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Poult Sci 2008. 87:885-892. doi:10.3382/ps.2007-00482
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GENETICS

Different Behavioral and Physiological Responses in Two Genetic Lines of Laying Hens After Transportation

H.-W. Cheng*,1 and L. Jefferson{dagger}

* Livestock Behavior Research Unit, USDA-Agricultural Research Service, West Lafayette, IN 47907; and {dagger} Department of Animal Sciences, Purdue University, West Lafayette, IN 47907

1 Corresponding author: hwcheng{at}purdue.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Physiological and behavioral responses to transportation stress were examined in a chicken strain selected for high group productivity and survivability (HGPS) resulting from reduced cannibalism and flightiness in colony cages and in chickens from Dekalb XL (DXL) commercial strain. At 13 wk of age, 96 pullets per strain were randomly assigned to 4-bird cages within the same strain. At 17 wk of age, half of the cages of each strain (n = 12) were randomly used as experimental group. The birds of the experimental group were crated by line, with a caution to ensure all the birds in the same cage were unfamiliar to each other, and then transported for 2 h on a country road. After transportation, the birds were recaged in groups of 4 within the same line. Behavioral data were collected immediately after the recaging of the birds. Physical parameters (BW and organ weight), plasma corticosterone levels, blood and brain serotonin (5-HT) concentrations, and 5-HT1A receptor mRNA expressions were measured at 1 d posttransportation. Results showed that, compared with the control birds of each strain, transportation stress-induced behavioral changes in eating, drinking, and preening were found in the birds from both strains, but the HGPS birds showed a greater increase in drinking and preening (P < 0.01). In addition, after transportation stress, the HGPS birds had heavier adrenal glands (P < 0.01) with higher concentrations of plasma corticosterone (P < 0.01) and a trend to higher central 5-HT levels (P = 0.09) with a downregulated 5-HT1A receptor gene expression (P < 0.05), whereas the DXL birds had a higher H:L ratio (P < 0.05). The data indicate that there are a genetic basis of variations in chickens in response to transportation stress. The HGPS birds may have a better coping capability to transportation stress than DXL birds.

Key Words: transportation stress • behavior • corticosterone • serotonin • chicken


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
In the egg production industry, chickens are transferred at least 3 times during their life span, including from grower house to layer house at about 17 wk old. This practice subjects chickens to stress, resulting from an accumulation of stressors during the process, including capturing, loading and unloading, overcrowding, dehydration, change of temperatures, vibration, novel environments, and fighting for a dominant position after relocation and mixing (Freeman et al., 1984; Carlisle et al., 1998; Warriss et al., 2005; Aksit et al., 2006; Bedanova et al., 2006; Huff et al., 2006; Vecerek et al., 2006). These stressors may lead to a deviation from physiological homeostasis, in turn, impairing bird well-being. One solution to these problems is to improve the ability of the bird to cope with the production practices through genetic selection. Selective breeding of chickens for genetic or phenotypic features associated with specific behavioral and physiological characteristics has become a major tool to improve bird well-being (Siegel and Dunnington, 1997). Understanding the interrelations between genetic factors, domestic behaviors, and hormonal homeostasis in birds in response to stressful stimulations is critical in preventing management practice-associated welfare problems in the poultry industry, including transportation stress (Mench, 1992; Craig and Swanson, 1994; Muir and Craig, 1998).

The cellular mechanisms of the avian stress response are unclear. Previous studies have shown evidence that the function of the avian neuroendocrine system in response to stimulation is analogous to that in mammals (Harvey et al., 1984). In humans and rodents, the genetic basis for differences in stress-associated behavioral adaptation and reproduction capability has been implicated in functional alterations of the neuroendocrine systems. Although multiple neurotransmitters and neurohormones have been linked to the stress response of an organism, disturbance in the serotonin (5-HT) and corticosterone (CORT) systems are most consistently associated with stress-induced pathophysiological outcomes (Dohms and Metz, 1991; Castanon et al., 1995; Siegel et al., 1999; López-Figueroa et al., 2004). Dysregulation of these biogenic amines and hormones, including their concentrations and metabolites as well as densities of their receptors, have been associated with abnormal behaviors (Valzelli, 1984; Bell and Hobson, 1994; Berman and Coccaro, 1998) and altered reproduction (Sharp et al., 1984; Sirotkin and Schaeffer, 1997). Similar to the findings in mammals, changes of those endogenous psychotropic compounds could be underlying the stress response of birds.

To detect the cellular mechanisms underlying bird stress response, a strain of White Leghorn chickens has been selected for high group productivity and survivability (HGPS) using a selection program called group selection (Craig and Muir, 1996a,b; Cheng et al., 2001a,b). Group productivity was based on average rate of lay and survivability determined by days of survival. Birds were not beak-trimmed, and high light intensity was used to provide conditions that allowed expression of aggressive behavior (Craig and Muir, 1996a,b). The advantage of the program is that it allows selection on production traits but takes into account competitive interactions in a group setting. Compared with Dekalb XL (DXL, a commercial line) birds, HGPS birds had a better feather score as well as reduced flightiness and cannibalism (Craig and Muir, 1996a,b). In addition, HGPS birds were more tolerant of heat and cold stress as indicated by a lower mortality and greater egg production (Hester et al., 1996c). The differences in survivability and resistance to various stressors between the strains may also differently affect their responses to transportation stress. However, the hypothesis has not been tested. The objective of this study was to determine the genetic-based variations of the behavioral and physiological response of birds to transportation stress and to evaluate how these changes affect bird well-being.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
Genetic Lines and Experimental Birds
The 11th generation of the HGPS and a commercial strain, DXL, were used in this study. The HGPS strain was produced from the birds selected for high group egg production and survivability, resulting from reduced aggression and cannibalism (Muir, 1996; Muir and Craig, 1998). The DXL strain was selected based on individual productivity and is known to have high mortality rates, resulting from aggression and cannibalism, in group housing situations (Craig and Muir, 1996a,b).

The birds were inoculated and transferred to the grower house at Purdue Poultry Research Center on d 1 posthatching. Beak trimming was not performed on the birds at any point in the experiment. Birds from the same strain were housed in cages with 61 x 61 cm of floor space, 61 cm of trough space, and 2 watering nipples per cage. Feed and water were provided ad libitum throughout the experiment. Overhead lights were on daily from 0630 until 1600 h starting from d 3 until 17 wk of age. Daily visual checks were performed to remove deceased birds. At 13 wk of age, 96 birds per line were transferred to new cages at 4 birds per cage (24 cages/line). The strains were balanced across rows and sides of the room. The experimental protocols were approved by the Institutional Animal Care and Use Committee at Purdue University (protocol 00-008-03).

Stress Procedure
Transportation was used as the stressor in this study. At 17 wk of age, half of the birds from each strain remained in the same cages in the grower house (control group, n = 12/line), whereas the other half were removed from the cages and crated for road transportation (experimental group). The birds were removed from each cage and crated together by strain with a caution that all birds in the same crate were unfamiliar to each other. The birds were transported for 2 h on a country road and then recaged in groups of 4 at the layer facilities of Purdue Poultry Research Center. Feed and water were provided ad libitum in the layer facilities. The wire mesh cages had 60.96 x 34.29 cm of floor space, 60.96 cm of trough space, and 2 watering nipples per cage. Overhead lights were on for 12 h daily.

Behavior Observations
Cameras were set up at both grower and layer facilities before caging and recaging of the birds, respectively. The control birds were recorded up to their sacrifice. The transported birds were recorded immediately after being recaged until sacrifice in the next day posttransportation. No human activity occurred in the egg production facility until the next day during sacrifice. The videotapes were analyzed twice using instantaneous scan sampling at 5-min intervals from 0630 to 0800 h, immediately after lights came on, and 1130 to 1300 h, during which the birds showed the most activity based on previous 24-h observations. Eating, drinking, walking, and preening were observed following the methods published previously (Craig and Muir, 1996a,b; Hocking et al., 1997; Webster, 2000).

Physical Parameter Collections
Body weights were taken immediately after collecting blood samples. The brain, heart, spleen, liver, and adrenal glands were dissected out. Based on the asymmetric development of the adrenal glands between the right and left side, and the irregular shape of the left adrenal gland resulting from development of the reproductive system, the right side adrenal gland was dissected for the study. All organs were dissected without fat and then immersed in 10% neutral-buffered formalin. After fixation, excess buffer was removed with paper towels, and then weights of the organs were measured and represented as absolute and relative organ weight. The relative weight of each organ represents a ratio of organ weight to BW (g/kg), respectively.

Blood Collecting
One bird was chosen at random from each cage for sample collection. Twenty milliliters of blood was collected into an ethylenediaminetetraacetic acid-coated tube via cardiac puncture. Blood smears were immediately prepared using a DiffSpin slide spinner, and an aliquot of 300 µL of whole blood was retained for 5-HT and Trp analysis. The remainder of the blood was separated by centrifugation at 1,000 x g for 15 min to obtain plasma for CORT RIA. Plasma was kept at –80°C until measurement.

Quantitative Analysis of Blood Parameters
Duplicated blood smears were prepared using a Diff-Spin slide spinner (Iris Sample Processing, Westwood, MA) and were stained with Wright’s stains (Campbell, 1988). A double blind design was used in the cell counts. One hundred leukocytes on each slide were examined at 2,000x magnification. Heterophils, lymphocytes, monocytes, basophils, and eosinophils were identified based on their characteristics described by Campbell (1988). The ratio of circulating heterophil:lymphocyte (H:L) was calculated.

RIA for Plasma CORT Concentrations
Total plasma CORT was measured in triplicate using a commercial 125I CORT RIA kit (ICN Biomedicals Inc., Costa Mesa, CA). A modification and validation were done based on the previously published method used in chickens (Cheng et al., 2001b). The concentration of CORT was calculated from a reference curve that ranges from 0.1 ng/mL (95.4% binding) to 4.0 ng/mL (14.9% binding), and the correlation coefficient was 0.9995. The sensitivity of the assay was 0.02 ng/mL. All samples within the experiment were analyzed at the same time.

HPLC Assay for 5-HT and Trp Concentrations
To measure blood concentration of 5-HT, whole blood samples were acidified in duplicate using 4 M perchloric acid and freshly prepared 3% ascorbic acid. After centrifugation, the acid-supernatants were filtered through a 0.22-µm syringe filter and then injected onto the columns of the CoulArray HPLC system automatically (ESA, Inc., Chelmsford, MA). To measure brain concentration of 5-HT, the hypothalamus and raphe nuclei from the left hemisphere of the brain were dissected. The brain regions were weighed and homogenized in ice-cold 0.2 M perchloric acid, at a 10:1 ratio (for µL of perchloric acid:mg of sample). The homogenized mixture was centrifuged at 14,000 x g for 30 min at 4°C. The resultant supernatant was drawn off and filtered through a 0.2-µm polyvinylidene fluoride filter into an HPLC sample vial. The mobile phase flow rate was 1.0 mL/min., and the concentration of 5-HT and Trp were calculated from a reference curve made using standard 5-HT (Cheng et al., 2001b).

Reverse Transcription PCR of Neurotransmitter Receptors
The hypothalamus and raphe nuclei from the right hemisphere of the brains of chickens were examined for the 5-HT1A receptor (5-HT1AR) gene. The expression of 5-HT1AR genes was analyzed by reverse transcription PCR according to the method described by Wong et al. (1994) and Mohanan et al. (2005). The brain regions were homogenized in a Buffer RLT and β-mercaptoethanol mixture. The RNA was extracted and quantified from this homogenate using a GeneAmp RNA PCR kit (Applied Biosystems, Norwalk, CT). Primer pairs and conditions used were as follows: 5-HT1AR (357 bp), 5'-GGCCGC CGTGCTCAT-3' and 5'-ATGGCGGGATGGATATCA-3', and housekeeping gene glyceraldehyde-3-phosphate de-hydrogenase (121 bp; a constitutively expressed gene), 5'-TGACAAGTCCCTGAAAATTGTCA-3' and 5'-CAAG-GGTGCCAGGCAGTT-3'. The samples and standard were amplified using an ABI Prism system (Applied Bio-systems, Foster City, CA) following the instruction of the manufacturer. The expression levels of target 5-HT1AR gene were normalized to the internal glyceraldehyde-3-phosphate dehydrogenase standard.

Statistical Analysis
All continuous data were analyzed by a 2-way ANOVA using PROC GLM in the SAS program (Windows, version 8.0). Log transformations were applied to physiological data to induce normality and homogenize variances. Arcsine square root transformations were applied to the behavior data to normalize and homogenize variances. Statistical significance was at P < 0.05.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
Behavioral Changes After Transport Stress
The baseline behavioral time budgets for eating, drinking, and preening were not different between the strains but were significantly affected by transportation (Table 1Go). In the afternoon (immediately posttransport), preening, as a comfort behavioral indicator, was significantly reduced in the birds from both strains, but a more prominent effect was found in the DXL birds than in the HGPS birds (P < 0.01 and 0.05, respectively, Table 1Go). Drinking was increased in the HGPS birds only (P < 0.01). Increased drinking may ensure that the HGPS birds were able to get rehydrated posttransportation, which is important to prevent water deprivation stress resulting from transportation and to maintain osmolality of the extracellular fluid. A stable osmolality is essential for neuroendocrine systems to function properly (Saini et al., 1990; Star, 1990; Lane and Feeback, 2002; Sawka et al., 2005). The different responses between the strains may indicate that the HGPS birds had greater resistance to transportation stress than the DXL birds. In the morning period observation time (the next day), preening was significantly increased, whereas eating, as a compensation, was reduced in the birds from both strains, but a more prominent effect was found in the HGPS birds (P < 0.01 and 0.05, respectively). The data may indicate that the birds from both strains had capacity to recover from the transport stress, but the HGPS birds had greater adaptability to the stress.


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  		Table 1. Genetic basis of different behavioral changes in laying hens after transportation stress
 
Physical Changes After Transport Stress
Body weights did not vary between the treatments in the same strain, but there were strain differences (Table 2Go). The means of relative weights of the heart and spleen did not show differences between the strains in the same treatment or between the treatments (P > 0.05), but the relative liver weight was affected by the treatments. Transported birds had higher relative liver weights regardless of strains (P < 0.01, Table 1Go). Although the cellular mechanisms underlying liver changes are unclear, it could be related to stress-induced changes in the liver functions, such as increased antioxidant system activities (Sahin and Gumuslu, 2007) or metabolic changes including alteration of gluconogenesis as seen in mammals (Christensen et al., 1975; Ricart-Jane et al., 2002; Lin et al., 2004), or both. The results indicate that the liver is very susceptible to stress, and future studies should be conducted to examine the biological function of liver in response to stress.


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  		Table 2. Genetic basis of different changes of BW and organ weights in laying hens after transportation stress
 
Physiological Changes After Transport Stress
The relative weight of the adrenal gland and the baseline concentrations of CORT were not significantly different between the strains (P > 0.05), but after transportation stress, both relative adrenal gland weight and CORT concentrations were greatly increased in the HGPS birds than in the DXL birds (P < 0.01, Table 3Go). The strain differences could be the result of different genetically mediated stress responses of the adrenal system as reported in the previous studies (Jones et al., 1992; Savory and Mann, 1997; Satterlee and Marin, 2006).


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  		Table 3. Genetic basis of different changes of corticosterone and hematological parameters in laying hens after transportation stress
 
The adrenal system has been considered to be one of the final common pathways to control animal adaptability in response to various stressors (Siegel, 1995). The effects of CORT on stress-induced responsiveness of an organism may depend on its levels (i.e., a level slightly or excessively changed from its physiological basis), which could protect or destruct the coping capability of the organism (Sapolsky and Meaney, 1986; Jones and Satterlee, 1996). The upregulated adrenal system, higher CORT concentrations, and heavier adrenal gland weights, in the stressed HGPS birds compared with the DXL birds, might be at the high end of physiologic levels, which may be as a part of defense mechanisms against the transportation challenge. The differences may also underlie the higher survivability, sedate and passive behaviors, and better coping to social, handling, and environmental stressors of the HGPS strain, as reported previously (Hester et al., 1996a,b; Craig and Muir, 1996a,b). Similar to the postulation, Siegel (1971) indicated that adrenal hypertrophy may be an indicator of greater adaptation to stress. Wingfield (2002) also indicated that CORT acts in maximizing fitness by ensuring immediate survival of a potentially catastrophic event but suppresses activities concerned with long-term survival and production. Alterations in regulation of adrenocortical activity appear to be essential in controlling coping strategy and activity, as well as mobilization of body energy sources such as glycogen and triglyceride in response to stressors (Gaillard and Al-Damluji, 1987; Tempel and Leibowitz, 1994). Conversely, CORT could have inhibitory effects on the coping ability of the animal, and negative effects on physical parameters have been reported. For example, in response to mechanical restraint, CORT concentrations were approximately 2- to 3-fold higher in birds genetically selected for high adrenal response compared with the birds of the low response line (Brown and Nestor, 1974). Birds of the high adrenal response strain failed to maintain physiological homeostasis, exhibited slower growth (Brown, 1959), overstated fear (Jones et al., 1992; Jones and Satterlee, 1996), were more highly excitable (Brown and Nestor, 1974), had a reduced number of eggs, and had higher natural mortality (Brown and Nestor, 1974). However, this is not the case in the HGPS birds, because a higher adrenal activity is correlated to a high egg production and great adaptability to various stressors, as reported previously (Hester et al., 1996a,b,c; Craig and Muir, 1996a,b).

Ratio of H:L has be used as physiological indicators of stress in evaluation of chicken responsiveness to novel environments and various stressors (Gross and Siegel, 1983; Beuving et al., 1989; Maxwell, 1993). The DXL birds but not the HGPS birds had a stress-induced increased H:L ratio (Table 3, PGo < 0.05). This may suggest that the DXL birds had a lower adaptive capability to transportation stress than the HGPS birds.

There were strain differences in the regulation of the 5-HT system in response to transportation stimulations. Compared with the DXL birds, the HGPS birds had a higher baseline blood Trp, which was reduced after transportation (Table 4Go; P < 0.01). Compared with the controls of each strain, the concentrations of 5-HT in the hypothalamus of the stressed HGPS birds tended to be higher (P = 0.09), and 5-HT1AR mRNA expression was reduced in both the hypothalamus (P < 0.05) and the raphe nucleus (data not shown). There were no stain differences in the blood 5-HT concentrations at both the baseline and post-transportation (P > 0.05).


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  		Table 4. Genetic basis of different regulations of serotonin system in laying hens after transportation stress
 
Tryptophan is the precursor amino acid for the synthesis of 5-HT. Tryptophan is acquired from foods and is transported from plasma to the brain across the blood-brain barrier. The present findings of stress-induced decrease in plasma Trp levels in the stressed HGPS birds may be associated with the increase of Trp entering the brain for synthesizing 5-HT. Although the concentrations of brain Trp were not examined, 5-HT levels tended to be increased in the brain of the stressed HGPS birds. Similar to the results, Dawood and Bano (2005) and Salim et al. (2003) reported that in rats, after 1 or 2 h of immobilization, Trp concentrations were increased in the brain but not in the peripheral systems, such as the liver and plasma.

Serotonin has multiple functions in controlling the biological processes of an organism. In the central nervous system, 5-HT functions to inhibit aggression and modulates stress response, including social and environmental adaptability (Martin et al., 2000). In the peripheral systems, however, biological roles of 5-HT in stress regulation are unclear. Decreased, increased, and unchanged blood 5-HT concentrations have been found in association with various stress responses (Hanna et al., 1995; Moffitt et al., 1998). The conflicting data from different investigations could be related to different genetic selection programs, species, behavioral evaluations and stressors used, as well as duration and frequency of stressor presentation.

In the present study, the results showed that there were no differences in the baseline of both blood and central 5-HT concentrations between the HGPS birds and DXL birds, whereas stress-induced higher central 5-HT levels were found in the HGPS birds but not in the DXL birds (Table 4Go). In the HGPS birds, the high 5-HT level in the brain coincided with their great survivability resulting from lower cannibalism and high stress resistance reported previously (Craig and Muir, 1996a,b; Hester et al., 1996a,b,c). The present findings indicate that in birds, similar to in mammals, there are genetic-based variations in the functions of 5-HT in regulating stress responses (Martin et al., 2000; Porter et al., 2004).

After transportation, 5-HT1AR mRNA expression was downregulated in the brains of the HGPS birds but not in the DXL birds (P < 0.05, Table 4Go). Similarly, the genetic bases of negative correlations between 5-HT levels and 5-HT1AR mRNA expression has been found in rodents diversely selected based on their aggressive behaviors after a resident-intruder test (Caramaschi et al., 2007). Compared with aggressive mice, the nonaggressive ones had lower 5-HT1AR density with higher 5-HT levels in the brains. Although the cellular mechanisms of down-regulated 5-HT1AR gene expression are still unknown in the current chicken strains, it could be similar to those proposed in rodents and humans. In mammals, it has been evidenced that 5-HT1A receptors are located at so-matodendrites, as autoreceptors, and function in the auto-regulation of the release of 5-HT of the brain from axonal terminals (Pineyro and Blier, 1999; de Boer and Koolhaas, 2005). Through the feedback loop, the serotonergic system maintains its pathophysiological balance. In the current study, stress-caused higher concentrations of 5-HT in the HGPS birds may negatively regulate 5-HT1AR density by downregulating its gene expression through the feedback loop. In addition, the reduced 5-HT1AR mRNA level could be related to transiently increased concentrations of CORT after transportation stress. It has been found that CORT regulates the activity of the serotonergic system by downregulation of 5-HT1AR activation, and gene expression has been found in humans and rodents (Meijer and de Kloet, 1998; Veenema et al., 2004). However, further studies are needed to confirm this hypothesis, such as examination of the changes of 5-HT1AR density and its gene expression after applying exogenous 5-HT or adrenocorticotropic hormone.

Our results demonstrate that there were strain differences in physical, behavioral, and physiological responses to transportation stress in chickens. The data further evidence that selection-associated functional integrations between the behavior, physiology, and production of birds may create suites of traits for improving bird well-being during routine production practices, such as the HGPS strain in response to transportation stress. The findings also support the potential for using behavioral and physiological indicators, such as 5-HT, to selectively breed animals with superior stress-coping abilities.


   ACKNOWLEDGMENTS
 
We would like to thank Fred Haan and the staff at the Purdue Poultry Facility as well as the technicians at the Livestock Behavior Research Unit of the USDA in West Lafayette for their outstanding assistance. This study was supported by a grant of USDA-National Research Initiative #2032.

Received for publication November 26, 2007. Accepted for publication January 30, 2008.


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