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205
World Rabbit Sci. 2006, 14: 205-230
© WRSA, UPV, 2003
Correspondence: L.Maertens, luc.maertens@ilvo.vlaanderen.be
Received May 2006 - Accepted October 2006.
ABSTRACT: This literature review focuses on the milk yield and milk composition of rabbits and the non-nutritional
factors affecting both quantity and quality. Actual highly efficient hybrid does have an average daily milk yield of 250
g or 60 g/kg of live weight during the 4-weeks lactation period. However, compared with cow and sow milk, rabbit’s
milk is much more concentrated in fat (12.9 g/100 g), protein (12.3 g/100 g) and energy (8.4 MJ/kg) which explains
the extremely rapid growth of the young (weight × 6 after 3 weeks). Characteristic of rabbit milk is also the nearly
absence of lactose (<2 g/100 g). At peak lactation, protein output per kg metabolic weight (13.4 g/day/kg0.75)
exceeds even those of Holstein milk cows. The non-nutritional factors having the largest impact on the milk yield are
the number of suckling kits, the parity order (primiparous vs. multiparous) and the gestation overlapping degree
(rapid decline after 17-20 days of gestation). However, also through the reduction of feed intake, heat stress has
a detrimental impact especially when the night temperature remains above 25°C. Rabbit milk lipids are highly
saturated (70.4% SFA) due to the high content of C8:0 – C12:0 (50% of total FA) and further characterised by nearly
equal quantities of oleic and linoleic acid and an w-6/w-3 ratio around 4. Finally some data about the amino acid, milk
proteins including the immmunoglobulins, mineral and vitamin composition are presented.
Key words: rabbit, milk, quantity, quality, affecting factors, review.
WORLD
RABBIT
SCIENCE
INTRODUCTION
Rabbit does are in general allowed to nurse their kits till weaning age (4-5 weeks of age). Kits are until
18-19 days of age exclusively depending from the milk of their mother (Maertens and De Groote,
1990; Fortun-Lamothe and Gidenne, 2000). Newborn rabbits have high energy requirements and a
low thermal isolation. Therefore early liveability and growth performances are closely related to the
quantity and quality of the milk ingested (Lebas, 1969 and 1976; McNitt and Moody, 1988; Fraga et
al., 1989; Szendrö and Maertens, 2001). Recently, this relationship has been stressed by Szendrö et
al. (2002) using 2 nursing does per litter.
The lactation requires a great energy effort of the doe and is closely related to some variables as
corporal condition, fecundity and foetal growth (Fortun-Lamothe and Bolet, 1995; Pascual et al.,
2003; Xiccato et al., 2004). Moreover, genetic selection in maternal lines has focussed mainly on
prolificacy resulting in parental lines with a litter size of over 10 kits (Tudela et al., 2003). Consequently,
demands and requirements of does for milk yield have increased greatly. However, strains were
primarily successfully selected for increased litter size but weaning weight of kits dropped
(Rochambeau, 1998). This indicates that the relative increase of milk yield was smaller than that of
litter size, leading to smaller amounts of milk available per kit (Szendrö and Maertens, 2001).
RABBIT MILK: A REVIEW OF QUANTITY, QUALITY AND NON-DIETARY
AFFECTING FACTORS.
Maertens L.*, Lebas F.†, Szendrö Zs.‡
*Inst. for Agricultural and Fisheries Research, Animal Science Unit, 9090 MELLE, Belgium.
†Cuniculture, 87a Chemin de Lasserre, 31450 CORRONSAC, France.
‡Univ. of Kaposvár, Faculty of Animal Science, 7400 KAPOSVAR, Hungary.
206
MAERTENS et al.
Rabbit milk is collected for the production of recombinant proteins in transgenic animals (Castro et
al., 1999; Bõsze and Houdebine, 2006). The high protein content of rabbit milk together with the high
yield/kg live weight and the rapid reproduction rhythm are attractive characteristics to use rabbits
for this purpose. Nevertheless, milking of rabbit does remain an exceptional goal. Consequently,
information relating with milk yield and composition remains relatively scarce although interesting
work was already executed, mainly in France, already 35 years ago (Lebas, 1968, 1969, 1971 and 1976;
Lebas et al., 1971). The present review intends to update this information and to discuss the main
factors influencing milk yield and milk composition of does used for meat production. Dietary effects
on milk yield and composition were recently reviewed by Pascual et al. (2003) and thus they should
be only marginally mentioned in this review.
METHODOLOGY USED TO MEASURE THE MILK YIELD OR TO
COLLECT SAMPLES
Direct method
In larger animal species (e.g. cows, sheep), mechanical or manual milking is used as direct method to
measure milk production. Also for rabbits milking machines were developed and described (Lebas,
1970; Schley, 1975; Marcus et al., 1990). Milking or sampling is always done after a 24-hour separation
of mother and kits avoiding the free suckling of kits. Females have to be treated with oxytocine in
order to stimulate the milk ejection. When the females are fixed in a comfortable position with suitable
milking equipment, equivalent or higher amounts than that ingested by the kits at one suckling can
be collected (Lebas, 1970). This methodology is generally used for the collection of milk from transgenic
rabbits (BioProtein Technologies, 2006). However, in animal research studies, this methodology is
not used to determine the milk yield capacities during the whole lactation period.
Indirect measurement
The nursing behaviour of the rabbit is characterised by a daily short event of only 3-4 minutes
(Cross, 1952; Hudson et al., 2000). Although most does show a strong circadian basis with one
nursing event every 24 hours, a limited number of females nurse their kits more than once a day
(Zarrow et al., 1965; Hoy and Selzer, 2002; Matics et al., 2004). However, it has not been demonstrated
that more milk is produced or that kits grow faster when the doe performs (or is allowed or not) more
than one nursing a day (Hudson et al., 2000). For example Zarrow et al. (1965) have observed exactly
the same daily gain, day after day, from 2 to 30 days after kindling for kits able to suckle their mother
freely, only once or twice a day. An explanation could be found in the observations of Calvert and
Knight (1982) that milk secretion is performed at a constant speed during the 24 hours following a
nursing and thereafter dropped dramatically. Nevertheless with the double suckling method, Gachev
(1971b) observed a slight reduction of milk production during the last 6 hours fraction of the 24 hours
period (19.4% of the total yield vs 24.8% to 28.0% for the 3 others 6 hours periods).
As a consequence of the nursing behaviour, daily milk yield can easily and accurately measured by
determining the weight difference of the doe before and after nursing (Lebas, 1968). This weight-
suckle-weight method is widespread used for research purposes and has an advantage over weighing
of the kits. Kit weighing is more difficult because they are nervous and the accuracy is lower because
kits show some urine losses even during the suckling event (Lebas, 1971).
During the first stage of the lactation period, the next box can be closed and daily opened to nurse
the kits and to determine the milk yield. However, once the kits starts to consume solid feed, from day
18 onwards (Fortun-Lamothe and Gidenne, 2000), housing of the kits has to be in a separated cage or
in an adapted cage to allow both the milk yield determination as the normal development of the kits
(Fortun-Lamothe et al., 2000).
207
NON-DIETARY FACTORS AFFECTING RABBIT MILK QUANTITY AND QUALITY
The indirect measurement of the milk yield is a time and labour consuming method. However, when
only 3 measures per week are executed, total yield can be calculated with a high accuracy (R²=0.982;
RSE=5.2) (Fernández-Carmona et al., 2004). Using a quadratic regression model obtained from 3
measurements per week (9 in total), Fortun-Lamothe and Sabater (2003) estimated daily and total milk
yield of each doe in the 0-21 days lactation period.
Estimation based on the growth of the suckling kits
There exist a high correlation between the milk production and the growth of the kits because rabbit
kits do not show significant feed intake before the age of 18-19 days (Maertens and De Groote 1990;
Fortun-Lamothe and Gidenne, 2000). The highest correlations reported are for the period between
birth and 21 days of age and amount to 0.90 (Lebas, 1969), 0.91 (Fortun-Lamothe and Sabater, 2003)
or even 0.99 (Lukefahr et al., 1983). Weight gain of the litter at a later stage is much less correlated
with the milk yield in the corresponding period (Lebas, 1969). Although litter weight at 21 days is
highly correlated with the milk yield (R²=0.917; RSE=11.5) (Fernández-Carmona et al., 2004), litter
weight gain at 21 days is a better predictor of the doe milk yield than litter weight at 21 days (Fortun-
Lamothe and Sabater, 2003).
For actual high productive hybrid does the following equation was drawn (Fortun-Lamothe and
Sabater, 2003):
Milk yield 0-21 d (g) = 1.69 × weight gain of the litter 0-21 d (g) + 362 (r=0.91)
Collection of samples
There are different methods to collect milk samples. Apart from a milking machine, samples can be
collected by manual milking by gently pushing on the mammary gland. An experienced person can
collect during 1-2 minutes easily 20 ml even without injection of oxytocin (authors’ personal
observations). Although Lebas (1971) did not find significant differences in the composition of 4
consecutive samples of 45-70 g, he recommends for analysis a sample quantity of at least a quarter of
the total amount present. However, it was never proved that the composition of the first 20 g by e.g.
hand milking is not representative for the total quantity.
Another milk collection method is to take, immediately after the nursing, a sample out of the kit’s
stomach by means of an orally introduced stomach tube (Fraga et al., 1989; De Blas et al., 1995). This
method is easy but some contamination may occur with gastric secretions and with the residual milk
still contained in the stomach even after a 24 hours period (authors’ personal observations).
MILK YIELD
The usual lactation period of does is between 4 and 5 weeks depending on the reproduction rhythm
and management system. However, mainly for experimental purposes, early weaning is sometimes
executed and a shorter lactation period is considered (Xiccato et al., 2004). In absence of a new
pregnancy, milk production can continue up to 6 weeks or even a longer period (Cowie, 1968; Lebas,
1969).
Papers dealing with milk yield of does are quite limited and most of them are linked with nutrition
experiments. In Table 1 only papers that have measured the milk yield and when does were fed ad
libitum are considered. Milk yield is often expressed in different ways: i) as the total quantity produced
in a certain period ii) as an average production during a period or iii) as the sum of a limited number
of determinations. Therefore, it is not easy to compare the data in the different papers including milk
yield data. Moreover, many of the results published are strongly influenced by diet or does genotype
but also by reproduction rhythm, environmental temperature, parity, and so on. A detailed discussion
about their impact on milk yield is presented below.
208
MAERTENS et al.
Based on the data of Table 1, actual strains used for commercial meat production have a 28-days milk
yield in their first lactation of about 5.5 kg (Xiccato et al., 1995; Pascual et al., 2002b, Maertens et al.,
2006). Multiparous hybrid does, nursing 9-10 kits, have a yield that exceed 7.0 kg during a 28-days
lactation period or 250 g/d or around 60 g/d when expressed per kg of live weight (LW) (Fortun-
Lamothe and Sabater, 2003; Xiccato et al., 2005; Maertens et al., 2006).
Table 1: Descrip tion o f the p ap e r s d e a ling with milk yield.
Reference Diet
Breed/
Strain/ Line Parity
Litter
size
No. of
lacta t io ns
Milk yield
Period
(d)
Tota l
(g)
Top
(g/d)
Average
(g/d)
g/kg
LW2
Lebas, 1968 Reproduction diet Fauve de
Bourgogne
Different 8-9 143 0-42 7090 242 169 42.3
Partridge and
Allen, 1982
a) Low protein diet
b) Medium protein diet
c) High protein diet
New Zealand
x C a lifo r nia n
2+ 8 6
6
6
0-28
0-28
0-28
3890
4820
5270
139
172
188
34.8
43.0
47.0
Luke fahr et al.,
1983
Reproduction diets NZW
Californian
Cal x NZW
NZW x Cal
Different NSLS1In total:
225
0-21
0-21
0-21
0-21
3970
3060
4030
3650
189
146
192
174
47.2(3)
38.4(3)
49.2(3)
44.6(3)
Maertens and De
Groote, 1988
Low energy diet
Medium energy diet
High energy diet
Hybrid (Elco) 2-5 8 15
16
15
0-28
0-28
0-28
6140
6330
6810
219
226
243
51.2
53.4
57.3
Fraga et al.,
1989
Different reproduction
diets
Californian x
New Zealand
NSLS 22
17
17
17
0-28
0-28
0-28
0-28
5680
4700
5020
4600
203
168
179
164
50.7
42.0
44.8
41.0
McNitt and
Lukefahr, 1990
Reproduction diet Californian
New Zealand
Palomino
White Satin
Different NSLS 19
23
22
21
0-29
0-29
0-29
0-29
4582
3973
3480
3683
158
137
120
127
40.0
31.9
29.0
29.9
Mohamed and
Szendrö, 1992
Reproduction diet Californian
(3.8 kg)
?6
8
10
4
8
8
0-21
0-21
0-21
3567
3686
3776
170
176
180
44.7(3)
46.3(3)
47.4(3)
Khalil, 1994 Commercial diet Giza White
(3.2 kg)
Different 222 0-35 3493 100 31.3
Taboada et al.,
1994
L-lysine level:
a) 0.64%
b) 0.68%
c) 0.71%
d) 0.76%
e) 0.82%
New Zealand
x C a lifo r nia n
2+ NSLS 14
14
14
14
14
0-30
0-30
0-30
0-30
0-30
5820
6280
6440
6850
6550
299
313
330
351
337
194
209
215
228
218
50.0
53.3
55.4
59.0
56.1
De Blas et al.,
1995
Lactation diets with
different starch and fat
content
New Zealand
x C a lifo r nia n
2+ NSLS 16
16
16
16
16
0-30
0-30
0-30
0-30
0-30
5830
5820
6060
5940
5730
297
296
307
292
297
194
194
202
198
191
47.8
49.2
51.3
49.4
48.8
Xiccato et al.,
1995
Medium ene rgy level
High energy level
High fat level
Hybrid
(Provisal)
1816
17
15
0-30
0-30
0-30
5130
5400
5730
171
180
191
42.3
44.3
47.3
De Blas et al.,
1998
Threonine le ve l:
a) 0.54%
b) 0.58%
c) 0.63%
d) 0.68%
e) 0.72%
Hybrids
(Hyplus)
2+ NSLS 16
16
16
16
16
0-30
0-30
0-30
0-30
0-30
5400
5650
5680
5830
5780
277
290
287
300
300
180
188
189
194
193
43.2
45.4
45.5
46.3
46.6
209
NON-DIETARY FACTORS AFFECTING RABBIT MILK QUANTITY AND QUALITY
Continuation Table 1.
Pascual et al.,
1998
a) Starch rich
lac tation diet
b) Soy oil rich
lac tation diet
Crossbreed
(V x A rabbit
does)
2
2
820
18
0-28
0-28
5348
6608
191 236 50.7
61.8
Pascual et al.,
1999a
a) Control
reproduction diet
b) With added
vegetable fat
c) With added animal
fat
Crossbreed
(V x A rabbit
does)
2+ 8 or 11 40
40
40
0-35
0-35
0-35
5540
6263
6365
158
179
182
40.2
47.3
46.0
Pascual et al.,
1999b
a) Low energy diet
b) Medium energy diet
c) High energy diet
Crossbreed
(V x A rabbit
does)
1-2+
1-2+
1-2+
± 8 21-46
20-38
18-49
0-35
0-35
0-35
5740-6090
5430-5425
5240-5495
164-174
155-155
150-157
44.5(3)
40.8(3)
40.3(3)
Xiccato et al.,
1999
Lactation diet Hybrid
(Provisal)
1 8 23 0-30 6150 205 52.6
Fraga et al.,
1989
Different reproduction
diets
Californian x
New Zealand
NSLS 22
17
17
17
0-28
0-28
0-28
0-28
5680
4700
5020
4600
203
168
179
164
50.7
42.0
44.8
41.0
Pascual et al.,
2000b
a) Reproduction diet
b) Alfalfa based diet
c) Alfalfa based +
animal fat
Crossbreed
(V x A rabbit
does)
1+2 8 51
52
49
0-28
0-28
0-28
5376
4480
4788
192
160
171
50.5(3)
42.1(3)
45.0(3)
Pascual et al.,
2002a
a) Animal fat enriched
diet
b) Vegetable oil
enriched diet
c) Starch rich diet
Crossbreed
(V x A rabbit
does)
11020
21
23
0-28
0-28
0-28
5087
5055
4550
182
181
163
49.7
46.2
42.2
Pascual et al.,
2002b
a) Control
reproduction diet
b) High fibre fo llowe d
by control diet
Crossbreed
(V x A rabbit
does)
1822
24
0-28
0-28
4844
5404
173
193
43.0
48.8
Fo rtun-Lamothe
and Sabater,
2003
Standard reproduction
diet
Hybrid
(INRA)
2+ 10 50 0-21 5300 315 252 62.2
Khalil et al.,
2004
not defined Ga bali x
Spanisch V
line crosses
(3.5 kg)
1-2+ NSLS 2141 0-28 4331 155 44.3(3)
Xiccato et al.,
2004
Lactation diet Hybrid
(Hyplus)
1; 2; 3 922
23
24
0-21
0-26
0-32
4242
4964
5774
202
191
180
53.6
52.3
49.8
Xiccato et al.,
2005
Lactation diet Hybrid
(Hyplus)
2+ 10 31 23 0-21
0-25
5417
6296
258
252
64.0
61.5
Zerrouki et al.,
2005
Reproduction diet Kabylian
(2.8 kg)
1-4+ 2-8 299 0-21 2180 147 104 37.2(3 )
Maertens et al.,
2005
a) Lactation diet
b) w-3 lactation diet
Hybrids
(4.2 kg)
1-6 8-9 179
205
d3,5,9,
12,16,19
244
236
58.1(3)
56.2(3)
Maertens et al.,
2006
Lactation diet Hybrids 1 2 7.4
8.8
45
35
0-29
0-29
5900
7600
256
317
203
262
50.2
61.8
1 NSLS : no t sta nd a rdise d litte r size; 2 Recalculated using the given average doe live weight (LW); 3 Recalculated using average strain LW if
data were lacking
210
MAERTENS et al.
Average peak lactation of multiparous commercial hybrids is around 320 g/d (Fortun-Lamothe and
Sabater, 2003; Xiccato et al., 2005; Maertens et al., 2006). Expressed per kg LW, peak yield is around
75 g/d and exceeds those of milk cows (Kay et al., 2005) or sows (Lauridsen and Danielsen, 2004)
(Table 2). When expressed per kg of metabolic weight, which is preferred by some scientists because
of its physiological basis (but not really accurate because it is a production of a milk mass by a body
mass), milk production of rabbit is still lower than that of productive Holstein cows or hybrid
sows.(Table 2).
FACTORS INFLUENCING MILK YIELD
Lactation stage
Average lactation curves of multiparous hybrid does at different physiological status are presented
in Figure 1 (adapted from Lebas, 1968; Szendrö et al., 1985; Xiccato et al., 1995; Maertens et al.,
2006).
The top lactation is situated on day 18-19 after kindling (Lebas, 1968; Maertens and De Groote, 1991;
Fortun-Lamothe and Sabater, 2003; Casado et al., 2006). However, in case of deficiencies in amino-
acid supply (De Blas et al., 1995; Taboada et al., 1994) or when primiparous does are submitted to the
intensive reproduction rhythm, the lactation peak is reached 2-3 days earlier (Maertens and De
Groote, 1991; Xiccato et al., 1995; Pascual et al, 1999b). Moreover, Lebas (1968) observed a breed
difference; Fauve de Bourgogne does reached top lactation 3-4 days (day 21) later than Californian
does.
The lactation curve of rabbits is asymmetric with a convex ascending and a concave descending
period (Lebas, 1968). The principle component analysis executed by the same author (Lebas, 1976)
using 975 lactation curves, revealed that 74.3% of the variability between lactation curves could be
explained by 3 main factors. The most important was the total daily amount, followed by a factor
expressing the asymmetry of the curve and finally a factor determining the amplitude of the curve,
explaining respectively 58.3, 10.1 and 5.8% of the variability.
Table 2: Comparison of daily milk yield, fat and protein output at lactation peak between multiparous
high productive rabbit does, cows and sows.
Hybrid rabbit does1Holstein cows2Hybrid sows3
Live weight (kg) 4.2 650 230
Peak milk yield (kg) 0.320 47.5 8.9
Milk fat (g/100 g) 12.9 3.7 6.5
Milk protein (g/100 g) 12.3 2.84 5.1
Output/kg live weight (LW)
Milk (g/d) 76 73 39
Fat (g/d) 9.8 2.7 2.5
Protein (g/d) 9.4 2.1 2.0
Out p ut/k g metabolic weight (LW0.75)
Milk (g/d) 109 369 151
Fat (g/d) 14.1 13.7 9.8
Protein (g/d) 13.4 10.5 7.7
1Based on data of Table 1 and Table 5; 2Kay et al. (2005); 3Lauridse n and Danielsen (20 04)
211
NON-DIETARY FACTORS AFFECTING RABBIT MILK QUANTITY AND QUALITY
Recently Casado et al. (2006) proposed different empirical models for the 28-day lactation curve,
based on 550 lactation records. The beta-modified equation had a better fit suitability than the
quadratic model and the advantage of a greater biological interpretation of its parameters. The
following prediction model is proposed (Casado et al., 2006):
Milk yield (g/day) = k × (day/30)a × (1− (day/30))b
where k regulates the height of the curve and a and b regulate the milk yield of the ascending and
descending period, respectively. In the equation given by these authors, values for the parameters k,
a and b are respectively 470.156; 0.489 and 0.371 (R²=0.986, RSD=5.648).
There are only few data available concerning the weekly yields of does. When we recalculate the
data of Lebas (1968) based on 143 lactations, on a 4 weeks lactation basis, 15.9, 24.4, 32.0 and 27.3%
were produced in weeks 1 till 4, respectively. The analysis of Fernández-Carmona et al. (2004), based
on 943 records obtained in their experimental farm, revealed a similar weekly partition of 18, 27, 30 and
25%, respectively for weeks 1-4. However, the partition between lactation weeks is strongly dependent
if the doe is concurrent pregnant or not (Lebas, 1972; Xiccato et al., 1995). According to Lebas
(1968), if the litter weaning is delayed to 35 or 42 days post parturition, and if the doe is not pregnant,
the milk production during the 5th or the 6th week represents 19.5% or 12.9% respectively of the 0-28
days milk production.
Gestation overlapping degree
The negative impact of the gestation overlapping on milk yield was already clearly demonstrated by
Lebas (1972) and confirmed in several other studies. In practise only 3 reproductive rhythms are
frequently used: intensive with complete overlapping, semi-intensive with overlapping from 11 days
after parturition and a rhythm without significant overlapping. Does submitted at the intensive
reproduction rhythm (mating or artificial insemination (AI), within 48 h after kindling) begin showing
decreased milk production after 17 days (Maertens and De Groote, 1991; Fraga et al., 1989; Xiccato
et al., 1995 and 2005; Pascual et al. 2002a) to 19 days (Lebas, 1972; Partridge et al., 1986a; Szendrö et
al., 1985; Kustos et al., 1996; Xiccato et al., 1995) of lactation with a sharp and quite linear decrease
during the last 10 days of pregnancy (Figure 1). However, in primiparous does that are concurrently
pregnant shortly after parturition, this decline starts already at day 16-17 of the lactation (Maertens
and De Groote, 1991; Xiccato et al., 1995; Pascual et al., 2002a). Moreover in some experiments peak
yield was lower in does pregnant immediately after parturition compared to does not pregnant before
day 11 post parturition (Szendrö et al., 1985; Xiccato et al., 1995).
Milk yield (g/d)
Figure 1. Lactation curve
of multiparous does
according to their
physiological status.
50
75
100
125
150
175
200
225
250
275
300
325
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35
lactation day
Not pregnant
PP pregnant
11d PP pregnant
212
MAERTENS et al.
The decrease in milk yield due to the gestation overlapping during the entire 28-day lactation period
was between 19-22% according to the diet (Maertens and De Groote, 1988) and in line with the 20%
decrease determined by Xiccato et al. (1995). Although the milk yield decrease between 21 and 28
days was 38% in the experiment of Pascual et al. (2002a), for the whole lactation period only a 9%
lower yield was determined in post-partum pregnant females compared to does without gestation
overlapping. When compared to females pregnant from day 9 post parturition off, total milk yield was
9% lower in females with complete gestation overlapping (Fraga et al., 1989).
When females are submitted to the usual semi-intensive reproductive system with AI 11 days
postpartum, the milk yield is only slightly decreased from day 25 off compared to females inseminated
after weaning (Szendrö et al., 1985; Casado et al., 2006). The decrease is limited to around 25 g during
the last days of a 28-day lactation period. If weaning is performed later, a sharp decline of the milk
yield is observed with virtual dried up does after 35 days of lactation (Figure 1). However, when no
concurrent gestation occurs, still a significant (70 g) yield was measured at day 38 (Szendrö et al.,
1985).
The decline in milk yield due to the gestation overlapping is a result of the pregnancy requirements
that consistently increase with the exponential foetal development (Parigi-Bini and Xiccato, 1998),
the increasing volume of the uterus reducing the voluntary feed intake and due to hormonal changes
caused by the imminent kindling contrasting with those for lactation.
Number of suckling kits
In various studies it has been demonstrated that the number of suckling kits is the main factor
affecting milk yield of does and by consequence the intake of the suckling kits (Lebas, 1969; Torres
et al., 1979; Partridge and Allen, 1982; McNitt and Lukefahr, 1990; Pascual et al., 1996 and 1999a). In
Figure 2, the relationship between the number of suckling kits and the milk yield is presented (Lebas,
1987). Based on these data, the following quadratic model was fitted between milk yield and number
of suckling kits:
Milk yield (g/day) =37.47x -1.56N² (R²=0.999, RSD=3.77)
where N is the number of kits (range=5-11).
In the experiments of Partridge and Allen (1982), does allowed to nurse 8 kits had a 24.1% higher yield
compared to does with only 4 kits. Mohamed and Szendrö (1992) found an increase with 3.3% and
5.4% of the milk yield with increasing litter sizes from 6 to 8 and 10 kits, respectively. Pascual et al.
Milk yield (g/d)
Figure 2. Relationship between the number of suckling kits and milk yield (Lebas, 1987).
140
150
160
170
180
190
200
210
220
230
567891011
N° of suckling kits
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NON-DIETARY FACTORS AFFECTING RABBIT MILK QUANTITY AND QUALITY
(1996) determined even a difference of 32% in milk yield in favour of litters of more than 10 kits
compared to litter sizes of 7-8 kits.
The effect of the number of suckling kits on milk yield was even clear if litter size was reduced from
10 to 4 kits at day 16 of the lactation (Fortun-Lamothe and Gidenne, 2000). Milk yield between 16 and
32 days of lactation dropped by 45% in does nursing only 4 kits. This indicates that the intake
capacity of the kits, suckling only once a day, is limited because in the experiments of Szendrö et al.
(2002) kits that nursed in morning and evening by 2 different does had a 89% higher intake compared
to single nursed kits.
However, not only an increasing number of suckling kits favours milk yield but also an increasing
litter weight at birth increases milk production as consequence of the uterine induction. Vásquez
Martínez et al. (1999) studied the interaction between both factors using a complete kit exchange at
birth and standardized litter sizes of 7, 8 or 9 suckling kits (Figure 3). Does with low litter weight (<450
g) showed no increase in milk yield with increasing number of suckling kits. On the contrary, does
with medium and high litter weight at birth (>450 g) had a significant higher yield by assigning
additional kits. Due to the limited number of kits born or suckling kits in some non selected lines or
populations, maximum milk production can therefore not be reached as demonstrated by Bolet et al.
(1996). However, Zerroucki et al. (2005) demonstrate in a local population that maximum does milk
production capacity can be reached for a number of kits lower than the maximum litter size naturally
observed in this population: in theses author’s observations milk production increases regularly
with the suckling kits number until a maximum (7 in the present case) above which a plateau production
is observed whatever the kits number (7, 8 or 9).
Both for experimental purposes as under commercial field conditions, due to the common practise of
cross fostering between does littering on the same day, the effect of litter size on milk yield is
minimised. Nevertheless when comparing does milk production published in the literature, attention
must be paid to the number of kits to which the litter size was adjusted in each case.
Parity order
The milk yield of does has a curvilinear relationship with parity (Khalil, 1994) and increases until the
third lactation and stabilizes thereafter (Casado et al., 2006). McNitt and Lukefahr (1990) reported
even an increase till the 7th litter; however because less productive females were progressively culled
out, their selection policy has favoured the milk yield with increasing parity order.
Figure 3. Effect of number of assigned kits on the milk yield of does dependent of the initial litter weight at
birth (Vásquez Martínez et al., 1999).
Milk yield 0-21d
0
1
2
3
4
5
6
<450 450-600 >600
Initia l litte r birth weig ht (g)
7
8
9
Assigned kits
aa
a
aa
bb
b
a
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MAERTENS et al.
The highest difference is found between the 1st and 2nd lactation. Even at standardised litter size,
Xiccato et al. (2004) reported an increase of 10% and 8% of the milk yield during lactation 2 and 3,
respectively. Pascual et al. (1999b) found a much more modest increase between primiparous and
multiparous does, on average only 3.6%. This difference was more pronounced (6.3%) when using a
low energy diet. Based on the litter weight at 3 weeks, Vicente and Garcia-Ximénez (1992) report a
difference of 14% in favour of multiparous does. Maertens et al. (2006) determined a 19.9% higher
yield in lactation 2 compared to lactation 1 even after a correction for the difference in litter size. Part
of this great difference could be explained by the early first insemination (15-16 weeks) compared to
the aforementioned studies.
The milk production increase is a response to the higher live weight and feed intake capacity of
multiparous does (Pascual et al., 1999b; Xiccato et al., 2004). Parigi-Bini and Xiccato (1998) mentioned
an increase of the voluntary feed intake of 10-20% from the first to the 2nd lactation and 7-15% from
the 2nd to the 3rd lactation. Moreover, primarily primiparous does have to share the energy between
the demands for milk (and eventually concurrent pregnancy) with those for body accretion because
they have not yet reached their adult weight (Parigi-Bini and Xiccato, 1998).
Number of nipples
A majority of does has 8 to 10 productive teats with independent mammary gland, although there is
a variation between 6 and 12 (Szendrö and Holdas, 1984; Fleischhauer et al., 1985). Nevertheless in
lines selected for litter size, teats number was increased as a passive answer to selection, and females
with 10 nipples may become the most numerous: 37% to 51% in 2 selected lines vs 27% in the control
line (Rochambeau et al, 1988). Females with less than 8 teats have a significant lower milk yield than
those with 8 or more teats (Fleischhauer et al., 1985). However, in this study, females with 6 teats
were obtained after surgically removing of 2 mammary glands. In the same study, females having
more than 8 teats showed a slightly higher milk yield (+2.2%). Szendrö and Holdas (1984) as did not
found significant differences in weight gain of kits till 21days of age between does having 8, 9 or 10
productive teats, although the highest value was obtained for does with 10. However Rochambeau et
al. (1988) considering only litters with more than 10 kits born alive, i.e. with kits number exceeding
that of nipples, observed higher litter weaning weights (28 days) for does having 10 nipples compared
to 8 (+13.2%), which implies a higher milk production.
Later on, limited attention has been putted on this factor. Only Mohamed and Szendrö (1992) compared
females with 8 and 10 nipples and determined a 4.8% higher milk yield in does having 10 nipples.
According to the observations of Petersen et al. (1989), milk secretion is higher in the middle pairs of
teats than in pairs 1 and 4.
Genotype
In the intensive rabbit meat production, pure breeds are still seldom used and replaced by specialised
strains or lines selected for a higher litter size and therefore indirectly for a higher milk yield (Garreau
et al., 2004). The populations originating these actual selected strains or lines belonged near
exclusively to breeds of medium size, as mainly the New Zealand White or/and Californian. Usually,
the females on commercial rabbit farms are obtained by crossbreeding of these strains or lines to gain
the heterosis effect. These females are named crossbreds or “commercial hybrids”.
Literature data comparing milk yield of different breeds are scarce. Lukefahr et al. (1983) demonstrated
that New Zealand White does are superior (+ 30%) to Californian does and that crossbred rabbits of
both breeds are superior than the pure breeds. However, in another study, the same team determined
a comparable milk production for the 4 breeds tested (Calfornian, New Zealand White, Palomino and
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NON-DIETARY FACTORS AFFECTING RABBIT MILK QUANTITY AND QUALITY
White Satin) (McNitt and Lukefahr, 1990), which indicate that the genetic background of the particular
populations is perhaps more important than the breed itself.
Vicente and Garcia-Ximénez (1992) found significant higher litter weights after the 2nd and 3rd lactation
week in 2 synthetic lines compared with purebred New Zealand White and Californian. Native breeds
as Giza White (Khalil, 1994) or Kabylian rabbit population (Zerrouki et al., 2005) have a modest yield
(average over the whole lactation period of 100 and 104 g/d, respectively) compared to the actual
production level of over 200 g/d for commercial parental does (Fortun-Lamothe and Sabater, 2003;
Xiccato et al., 2005; Casado et al., 2006). However, these native breeds have a low adult weight.
When their milk yield is expressed per kg LW, the difference with medium-size breeds or hybrids is
less pronounced (Table 1). Moreover, comparing milk yield between different experiments (and strains)
remains difficult because especially for these native breeds temperature conditions were not
favourable. Under favourable housing conditions, recent reported data of multiparous females of
hybrid dam lines demonstrate an average daily yield of 250-260 g during the 4-weeks lactation period
(Xiccato et al., 2005; Maertens et al., 2006).
Even in the same population a large individual variability has been observed. Fernández-Carmona et
al. (2004) used the records of 943 lactations of crossbreds from 2 lines selected for litter size (V x A)
and milk yield ranged between 46 and 306 g/d during the 28 days lactation period. Also Khalil et al.
(2004) obtained, using a large data set, a variation coefficient of 38% for milk yield (0-21 d). Moreover,
heritability of milk production is low and amounts only 0.14 (Lukefahr et al., 1996) or 0.18 (Khalil et
al., 2004) for the cumulative 1 to 21 days of lactation. However, under current field conditions, litters
are equalised at parturition and by consequence milk yield is much more homogeneous with the
exclusion of the initial litter size effect (Casado et al., 2006).
Finally, in a study using transgenic does (for obtaining the presence of human clotting factor VIII,
hFVIII in their milk) milk yield was not significantly different from non-transgenic does descending
from the same founder females (Rafay et al., 2004). However, as the authors pointed out, it is necessary
to verify these preliminary results on a larger set of animals before to generalize this observation for
all transgenic does.
Temperature
High environmental temperatures have a detrimental effect on milk yield of does. Several studies
have clearly demonstrated that the effect of high temperature can be explained by the drop in feed
intake which is in the same range as the drop in milk yield (Rafai and Papp, 1984; Maertens and De
Groote, 1990; Pascual et al., 1996; Szendrö et al., 1999a).
Under constant ambient temperatures, Rafai and Papp (1984) found a decrease of 7.7 g/d with each
centigrade of temperature rise above 20°C. Moreover, the relative decrease is depending from the
lactation stage, being largest in the week with the highest yield (3rd week) (Rafai and Papp, 1984;
Pascual et al., 1996; Szendrö et al., 1999a). The detrimental effect of high temperature on milk yield
was also clearly observed by Fernández-Carmona et al. (2000). When housed in a climatic chamber at
30°C, milk yield dropped with 30-40% according to diet compared with housing under conventional
circumstances (Pascual et al., 2000b).
In the study of Szendrö et al. (1999a) the heat stress was not yet pronounced on milk yield when
housed at 23°C (Figure 4). However, at 30°C, average daily milk yield was reduced with 29% (114 g vs.
161 g/d).
Under natural housing conditions, with varying temperature between day and night, heat stress is
less pronounced and seems to be linked with the minimal temperature during the active feeding
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MAERTENS et al.
period (Maertens & De Groote, 1990). However, when the minimum temperature was above 24°C total
lactation yield was reduced with 17.3% compared to conditions below 24°C (Pascual et al., 1996).
Rearing, feeding, body weight and body condition
The litter size in which does were raised in before weaning did not influence their later milk yield
(Rommers et al., 2001). However, it has been shown that the feeding regime during the rearing period
has an influence on the subsequent litter weight (milk yield) of primiparous does and even in
multiparous does. Primiparous does fed restrictively during rearing and ad libitum later had an
increased litter weight at 16 days (Rommers et al., 2004) or 21 days (Gyovai et al., 2004) compared to
always ad libitum fed young does. The significant increased feed intake during the subsequent
lactation observed in previously restricted reared does seems responsible for this effect in primiparous
does (Rommers et al., 2004). However, in the 2 following lactations an effect on the feed intake was
not more clear in this study indicating that some other factors could be involved, such as higher
body weight and/or appropriate body condition. Gyovai et al. (2004) observed higher body weight
(at 1st kindling and maintaining during the successive cycles) in does reared under feed restriction. In
contrast, Rommers et al. (2004) reported higher body weight in ad libitum reared does but their lower
milk yield fall essentially on the very heavy young does (>4,5 kg at first insemination at 17.5 weeks
of age), perhaps excessively fatty (Rommers, 2004). In earlier experiments, Coudert and Lebas (1985)
did not observe any significant effect of feed restriction during rearing on does LW measured 7 days
after the kindling in the 3 first lactations. Thus some factors other than rearing conditions seem to be
as well important for milk production or does body weight as the feed restriction itself.
Complementarily, in ad libitum reared does inseminated at early age (14.5 weeks), small young does
(<3.5 kg, averaging 3.18 kg at insemination) had significant lower litter weight at 16 days (milk yield)
than heavier, in their two first lactations (Rommers et al., 2002).
Milk yield (g)
Figure 4. Effect of temperature ( ) on milk yield of does (Szendrö et al., 1999a).
40
60
80
100
120
140
160
180
200
220
0 3 6 9 12 15 18 21 24 27 30
Days after kindling
15°C
23°
30°
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NON-DIETARY FACTORS AFFECTING RABBIT MILK QUANTITY AND QUALITY
Body weight of different dam lines did not have a significant effect on milk yield although their
weight differed by 10% at their first parturition (Fortun-Lamothe and Bolet, 1998). However, Pascual
et al. (2002a) observed that does presenting a better body condition at partum showed higher milk
yield. Perirenal fat thickness at parturition used as indicator for body condition revealed to be
positively correlated (r=+0.36) with the subsequent milk yield. However, the change of the body
condition during the lactation is negatively correlated with milk yield (r=−0.24 and −0.61, Fortun-
Lamothe and Lebas, 1996 and Pascual et al., 2002a, respectively). This shows that does exhibiting
higher body-fat losses during the lactation have also a higher milk yield. This relation could be
reinforced or reduced according to diet’s composition as demonstrated by Pascual et al. (2003) in
their review.
MILK COMPOSITION
Major components
The average chemical composition of rabbit milk is presented in Table 3 and Figure 5. In total 20
original publications were found with determined data of the macro nutrient composition from does
fed a standard diet. Data referring to experimental diets with high fat content were excluded from the
dataset used for this review. Literature data are grouped per lactation week.
The lactose content of doe milk was determined only in few experiments because of the minor
importance due the low content (<2 g/100 g) especially at a later stage of the lactation (Lebas, 1971).
Moreover, in several experiments the content was calculated by difference with the other nutrients.
As a result, the variation coefficient is high for lactose (Table 2).
There exists little information concerning the composition of the colostrum of does (Lebas, 1971; El-
Sayiad et al., 1994; Christ et al., 1996). Based on these data the colostrum DM is higher than milk DM
(33 vs. 30 g/100 g) due to a higher protein content and fat content. However, this composition has to
be taken with caution because the samples were collected on the day after kindling. The real colostrum
is already consumed by the kits during the initial suckling which takes place during the parturition
(Hudson et al., 2000).
Based on the overview of literature data (Figure 5), the composition of rabbit milk is quite stable
during the 2nd and 3rd week of the lactation, except for the protein content which shows a decreasing
trend (from 12.8 till 11.9 g/100 g) with increasing daily milk yield. This quite constant composition
during the 3 first weeks of the lactation (with exception of the first days) is remarkable because milk
yield increases in that period with a factor of 2 till 3.
Already in week 4, the DM content is on average 2.6 points (+ 8.7%) higher and the fat and protein
content increase by 1.1 g/100 g (+ 8-9 %) compared to the average of the first 3 weeks (Table 3). In
week 5, a strong concentration of the milk is observed which results in a DM, fat and energy content
of 36.9 g/100 g, 18.7 g/100 g and 10.5 MJ/kg, respectively. Ash and protein increase more slowly in the
final week of the lactation.
The changes in composition in the later stage of the lactation period are closely related with the
decrease in milk yield (Lebas, 1971; Partridge at al., 1986a). The dramatic reduction of the lactose
content is even higher than the corresponding drop in milk yield (Lebas, 1971). In does immediately
pregnant after parturition, dry matter, protein and fat increases one week earlier than in does not
concurrently pregnant (Kustos et al., 1996). An interruption of the lactation by omission of one
suckling leads to changes in milk composition similar to those observed with declining milk yield
(Szendrö et al., 1999b). However, some days later the composition returns to levels approaching the
original values.
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MAERTENS et al.
Table 3: Che mic a l co mp o s it io n of rabbit milk dep e nding o f the lactatio n st a ge
Lactation week Mean Range CV(%) n1
Dry matter (g/100 g) Colostrum 32.6 31.4-33.7 5 2
1 29.8 25.6-31.4 9 5
2 30.0 25.7-33.1 9 9
3 29.5 25.8-33.2 7 19
4 32.4 29.8-33.7 5 6
5 37.7 34.2-42.1 7 6
Ash (g/100 g) Colostrum 1.8 1.7-2.0 18 2
1 1.9 1.8-2.0 6 3
2 1.9 1.3-2.2 16 7
3 2.2 1.5-2.6 13 13
4 2.4 1.8-2.6 15 5
5 2.4 2.0-2.8 12 5
Protein (g/100 g) Colostrum 14.7 13.5-15.9 12 2
1 12.8 11.2-14.8 11 6
2 12.2 10.1-14.1 10 11
311.99.9-14.31020
4 13.4 10.6-15.5 12 7
5 14.1 12.4-16.9 11 6
Fat (g/100 g) Colostrum 16.3 13.7-20.4 22 3
112.79.1-16.1205
213.18.9-17.0199
3 12.9 10.0-16.6 16 19
4 14.0 12.2-15.7 11 5
5 18.9 16.9-21.4 9 6
Lactose (g/100 g) Colostrum 1.9 1.6-2.1 18 2
1 1.6 1.0-2.0 36 3
2 1.4 1.0-1.9 33 3
3 1.9 0.3-3.2 50 8
4 1.8 0.8-2.6 51 3
5 1.0 0.2-1.8 9 2
Energy (MJ/kg) Colostrum 9.3 - - 1
1 8.4 8.4-8.4 0.1 3
2 8.5 7.5-9.6 10 6
3 8.3 7.1-9.2 7 9
4 9.2 8.5-10.0 8 3
510.59.8-11.693
1n= number of literature references used to calculate the values in table.
References: Castellini et al. (2004), Christ et al. (1996), Cole et al. (1983), El-Sayiad et al. (1994), Fraga et al. (1989), Kowalska
and Bielanski (2004), Kustos et al. (1999), Lebas (1971), Lebas et al. (1996), Maertens et al. (1994, 2005 and 2006), Partridge
and Allan (1982), Partridge et al. (1983, 1986a and 1986b), Pascual et al. (1996, 1999a and 2000a) and Xiccato et al. (1999)
219
NON-DIETARY FACTORS AFFECTING RABBIT MILK QUANTITY AND QUALITY
Figure 5. Milk composition changes during the lactation period (literature compilation, see Table 3).
Milk composition did not vary significantly between New Zealand White and Duch rabbits (Cowie,
1968) or between commercial hybrids (Maertens et al., 2006). However, El Sayiad et al, (1994) found
significant higher crude protein levels in Californian does (12.02 g/100 g) than in New Zealand
females (11.02 g/100 g) The effect of temperature or the feeding level seems not very outspoken.
Only at 30°C a trend to decreasing fat, protein and especially lactose content was observed (Kustos
et al., 1999).
In general, rabbit milk can be characterised as a very protein and fat rich milk (12.3 and 12.9 g/100 g,
respectively) but with low lactose content (1.7 g/100 g). Compared to cow and sow milk, rabbit milk
is respectively 2 and 3 times more concentrated in fat and protein (Table 5). The lactose content is
only one third of the 2 other species. Remarkable is also the high energy content of rabbit milk (8.4
MJ/kg) which explains the rapid growth of the kits (LW x 6 after 3 weeks).
At peak lactation, fat and protein output per kg LW are 3 to 4 times higher in rabbits compared with
cows and sows (Table 2). This explains why rabbits are searched as bioreactor for the production of
recombinant proteins. The fat production per kg metabolic weight at peak lactation equals (14.1 g/
kg0.75) that of high productive Holstein cows and exceeds that of hybrid sows (Table 2). The protein
production (13.4 g/kg0.75) exceeds largely those of both cows and sows.
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MAERTENS et al.
Milk lipids
With an average lipid content of 12.9 g/100 g (Table 5), it is clear that the greatest energy source
quantitatively for the suckling kit is the fat component. The milk lipids are composed mainly of
triglycerides with small proportions of di- and monoglycerides, phospholipids, cholesterol, fat-soluble
vitamins and free fatty acids (Smith et al., 1968; Perret et al., 1977; Demarne et al., 1978; Christie,
1985). Triglycerides of acyl carbon number less than 42 made up about 75% of the total glycerides in
rabbit milk (Smith et al., 1968).
The fatty acid (FA) profile of rabbit milk is characterized by a very high content of short-chain FA,
mainly caprilic (C8:0), capric acid (C10:0) and, to a smaller extent, lauric acid (C12:0), which represent 50%
of the total FA (Table 4). Consequently, milk fat of rabbits differ very markedly from the carcass depot
fats. On average 70% of the milk FA are saturated (SFA), 13% monounsaturated (MUFA) and 16%
polyunsaturated FA (PUFA). Nevertheless it must be pointed out that in the suckling kit, the fate of
the saturated FA is very different according to the carbon chain length: short chained FA (70.0% of
saturated FA) are almost exclusively used as energy source (or basis for length elongation) and only
the longer ones are transferred in the body fat (Ouhayoun et al, 1985).
The milk contains nearly equal proportions of oleic and linoleic acid, and some ù-3 linolenic acid.
Concerning the longer w-3 FA searched for their potential as beneficial for health, small amounts of
C20:5,w-3 (EPA: 0.04%) and C22:6,w-3 (DHA: 0.06%) are mentioned by Castellini et al. (2004) and Kowalska
and Bielanski (2004). Moreover, these last authors found also a small amount of conjugated linoleic
acid (CLA) (0.08%). The proportions of these polyunsaturated FA are mainly dependent of the
lactation diet.
Fatty acids in milk are derived from blood triglycerides and de novo synthesis in the mammary gland.
Short-chain FA are synthesized within the mammary gland rather than by FA uptake from circulating
blood or by oxidation of long-chain FA (Carey and Dils, 1972). Acetate is an important precursor of
both C8:0 and C10:0 (Jones and Parker, 1978).
Diet has a very strong influence on the FA profile of rabbit milk especially on the medium and long-
chain FA (see the review of Pascual et al., 2003), but only little information exists concerning the non-
nutritional factors affecting FA composition. Perret et al. (1977) determined an increase of short
triglycerides (C<36) at the expense of long triglycerides (C>46) after the 10th day of lactation and the
same effect but less pronounced for FA (Hall, 1971). Significant changes of the FA profile during the
lactation stage were confirmed by Pascual et al. (1999a). Short-chain FA and by consequence SFA
showed a significant increase at the 21st and 28th day. The trend for medium-chain FA was opposite,
showing the highest proportions on day 7 of the lactation except for C15:0 and C17:0 that remained
constant during lactation (Pascual et al., 1999a; Christ et al., 1996).
The FA profile of rabbit milk is strikingly different from cow and sow milk (Table 5). Data refer to a
standard feeding of these species because especially fat-enriched diets manipulate to a large extend
the FA profile (Pascual at al., 2003). The high concentration of short-chain FA (C6:0 to C12:0) results in
a more saturated milk compared to especially sow milk. On the contrary, medium-chain FA (C14:0 to
C17:1) are nearly three times as high in cow and sow milk. Due to the low content of C18:1, rabbit milk
has a rather low MUFA content MUFA (12.8%) compared to cows (30.1%) and sows (41.5%). The
PUFA content is comparable with sows and much higher than in cow milk. The ratio w-6/w-3 FA
(around 4) is intermediate between sows and cow milk.
The FA profile is also remarkable different from the hare or rodents fed the same diet. The concentration
of short-chain FA are 2.1 times lower in hare milk compared to rabbit milk (Demarne et al., 1978).
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NON-DIETARY FACTORS AFFECTING RABBIT MILK QUANTITY AND QUALITY
Short-chain FA are even absent in guinea pig milk, and to a much lesser extent are present in mouse
(one third of rabbit) or rat milk (half of rabbit) (Smith et al., 1968).
Rabbits are known for their sensitivity to dietary-induced hypercholesterolemia but their milk
cholesterol levels can be normally maintained unless the maternal plasma cholesterol concentration
is extremely elevated (Whatley et al., 1981). Milk cholesterol concentration increases from 28.0 (day
5) till 89.7 mg/100 ml (day 35 of the lactation) in close correlation with the milk triglycerides and
drying up of the females (Whatley et al., 1981). In the mammary gland the cholesterol excretion in
milk is regulated but without local synthesis: nearly all the milk cholesterol derived from the blood
plasma cholesterol (Connor and Lin, 1967).
Milk protein composition
Rabbit milk proteins have been studied intensively in view of biomedical research for e.g. the production
of recombinant proteins in the milk or serum. A recent successfully example is the human a-glucosidase
produced in the milk of transgenic rabbits to treat the Pompe´s disease (Van den Hout et al., 2001).
However, in this review the information will be limited to the composition of the main constituents,
referring for specific information to other reviews (Fan and Watanabe, 2003; Bõsze and Houdebine,
2006).
Table 4: Fatty acid comp o s itio n of rabbit milk.
Fatty acids (% of total fatty acids)
Mean CV(%) n1
C4:0; C5:0; C7:0 Traces - 1
C6:0 0.4 20 3
C8:0 26.3 27 6
C10:0 20.1 21 6
C12:0 2.9 30 5
C14:0 1.6 39 6
C15:0 0.8 79 3
C16:0 12.8 23 6
C17:0 0.7 55 3
C18:0 2.9 11 6
C20:0; C22:0 Traces - 2
Total saturated fatty acids (%) 70.4 14 7
C14:1;C17:1; C20:1 Traces - 2
C16:1 1.5 59 6
C18:1 11.3 18 6
Total monounsaturated fatty acids (%) 12.8 17.6 7
C18:2 12.8 37 7
C18:3 2.5 36 7
CLA 0.08 - 1
C20:4 0.5 49 2
EPA (C20:5 w-3) 0.04 47 2
DHA (C22:6 w-3) 0.06 64 2
Total polyunsaturated fatty acids (%) 15.6 35 7
1n= number of literature references used to calculate the values in table.
References: Caste llini et al. (2004), Christ et al. (1996), Fraga et al. (1989), Kowalska and Bielanski (2004), Lebas
et al. (1996), Maertens et al. (2005), Pascual et al. (1999a).
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MAERTENS et al.
The protein-rich milk of rabbits provides primarily the amino acids essential for tissue growth and
maintenance but also to continue a certain degree of immune protection through the presence of
specific whey proteins. Information concerning the amino acids composition is given in Table 6.
However, the data of rabbit milk have to be taken with caution because the total sum of amino acids
expressed per 100 g amino acids is 118.6 g (recalculated data from Uribe et al., 1980) or only 76.9 g
(Kustos et al., 1999).
Rabbit milk proteins as for other mammals, are grouped in two main types: caseins which precipitate
in the isoelectric conditions (pH 4.6) and represent about 70% of the total milk proteins and whey
proteins which do not precipitated in these conditions (Dayal et al, 1982). After numerous attempts
to identify the various types of casein present in rabbit milk (Allais and Jollès, 1970; Majumder and
Ganguli, 1970; Testud and Ribadeau-Dumas, 1973; Al Sarraj et al., 1978; Dayal et al., 1982; Baranyi et
al., 1995; Grabowski et al, 1991, Virag et al., 1996), 4 types can be clearly distinguished now: aS1-
casein, aS2-casein, a-casein and k-casein. Total of caseins represent about 90 g/l with a specific
contribution for example of 45 g/l of b-casein and 16 g/l of aS1-casein (Grabowski et al, 1991). Virag et
Table 5: Comparative composition of milk from rabbits, cows and sows.
Rabbit does1Cows2Sows3
Dry matter (g/100 g) 29.8 12.5 - 13.5 17.9
Protein (g/100 g) 12.3 3.0 - 4.0 5.1
Fat (g/100 g) 12.9 3.5 - 5.0 6.5
Lactose (g/100 g) 1.7 4.5 - 5.0 5.7
Energy (MJ/kg) 8.4 2.7- 3.2 4.5
Fatty acids (% of total FA) C6:0 0.4 1.5 n.r.
C8:0 26.3 0.9 n.r.
C10:0 20.1 2.0 0.4
C12:0 2.9 2.4 0.5
C14:0 1.6 14.3 5.6
C16:0 12.8 24.4 29.4
C16:1 1.5 1.7 13.7
C18:0 2.9 11.9 6.3
C18:1 11.3 27.5 27.6
C18:2 12.8 1.6 13.3
CLA 0.08 1.26 n.r.
C18:3 2.5 0.71 1.4
C20:1 n.r.4n.r. 0.2
C20:4 0.5 0.04 0.09
C20:5 (EPA) 0.04 0.01 0.16
C22:6 (DHA) 0.06 0.04 0.20
Other 4.2 6.3 1.2
Total SFA 70.4 60.0 42.2
Total MUFA 12.8 30.1 41.5
Total PUFA 15.6 3.6 16.3
Ratio w-6/w-3 4.1 2-3 7.2
1Average composition of lactation weeks 1-3 (Table 2). 2
FA adapted from Rego et al. 2005 (Control diet, pasture). 3
Lauridsen
and Danielsen, 2004 (Control diet). 4Not reported.
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NON-DIETARY FACTORS AFFECTING RABBIT MILK QUANTITY AND QUALITY
al. (1996) mentioned a micelles size of skimmed rabbit milk varying from 210 to 230 mm in relation with
the 8 patterns of aS2-caseins observed in the milk of New Zealand White does. One of the functions
of the k-casein is the formation, stabilisation and aggregation of the micelles (Gerencsér et al, 2002).
In addition some hydrolysed fractions of aS1 and b-casein have a clear antibacterial activity which
most probably participate in the protection of digestive tract of suckling kits (Baranyi et al., 2003).
The main types of whey proteins are a-lactalbumin, tranferrin, serum albumin, whey acidic protein
(WAP) and immunoglobulins (Baranyi et al; 1995). Transferrin is present at 17 to 23 g/l (Jordan and
Morgan, 1970) and is an iron binding protein identical to the serum transferrin (Baker et al., 1968)
which has no immunological reaction with the classical lactoferrin (Lyster, 1967). This specificity
explains for example why Masson and Hermann (1971) failed to find lactoferrin in the rabbit milk in an
extensive study of lactoferrin in different species conducted with an immuno-methodology. Despite
its identity with serum transferrin, the milk transferrin is almost exclusively synthesised and secreted
in the mammary gland (Jordan and Morgan, 1970). This protein has an in vitro antibacterial activity
against Escherichia coli, but it is not clear if this function is still active in vivo in the kits digestive
tract (Baker et al., 1968).
As previously mentioned, other whey main proteins detected in rabbit milk are serum albumins (4-5
g/l), different lactalbumins, WAP (15 g/l) (Jordan and Morgan, 1970; Grabowski et al, 1991; Baranyi
et al., 1995) and different immunoglobulins but no protein resembling to the cow b-lactoglobulin (the
main whey protein in cow milk) was detected (Lyster, 1967). Nevertheless this affirmation disagrees
with the results of Stambolova and Gachev (1972) which have identified a rabbit whey protein with an
electrophoretic pattern identical to that of the bovine b-lactoglobulin.
The g-globulin concentration is around 10 g/l and increases in milk during lactation (Jordan and
Morgan, 1970; Maertens et al., 1994). According to Berthon and Salmon (1993), the specific
immunoglobulins concentration decreases from colostrum to milk. They are represented mainly by
the IgG form, which represents 95.2% of the total immunoglobulins of colostrum (30 g/l) and 98% of
milk ones (5 g/l). The IgA represent a higher proportion in colostrum (4.7%) than in milk (2.0%). In
addition the presence of few IgM can be noticed in colostrum (0.1% of the total) but only traces are
present in milk. During g-globulin secretion in the mammary gland, the initial serum IgA is modified
and T-Chains are added (Asofsky and Small, 1967). The immunoglobulins present in the first suckled
colostrum seem to be transferred to the kit serum (Goszinska et al, 1969). But later, absorption
Table 6: Amino acid compo sition o f rab b it a nd sow milk .
Amino acid
g/100 g amino acid
Amino acid
g/100 g amino acid
Rabbit1Sow2Rabbit1Sow2
Lysine 9.0-7.6 7.5 Valine 8.0-5.9 4.7
Methionine 3.0-1.6 1.7 Tryptophan 1.3 -3 1.4
Cysteine -31.5 Arginine 6.4- 4. 8 5.2
His tidine 5.3 - 2.3 2.4 Proline 3. 2 - 3 11.3
Phenylalanine 4.9-3.3 3.9 Glycine 1.5-3.7 2.8
Tyrosine 6.2-2.6 4.2 Glutamic acid 25.0-12.7 21.6
Threonine 7.3-4.1 3.9 Aspartic acid 8.1-4.0 7.9
Isoleucine 4.2-3.6 3.8 Serine 5.6-6.1 5.2
Leucine 11.9-8.9 8.8 Alanine 7.7-5.7 3.2
1Left values from Uribe et al. (1980); right values from Kustos et al. (1999). 2
Acc ording to Dar ra gh and M oughan (19 98). 3Traces
for Ur ibe et al. (1980) and not determined by Kustos et al. (1999).
224
MAERTENS et al.
throught the intestinal epithelial cells of the kits in direction of blood is generally stopped inside the
enterocytes (Krahenbuhl and Campiche, 1969).
The immunisation of does against specific agents such as E. coli or Vibrio cholerae induce the
presence of specific IgA antibodies in the milk during the whole lactation (Yoshiyama and Brown,
1987; Milon and Camguilhem, 1989). These IgA can be immediately locally active in the kit digestive
tract. But their short half-life (3 days) makes them ineffective after weaning (Milon and Camguilhem,
1989).
Also prolactin and growth hormone binding proteins have been identified in rabbit milk (Postel-
Vinay et al., 1991) as well as thyroid hormones (Slebodzinski and Gawecka, 1983). In addition a lot of
active enzymes are detectable in rabbit milk (Hellung-Larsen, 1968).
Mineral content
The ash content of rabbit milk (Table 3) increases from about 1.8% during the first weeks of the
lactation till 2.4% in the 4th and 5th week of the lactation. This increase can partly be ascribed to the
drying up of the does and as consequence of the higher dry matter content with declining milk yield.
Rabbit milk is rich in calcium although its concentration varies according to the source (Table 7).
Also sodium and potassium concentration is high compared to sow milk (Darragh and Moughan,
1998). Since lactose and sodium are two of the main constituents concerned in maintaining the
constancy of the osmotic properties of milk it is not surprising that the low level of lactose in rabbit
milk is compensated by a sodium concentration higher than in cow milk (Coates et al., 1964). The
reduction of milk lactose concentration observed after the lactation peak is clearly associated with a
decrease of sodium and a correlative increase of potassium content because of the osmolarity
regulation (Gachev, 1971a)
As for the major components, mineral composition changes substantially after lactation peak
especially when does are concurrently pregnant and a very rapid drying up of their milk yield occurs.
Calcium concentration and to a lesser extend phosphorus increase with progressing lactation stage
(Lebas et al., 1971; Perret et al. 1977; Kustos et al., 1996) while the effect for potassium and sodium
is less clear. Potassium concentration drops dramatically with decreasing milk yield according to
Kustos et al. (1996) but this was not very outspoken in earlier work of Lebas (1971), Gachev (1971a)
and El-Sayid et al. (1994). El Sayid et al. (1994) reported a gradual increase of the sodium content
Table 7: Mineral compo sition (g/kg milk) of ra b b it milk 1.
Lebas et al.
(1971)
Perret et al.
(1977)
El-Sayid et al.
(1994)
Kustos et al.
(1996)
Kustos et al.
(1999)
Sodium 1.03 0.82 1.16 0.84
Potassium 1.981.771.682.01
Calcium 5.36 3.64 4.82 2.76 2.71
Magnesium 0.35 0.36 0.45
Phosphorus 3.28 2.61 2.44
Chlorine 0.66
Zinc 0.02 0.021 0.034
Iron 0.003 0.003
Copper 0.002 0.002
Manganese 0.0001 0.0002
1Average value determined during lactation (colostrum excluded).
225
NON-DIETARY FACTORS AFFECTING RABBIT MILK QUANTITY AND QUALITY
while Lebas et al. (1971) and Kustos et al. (1996) mention a tendency to a higher content at the
beginning and near the end of the lactation period. Magnesium content increases with lactation
stage (Lebas et al., 1971; Kustos et al., 1999) while the microelements (zinc, copper, iron and
manganese) decrease gradually in concentration as lactation progressed (Kustos et al., 1996 and
1999). For example, Tarvydas et al. (1968) observed a reduction of iron content from 3.9-4.6 mg/l 3-4
days after kindling down to 2.3 mg/l on day 17.
Phosphorus concentration decreases in pregnant does at the end of the lactation period probably
due to more phosphorus being derived to foetal growth (El-Sayid et al., 1994; Kustos et al., 1996).
However, the pregnancy effect was much less clear in the work of El-Sayid et al., (1994), because
females were not remated immediately after parturition. Calvert et al. (1985) observed a rise in milk
sodium and chlorine concentration and a decline in potassium and lactose during the milk accumulation
24 h after the last nursing.
Vitamin content
Few data can be found about the vitamin content of rabbit milk. The research done by Coates et al.
(1964) can therefore still be considered as basic information although only 1 or 2 samples per lactation
day were analysed. Rabbit milk is richer than cow milk in all the water-soluble vitamins and vitamin A
(Coates et al., 1964). The high level of vitamin A in the colostrum (6-7 mg/ml) was confirmed by El-
Sayiad et al. (1994) and also the gradually decreasing levels as the lactation proceeds. This fits with
the function of retinol being important for the kit eye development. Basic level of vitamin D3 is fairly
low in milk (0.6 mg/l or 24 IU/l), but very sensitive to doe circulating vitamin D3 level, since a single
injection of a massive vitamin D3 dose increases the milk vitamin D3 for minimum 5 days (Hidiroglou
and Williams , 1985)
The following levels for biotin (0.45 mg/ml), folic acid (0.30 mg/ml), niacin (4.9 mg/ml), pantothenic acid
(14.5 mg/ml), riboflavin (4.6 mg/ml), thiamin (1.6 mg/ml), pyridoxine (B6) (3.6 mg/ml) and B12 (0.07 mg/ml)
were determined on the 18th day of the lactation (Coates et al., 1964). However, some effects of stage
of lactation were observed e.g. an increase for biotin between 1st and 40th day of lactation (multiplied
by 2.7), and simultaneously a decrease of pyridoxine (divided by 6) (Gogeliya, 1970). More recently,
Cole et al. (1983) determined comparable levels for folic acid and vitamin B12 as the aforementioned
values.
Some other components
It has been shown that rabbit milk has antibacterial effects (Canas-Rodriguez and Smith, 1966;
Marounek et al., 2002). When rabbit milk is added in cultures of rabbit caecal contents, a significantly
decreased production of microbial metabolites was determined, whereas no inhibitory effect of a
corresponding mixture of cow milk fat, casein and lactose was observed (Marounek et al., 1999).
The bactericidal effect is linked to the short-chain FA (C8:0 and C10:0) which make that suckling rabbits
are unique amongst other species in the contents of the stomach and small intestine that are almost
completely sterile. This is a natural protection against the risks of the very high milk intake in only
one meal a day. In rabbit milk triglycerides, C8:0 and C10:0 are mainly in the external position on the
glycerol molecule while C16:0 is mainly in the central position (Demarne et al., 1978; Christie, 1985).
This explains the quickly hydrolysis in the stomach which enables their antibacterial role in this gut
segment. In addition and as shown in the protein section, some proteic milk components have their
own anti-bacterial activity such as aS1 and b-casein fractions or transferrin, in addition to the classical
immunoglobulins activity. However, rabbit milk contains only few orotic acid (0.5 mg/l, compared to
the 18 mg/l of cow milk; Gajos and Krêzlewicz, 1974), a residue of arginine catabolism sometimes used
in human medicine in diarrhoea control.
226
MAERTENS et al.
Finally, rabbit milk can contain undesirable components transferred from contaminated diets or
treatments. For example an effective transfer of ochratoxin A from plasma to milk has been
demonstrated (Galtier et al., 1977; Ferrufino-Guardia et al., 2000). Also antibiotic residues are found
in milk as has been demonstrated after a tilmicosin treatment of does (Saggiorato et al., 2004).
CONCLUSIONS
Due to the time consuming determination of the milk yield and the divergent methodology used,
published data concerning the production capacities of does are quite scarce and difficult to be
compared. However, the production level of actual highly efficient hybrids used for commercial
rabbit production can be situated around 250 g/d (or 60 g/d/kg LW). By consequence, during a 30
days lactation period, total milk yield exceeds 7 kg in multiparous does.
There are much more data available of the macro nutrient composition of rabbit milk. Both the macro
composition as the fatty acid composition is widely different from cow or sow milk. Due to the high
yield of does and their concentrated milk, at peak lactation protein output per kg LW and even per
kg0.75 exceeds those of Holstein cows.
Rabbit milk distinguishes from other milks by its extremely high content of short chain FA. Their
antibacterial effects in the gut protect the kits against enteritis risks which are high due to the natural
suckling behaviour (only one daily quantitatively rich meal).
The non-nutritional factors having the largest impact on the milk yield are the lactation stage, the
number of suckling kits, the gestation overlapping degree (rapid decline after 17-20 days of gestation),
the parity order and heat stress (through feed intake depression for the later factor). However, due to
the common practise of equalizing the litter size at parturition, commercial strains are capable to
express their maximal yield aptitude.
Milk production has had little attention in selection programs in spite of its large importance in kit
survival and post-weaning growth.
Acknowledgment: The authors are very grateful to Andre Vermeulen for the help with literature search and data
treatment.
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