The effect of dietary fat on the performance
and body composition of rabbits in
their second lactation
J.J. Pascual
*, C. Cervera, J. FernaÂndez-Carmona
Departamento de Ciencia Animal, Universidad PoliteÂcnica de Valencia, P.O. Box 22012,Valencia 46071, Spain
Received 3 November 1999; received in revised form 10 March 2000; accepted 8 June 2000
Abstr act
The in¯uence of fat addition to diet on performance and body composition was studied in 53 crossbreed rabbit does (CalifornianNew Zealand) by comparative slaughter during the second lactation. Fifteen does were slaughtered immediately after their second parturition (preliminary slaughter group) to estimate initial empty body weight and composition. The 38 remaining does were divided into two groups offered one of two pelleted diets: a control diet (diet C) with 26 g ether extract (EE) kgÿ1
dry matter (DM), and a diet with added fat from vegetable sources at 99 g EE kgÿ1 DM (diet V). The does were slaughtered after a lactation period of 28 days with
standardized litters of eight pups. Fat addition did not affect food intake (117.8 and 116.5 g DM per day kgÿ0.75
for C and V diets, respectively), but increased the digestible energy intake (1296 and 1445 kJ per day kgÿ0.75
; P<0.01), digestible protein intake (15.3 and 17.6 g per day kgÿ0.75
;
P<0.01), milk production (191 and 237 g per day;P<0.01) and litter weight at weaning (3.934 and 4.691 kg;P<0.01). During lactation, rabbit does lost empty body weight (ÿ57 g) and had negative protein, fat and energy balances (ÿ21 g protein,ÿ79 g fat andÿ3.4 MJ energy), but diet had no effect.#2000 Elsevier Science B.V. All rights reserved.
Keywords:Rabbit does; Body composition; Dietary fat; Reproductive performance
1. I ntr oduction
Past energy balance experiments have clearly shown an energy de®ciency during the ®rst lactation period of reproductive rabbit does (Partridge et al., 1983; Parigi-Bini et al.,
86 (2000) 191±203
*Corresponding author. Tel.:34-63-877432; fax:34-63-877439.
E-mail address: [email protected] (J.J. Pascual).
1992, 1996; Xiccato et al., 1995; Fortun-Lamothe and Lebas, 1996), which lose weight and mobilize body tissue. The balance seems to deteriorate further when does are concurrently pregnant (Parigi-Bini et al., 1992, 1996; Xiccato et al., 1995). However, protein mobilization appears to be less predictable and relevant in primiparous does, where little difference has also been detected between pregnant and non-pregnant does (Parigi-Bini et al., 1992; Xiccato et al., 1995).
In the second lactation, energy intake and milk yield increase by varying amounts, but the energy balance should be better maintained. Most research on nutrient balance in multiparous rabbit does have focussed mainly on assessment of protein requirements in lactating and pregnant does; some work found a positive nitrogen balance (Partridge and Allan, 1982; Partridge et al., 1983), but a loss of body tissue nitrogen was observed in the ®rst 16 days of lactation, with a gain thereafter (Partridge et al., 1986b), the recovery apparently being related to a reduction of milk yield. In some of these studies (Partridge et al., 1986a,b) mobilization of body fat was also found. The body fat lost mainly in early and mid lactation was recovered afterwards, when milk output declined, although rabbit does continued mobilizing body tissue up to 32 days of lactation. The ®nal value partially depends upon the physiological condition of the animals. Partridge et al. (1986a) showed a small variation in fat stores in non-pregnant animals, but the amount of fat lost was very high in does on a low energy diet mated inmediately after parturition (Lamb et al., 1984). Several studies have shown that an increase in digestible energy (DE) content of the diet increases the DE intake of the lactating doe, particularly with fat-enriched diets, which leads to higher milk production (Xiccato et al., 1995; Fortun-Lamothe and Lebas, 1996; Parigi-Bini et al., 1996; Pascual et al., 1999). Some authors have found that fat-enriched diets seem to have little in¯uence on body composition of primiparous rabbit does (Fortun-Lamothe and Lebas, 1996; Lebas and Fortun-Lamothe, 1996), but others suggest that high fat diets could accentuate body reserve mobilization, as they mainly stimulate milk yield (Xiccato et al., 1995; Parigi-Bini et al., 1996).
The only available reference for multiparous does comes from Partridge et al. (1986a), who reported that the body fat mobilized in lactation was independent of the diet given in the previous gestation period. Therefore, the present study was designed to obtain more information on the effect of dietary fat on the performance and body change in lactation of multiparous rabbit does.
2. M ater ial and methods
2.1. Diets
The composition and chemical analysis of diets are summarized in Table 1. Two pelleted diets were formulated with different ether extract (EE) and DE content. The control (diet C) was similar to a typical commercial rabbit diet, with 26 g EE kgÿ1
dry matter (DM) and 11 MJ DE kgÿ1
DM. The high energy diet (diet V) was formulated adding vegetable fat at 99 g EE kgÿ1
DM and 12.4 MJ DE kgÿ1
DM. Acid detergent ®bre (ADF) was similar in the two diets (199 and 197 g kgÿ1
(alfalfa hay) were used. Values for DE and digestible protein (DP) were calculated using the apparent digestibility coef®cients obtained by Pascual et al. (1998a) with the same diets. The pelleted diets were offered ad libitum during the experimental period.
2.2. Animals and experimental procedures
Fifty-three crossbreed rabbit does (CalifornianNew Zealand) were used during their second lactation to study the in¯uence of the two experimental diets on the performance and body composition of rabbit does. Until second parturition, all animals received a commercial diet suitable for reproducing does.
Within a few hours after second parturition 15 does were slaughtered (preliminary slaughter group; P group) in order to estimate the initial empty body composition of the 38 remaining does, using the comparative slaughter technique (Parigi-Bini et al., 1992; Xiccato et al., 1995). After second parturition, 20 does were assigned to C diet (C group) and 18 to V diet (V group).
Table 1
Main ingredients (g kgÿ1) and chemical composition (g kgÿ1DM) of diets
Diets
Digestible energy (DE; MJ kgÿ1DM) 11.0 12.4
DE/DP (kJ gÿ1) 84.6 82.1
aAll diets contain 120 ppm BHT antioxidant and 66 ppm robenidine.
bContains (g kgÿ1): thiamin, 0.25; ribo¯avin, 1.5; calcium pantothenate, 5; pyridoxine, 0.1; nicotinic acid,
12.5; retinol, 2; cholecalciferol, 0.1;a-tocopherol, 15; phytylmenaquinone, 0.5; cyanocobalamin 0.006; choline chloride, 100; MgSO4H2O, 7.5; ZnO, 30; FeSO47H2O, 20; CuSO45H2O, 3; KI, 0.5; CoCl26H2O, 0.2;
Na2SeO3, 0.03.
The litter sizes were equalized at eight pups by removing pups or cross-fostering when appropriate and were kept constant throughout lactation, dead pups being replaced daily with pups of a similar weight and age provided from nurse does. Litters were housed in separate cages and the mothers were allowed to enter the nest and suckle once daily in the morning for a short time. Milk production was measured daily during the entire lactation of 28 days by weighing the doe immediately before and after suckling. Food intake and weight of does were recorded weekly. Suckling pups were offered the experimental diets between day 21st until weaning. During this period, solid food intake of litters was measured.
At weaning all does were killed after suckling and weight of does before and after slaughtering was recorded. Carcass measurements were made according to the criteria of Blasco and Ouhayoun (1996). The pelt and bladder were removed and the gut was weighed before and after emptying. After 24 h of refrigeration the empty body was weighed and dissected. The major fat depots were weighed individually: perirenal fat and scapular fat. Inguinal fat weight was included in the perirenal fat weight. The mammary gland, liver and kidney were weighed. The whole empty body was then minced through a cutter-mincer to produce a homogeneous sample suitable for chemical analysis.
2.3. Analytical procedures
The DM, EE, ash, crude ®bre and protein contents of diets and empty bodies of the does were determined using the method of the Association of Of®cial Analytical Chemists (1984), and that of Van Soest et al. (1991) was used for the ADF of diets, with a thermo-stable amylase pre-treatment. Starch in diets was hydrolysed according to a two-step enzymatic procedure, using a thermostable amylase followed by amyloglucosidase (Tecator, application note 85/86), the resulting glucose being measured by the hexokinase/glucose-6-phosphate dehydrogenase/NADP system (Boeringher). The gross energy content of diets and empty bodies of does was determined by adiabatic bomb calorimetry.
2.4. Data analysis
The energy and material balances of the does were calculated on the basis of the difference between the weaning and partum empty body composition. The empty body weight of group P was related to live body weight of does and litter weight at partum by a linear regression equation according to the regression procedure of SAS (PROC REG; Statistical Analysis Systems Institute, 1990). This equation was applied to estimate the empty body weight at partum of the experimental groups of does C and V. In order to determine the ef®ciency of utilization of DE for milk production (milk energy obtained from the DE intake versus DE utilized for milk production), the assumed requirements for maintenance (430 kJ DE kgÿ0.75
per day) and the ef®ciency of utilization of energy reserves for milk production (0.81) recommended for non-pregnant lactating does was also reported by Xiccato (1996).
Analysis Systems Institute, 1990) with a model accounting for the ®xed effect of the diet or group. Comparison between ef®ciency slopes was obtained from the dietDE used for milk production interaction. Comparative analyses between partum group and weaning groups (P versus CV) were also made, using the contrast method of GLM for the variables analysed. The simple correlation coef®cients between the weekly DM intake, milk yield and energy balance were obtained using the Pearson correlation coef®cient (r; procedure PROC CORR of SAS).
3. Results
3.1. Performance and food intake of does
Table 2 shows the effect of diet on the performance of rabbit does and their litters during lactation. There was no signi®cant difference between groups of females in DM intake during lactation, and consequently DE and DP intakes with V diet were signi®cantly higher (P<0.01). Milk yield (P<0.01) and litter weight at weaning (P<0.01) were signi®cantly higher for does given V diet. Finally, an increase in dietary fat content tended to decreased solid food intake of litters (P<0.1) and hence their solid DE and DP intakes were similar with both diets.
Table 2
Effect of diet on the food, energy and protein intakes, live weight, milk yield and performance of does
Diets S.D.a Effect of dietb
C V
Number of observations 20 18
Intake of does during lactation
Dry matter (g kg-0.75per day) 117.8 116.5 13.29 NS
Digestible energy (kJ kg-0.75per day) 1296 1445 156.2 * * Digestible protein (g kg-0.75per day) 15.32 17.59 1.879 * *
Live weight (kg) of does at
Digestible energy (kJ kgÿ0.75per day) 291 237 135.0 NS
Digestible protein (g kgÿ0.75per day) 3.44 2.88 1.607 NS
aS.D.: standard deviation. bNS: not signi®cant;* *
P<0.01;
Trend (P<0.1).
3.2. Ef®ciency of utilization of energy for milk production.
Type of diet had a signi®cant effect on the ef®ciency of utilization of DE for milk production. The addition of high levels of fat to the diet seems to increase signi®cantly this ef®ciency: 0.712 (S.E. 0.012) and 0.787 (S.E. 0.014) for C and V diets, respectively (P<0.001). Fig. 1 shows the relationship between the DE intake used for milk production and the milk energy obtained from the DE intake for both groups. The regression equation of data from does given the high fat diet showed a slightly greater slope than that from does given the control diet, although slopes were not signi®cantly different (P0.13).
3.3. Body composition and energy balance of does
Table 3 shows the weights and body composition at partum and at the end of lactation of does. There was a trend for the weights of gut content, mammary gland and kidneys to be higher (P<0.01) and for the fat depots to be slightly lower (P<0.1) at the end of lactation. The type of diet affected the mammary gland and kidney weights of does; being higher with V diet (P<0.05). The empty body composition of does changed during lactation, the water content increasing (P<0.01) and both fat and energy content decreasing (P<0.05). No differences in body composition between diets were found, and the losses of energy (ÿ43.6 andÿ44.5 kJ kgÿ0.75
per day for C and V diets, respectively) and protein (ÿ0.24 andÿ0.32 g kgÿ0.75
per day for C and V diets, respectively) were similar for both diets.
The net difference between the experimental groups at the 28th day of lactation and the reference group at partum has been calculated in Table 4. The weights of gut content, mammary gland and kidneys increased during lactation, but the does lost liver and fat
Fig. 1. Relationship between the digestible energy intake used for milk production and the milk energy obtained from the digestible energy intake in does given C diet (^) or V diet (&) (unit of energy: kJ kgÿ0.75
Table 3
Effect of lactation on the body composition of does at slaughteringa
Group S.D.b Effectc
P C V Diet P vs. C,V
Number of does 15 20 18
Live body weight (g) 3712 3799 3846 327.4 NS NS
Gut content weight (g) 300 a 401 b 377 b 89.1 * * * *
Pelt weight (g) 403 415 416 39.8 NS NS
Empty body weight (g) 2259 2309 2337 227.2 NS NS
Mammary gland weight (g) 101 a 153 b 189 c 24.0 * * * *
Liver weight (g) 109 107 114 17.5 NS NS
Kidney weight (g) 18 a 19 b 21 c 1.9 * * * *
Fat depots weight (g) 75 54 56 33.9 NS
Composition of empty body (g kgÿ1)
Water 642 a 676 b 677 b 33.7 * * * *
Ash 38 41 41 5.1 NS
Protein 192 189 186 10.5 NS NS
Fat 128 a 94 b 97 b 35.4 * * *
Energy (MJ/kg) 9.5 a 8.2 b 8.2 b 1.40 * * *
aa, b, c, means within a row with different superscripts are signi®cantly different atP<0.05. bS.D.: standard deviation.
Composition of empty body gain of rabbit does during the second parturition
Diets S.D.a Effect of dietb
C V
Weight gain (g)
Live weight ÿ69.0 ÿ35.3 274.45 NS
Gut content 119 95 109.8 NS
Empty body weight ÿ57.7 ÿ56.9 187.14 NS
Mammary gland 39.5 75.6 26.12 * * *
depots weight. The weight and composition of empty body gain of does during lactation were similar for both diets, and hence diet only affected the mammary gland (P<0.001) and kidney (P<0.01) weight gains, which increased more with V diet.
A close relationship between the DM intake and the milk yield of does was found (P<0.001) for both diets during the ®rst 3 weeks of lactation, but it was lower during the 4th (Table 5), especially on C diet (0.269). The data in Table 5 show that there was a negative correlation between the milk production of does during the 4th week of lactation and their fat and energy balance, especially for does given V diet (ÿ0.56 and ÿ0.60, respectively;P<0.01). During the last week of lactation, DM intake of does given V diet was positively correlated with their milk production (0.63;P<0.01), but negatively with their fat and energy balance (ÿ0.44 andÿ0.33, respectively). Fig. 2 shows the different pattern of live weight, milk yield and DM intake of does on V diet that showed a high (284 g) or a low (227 g) milk yield during the 4th week of lactation. As can be seen, the animals that presented a higher DM intake and milk yield during the 4th week were those that showed a higher live weight loss (ÿ127 versus57 g) and negative energy balance during lactation (ÿ6.45 versusÿ0.32 MJ), also showing higher live weight at partum (3.92 versus 3.78 kg).
4. Discussion
The addition of high levels of fat to the diet did not have any signi®cant effect on live weight of females, in agreement with previous work on moderate (Maertens and de Groote, 1988; Cervera et al., 1993; Xiccato et al., 1995; Lebas and Fortun-Lamothe, 1996) or high levels of fat addition of dietary fat (Pascual et al., 1998a, 1999). However, an increase of the dietary energy content, through the addition of fat, increased signi®cantly the DE intake of lactating rabbit does, although DM intake was similar for both diets during the entire lactation. A moderate increase of dietary fat content has been related to a lower (Maertens and de Groote, 1988; Castellini and Battaglini, 1991) or similar DM intake (Fraga et al., 1989; Barreto and de Blas, 1993; Cervera et al., 1993; Xiccato et al., 1995), but a higher DE intake has always been reported. The results of the
Table 5
Simple correlation coef®cients between food intake, milk production and energy balancea
Diet C V
Week
1 2 3 4 1 2 3 4
MP-DMI 0.773* * * 0.728* * * 0.815* * * 0.269 0.508* 0.874* * * 0.794* * * 0.630* * * Fbal-DMI 0.219 0.177 0.312 0.030 0.294 0.397 ÿ0.121 ÿ0.440
Ebal-DMI 0.307 0.185 0.339 ÿ0.044 0.337 0.433
ÿ0.119 ÿ0.333 MP-Fbal ÿ0.133 ÿ0.013 0.123 ÿ0.275 ÿ0.145 0.478*
ÿ0.082 ÿ0.556* * MP-Ebal ÿ0.021 0.035 0.105 ÿ0.359 ÿ0.178 0.460*
ÿ0.047 ÿ0.599* *
aMP: milk production; DMI: dry matter intake; Fbal: fat balance; Ebal: energy balance.
(Trend)P<0.1;*P<0.05;* *P<0.01;* * *P<0.001.
energy balance and they could not adjust their voluntary food intake, showing a high consumption independently of the dietary DE.
The inclusion of high fat levels in the diet improved milk yield and litter weight at weaning, this result being consistent with those of all the authors mentioned above. This substantial improvement in milk production and problably in the fat milk content (as found by Pascual et al. (1999) for these same diets) could be inversely related to the consumption of solid food by litters in the last two weeks of lactation (Fortun-Lamothe and Lebas, 1996; Pascual et al., 1998a) because it seems unlikely that a regulation of energy intake would be found at this early age.
From the current results, high fat diets were not able to solve the energy de®cit problems of lactating does. However, the results from the literature for the effect of high fat diets on the body condition of rabbit does are controversial. In rats, some authors have found different responses in the adipose tissue mobilization as a function of different fat sources (Van Amelsvoort et al., 1988; Field et al., 1989); diets rich in saturated fatty acids usually tend to orient the ingested fat to non adipose tissues and to prevent excessive fat storage in adipose tissues, but diets rich in polyunsaturated fatty acids may increase the insulin action on incorporation of glucose into adipose tissue lipids in rats. So, it also seems to be necessary to take into account the source of fat used in rabbit studies. In fact, reports that showed a decrease of adipose reserves in lactating rabbit does given fat diets (Xiccato et al., 1995; Parigi-Bini et al., 1996) used pork lard rich in saturated fatty acids, while those that did not show any dietary difference (Fortun-Lamothe and Lebas, 1996; Lebas and Fortun-Lamothe, 1996; and the present work) used sun¯ower and soya oils rich in polyunsaturated fatty acids.
On the other hand, while the energy balance was negative for both diets, a more detailed study of the current data con®rms the existence of individual animals giving very different results. Not all the does showed a negative energy balance. The energy balance was 2.2 MJ in 10 does distributed equally in the two experimental groups, and consequently the balance in the others was 2 MJ worse than that shown in Table 4. The energy balance was weakly correlated with the live weight of does at partum (rÿ0.24; P<0.1). However, when only does of diet V were considered, does which showed a higher negative energy balance were those that presented a higher live weight at partum and a higher live weight loss during lactation (Fig. 2). Consequently, if body fat losses during lactation may be partially related to the initial body condition of animals, it seems to be necessary to use in vivo methods to study the body changes of particular animals over time; such as magnetic resonance imaging tomography (KoÈver et al., 1996, 1998) or ultrasound (Pascual et al., 2000). In other species, Chilliard (1986) found that lactating rats given high fat diets showed body fat losses that varied from 0 to 43 g during lactation, but this variability was partially attributed to the amount of body fat in animals at parturition. This could explain partially the improvements in the ef®ciency of utilization of DE shown in lactating rabbit does given high fat diets throughout their reproductive cycle (Pascual et al., 1998b, 1999).
In conclusion, the results studied in the present work con®rm that the addition of dietary fat increases the energy intake of rabbit does in their second lactation and consequently their milk yield and litter growth. Non-pregnant lactating rabbit does showed a reduction in body protein, fat and energy during the second lactation, which was not affected by the type of diet. However, the effect of dietary fat on the body condition of lactating rabbit does continues to be controversial, and further research is needed to study the effect of other factors including the initial body condition of does and the type of fat.
Acknowledgements
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