.g., palatability, acceptability) and performance of
almond (Amygdalus communis L.), plum (Prunus
domestica L.), and willow (Salix alba L.) ruminants
are largely unknown but have been reported to
seldom cause gastrointestinal disturbances and toxicity (Knight and Walter 2003). Due to the limitation of
available data, comparisons of nutrient composition
and nutritive value of the mistletoe tested in the
present experiment will be limited to feedstuffs
commonly fed to ruminants.
Dry matter content ranged from 300 g kg1 to
400 g kg1 and varied with the type of tree that the
mistletoe was growing on (Table 2) and the vegetation stage (Fig. 1A). Crude protein content of the
mistletoe species was 53–69 g kg1 (Table 2), which
is much lower than commonly used forage sources in
intensive animal production facilities, including
leguminosea and graminea (NRC 2001). Our results
suggest that the species of host tree and the stage of
vegetation should be considered when mistletoe is fed
to ruminants, although differences in CP content by
host tree species and stage of vegetation were
relatively small. At onset of spring, CP content was
highest and decreased gradually to autumn (Table 2).
Other mistletoe species (V. verrucosum and V.
rotundifolium) have also contained high CP
123
* = P < 0.05; ** = P < 0.01; *** = P < 0.001; NS = nonsignificant
b = the amount gas produced from insoluble but slowly fermentable portion; c = rate of gas production
2
1
***
***
***
NS
***
1.5
0.001
0.0980
48.8
62.0
0.1080
0.1100
72.3
49.2
0.1020
0.1060
55.1
75.4
50.7
0.1060
0.1080
0.1020
c, ml h1
52.9
62.8
b, ml
0.0980
***
***
NS
0.4
53.7
56.9
57.9
53.4
53.6
58.9
Gas kinetics parameters
Variable2
52.7
54.3
48
38.5
49.1
36.6
49.3
12
24
57.0
***
*
NS
*
0.3
0.4
38.8
49.4
40.7
53.0
39.0
53.4
39.4
49.5
38.6
49.5
21.1
27.2
25.0
29.0
25.3
20.9
6
Gas production, 200 mg DM ml1
19.3
Jul
Apr
Jul
Oct
Apr
38.0
53.2
0.5
27.2
25.2
Oct
Jul
Apr
Oct
Willow
Plum
Almond
41.4
52.3
NS
*
Tree (T)
***
Stage (S)
Statistical significance, P <1
SEM
Mistletoe source
Time, h
123
NS
Table 5 The effect of mistletoe (Viscum album) host tree species and vegetation stage on cumulative gas production and gas kinetics parameters
concentration in spring (Madibela et al. 2000),
whereas CP content remain unchanged during a
period of drought (Madibela et al. 2002). In these
species, CP content (79 and 128 g kg1) was greater
than the mistletoe species utilized in the present
experiment.
Fibre level is one of the most important concerns
for forage choice because it influences feed intake
(Romney and Gill 2000) through its gut filling effect.
Forages typically contain 400 g kg1 or more NDF
(NRC 2001). The mistletoe contained approximately
300 g kg1 NDF (Table 2). Similarly, ADF content
in the mistletoe was lower than other conventional
forages (Table 2). Lower level of structural carbohydrates could lead to higher level of soluble
carbohydrate fraction, which should also be investigated. Significant effects of vegetation stage on ADF
and NDF (Table 2) reveals that the mistletoe undergoes lignification, but to a greater extent when hosted
by plum and willow than almond (Fig. 2B). In a study
dealing with 40 different tropical plants by Kaitho
et al. (1998), it was shown that CP level ranged
between 79 g kg1 and 307 g kg1 and NDF level
ranged between 220 g kg1 and 694 g kg1 on a DM
basis. Crude protein and NDF concentrations of
mistletoe species used in the present experiment were
lower than those reported for other alternative plants,
which could be related to the flora of origin,
composition of soil, and other environmental factors.
The mistletoe species used in the present experiment contained ME ranging from 7.8 MJ kg1 DM
to 8.4 MJ kg1 DM (Table 2 and Fig. 2C), with
in vitro digestibilities of DM and OM (Table 2 and
Fig. 2D) ranging from 843 g kg1 to 870 g kg1 and
from 522 g kg1 to 558 g kg1, respectively. Energy
content of 22 different conventional forages ranged
from 8 MJ kg1 DM to 11 MJ kg1 DM (Long et al.
1999). Compared with commonly used forages (NRC
2001), our data suggest that the mistletoe species
could be a considered as forage sources. In agreement
with the present data, IVDMD values were reported
to be about 53% in other Viscum species (Madibela
et al. 2000).
Minerals in forages also contribute to animal
nutrition and wellbeing. Calcium level did not differ
with host tree species (about 13 g kg1, Table 3) and
was as high as that in legume species (NRC 2001).
Minimum requirements of Ca and P level for
ruminants are 3 and 2.5 g kg1 DM (MacPherson
***
***
Agroforest Syst (2007) 71:77–87
TxS
84
Agroforest Syst (2007) 71:77–87
2000). As vegetation continued, Ca level linearly
increased (P < 0.001). Similarly, P content was
within the range of that in conventional forage
sources (NRC 2001). Madibela et al. (2002) reported
that V. verrucosum and V. rotundifolium contained 9
and 7 g Ca kg1 DM and 1 and 1.1 g P kg1 DM,
and 2.5 and 3.1 mg Cu kg1 DM, which were lower
than those measured in the present experiment
(Table 3). Iron content was lower than legume and
grass forages, whereas Cu content was within the
ranges published for these plant forms (NRC 2001).
Copper level is recommended not to exceed 40 mg
kg1 DM (NRC 2001). Thus, mistletoe feeding
would not cause Cu toxicity. Zinc content was highly
variable by the type of tree (Table 3 and Fig. 3),
particularly for willow, which was 3-fold greater than
conventional forage sources (27–36 mg kg1 DM)
(MacPherson 2000). In agreement with this, Madibela et al. (2000) reported that V. verrucosum and
V. rotundifolium contained 18.9 and 24.0 mg Zn
kg1 DM. Thus, due to a high level of Zn, mistletoe
from willow (85.8 mg kg1) could be fed to eliminate deficiency. Similar to changes in mineral content
with advancing the vegetation, Ramirez et al. (2001)
investigated mineral content of 14 different short
shrubs and reported that mineral content was the
highest in summer. In general, the mistletoes are rich
in concentrations of Ca, Cu, Fe, Mg, Mn, N, P, K, Na,
and Zn and also have capability of tolerating longterm water-use efficiency (Panvini and Eickmeier
1993).
Dry matter degradation was almost completed
within 48 h relative to incubation (Table 4). As
vegetation advanced from spring to autumn, the
soluble portion of DM (fraction ‘‘a’’) increased,
whereas insoluble but degradable portion of DM
(fraction ‘‘b’’) decreased. As fraction ‘‘a’’, in effective
degradability of dry matter degraded increased with
advancing vegetation (Fig. 3A). This could be linked
to decreased NDF level (Table 2). Studies on DM
degradability of Viscum species are limited. As
compared with other Viscum species (V. verrucosum
and V. rotundifolium) as reported by Madibela et al.
(2003), fraction ‘‘a’’ in the present experiment was
lower. The same researcher also reported that fraction
‘‘b’’ was 44.2 and 44.0% and EDDM was 52.4% and
60.8%, respectively, which are similar to those
measured in this study (Table 4). Degradability of
DM greatly varies in shrubs (Baba et al. 2002;
85
Camero et al. 2001; Tolera et al. 1997). In clover
and orchard grass, fraction ‘‘a’’ and EDDM decrease
with stage of maturity (Balde et al. 1993). In opposite
to conventional forages, these parameters increased
with advancing vegetation stage.
Decreased cumulative gas production within 48 h
of incubation and the amount of gas produced from
the insoluble but slowly fermentable portion (fraction
‘‘b’’) with advancing vegetation stage (Table 5 and
Fig. 3B) could be related to decreased structural
carbohydrates. Cumulative gas production and the
amount of gas produced from the insoluble but slowly
fermentable portion (fraction ‘‘b’’) ranged from
52.7 ml to 58.9 ml and from 48.8 ml to 75.4 ml,
respectively. After 48 h incubation, these parameters
were estimated to range from 37.2 ml to 51.3 ml and
from 54.9 ml to 65.2 ml in four different legume
bushes (Nherera et al. 1999). In a similar experiment,
these parameters for 10 different legume and grass
species at three different vegetation stages were
reported to range between 32.4 ml and 40.3 ml and
between 34.9 ml and 45.0 ml (Khazaal et al. 1993).
Conclusion
This experiment was conducted to investigate nutrient contents and nutritive values of different
mistletoe species in relationship to differing vegetation stage for ruminant nutrition. In comparison with
commonly used conventional forages, mistletoe was
low in protein, moderate in fibre, and high in
minerals. In conclusion, as long as a lack of
deleterious effects on health and performance is
shown in controlled in vivo feeding trials, mistletoe
can be used as a dietary component for ruminants.
References
AFRC (1992) Nutritive requirements of ruminant animals:
protein. AFRC Technical Committee on Responses to
Nutrients. Report No. 9. Nutrition abstracts and reviews
(Series B), 62:787–835
AOAC (1984) Official methods of analysis (1984) 14th edn, Ed
by Sidney Williams, Arlington, VA, USA
Baba ASH, Castro FB, Ørskov ER (2002) Partitioning of
energy and degradability of browse plants in vitro and the
implications of blocking the effects of tannin by the
addition of polyethylene glycol. Anim Feed Sci Technol
95:93–104
123
86
Balde AT, Vandersall JH, Erdman RA, Reeves JB, Glenn BP
(1993) Effect of stage of maturity of alfalfa and
orchardgrass on in situ dry matter and crude protein
degradability and amino acid composition. Anim Feed Sci
Technol 44:29–43
Baykal N (1995) Fitopatoloji. Uludağ Üniversitesi Basımevi,
No: 7-027-0229, Bursa, Turkey
Bhattacharyya B, Johri BM (1998) Flowering plants. Narosa
Publishing House, India
Camero A, Ibrahim M, Kass M (2001) Improving rumen
fermentation and milk production with legume-tree fodder
in the tropics. Agrofor Syst 51:157–166
Close W, Menke KH (1986) Selected topics in animal
nutrition. Deutsche Stiftung für Internationale Entwicklung, Dok 1350 C/a, Germany, p170
Davis PH (1982) Flora of Turkey and the East Aegean Islands,
vol 4. Edinburgh of the University Press, pp 386–387
De Buen LL, Ornelas JF (2001) Seed dispersal of the mistletoe
Psittacanthus schiedeanus by birds in Central Veracruz,
Mexico. Biotropica 33:487–494
Dugenci SK, Arda N, Candan A (2003) Some medicinal plants
as immunostimulant for fish. J Ethnopharmacol 88:
99–106
Garnett GN, Chambers CL, Mathiasen RL (2006) Use of
witches’ brooms by Abert squirrels in ponderosa pine
forests. Wild Soc Bull 34:467–472
Giudici M, Poveda JA, Molina ML, de la Canal L, GonzalezRos JM, Pfuller K, Pfuller U, Villalain J (2006)
Antifungal effects and mechanism of action of viscotoxin
A(3). FEBS J 273:72–83
Godschalk SKB (1983) Mistletoe dispersal by birds in South
Africa. In: Calder M, Bernhardt P (eds) The biology of
mistletoes. Academy press, Sydney, New South Wales,
Australia, pp 117–128
Goering HK, Van Soest PJ (1970) Forage fiber analysis
(apparatus, reagents, procedures and some applications).
Agricultural Handbook 379. United States Government
Pressing Office, Washington DC, USA
Hajto T, Hostanska K, Saller R (1999) Pharmacological
perspectives of mistletoe therapy. Forschende Komplementarmedizin 6:186–194
Hawksworth FG, Geils BW (1990) How long do mistletoeinfected ponderosa pines live? West J Appl Forestry 5:
47–48
Hawksworth FG, Wiens D (1996) Dwarf mistletoes: biology,
pathology, and systematics. United States Forest Service
Agricultural Handbook 709, Washington DC, USA
Kaitho RJ, Nsahlai IV, Williams BA, Umunna NN, Tamminga
S, Van Bruchem J (1998) Relationships between preference, rumen degradability, gas production and chemical
composition of browses. Agrofor Syst 39:129–144
Khazaal K, Dentinho MT, Ribeiro JM, Ørskov ER (1993) A
comparison of gas production during incubation with
rumen contents in vitro and nylon bag degradability as
predictors of the apparent digestibility in vivo and
voluntary intake of hays. Anim Prod 57:105–112
Knight AP, Walter RG (2003) Plants affecting the digestive
system. In: A guide to plant poisoning of animals in North
America. International Veterinary Information Service,
www.ivis.org
123
Agroforest Syst (2007) 71:77–87
Liu SL, Du XB, Kong JL (2006) New polypeptides from
Chinese mistletoe, Viscum coloratum (Kom.) Nakai.
Chinese Chem Lett 17:41–44
Long RJ, Apori SO, Castro FB, Ørskov ER (1999) Feed value
of native forages of the Tibetan plateau of China. Anim
Feed Sci Technol 80:101–113
MacPherson A (2000) Trace-mineral status of forages. In:
Givens DI, Owen E, Axford RFE, Amed HM (eds) Forage
evaluation in ruminant nutrition. CAB International, UK,
pp 345–370
Madibela OR, Boitumelo WS, Letso M (2000) Chemical
composition and in vitro dry matter digestibility of four
parasitic plants (Tapinanthus lugardii, Erianthenum
ngamicum, Viscum rotundifolium and Viscum verrucosum) in Botswana. Anim Feed Sci Technol 84:97–106
Madibela OR, Letso M, Boitumelo WS, Masedi M, Alton K
(2002) Chemical composition of four parasitic plants
harvested over a period of 6 months from two sites in
Botswana. Anim Feed Sci Technol 95:159–167
Madibela OR, Mabutho S, Sebolai B (2003) Dry matter and
crude protein degradability of four parasitic plants
(Mistletoes) associated with browse trees in Botswana.
Trop Anim Health Prod 35:365–372
McDonald P (1981) A revised model for the estimation of
protein degradability in the rumen. J Agric Sci Camb
96:251–252
Menke KH, Steingass H (1988) Estimation of the energetic
feed value obtained from chemical analysis and in vitro
gas production using rumen fluid. Anim Res Dev 28:7–55
Nherera FV, Ndlovu LR, Dzowela BH (1999) Relationships
between in vitro gas production characteristics, chemical
composition and in vitro quality measures in goats fed
tree fodder supplements. Small Rumin Res 31:117–126
NRC (1989) Nutrient requirements of dairy cattle, 6th edn.
National Academy Press, Washington, DC, USA
NRC (2001) Nutrient requirements of dairy Cattle, 7th edn.
National Academy Press, Washington, DC, USA
Ohiri FC, Esimone CO, Nwafor SV, Okoli CO, Ndu OO (2003)
Hypoglycemic properties of Viscum album (mistletoe) in
alloxan-induced diabetic animals. Pharm Biol 41:184–187
Ørskov ER, McDonald I (1979) The estimation of protein
degradability in the rumen from incubation measurements
weighted according to rate of passage. J Agric Sci Camb
92:499–503
Panvini AD, Eickmeier WG (1993) Nutrient and water
relations of the mistletoe Phoradendron-Leucarpum
(Viscaceae)—how tightly are they integrated. Am J Bot
80:872–878
Parks CG, Bull EL, Thinn RO, Shepard JF, Blumton AK
(1999) Wildlife use of dwarf mistletoe brooms in
northeastern Oregon. West J Appl For 14:100–105
Pryme IF, Bardocz S, Ousztai A, Ewen SWB (2006) Suppression of growth of tumor cell lines in vitro and tumors
in vivo by mistletoe lectin. Histol Histopathol 21:285–299
Radenkovic M, Ivetic V, Popovic M, Mimica-Dukic N,
Veljkovic S (2006) Neurophysiological effects of
mistletoe (Viscum album L.) on isolated rat intestines.
Phytother Res 20:374–377
Ramirez RG, Haenlein GFW, Núñez-González MA (2001)
Seasonal variation of macro and trace mineral contents in
Agroforest Syst (2007) 71:77–87
14 browse species that grow in Northeastern Mexico.
Small Rumin Res 39:153–159
Romney DL, Gill M (2000) Intake of forages. In: Givens DI,
Owen E, Axford RFE, Amed HM (eds) Forage evaluation
in ruminant nutrition. CAB International Publishing, UK,
pp 43–62
Sarı M (1976) Meşe yaprakları ile kengel dikenlerinin hayvan
besleme bakımından analizleri. Fırat Üniv Vet Fak Derg
3:7–14
SAS (1998) Statistical Analysis System. User’s guide:
statistics, version 7th. SAS Inst., Inc., Cary, NC, USA
87
Stec B (2006) Plant thionins -the structural perspectives. Cell
Mol Life Sci 63:1370–1385
Tilley MA, Terry RA (1963) A two-stage technique for in vitro
digestion of forages. J Br Grassl Soc 18:104–111
Tolera A, Khazaal ER, Ørskov ER (1997) Nutritive evaluation
of some browse species. Anim Feed Sci Technol 67:
181–195
Turquet C, Salle G (1996) Characteristics of chloroplasts
isolated from two mistletoes originating from temperate
(Viscum album) and tropical (Tapinanthus dodeneifolius)
areas. Plant Physiol Biochem 34:283–292
123
View publication stats
Behiç Coşkun