| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
PHYSIOLOGY, ENDOCRINOLOGY, AND REPRODUCTION |
* Adaptation Physiology Group, Animal Sciences Group, Wageningen University, Lelystad, The Netherlands; and Department of Biosystems, Laboratory for Physiology, Immunology and Genetics of Domestic Animals, Catholic University of Leuven, Belgium
1 Corresponding author: Ellen.vanEerden{at}wur.nl
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Key Words: residual feed intake • Salmonella • energy metabolism • thyroid hormone • chicken
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Previously, we demonstrated that the BW of phenotypically selected R– and R+ pullets did not differ but that R+ pullets had significantly heavier organ weights at 20 wk of age (Van Eerden et al., 2004a). It was concluded that R+ pullets put more resources into organ development than R– pullets. Adult R– hens from genetically selected RFI lines were shown to have more carcass lipid and abdominal fat than R+ hens (Zein-el-Dein et al., 1985; Tixier et al., 1988; El Kazzi et al., 1995; Gabarrou et al., 1998). However, carcass composition and the amount of abdominal fat were not recorded in our previous experiment with phenotypically selected pullets (Van Eerden et al., 2004a). Therefore, it remained to be established whether energy allocated to growth would be different for R– and R+ pullets, particularly differences in protein and fat deposition.
If such a difference in protein and fat deposition exists, it can be questioned whether this partitioning is affected by energy-demanding processes, such as an activated immune system. Furthermore, it can be questioned whether, in that case, energy is reallocated from production processes, such as growth or egg production, toward maintenance processes.
The period during which antibodies are formed is shown to cause a shift in metabolism in favor of fat deposition (Henken and Brandsma, 1982; Parmentier et al., 2002), although ME for maintenance was not increased in these studies. This latter observation could be because the energy-demanding part of the immune response seems to be restricted to infections with an acute phase response (Klasing, 1998) because of the occurrence of fever and the release of cytokines. Both events interfere with metabolism, because fever involves a change in body temperature set point and cytokines stimulate hepatocytes to synthesize and secrete acute phase proteins. Therefore, it is hypothesized that an infection with an acute phase response will cause a change in heat production and a shift in energy partitioning between maintenance and production processes, with more energy being spent on maintenance and less on growth or egg production.
The objective of the current experiment was to investigate whether there are differences between young R– and R+ pullets in energy partitioning toward maintenance processes instead of growth or egg production and whether this partitioning is affected by a bacterial infection, particularly protein and fat deposition. We used Salmonella enteritidis as a model pathogen. Salmonella enteritidis is a nonhost specific pathogen. It is able to invade and colonize the chicken intestines (Suzuki, 1994) and elicits both humoral and cellular immune responses, including an acute phase response (Holt and Gast, 2002).
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Birds, Selection, and Housing
This experiment was carried out in 8 consecutive trials. For every trial, 176 Lohmann Brown egg-type pullets were housed individually in battery cages from 4 until 14 wk of age. Feed (2,600 kcal of ME/kg, 175 g/kg of CP) and water were available ad libitum. Individual BW and FI were recorded once a week. These data were used to calculate RFI as a measure for efficiency (Van Eerden et al., 2004b). At 14 wk of age, the 10 hens with the highest and the 10 hens with the lowest values for RFI were selected; all other hens were removed from the experiment. At 15 wk of age, 2 hens from each selected group were killed through i.v. administration of Euthasan (Anisane, Pet Health Products, Raamsdonksveer, The Netherlands) and were dissected to determine heart weight, liver weight, spleen weight, and intestinal length, to examine potential differences in organ weights before Salmonella treatment. The remaining 16 hens were individually housed in 2 identical, open-circuit climate respiration chambers (Verstegen et al., 1987) for 5 wk. Each chamber contained 8 R– or 8 R+ hens. Temperature was maintained at 21°C and RH was 60% in both chambers. The lighting schedule was 9L:15D (onset of light was 0700 h) during the whole experiment. The total number of birds used was 160: 32 for evaluation of organ weights at 15 wk of age (16 R– and 16 R+) and 128 for further examination of energy partitioning (64 R– and 64 R+).
Treatment
After entering the chambers, the first week was for acclimation to the chambers. On the first day of wk 16, the pullets in 4 trials were orally inoculated with 108 cfu of S. enteritidis (S+). In the other 4 trials, the hens were not inoculated (S–). Salmonella and S– treatments were applied alternately.
A blood sample of each pullet was taken in heparinized tubes at 16, 17, and 19 wk of age (i.e., on d 0 before inoculation and on d 7 and 21 after inoculation in S+ trials). The blood samples were centrifuged, and plasma was stored at –20°C until further processing.
Energy and N Partitioning
In each trial, energy and N partitioning were determined per chamber during 5 consecutive balance periods of 1 wk each. After each balance period, the pullets were weighed, and individual FI was recorded. Feces (including urinary compounds), feathers, dust, and, if applicable, eggs were collected quantitatively per chamber and sampled for energy and N analysis, using bomb calorimetry and Kjeldahl analysis, respectively.
Respiration measurements were conducted throughout the balance period in 9-min intervals. Heat production (HP) per chamber was calculated from the O2 consumed and CO2 produced, according to the formula of Romijn and Lokhorst (1961). Physical activity was measured using Doppler radar equipment.
Metabolizable energy intake was calculated as the difference between gross energy (GE) intake and energy content of feces, including urinary components. Total net energy (NE) for BW gain and egg production (NEtot) was calculated as ME – total HP. Net energy for BW gain (NEbwg) was calculated as NEtot – NE in eggs (NEegg).
Nitrogen retention in protein for BW gain (NEbwgP) was calculated as N in feed – N in feces (including urinary components), feathers, dust, eggs (NEeggP), aerial NH3 and NH4+ in water that condensed on the heat exchanger. For aerial NH3 measurements, samples of the total outgoing airflow were directed through a wash bottle filled with a 25% H2SO4 solution. Samples from the wash bottle content were collected after each balance period and analyzed for N content. Fat retention for BW gain (NEbwgF) was calculated as NEbwg – NEbwgP. Fat retention in eggs (NEeggF) was calculated as NEegg – NEeggP.
Metabolizable energy for maintenance (MEm) was calculated as total ME – ME for BW gain and ME for egg production. Metabolizable energy for BW gain was calculated as NEbwgP/0.59 + NEbwgF/0.83 (Chwalibog and Thorbek, 1980). Metabolizable energy for egg production was calculated as NEeggP/0.50 + NEeggF/0.79 (Chwalibog, 1985). In addition to BW gain in terms of energy (in kJ per kg0.75), we calculated growth in terms of weight (in g per bird).
S. enteritidis Preparation
A nalidixic acid resistant strain of S. enteritidis was used in this experiment. A sample of the bacterial stock, which was stored in glycerol at –80°C, was first grown overnight at 37°C on a brilliant green agar plate containing 0.01% nalidixic acid. A few colonies were transferred into 0.5 L of buffered peptone water and grown overnight. The bacterial suspension was centrifuged at 3,000 x g for 15 min. The bacteria were washed twice in sterile PBS. The final concentration was 2 x 108 cfu/mL. The inoculation dose was 0.5 mL.
Hormone Assays
Triiodothyronine (T3) and thyroxine (T4) concentrations were measured in all plasma samples by radioimmunoassays, as described by Darras et al. (1990) for T3 and by Darras et al. (1991) for T4. All samples were analyzed per hormone in the same assay.
Postmortem Examination
After the 5-wk balance period, the now 20-wk-old hens were killed through i.v. administration of Euthasan. Body, heart, liver, spleen, ovary, and stroma (defined as an ovary without large yellow follicles) weights were recorded, and total intestinal length was measured. Large yellow follicles (>10 mm) and small yellow follicles (5 to 10 mm) were counted.
Statistical Analysis
The PROC GLM procedure of SAS was used for statistical analysis (SAS Institute, 2004).
The pullets that were killed immediately after selection had not been subjected to Salmonella treatment. Therefore, differences in organ weights were tested only for efficiency type effects, using the model
 |
where Y = dependent variable; µ = overall mean; R = efficiency type (R– or R+); and e = residual error.
The energy balance experiment consisted of 16 balance groups: 8 trials x 2 respiration chambers, each containing R– or R+ selected pullets. There were 4 treatment combinations, arranged as a 2 x 2 factorial model: each of treatment S– and S+ at 2 levels (R– and R+). Salmonella exposure and S– trials were applied alternately. Therefore, trial was nested within treatment. We used a model with repeated measurements
 |
where Y = dependent variable; µ = overall mean; S = Salmonella treatment (S– or S+); trial(S) = trial nested within treatment; R = efficiency type (R– or R+); R x S = interaction between efficiency type and treatment; group (R x S x trial) = balance group nested within efficiency type, treatment, and trial; time = week of sampling after a balance period (wk 16, 17, 18, 19); and e = residual error. Treatment was tested with trial(S) as an error term, efficiency type and its interaction were tested with group(R x S x trial) as error term, and time and its interactions were tested against the residual error. Results from the first week in the chambers were omitted from analysis, because this week was for adaptation only. In view of the obtained results, we performed a more detailed analysis by hour on HP (total, activity-related, and nonactivity-related) for the first week after Salmonella inoculation.
Thyroid hormone levels and postmortem data from the pullets after the 5-wk balance period were analyzed using the model
 |
where Y = dependent variable; µ = overall mean; S = Salmonella treatment (S– or S+); trial(S) = trial nested within treatment; R = efficiency type (R– or R+); R x S = interaction between efficiency type and treatment; and e = residual error. Salmonella treatment was tested with trial(S) as an error term, whereas efficiency type and its interaction were tested against the residual error. Numbers of large and small yellow follicles were analyzed only for pullets with ovarian development, which is defined as presence of at least 1 large or small yellow follicle on the ovary. Number of pullets with ovarian development was analyzed with multivariate logistic regression (PROC LOGISTIC from SAS; SAS Institute, 2004). Thyroid hormone levels were not analyzed with repeated measurements, to account for the onset of laying eggs.
Unless otherwise stated, all levels of significance were tested at the P < 0.05 level.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Energy Partitioning
The results of energy partitioning measurements are shown in Table 1
. There were no interactions between efficiency type and Salmonella treatment or Salmonella treatment effects.
|
).
|
. Inoculated pullets in this period have a higher activity-related HP than control pullets. Salmonella effects for nonactivity-related HP were significant at 4 time points from 21 h until 27 h after inoculation, and they are presented in Figure 3. Inoculated pullets in this period have a higher nonactivity-related HP than control pullets.
|
|
, because this variable is calculated and expressed differently (in g per bird). There was no interaction between efficiency type and Salmonella treatment, and there were no significant main effects, but there was a significant time x efficiency type interaction (P = 0.01). Therefore, growth was analyzed by week for R– and R+ pullets, and the results are presented in Figure 4. It shows that growth in wk 15 was low in R+ pullets and negative in R– pullets. Results from this first balance week were not further elaborated, because this week was for adaptation only. The low or negative level of growth can be explained by the strong reduction in FI in both efficiency groups during wk 15, probably as a result of stress due to transportation, a new environment, or both. Growth rate in R– pullets increased from wk 16 until the end of the experiment, whereas R+ pullets showed an increased growth rate until wk 17 and a decreased growth rate in wk 18 and 19.
|
Intraassay CV for T3 and T4 assays were 4.5 and 5.4, respectively.
The results of T3 and T4 hormone assays are shown in Table 2. There were no Salmonella treatment effects. Levels of T3 in R+ pullets were higher than in R– pullets at 16 and 17 wk of age (1.52 vs. 1.39 ng/mL and 1.53 vs. 1.37 ng/mL for 16 and 17 wk, respectively) but lower at 19 wk of age (0.9 vs. 1.0 ng/mL; P = 0.06). At 16 wk of age, levels of T4 were higher in R– than in R+ pullets (9.7 vs. 7.8 ng/mL). There were significant interactions between efficiency type and Salmonella treatment in T4 levels at 17 and 19 wk of age, with R+ pullets having lower levels of T4 in control situations but having higher levels in infection trials compared with R– pullets.
|
Organ weights of R– and R+ pullets that were killed at 15 wk of age were not different (data not shown).
The results of postmortem examination of the pullets that were killed after the balance trials are shown in Table 3. There were no interactions between efficiency type and Salmonella treatment, except for intestinal length. Body weights, spleen weights, and the numbers of small yellow follicles did not differ between efficiency types. Nonefficient pullets had a heavier heart (5.91 vs. 5.67 g; P = 0.06), heavier liver (41.37 vs. 37.89 g; P = 0.08), heavier ovary (18.62 vs. 8.49 g) and stroma (2.78 vs. 2.12 g), and they had more large yellow follicles (5.23 vs. 2.65 g) than R–pullets, but there were no Salmonella effects. Prevalence of ovarian development was 74.2% for noninfected pullets and 52.4 for infected pullets (odds ratio = 2.6; 95% confidence interval = 1.2 to 5.6; P = 0.01). Ovarian development did not differ between efficiency types.
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Although allocation toward production processes was not different, there were significant differences between R+ and R– pullets on the level of energy intake and use. Nonefficient pullets had a higher GE intake, and despite the lower ME:GE ratio, they still had a higher ME intake. As there were no differences between efficiency types in allocation toward production processes, the higher ME in R+ pullets was spent on maintenance processes. Higher MEm will result in higher HP, which we found to be the case, because energy spent on maintenance is completely converted to heat. Gabarrou et al. (1998) found a higher HP in genetically selected R+ hens and related the higher HP to the "excessive" energy intake through involvement of an increased diet-induced thermogenesis (Gabarrou et al., 1997). As an approximation of diet-induced thermogenesis, we calculated, for both efficiency types, the difference between nonactivity-related HP during the light period (representing the fed state) and the dark period (representing the fasted state) as a percentage of ME intake, but there were no efficiency type effects (data not shown). Therefore, it is likely that the investment in higher heart and liver weights, organs which are metabolically highly active, may partly explain the higher MEm and, thus, the higher HP in our pullets.
From behavioral studies, it was concluded that R+ hens from a genetically selected RFI line were physically more active (Braastad and Katle, 1989) than R– hens, but this conclusion was not reflected in activity-related HP in phenotypically selected hens in metabolic studies (Luiting et al., 1991) or in this study. Our results showed that total HP in R+ pullets was higher than in R– pullets; however, this was attributable to higher nonactivity-related HP. This result indicates that R+ pullets produce more heat due to a higher metabolic activity and that differences in physical activity play only a minor role.
The higher metabolic rate in R+ pullets is linked with higher levels of the metabolically active T3. Bordas and Minvielle (1999) found that T3 levels were higher in R+ pullets from genetic RFI lines at 17 wk of age, which is in agreement with our findings that T3 levels were higher in R+ pullets at 16 and 17 wk of age. Gabarrou et al. (1998) found that 18-wk-old R+ chickens from genetically selected RFI lines had higher levels of T3 only after a fasting period of 2 d, but it must be noted that their experiment contained only 5 chickens per efficiency group. However, at 19 wk of age, T3 levels were lower in our phenotypic R+ pullets compared with R– pullets. It is likely that a developmental issue played a role here. During the onset of lay, plasma T3 levels are decreased, as described for turkeys by Lien and Siopes (1993); more- over, levels of T3 seem to be positively correlated with relative growth (Kühn et al., 1982). Around 18 wk of age, some pullets in our experiment, mostly R+ pullets, started laying eggs. At necropsy, it was also shown that reproductive development in R+ pullets was ahead of R– pullets, as indicated by the larger number of large yellow follicles on the ovary. Together with the fact that growth in R+ pullets decreased from 18 wk of age onwards, whereas growth in R– pullets increased through the end of the experiment, it is likely that, at 19 wk of age, R– pullets still had priorities for growth. Meanwhile, R+ pullets had already set priorities for laying eggs, resulting in a more pronounced decreased T3 level in the latter.
The Salmonella challenge did not cause a reallocation of energy toward maintenance and production processes; furthermore, not a single energy balance parameter was affected by the Salmonella challenge, neither in the overall analysis for 4 wk, nor in the analysis by week. It is unlikely that this result was caused by too low of an inoculation dose, because shedding parameters showed that only 1 out of 61 chickens remained negative during the entire infection experiment (E. Van Eerden, unpublished data). In contrast to a previous experiment (Van Eerden et al., 2004a), there were also no effects of Salmonella on organ weights, except for ovarian development, which was delayed in inoculated pullets. There may be 2 causes to explain why the Salmonella challenge did not result in a shift in energy partitioning between maintenance and growth: the pullets were relatively old when they were inoculated or the interval between 2 balances may have been too long to measure short-term effects. It is known that the response to a Salmonella infection is strongly age-dependent: Chicks older than 2 wk are much more resistant to intestinal colonization than younger chicks, and chicks older than 1 mo generally do not show clinical signs of disease or mortality (Desmidt et al., 1997). Nevertheless, Salmonella treatment elicited a strong humoral immune response in 16- to 20-wk-old pullets (Van Eerden et al., 2004a) and an acute phase response in chickens older than 50 wk (Holt and Gast, 2002). The responses in the present study, however, were obviously not energetically costly enough to be detected in the energy balance. Moreover, the interval between 2 balances was 1 wk. It is likely that there were some effects, but those effects were probably mild and compensated within the same balance period, resulting in a zero net effect. There is some evidence for this hypothesis when we take a closer look at HP within a balance period. Heat production was the only parameter that was measured continuously during the entire experiment, in contrast to all other parameters, which were determined only once a week. Further analysis by hour for this parameter revealed that there indeed was a Salmonella effect: Nonactivity-related HP was higher in S+ pullets than in S– pullets on d 1 after inoculation, but this effect was reversed on d 2, although S+ and S– did not differ significantly at that moment. From d 3 postinoculation, there were no longer Salmonella effects for nonactivity-related HP. Instead, there were Salmonella effects for activity-related HP on this day, which may have been attributable to a compensatory feeding activity. These results support our hypothesis that possible differences in energy balance parameters between treatment groups were averaged out within 1 balance period.
As an overall conclusion, we state that, despite differences in age-dependent developmental priorities and differences in the basis for RFI selection, both young pullets and mature hens with high RFI have higher FI, GE, and ME intake; higher MEm; and higher HP compared to young pullets and mature hens with low RFI. S. enteritidis infection caused, in our phenotypically selected pullets, only a short-term increase in nonactivity-related HP and did not result in a change in energy partitioning between maintenance and production processes, regardless of efficiency type.
|
ACKNOWLEDGMENTS |
|---|
Received for publication March 10, 2006. Accepted for publication May 11, 2006.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Bordas, A., and P. Merat. 1974. Genetic variation in laying hens and phenotypic correlations of feed consumption corrected for body weight and egg production. Ann. Genet. Sel. Anim. 6:369–379.
Bordas, A., and F. Minvielle. 1999. Patterns of growth and feed intake in divergent lines of laying domestic fowl selected for residual feed consumption. Poult. Sci. 78:317–323.
Braastad, B. O., and J. Katle. 1989. Behavioural differences between laying hen populations selected for high and low efficiency of food utilisation. Br. Poult. Sci. 30:533–544.[Web of Science][Medline]
Chwalibog, A. 1985. Studies on Energy Metabolism in Laying Hens. Statens Husdyrbrugsforsøg, Copenhagen, Denmark.
Chwalibog, A., and G. Thorbek. 1980. Nitrogen retention and energy cost of protein retention in chickens kept at different temperatures. Pages 318–328 in Protein Metabolism and Nutrition. H. J. Oslage and K. Rohr, ed. European Association of Animal Production, Braunschweig, Germany.
Darras, V. M., L. M. Huybrechts, L. Berghman, E. R. Kuhn, and E. Decuypere. 1990. Ontogeny of the effect of purified chicken growth hormone on the liver 5' monodeiodination activity in the chicken: Reversal of the activity after hatching. Gen. Comp. Endocrinol. 77:212–220.[Web of Science][Medline]
Darras, V. M., A. Vanderpooten, L. M. Huybrechts, L. R. Berghman, E. Dewil, E. Decuypere, and E. R. Kuhn. 1991. Food intake after hatching inhibits the growth hormone induced stimulation of the thyroxine to triiodothyronine conversion in the chicken. Horm. Metab. Res. 23:469–472.[Web of Science][Medline]
Desmidt, M., R. Ducatelle, and F. Haesebrouck. 1997. Pathogenesis of Salmonella enteritidis phage type four after experimental infection of young chickens. Vet. Microbiol. 56:99–109.[Web of Science][Medline]
El Kazzi, M., A. Bordas, G. Gandemer, and F. Minvielle. 1995. Divergent selection for residual food intake in Rhode Island Red egg-laying lines: Gross carcase composition, carcase adiposity and lipid contents of tissues. Br. Poult. Sci. 36:719–728.[Web of Science][Medline]
Gabarrou, J. F., P. A. Geraert, N. Francois, S. Guillaumin, M. Picard, and A. Bordas. 1998. Energy balance of laying hens selected on residual food consumption. Br. Poult. Sci. 39:79–89.[Web of Science][Medline]
Gabarrou, J. F., P. A. Geraert, M. Picard, and A. Bordas. 1997. Diet-induced thermogenesis in cockerels is modulated by genetic selection for high or low residual feed intake. J. Nutr. 127:2371–2376.
Henken, A. M., and H. A. Brandsma. 1982. The effect of environmental temperature on immune response and metabolism of the young chicken. 2. Effect of the immune response to sheep red blood cells on energy metabolism. Poult. Sci. 61:1667–1673.[Web of Science][Medline]
Holt, P. S., and R. K. Gast. 2002. Comparison of the effects of infection with Salmonella enteritidis, in combination with an induced molt, on serum levels of the acute phase protein, 
1 acid glycoprotein, in hens. Poult. Sci. 81:1295–1300.
Katle, J. 1991. Selection for efficiency of food utilization in laying hens: Causal factors for variation in residual food consumption. Br. Poult. Sci. 32:955–970.
Klasing, K. C. 1998. Nutritional modulation of resistance to infectious diseases. Poult. Sci. 77:1119–1125.
Kühn, E. R., E. Decuypere, L. M. Colen, and H. Michels. 1982. Posthatch growth and development of a circadian rhythm for thyroid hormones in chicks incubated at different temperatures. Poult. Sci. 61:540–549.[Web of Science][Medline]
Lien, R. J., and T. D. Siopes. 1993. The relationship of plasma thyroid hormone and prolactin concentrations to egg laying, incubation behavior, and molting by female turkeys exposed to a one-year natural daylength cycle. Gen. Comp. Endocrinol. 90:205–213.[Web of Science][Medline]
Luiting, P., J. W. Schrama, W. van der Hel, and E. M. Urff. 1991. Metabolic differences between White Leghorns selected for high and low residual food consumption. Br. Poult. Sci. 32:763–782.[Web of Science][Medline]
Parmentier, H. K., S. Bronkhorst, M. G. B. Nieuwland, G. de Vries Reilingh, J. M. van der Linden, M. J. Heetkamp, B. Kemp, J. W. Schrama, M. W. Verstegen, and H. van den Brand. 2002. Increased fat deposition after repeated immunization in growing chickens. Poult. Sci. 81:1308–1316.
Romijn, C., and W. Lokhorst. 1961. Some aspects of energy metabolism in birds. Pages 49–59 in 2nd Symp. Energy Metab. Farm Anim. Eur. Assoc. Anim. Prod., Wageningen, The Netherlands.
SAS Institute. 2004. SAS/STAT 9.1 User’s Guide. SAS Inst. Inc., Cary, NC.
Suzuki, S. 1994. Pathogenicity of Salmonella enteritidis in poultry. Int. J. Food Microbiol. 21:89–105.[Web of Science][Medline]
Tixier, M., A. Bordas, and P. Merat. 1988. Divergent selection for residual feed intake in laying hens: Effects on growth and fatness. Pages 129–132 in Leanness in Domestic Birds: Genetic, Metabolic and Hormonal Aspects. B. Leclercq and C. C. Whitehead, ed. Buttersworth-Heinemann, London, UK.
Van Eerden, E., H. Van Den Brand, G. De Vries Reilingh, H. K. Parmentier, M. C. M. De Jong, and B. Kemp. 2004a. Residual feed intake and its effect on Salmonella enteritidis infection in growing layer hens. Poult. Sci. 83:1904–1910.
Van Eerden, E., H. Van Den Brand, H. K. Parmentier, M. C. M. De Jong, and B. Kemp. 2004b. Phenotypic selection for residual feed intake and its effect on humoral immune responses in growing layer hens. Poult. Sci. 83:1602–1609.
Verstegen, M. W. A., W. van der Hel, H. A. Brandsma, A. M. Henken, and A. M. Bransen. 1987. The Wageningen respiration unit for animal production research: A description of the equipment and its possibilities. Pages 21–48 in Energy Metabolism in Farm Animals: Effects of Housing, Stress and Disease. M. W. A. Verstegen and A. M. Henken, ed. Martinus Nijhoff Publishers, Dordrecht, The Netherlands.
Zein-el-Dein, A., A. Bordas, and P. Merat. 1985. Selection divergente pour la composante "residuelle" de la consommation alimentaire des poules pondeuses: Effets sur la composition corporelle. Arch. Geflügelkd. 49:158–160.
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
