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Poult Sci 2006. 85:1722-1728
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IMMUNOLOGY, HEALTH, AND DISEASE

Altered Circulating Levels of Serotonin and Immunological Changes in Laying Hens Divergently Selected for Feather Pecking Behavior

A. J. Buitenhuis*, J. B. Kjaer*,1, R. Labouriau* and H. R. Juul-Madsen{dagger},2

* Department of Genetics and Biotechnology, and {dagger} Department of Animal Health, Welfare and Nutrition, Danish Institute of Agricultural Sciences, 8830 Tjele, Denmark

2 Corresponding author: Helle.JuulMadsen{at}agrsci.dk


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The aim of this study was to investigate the changes in immunological parameters as well as changes with respect to plasma levels of serotonin and tryptophan in lines selected for and against feather pecking (FP) behavior [high FP (HP) line and low FP (LP) line] for 5 generations. The hens from the HP line had a higher plasma serotonin level than those from the LP line (0.059 vs. 0.037 µmol/L, F2,27 = 0.031, P < 0.05). The plasma level of tryptophan was, on average, 67.30 µmol/L and did not differ between the lines (68.3 vs. 66.3 µmol/L, F2,28 = 0.36, P < 0.05). The HP line had a higher response to infectious bursal disease virus vaccination after 1 wk post-vaccination compared with the control and LP lines. The number of white blood cells (P < 0.0001) and the expression of MHC class I molecules on CD4 (P < 0.02), CD8ß (P < 0.006) and on B cells (P < 0.03) were highest in the LP line compared with the control and HP lines. Selection for or against FP, therefore, changes the number of white blood cells and the expression of MHC class I molecules on T and B cells, which may influence the health status of the birds.

Key Words: feather pecking • genetic selection • immune system • serotonin


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Feather pecking (FP) is a behavior by which hens destroy the feathers of other hens, in some cases, even plucking out feathers and eating them. In some severe cases, FP can be followed by cannibalism, in which hens eat the blood and tissue of other hens. Feather pecking is widespread; a representative survey revealed that, in Switzerland, 37.5% of the flocks were judged by their owners as having problems with FP during the rearing period (Huber-Eicher, 1999). A wide range of causal factors of FP, such as housing, rearing, and feeding factors, have been reported (Sharma et al., 1999; Green et al., 2000). Management procedures, such as beak trimming, improving rearing conditions and feed, and optimizing the laying environment, can be used to reduce FP behavior. However, it has been shown that genetic selection can effectively reduce FP. Craig and Muir (1993) showed that direct selection against cannibalistic pecking could be successful using group selection. They selected for hen days without beak-inflicted injuries for 168 d based on sire family averages. The resulting lines differed in production and longevity after the first generation. After a major improvement in the reduction of mortality due to beak-inflicted injuries in the first generation, there was little additional improvement of mortality in later generations (Muir, 1996). The line with the highest production and longevity [i.e., low FP (LP) levels] also had a higher serotonin (5-HT) turnover compared with the line with the lowest production and longevity [i.e., high FP (HP) levels; Cheng et al., 2001a]. Selection did not change the humoral immune response to sheep red blood cells (Hester et al., 1996), but, on average, birds from the LP line had higher percentages of blood lymphocytes and CD4+:CD8+ ratios of circulating T cells. In contrast, the HP line exhibited higher plasma IgG (Cheng et al., 2001b).

Kjaer et al. (2001) have shown that it is possible to select for FP using "number of bouts" as a selection criterion, in which bouts is repeated pecking at the same bird. This selection criterion is a combined trait for both gentle and severe pecking. After 3 generations, a significant difference in FP behavior in terms of bouts was observed. There was no change observed in the level of aggressive pecking. The line showing reduced pecking behavior, had a higher BW (Kjaer, 2005), and had better feed efficiency and egg production (Su et al., 2004, 2006). The neuronen-docrine and immunological changes in these lines have not been investigated yet. Therefore, the objective of the present study was to investigate changes in plasma 5-HT and tryptophan levels as well as changes in hematological and immunological parameters in lines selected for and against FP behavior for 5 generations (Kjaer et al., 2001).


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Development of Genetic Lines
The data were collected from an experiment with 3 experimental lines of White Leghorn laying hens, among which the LP line was selected for low FP, the HP line was selected for high FP, and the control line was a random mating control line. The 3 lines were established in 1995 and derived from a White Leghorn layer line, which was formed in 1970. Feather pecking behavior was measured at about 30 wk of age by counting FP events (FP pecks) and then grouping the events into several bouts (FP bouts). One bout was defined as a series of continuous pecking to the same individual. Selection was based on the number of FP bouts.

The experiment was conducted for the hens in the fifth generation of selection. The birds were reared in floor pens covered with a 5-cm thick layer of wood shavings. The temperature was 34°C at 1-d-old and was gradually reduced to 20°C at 8 wk of age. This temperature was kept throughout the rest of the experiment. The light regimen was 12L:12D from 0 to 14 wk and then 1 h of light per week was added until the light regimen was 16L:8D at 18 wk of age. At 18 wk of age, the pullets were transferred to 4-bird battery cages. At 42 wk, they were transferred to single bird cages for the evaluation of production and feed conversion. These data are presented elsewhere (Su et al., 2004, 2006).

Measurement of 5-HT and Tryptophan
Blood samples stabilized with EDTA were collected from the wing vein of fifteen 31-wk-old birds from the LP and the HP lines to measure 5-HT and tryptophan content in the blood samples. Plasma samples (50 µL) were added to 200 µL of a freshly prepared solution containing 2 mmol/L of Na-EDTA, 0.1% ascorbic acid, 12.5% sulfosalicylic acid, and 3.5 µmol/L of deoxyepi-nephrine (internal standard). After cooling on ice for 60 min, the proteins were removed by centrifugation for 2 min at 20,000 x g. Twenty microliters of supernatant was injected into a reversed-phase HPLC system and separated on a Xorbax Eclipse XDB-C18 (3.0 x 150 mm, 3.5 µm) column thermostated at 40°C (Agilent Technologies A/S, Naerum, Denmark). The fluorescent detector was operated with an excitation wavelength of 285 nm and an emission wavelength at 325 nm. The individual compounds were separated using binary gradient ranging from 8% B to 41% B in 21 min. Both mobile phases contained 0.05 mol/L of citric acid, 0.005 mol/L of triethyla-mine, and 10 mmol/L of octanesulfonic acid. Mobile phase B contained 90% acetonitrile; the low rate was 0.57 mL/min. The concentrations (in µmol/L) of 5-HT or tryp-tophan were calculated from a reference curve using deoxyepinephrine as internal standard.

Blood Sampling for Immunological Parameters
Blood was taken from the wing vein of 24 birds from each line (LP, HP, and control lines) at 46 wk of age. These birds were used for the infectious bursal disease virus (IBDV) response test as well as the hemocytometry and flow cytometry, as described below. The collected blood was divided into 2 tubes. One tube contained citrate stabilizer, which was used for the hemocytometry and flow cytometry, and 1 tube without stabilizer, which was used for making serum for the d 0 titer for the IBDV response (see below).

Vaccination and Serum Antibody Titers Against IBDV
Twenty-four birds from each line, as mentioned above, were vaccinated intramuscularly with 1 dose (0.5 mL) of inactivated IBDV vaccine (Nobilis Gumboro INAC:VET 452037, Intervet Danmark A/S, Skovlunde, Denmark). Serum samples were collected at 0, 1, 3, 5, and 7 wk postvaccination, and the serum was assessed for the titer of specific IBDV antibodies.

The ProFLOK IBD Elisa test kit (Kirkegaard and Perry Laboratories Inc, Gaithersburg, MD) was used to measure serum IgG antibody titers against IBDV. The Elisa assay was performed according to the kit manual. Briefly, 96-well microtiter plates coated with IBDV antigen were incubated for 30 min at room temperature (approximately 20°C) with 5 µL of serum samples and positive and negative controls included in the kit, followed by incubation for another 30 min at room temperature with a horseradish peroxidase-conjugated affinity-purified antibody from a pool of serum from goats immunized with chicken IgG (H + L). Furthermore, 2,2'-azino-di(3-ethylbenzthi-azoline sulfonic acid was used as chromogen and 5% sodium dodecyl sulfate as stop solution. The result was monitored as optical density at 405 nm, and the antibody titer was calculated from the following equation format: SP = (sample absorbance) – (average normal control absorbance)/corrected positive control absorbance).

Hemocytometry
The concentration of white blood cells (WBC; WBC x 109/L) in the citrate-stabilized blood was assessed by a hemacytometer. Approximately 100 µL of blood was analyzed in a CELL-DYN 3500 hemacytometer from Abbott Laboratories (Abbott Park, IL) using a specialized con-figuration for chicken blood. The apparatus was standardized daily using CELL-DYN 22 controls.

Flow Cytometric Analysis
Isolation of mononuclear cells from citrate-stabilized blood samples was performed according to the manufacturer’s procedure using Lymphoprep 1.077 (Nycomed Pharma, Oslo, Norway). The mononuclear cells were washed and resuspended in a RPMI medium without a pH indicator (Gibco BRL, Life Technologies Inc., Gaithers-burg, MD) containing 2% fetal bovine serum (BioWhi-taker, Wakersville, MD). The preparation of mononuclear cells was not tested for contamination of heterophils and thrombocytes. Cells were counted, diluted to a final concentration of 1 x 107 cells/mL, and stored overnight at 4°C. For the flow cytometric analysis, we used 50-µL cells from each sample in a total volume of 200 µL of fluorescence-activated cell sorter-buffer (0.2% BSA, 0.2% sodium azide, 0.05% horse serum in PBS pH = 7.4). The antibody incubation was performed for 15 min at 4°C.

The antibodies were as follows: anti-chicken ß2-micro-globulin [fluorescein isothiocyanate (FITC; F21–21), anti-chicken B-Lß (2G-11), anti-chicken CD4 (R-phycoerythrin-conjugated CT4), anti-chicken CD8{alpha} (FITC-conjugated CT8), anti-chicken CD8ß (R-phycoerythrin-conjugated EP42), anti-chicken CD45 (FITC-conjugated LT40), and anti-chicken BU-1 (FITC-conjugated AV20). Because the anti-chicken B-Lß antibody was unlabeled, a secondary antibody incubation was performed in a total volume of 150 µL of fluorescence-activated cell sorter-buffer containing FITC-labeled goat F(ab’)2 fragment antimouse IgG (H + L; Coulter Immunotech, Miami, FL) diluted 1:50 for 15 min in darkness at 4°C. The hybridoma 2G-11 was kindly donated by K. Skjoedt, Odense, Denmark, and CT4, CT8, EP42, LT40, and AV20 were obtained from the Southern Biotechnology Association Inc, Birmingham, AL, and the secondary antibody was procured from Coulter Immunotech. Samples were analyzed on a Coulter Epics flow cytometer with excitation at 488 nm from an argon laser. Analytic gates were chosen based on forward and side scatter to include small mononuclear cells and to exclude debris, dead cells, and erythrocytes. Flow cytometer alignment verification was performed using Flow-Check fluorospheres (Abbott Laboratories), and day-to-day standardization of the flow cytometer was performed using uniform dyed microspheres (0.96µm, Bangs Laboratories Inc., Fishers, IN). Single and double protocols were performed as indicated in Table 1Go. For each of the protocols, control samples without any antibody and with secondary antibody were performed.


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  		Table 1. Six different 1- or 2-colored immunofluorescent stained protocols1
 
Statistical Analysis
With respect to 5-HT and tryptophan, the experimental design was a completely randomized design with genetic line as the main effect and individual bird as the experimental unit. Serotonin recordings were log-transformed to obtain a normal distribution. Because statistical trends were similar for the transformed and untransformed data, the untransformed results are presented. Differences between lines were determined using a single degree of freedom F-test. Analyses of variance were performed using SAS statistical software (PROC GLM; SAS Institute, 1994), with line as a fixed effect in the model.

The time development of the responses to IBDV of each line was studied using a suitable gamma mixed model (McCullagh and Nelder 1989; Fahrmeir and Tutz, 2001). The fixed part in the model was line (control, high and low selected), time (wk), and the interaction between those 2 factors. The adequacy of the gamma distribution for modeling the current data was determined by exploratory analyses showing that the variances increased proportionally to the square of the means and verified by residual analyses for generalized linear mixed models (not shown). The random part of the model contained 2 random components. The first random component took the same value for each bird, representing the general dependencies generated by the repeated measurements. The second random component represented a latent autoregressive process for each animal. This autoregressive random component allowed the model to represent a special dependency structure. That is expected to be present in the data due to the cumulative behavior characteristic of the immunological determinations.

White blood cells and the flow cytometry data were not normally distributed; therefore, a Kruskal-Wallis rank sum test was used to test for differences between the lines. This test is a nonparametric test, not assuming any distribution of the trait. Infectious bursal disease virus, WBC, and the flow cytometry data were analyzed using R-software (version 2.1.0; http://r-project.org).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Plasma Levels of 5-HT and Tryptophan
The HP hens had a higher plasma 5-HT level than the LP hens (0.059 vs. 0.037 µmol/L, F2,27 = 0.031, P < 0.05; Figure 1Go). The plasma level of tryptophan was, on average, 67.30 µmol/L and did not differ between the lines (68.3 vs. 66.3 µmol/L, F2,28 = 0.36, P > 0.05).


Figure 1
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  		Figure 1. Plasma serotonin (5-HT) values (y-axis) plotted against breeding value for feather pecking (FP; x-axis) for the low FP (LP) line (+) and the high FP (HP) line ({blacktriangleup}) at 31 wk of age. Breeding value was calculated with an animal model as described in Kjaer et al. (2001) from the number of FP bouts of the bird and its sisters. There were 15 hens used of each of the LP and the HP line.

 
Response to IBVD Vaccination
Figure 2Go displays the corrected responses to IBDV for all the combinations of line and week. The gamma mixed model revealed that the interaction between line and time for the response to IBDV was significant (P = 0.004; Table 2Go). No significant differences were found between the control line and the LP line. Moreover, no statistically significant differences among the IBDV response of the HP, control, and LP lines at the first week were detected. Increasing significant differences were found in the following weeks. The coefficient of the autoregressive process used to model the covariance structure within individuals was estimated as 0.704 (significantly different from 0 at P = 0.01), confirming the presence of the conjectured autocorrelation among measurements performed in the same individuals.


Figure 2
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  		Figure 2. The logarithm of the predicted specific antibody titer (y-axis) against infectious bursal disease virus (IBDV) measured by the Elisa test in wk 1, 3, 5, and 7-wk postvaccination at 46 wk of age (x-axis) for the low feather pecking (LP) line (- - -), high feather pecking (HP) line (····), and the control line (solid line: —). There were 24 hens used of each of the LP, HP, and control lines.

 

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  		Table 2. Details on the interaction between line and time (wk)1
 
Number of WBC
The number of WBC was lower in HP lines (P < 0.0001) compared with the LP and control lines, which did not differ (Table 3Go).


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  		Table 3. Least significant means of the white blood cell (WBC) content and lymphocyte immunophenotyping for the control, low feather pecking (LP), and high feather pecking (HP) lines
 
Lymphocyte Immunophenotypes
A range of immunological parameters were recorded by use of flow cytometry. An example of dot plots is shown in Figure 3Go. The results are shown in Table 3Go. Differences between the lines were found for the percentage of single-positive CD4 cells, in which the LP line had a higher percentage than the HP and the control lines (P = 0.004). Furthermore, a difference between the lines for the percentage of double-positive CD4CD8-cells was found. The LP line had a higher percentage than the control and HP lines (P = 0.0005). Differences between the lines were also found for the expression (mean fluorescent intensity) of CD4 on CD4+ cells, in which the control line was higher than the LP and HP lines (P = 0.03). The expression of CD8{alpha} on CD8+ cells was higher in the LP line than in the HP and control lines (P = 0.017). The expression of MHC class I on CD4+ cells was lowest in the HP line compared with the control and the LP lines (P = 0.02). This trend also holds for the expression of MHC class I on CD8ß cells and BU-1 cells (B cells). The expression of CD45 on lymphocytes was lowest in the HP line compared with the control line and the LP line (P = 0.04).


Figure 3
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  		Figure 3. Representative dot plot of BU-1 and MHC class I-defined small chicken peripheral blood mononuclear cell (PMNC) populations. Peripheral blood mononuclear cells were labeled with R-phycoerythrin- (RPE) conjugated mouse monoclonal anti-chicken B-cell antibody (BU-1) and fluorescein isothiocyanate (FITC)-conjugated mouse monoclonal anti-chicken ß2-microglobulin antibody (F21-21) using a 2-color immunofluorescent staining procedure and analyses by flow cytometry. For cell population analysis, a gate was drawn around the small PMNC population (lymphocytes and thrombocytes). Relative fluorescent intensity (log) for BU-1 and MHC class I is shown on the y- and x-axes, respectively. Data reported based on flow cytometric analysis included the percentage of BU-1- and MHC class I-defined populations as well as the mean fluorescence intensity (MFI) for each population. LP = the low pecking line; HP = the high pecking line.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In the central nervous system, 5-HT plays a role in the modulation of behavioral and physiological processes and is used as an indicator to evaluate alterations in behavioral adaptation and reproduction (Maswood et al., 1998). A low level of 5-HT in the central nervous system has been suggested to be of importance to several behavioral disorders, for instance, depression, aggression, and obsessive-compulsive spectrum disorders. Feather pecking has been suggested as an animal model of human obsessive-compulsive spectrum disorders (Bordnic et al., 1994), and reduction of FP. In the peripheral system, the role of 5-HT in relation to behavioral adaptation is not directly clear, nor is the relation to the 5-HT level in the brain, as 5-HT cannot pass the brain-blood barrier (Pietraszek et al., 1992). However, data presented in this study showed that the peripheral 5-HT concentration is higher in chickens from the HP line than chickens from the LP line. This result is in agreement with the data presented by Cheng et al. (2001a), showing that higher blood 5-HT levels were associated with lower survivability, resulting from higher cannibalism in their HP hens.

Selection for or against FP behavior has previously been shown to change the capability to respond to foreign antigens. A correlation between pecking behavior and primary response to keyhole limpet hemocyanin was found by Buitenhuis et al. (2004). The data presented in this paper showed that the HP line had a higher response to IBDV after 1-wk postvaccination. On the other hand, Hester et al. (1996) did not find any change in the primary response to sheep red blood cells when selected for survivability, indicating that the correlation between pecking behavior and immune response may be dependent on the type of antigens used; however, a good comparison of these studies is difficult, because different populations of chickens and antigens were used.

Even though the direct response to an antigen might not be changed during selection for survivability, Cheng et al. (2001b) did find evidence of hematological and immunological changes. Cheng et al. (2001b) found that the hens from their LP line had higher levels of blood lymphocytes. The data from our study may support this, because hens from the LP line have a higher WBC concentration compared with the hens from the HP line. In our study, we did not measure the lymphocyte concentration in the blood, only the concentration of total WBC. Therefore, it is not possible to verify whether the increase in WBC was due to differences in lymphocytes only or other types of WBC. In addition, Cheng et al. (2001b) showed that the percentage of CD4-positive cells was higher in the LP line than in the HP line. This is consistent with our data, in which the LP hens showed a higher percentage of CD4-positive cells than the HP birds. However, there was no difference in percentage of CD8-positive cells found in our study, whereas Cheng and coworkers (2001b) found a higher percentage of CD8 in hens of the HP line than in the LP line. On the other hand, our data showed a difference in percentage of double-positive CD4CD8-cells, which were not measured by Cheng et al. (2001b). At this stage, we cannot firmly conclude that the changes in hematological and immunological parameters are a consequence of selection for FP behavior, but the results strongly indicate that there was indeed a change in hematological and immunological parameters that point in the same direction as the results obtained by Cheng et al. (2001b).

The MHC, which is named the B system in chickens, has been closely associated with resistance or susceptibility to many diseases, including viral infections (Bumstead, 1998) and bacterial (Guillot et al., 1995), protozoal (Caron et al., 1997), and autoimmune diseases (Rose, 1994). The relative expression of MHC class I molecules on WBC was furthermore found to be low in Marek’s disease-resistant B haplotypes (B21 and B21-like) and high in Marek’s disease-susceptible B haplotypes (B15 and B19; Juul-Madsen et al., 2000; Kaufman, 2000). The expression of the MHC class I was lower in the HP line for all 3 cell types measured compared with the LP line, which indicates that selection for FP behavior resulted in a shift in MHC class I expression in different cell types and may indirectly change the capacity of the bird to deal with different pathogens.

In conclusion, we find differences in peripheral 5-HT concentration between the LP and HP lines as well as in hematological and immunological parameters. The results presented in this study point in the same direction as the study done by Hester et al. (1996) and Cheng et al. (2001a, b), indicating that changes in the endocrine and immune systems occur due to (in)direct selection on FP behavior and, hence, may change the health status of the birds.


   ACKNOWLEDGMENTS
 
We thank the staff of the experimental farm at the Danish Institute of Agricultural Sciences for taking good care of the laying hens. Lene Rosborg Dal is kindly acknowledged for technical assistance. Karin V. Østergaard is kindly acknowledged for critical reading of the manuscript. A.J. Buitenhuis was supported by a grant from the Danish Ministry of Science, Technology and Innovation (FTP no. 274-05-0239).


   FOOTNOTES
 
1 Present address: Federal Agricultural Research Centre, Institute for Animal Welfare and Animal Husbandry, Dörnbergstrasse 25-27, 29223 Celle, Germany Back

Received for publication November 22, 2005. Accepted for publication April 20, 2006.


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