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Stress in lambs (Ovis aries) during a routine management procedure: Evaluation of acute and chronic responses
0300-9629/94 S6.00+0.00
Camp. Eiochem.Physiol. Vol.107A,No. 1,pp.181-185, 1994
0 1993Pergamon Press Ltd
Printed in Great Britain
Stress in lambs (Ovis aries) during a routine management procedure: evaluation of acute and chronic responses R. C. Rhodes III, M. M. Nippo and W. A. Gross Department of Fisheries, Animal and Veterinary Science, University of Rhode Island, Kingston, RI 02881, U.S.A. These experiments were performed to evaluate the acute and chronic stress responses of lambs during a common, yet invasive management procedure, tail docking (tail amputation). Tail docking had no effect on the average daily weight gain of lambs. Tail docking had a significant acute endocrine effect; cortisol levels were consistently higher in the docked animals (17.1+ 1.6 ng/ml) versus the control animals (7.4 + 0.8 ng/ml). Chronically, cortisol levels were highest shortly after docking and returned to basal levels by 3 days after docking. These data indicate that tail docking elicits an immediate, but not sustained, stress response. Key words: Stress; Ouis aries; Tail docking; Cortisol.
Comp. Biochem. Physiol. 107A, 181-185, 1994.
Introduction The welfare of agriculturally important domestic animals has become a topic of extensive interest. To this end, most industrialized nations have promulgated regulations for animals used in agriculture. However, our understanding of welfare, stress and animal production is incomplete. The mechanisms that enable animals to respond adequately to changes in the environment depend on close interaction between the nervous and endocrine systems. This has been apparent since the 1930s when Cannon (1935) proposed that catecholamines mediated short-term “flight and fight” responses and Selye (1936) postulated that adrenal output mediated chronic stress responses. Numerous investigators have reported that any number of noxious stimuli result in an increase of catecholamine and corticosteroid levels in domestic animals (see review by Stephens, 1980). Correspondence
to: R. C. Rhodes III, Department of Fisheries, Animal and Veterinary Science, University of Rhode Island, Kingston, RI 02881, U.S.A. Tel: 401-7922487. Received 15 February 1993; accepted 19 March 1993. CBPA
107/1-M
In sheep, cortisol is the primary corticosteroid released during stressful stimuli or stressors. In the past two decades, the role of husbandry manipulations as potential stressors has become a significant concern of both researchers and producers. Procedures such as shearing, castration, docking, vaccination, isolation, herding and transportation have been reported to be stressful to animals (Reid and Mills, 1962; Kilgour and DeLangen, 1970; Purchas, 1973; Thurley and McNatty, 1973; Fulkerson and Jamieson, 1982; Harlow et al., 1987; Shutt et al., 1987, 1988). In fact, some husbandry practices that involve minor surgical manipulation (e.g. castration and docking) have traditionally been performed without administration of analgesics, anesthetics or tranquilizers. Dantzer and Mormede (1983) have suggested that elevated cortisol levels might account for production losses and the increased susceptibility of animals to disease during stressful situations. The term stress is often used synonymously with distress; corticosteroids are often used as indicators of distress. Although a number of Australian scientists (Blackshaw, 1986; Rushen, 1986) have expressed concern over using only corticosteroid levels as indicators of distress or 181
182
R. C. Rhodes III et al.
welfare, several researchers have shown, at least in mature sheep, that plasma corticosteroid levels are positively correlated with the presumed severity of a procedure (Shutt et al., 1987; Mellor and Murray, 1989b). In the United Kingdom, most lambs are docked within days of birth (Mellor and Murray, 1989a). Alternatively, in the United States, lambs are frequently docked as a mass procedure once the last lamb has been born. Although the notion is that docking younger lambs is preferable, this is not always a readily attainable production goal. Hence the objectives of these experiments were to evaluate performance and the severity of the stress response in both an acute (Experiment 1) and chronic (Experiment 2) context.
Materials and Methods Experiment I, acute phase Twelve, spring-born Dorset lambs (Ok aries) (16 & 1.2 days of age) were either docked (n = 6) or tails were left intact (n = 6) at 0630 hours. The docking procedure involved applying a Burdizzo-type clamp caudal to the third palpable vertebra distal to the tailhead. The tail was then severed with a sterile scalpel blade, and the clamp was maintained for 3 min. Control animals were restrained in a similar fashion, although the tail was not clamped or removed. After removal of the clamp or control restraint, lambs were returned to their dams. Blood samples were drawn via jugular venipuncture immediately after docking (0 h) and thereafter at 3,6,9 and 12 hr. Blood was allowed to clot at outdoor ambient temperature (winter) then centrifuged for 45 min at 1OOOg.Serum was aspirated, placed into 12 x 75 mm glass tubes and frozen at - 30°C until analysis for cortisol by solid phase radioimmunoassay.
CORTISOL -
Twenty-three, spring-born Dorset lambs (7 + 0.8 days of age) were either docked (n = 11) or left intact (n = 12) using procedures previously described. Blood samples were taken by jugular venipuncture 3 days prior to, shortly after the time of docking (within 10 min, day 0), then 3 and 6 days after treatment. Blood was processed and stored as described previously until analysis. Starting at birth, lambs were weighed on a spring balance scale every 4 days for a period of 16 days. Average daily gain was then calculated.
DOCKED
--.-
1 CONTROL
-t 3
0
6
9
12
HOURS
Fig. I. Cortisol concentrations in docked and intact lambs during the acute, 12-hr period following docking. A significant treatment effect (P < 0.05) was detected.
Cortisol radioimmunoassay All blood samples were evaluated for cortisol by a solid phase radioimmunoassay using a commercially available kit (Diagnostic Products Corporation, Los Angeles, CA, USA). Regression analysis of the log-logit transformed standard curves was used to calculate the cortisol concentration of unknowns (Rodbard et al., 1969). In our laboratory, the assay had a minimal detection limit of approximately 1 ng per tube, an intra-assay coefficient of variation of 3.5% and an interassay coefficient of variation of 7.0%. Tests of significance were made by an analysis of variance which accounted for repeated measurements of experimental units (Gill and Hafs, 1971). Differences with a value of P < 0.05 were considered to be significant. Average values shown throughout are followed by standard error of the mean.
CORTISOL
LEVELS
EXPERIMENT -
Experiment 2, chronic phase
LEVELS
EXPERIMENT
DOCKED
--*-
2 CONTROL
JoI
I
0’
-3
0
3
6
DAYS
2. Cortisol concentrations in docked and intact lambs aurmg the chronic, dday period following docking. A significant treatment x day effect (P < 0.05) was detected.
Stress responses in lambs
Results Experiment
1
In this phase of the study, a significant time effect was observed. Cortisol levels were consistently higher in the docked animals versus the control animals throughout the 12-hr sampling period (Fig. 1). Experiment
2
Docking the lambs had no significant effect on the production performance of the lambs. The average daily gain (kg head-’ day-‘) of the control lambs was 0.25 f 0.02 while docked lambs gained 0.24 & 0.02. Consistent with the results in experiment 1, docking in experiment 2 had a significant effect on serum profiles of cortisol (Fig. 2). A significant day effect and a significant treatment x day interaction were detected. However, this effect was manifested primarily during the period immediately following docking, a period when cortisol levels appeared to reach highest concentrations. Three days after docking, cortisol levels approximated basal levels observed in control lambs.
Discussion In this study, docking did not appear to alter the growth of the lambs, as indicated by the identical average daily weight gains of docked and control animals. This observation is consistent with that of Wohlt et al. (1982) who reported gains (kg head-’ day-‘) of 0.25 + 0.03 in docked and 0.27 f 0.02 in control animals, manipulated at an age of 14 days. Hence, performance does not appear to be altered by tail docking. Interestingly, the cortisol levels of controls appeared to be higher during the chronic phase versus levels found in the acute phase. This apparent difference might be accounted for by the age of the lambs used in each experiment. The average age of the lambs in the chronic phase was younger than lambs used in the acute phase. This supposition is supported by the observation that basal levels of corticoids decreased with neonatal age (Martin, 1985; Mellor and Murray, 1989a). Lastly, support for this conclusion was seen in the profiles of the controls during the chronic phase (Fig. 2). As the animals aged, an apparent trend toward a decrease in basal cortisol levels occurred. In experiment 1, a significant elevation in cortisol was observed in the docked animals, but not in the controls. These observations are consistent with those made by previous re-
183
searchers. In domestic livestock, a number of management situations such as shearing, castration, docking, vaccination, isolation, herding and transportation have been reported to induce an acute stress response (i.e. a response lasting up to several hours) (Reid and Mills, 1962; Kilgour and DeLangen, 1970; Purchas, 1973; Thurley and McNatty, 1973; Fulkerson and Jamieson, 1982; Harlow et al., 1987; Shutt et al., 1987, 1988, 1989; Mellor and Murray, 1989a,b). However, in these previous studies, sampling was often terminated within 24 hr of the stressor, thus representing only an acute phase. Although no persistence in the stress response was observed in the current study, this is the first report of the chronic hormonal effects of tail docking. Recently, French and Morgan (1992) observed the formation of neuromata in the stump of the tail of docked lambs. The presence of neuromata indicate the potential for chronic pain (phantom limb syndrome) in this area long after docking. However, if cortisol levels indicate level of distress, then chronic pain was not apparent in the docked lambs in experiment 2; cortisol levels had returned to baseline within 3 days of docking. Although the elaboration of adrenal steroids assists the animal in coping with stress, the effects elicited by the corticosteroids can have a detrimental effect on the organism. In domestic animals, stressors have been implicated in the onset of pathological lesions (eg. gastric ulcers, coliform enteritis) and death (Fraser et al., 1975; Dantzer and Mormede, 1983). The precise immunosuppressive effect of stressors has not been elucidated, however, the role of glucocorticoids as modulators of immunity has been known for over three decades. In laboratory animals, short-term exposure to noxious stimuli suppresses humoral immunity (Rasmussen et al., 1959). Furthermore, stress-induced levels of corticoids have been demonstrated to suppress cellular immunity (Gisler et al., 1971; Gisler and Schenkel-Hulliger, 1971; Folch and Waksman, 1974; Monjan and Collector, 1977). Similarly, administration of ACTH, cortisol or dexamethasone, the synthetic corticoid analogue, altered leukocyte number and immune function in domestic animals, although the action of exogenous cortisol appears to be more severe than similar levels of endogenous cortisol (Gwazdauskas et al., 1980; Roth and Kaeberle, 1981, 1983; Roth et al., 1982; Collins and Suarez-Guemes, 1985; Martin, 1985; Yang and Schultz, 1986, McGlone er al., 1990). Endogenous increases in cortisol due to stress have been reported to inhibit lymphocyte responses in shipped calves (Blecha et al., 1984) and restrained pigs (Westly and Kelley, 1984).
184
R. C. Rhodes III er al.
Alternatively, Minton and Blecha (1990) reported that heat stress and restraint of yearling lambs significantly increased cortisol, but did not alter the ability of lymphocytes to respond to mitogens. These researchers suggested that acute stressors might not be of sticient duration or intensity to alter immune func~on in sheep. Whether subjecting IamPS to other stressors, such as those commonly encountered in production contexts would be of sufficient duration and intensity to limit immune function, remains to be determined. Acknowledgements-This research is Contribution # 2820 of the College of Resource Development, University of Rhode Island, with support from the Rhode Island Agricultural Experiment Station. We thank Drs M. W. Fleming and U. G. Whitworth for critical review of the manuscript.
References Blackshaw J. K. (1986) Objective measure of welfare in farming environments. Aust. vet. J. 63, 361-364. Blecha F., Boyles S. L. and Riley J. G. (1984) Shipping suppresses lymphocyte blastogenic responses in Angus and Brahman x Angus feeder calves. J. Anim. Sci. 59, 576583. Cannon W. B. (1935) Stresses and strains of homeostasis. Am. J. Med. Sci. 189, 1-14. Collins M. T. and Suarez-Gu-+s F. (1985) Effect of hydrocortisone on circulating lymphocyte number and their mitog-induced blastog-esis in lambs. [Am. J. oet. Res. 46, 836-840. Dantzer R. and Morm&de P. (1983) Stress in farm animals: a need for reevaluation. J. Anim. Sci. 57, 6-18. Folch H. and Waksman B. H. (1974) The splendid suppressor cell I. Activity of thymus dependent adherent cells: changes with age and stress. J. Immunol. 113, 127-139. Fraser D., Fraser J. S. D. and Fraser A. F. (1975) The term “stress” in a veterinary context. Br. vet. J. 131, 653662. French N. P. and Morgan K. L. (1992) Neuromata in docked lambs’ tails. Res. vet. Sci. 52, 389-390. Fulkerson W. J. and Jamieson P. A. (1982) Pattern of cortisol release in sheep following administration of synthetic ACTH or imposition of various stressor agents. Aust. J. biol. Sci. 35, 215-222. Gill J. L. and Hafs H. D. (1971) Analysis of repeated measurements of animals. J. Anim. Sci. 33, 331-336. Gisler R. H. and Schenkel-Hulliger L. (1971) Hormonal regulation of the immune response II. Influence of pituitary an adrenal activity on immune responsiveness in o&o. Cell Immunol. S-646-657. Gisler R. H.. Bussard A. E.. Maize J. C. and Hess R. (1971) Hormonal regulation of the immune response I. Introduction of an immune response in oitro with lymphoid cells from mice exposed to acute systemic stress. Cell. Immunol. 2, 634-645. Gwazdauskas F. C., Pappe M. J., Peery D. A. and McGiiard M. L. (1980) Plasma ghtcocorticoid and circulating blood leukocyte responses in cattle after sequential intramuscular injections of ACM-I. Am. J. vet. Res. 41, 1052-1056. Harlow H. J., Thome E. T., Williams E. S., Belden E. L. and Gem W. A. (1987) Adrenal responsiveness in domestic sheep (Ovis aries) to acute and chronic stressors as predicted by remote monitoring of cardiac frequency. Can. J. Zool. 66, 2021-2027. Kilgour R. and DeLangen H. (1970) Stress in sheep result-
ing from management practices. Proc. N.Z. Sot. Anim. Prod. 30, 65-76. Martin C. R. (1985) The ghtcocorticoids. In Endocrine Physiology, pp. 215-251. Oxford University Press, New York. McGlone J. J., Gibson M. L., Miller E. A., Hurst R. J. and Salak J. L. (1990) Cortisol suppresses in vitro neutrophil chemotaxis and NK cell function. J. Anim. Sci. 68, (Suppl. l), 259. Mellor D. J. and Murray L. (1989a) Effects of tail docking and castration on behaviour and plasma cortisol concentrations in young lambs. Res. uer. Sci. 46, 387-391. Mellor D. J. and Murray L. (1989b) Changes in the cortisol responses of lambs to tail docking, castration and ACTH injection during the first seven days after birth. Res. vet. Sci. 46, 392-395. Minton J. E. and Blecha F. (1990) Effect of acute stressors on endocrinological and immunological functions in lambs. J. Anim. Sci. 68, 3145-3151. Monjan A. A. and Collector M. I. (1977) Stress-induced modulation of the immune response. Science I%, 307-308 Purchas R. W. (1973) The response of circulating cortisol levels in sheep to various stresses and to reserpine admin&ration. Aust. J. biol. Sci. 26, 477489. Rasmussen A. F., Spencer E. S. and Marsh J. T. (1959) Decrease in susceptibility of mice to passive anaphylaxis following avoidance learning stress. Proc. Sot. exp. biol. Med. 108, 878479. Reid R. L. and Mills S. C. (1962) Studies on the carbohydrate metabolism of sheep. XIV. The adrenal response to psychological stress. Ausf. J. ugric. Sci. 13, 289-295. Rodbard D., Bridson W. and Rayford P. L. (1969) Calculation of radioimmunoassay results. J. lab. clin. Med. 74, 77&78 1. Roth J. A. and Kaeberle M. L. (1981) Effects of in viuo dexamethasone administration on in vitro bovine polymorphonuclear leukocyte function. Infect. Immun. 33, 434441. Roth J. A. and Kaeberle M. L. (1983) Suppression of neutrophil and lymphocyte function induced by a vaccinal strain of bovine viral diarrhea virus with and without the administration of ACTH. Am. J. vet. Res. 44, 2366-2372. Roth J. A., Kaeberle M. L. and Hsu W. H. (1982) Effects of ACTH administration on bovine polymorphonuclear leukocyte function and lymphocyte blastogenesis. Am. J. vet. Res. 43, 412-416. Rushen J. (1986) Some problems with the physiological concept of “stress”. Auk. vet. J. 63, 359-361.Selye H. (1936) A syndrome produced by diverse nocuous agents. Nafure 138, 32. Shutt D. A.. Connell R. and Fell L. R. (1989) Effects of ovine corticotropin-releasing factor and vasopressin on plasma B-endorphin and cortisol in response to routine surgical procedures in lambs. Life Sci. 45, 257-262. Shutt D. A., Fell L. R., Connell R. and Be.11A. K. (1988) Stress responses in lambs docked and castrated surgically or by the application of rubber rings. Aust. vet. J. 65.5-7. Shutt b. A.,-Fell L. R., Connell R, Bell A. K., Wallace C. A. and Smith A. I. (1987) Stress-induced changes in plasma concentrations of in&unoreactive B-end&phin and cortisol in response to routine surgical procedures in lambs. Aust. J. biol. Sci. 40, 97-103. Stephens D. B. (1980) Stress and its measurement in domestic animals: A review of behavioral and physiological studies under field and laboratory situations. A& uer. Sci. camp. Med. 24, 179-210. Thurley D. C. and McNatty K. P. (1973) Factors affecting peripheral cortisol levels in unrestricted ewes. Acta Endocrinol. 74, 331-337.
Stress responses in lambs Westly H. J. and Kelley K. W. (1984) Physiologic concentrations of cortisol suppress cell mediate immune events in the domestic pig. Proc. Sot. exp. biol. Med. 177, 156164. Wohlt J. E., Wright T. D., Sirois V. S., Kniffen D. M. and Lelkes L. (1982) Effect of docking on health, blood cells
185
and metabolites and growth of Dorset lambs. J. Anim. Sci. S4, 23-28. Yang W. C. and Schultz R. D. (1986) Effect of corticosteroid on porcine leukocytes: age related effects of corticosteroid inhibition on porcine lymphocyte responses to mitogens. Vet. Immunol. Immunopath. 13, 19-29.
Camp. Eiochem.Physiol. Vol.107A,No. 1,pp.181-185, 1994
0 1993Pergamon Press Ltd
Printed in Great Britain
Stress in lambs (Ovis aries) during a routine management procedure: evaluation of acute and chronic responses R. C. Rhodes III, M. M. Nippo and W. A. Gross Department of Fisheries, Animal and Veterinary Science, University of Rhode Island, Kingston, RI 02881, U.S.A. These experiments were performed to evaluate the acute and chronic stress responses of lambs during a common, yet invasive management procedure, tail docking (tail amputation). Tail docking had no effect on the average daily weight gain of lambs. Tail docking had a significant acute endocrine effect; cortisol levels were consistently higher in the docked animals (17.1+ 1.6 ng/ml) versus the control animals (7.4 + 0.8 ng/ml). Chronically, cortisol levels were highest shortly after docking and returned to basal levels by 3 days after docking. These data indicate that tail docking elicits an immediate, but not sustained, stress response. Key words: Stress; Ouis aries; Tail docking; Cortisol.
Comp. Biochem. Physiol. 107A, 181-185, 1994.
Introduction The welfare of agriculturally important domestic animals has become a topic of extensive interest. To this end, most industrialized nations have promulgated regulations for animals used in agriculture. However, our understanding of welfare, stress and animal production is incomplete. The mechanisms that enable animals to respond adequately to changes in the environment depend on close interaction between the nervous and endocrine systems. This has been apparent since the 1930s when Cannon (1935) proposed that catecholamines mediated short-term “flight and fight” responses and Selye (1936) postulated that adrenal output mediated chronic stress responses. Numerous investigators have reported that any number of noxious stimuli result in an increase of catecholamine and corticosteroid levels in domestic animals (see review by Stephens, 1980). Correspondence
to: R. C. Rhodes III, Department of Fisheries, Animal and Veterinary Science, University of Rhode Island, Kingston, RI 02881, U.S.A. Tel: 401-7922487. Received 15 February 1993; accepted 19 March 1993. CBPA
107/1-M
In sheep, cortisol is the primary corticosteroid released during stressful stimuli or stressors. In the past two decades, the role of husbandry manipulations as potential stressors has become a significant concern of both researchers and producers. Procedures such as shearing, castration, docking, vaccination, isolation, herding and transportation have been reported to be stressful to animals (Reid and Mills, 1962; Kilgour and DeLangen, 1970; Purchas, 1973; Thurley and McNatty, 1973; Fulkerson and Jamieson, 1982; Harlow et al., 1987; Shutt et al., 1987, 1988). In fact, some husbandry practices that involve minor surgical manipulation (e.g. castration and docking) have traditionally been performed without administration of analgesics, anesthetics or tranquilizers. Dantzer and Mormede (1983) have suggested that elevated cortisol levels might account for production losses and the increased susceptibility of animals to disease during stressful situations. The term stress is often used synonymously with distress; corticosteroids are often used as indicators of distress. Although a number of Australian scientists (Blackshaw, 1986; Rushen, 1986) have expressed concern over using only corticosteroid levels as indicators of distress or 181
182
R. C. Rhodes III et al.
welfare, several researchers have shown, at least in mature sheep, that plasma corticosteroid levels are positively correlated with the presumed severity of a procedure (Shutt et al., 1987; Mellor and Murray, 1989b). In the United Kingdom, most lambs are docked within days of birth (Mellor and Murray, 1989a). Alternatively, in the United States, lambs are frequently docked as a mass procedure once the last lamb has been born. Although the notion is that docking younger lambs is preferable, this is not always a readily attainable production goal. Hence the objectives of these experiments were to evaluate performance and the severity of the stress response in both an acute (Experiment 1) and chronic (Experiment 2) context.
Materials and Methods Experiment I, acute phase Twelve, spring-born Dorset lambs (Ok aries) (16 & 1.2 days of age) were either docked (n = 6) or tails were left intact (n = 6) at 0630 hours. The docking procedure involved applying a Burdizzo-type clamp caudal to the third palpable vertebra distal to the tailhead. The tail was then severed with a sterile scalpel blade, and the clamp was maintained for 3 min. Control animals were restrained in a similar fashion, although the tail was not clamped or removed. After removal of the clamp or control restraint, lambs were returned to their dams. Blood samples were drawn via jugular venipuncture immediately after docking (0 h) and thereafter at 3,6,9 and 12 hr. Blood was allowed to clot at outdoor ambient temperature (winter) then centrifuged for 45 min at 1OOOg.Serum was aspirated, placed into 12 x 75 mm glass tubes and frozen at - 30°C until analysis for cortisol by solid phase radioimmunoassay.
CORTISOL -
Twenty-three, spring-born Dorset lambs (7 + 0.8 days of age) were either docked (n = 11) or left intact (n = 12) using procedures previously described. Blood samples were taken by jugular venipuncture 3 days prior to, shortly after the time of docking (within 10 min, day 0), then 3 and 6 days after treatment. Blood was processed and stored as described previously until analysis. Starting at birth, lambs were weighed on a spring balance scale every 4 days for a period of 16 days. Average daily gain was then calculated.
DOCKED
--.-
1 CONTROL
-t 3
0
6
9
12
HOURS
Fig. I. Cortisol concentrations in docked and intact lambs during the acute, 12-hr period following docking. A significant treatment effect (P < 0.05) was detected.
Cortisol radioimmunoassay All blood samples were evaluated for cortisol by a solid phase radioimmunoassay using a commercially available kit (Diagnostic Products Corporation, Los Angeles, CA, USA). Regression analysis of the log-logit transformed standard curves was used to calculate the cortisol concentration of unknowns (Rodbard et al., 1969). In our laboratory, the assay had a minimal detection limit of approximately 1 ng per tube, an intra-assay coefficient of variation of 3.5% and an interassay coefficient of variation of 7.0%. Tests of significance were made by an analysis of variance which accounted for repeated measurements of experimental units (Gill and Hafs, 1971). Differences with a value of P < 0.05 were considered to be significant. Average values shown throughout are followed by standard error of the mean.
CORTISOL
LEVELS
EXPERIMENT -
Experiment 2, chronic phase
LEVELS
EXPERIMENT
DOCKED
--*-
2 CONTROL
JoI
I
0’
-3
0
3
6
DAYS
2. Cortisol concentrations in docked and intact lambs aurmg the chronic, dday period following docking. A significant treatment x day effect (P < 0.05) was detected.
Stress responses in lambs
Results Experiment
1
In this phase of the study, a significant time effect was observed. Cortisol levels were consistently higher in the docked animals versus the control animals throughout the 12-hr sampling period (Fig. 1). Experiment
2
Docking the lambs had no significant effect on the production performance of the lambs. The average daily gain (kg head-’ day-‘) of the control lambs was 0.25 f 0.02 while docked lambs gained 0.24 & 0.02. Consistent with the results in experiment 1, docking in experiment 2 had a significant effect on serum profiles of cortisol (Fig. 2). A significant day effect and a significant treatment x day interaction were detected. However, this effect was manifested primarily during the period immediately following docking, a period when cortisol levels appeared to reach highest concentrations. Three days after docking, cortisol levels approximated basal levels observed in control lambs.
Discussion In this study, docking did not appear to alter the growth of the lambs, as indicated by the identical average daily weight gains of docked and control animals. This observation is consistent with that of Wohlt et al. (1982) who reported gains (kg head-’ day-‘) of 0.25 + 0.03 in docked and 0.27 f 0.02 in control animals, manipulated at an age of 14 days. Hence, performance does not appear to be altered by tail docking. Interestingly, the cortisol levels of controls appeared to be higher during the chronic phase versus levels found in the acute phase. This apparent difference might be accounted for by the age of the lambs used in each experiment. The average age of the lambs in the chronic phase was younger than lambs used in the acute phase. This supposition is supported by the observation that basal levels of corticoids decreased with neonatal age (Martin, 1985; Mellor and Murray, 1989a). Lastly, support for this conclusion was seen in the profiles of the controls during the chronic phase (Fig. 2). As the animals aged, an apparent trend toward a decrease in basal cortisol levels occurred. In experiment 1, a significant elevation in cortisol was observed in the docked animals, but not in the controls. These observations are consistent with those made by previous re-
183
searchers. In domestic livestock, a number of management situations such as shearing, castration, docking, vaccination, isolation, herding and transportation have been reported to induce an acute stress response (i.e. a response lasting up to several hours) (Reid and Mills, 1962; Kilgour and DeLangen, 1970; Purchas, 1973; Thurley and McNatty, 1973; Fulkerson and Jamieson, 1982; Harlow et al., 1987; Shutt et al., 1987, 1988, 1989; Mellor and Murray, 1989a,b). However, in these previous studies, sampling was often terminated within 24 hr of the stressor, thus representing only an acute phase. Although no persistence in the stress response was observed in the current study, this is the first report of the chronic hormonal effects of tail docking. Recently, French and Morgan (1992) observed the formation of neuromata in the stump of the tail of docked lambs. The presence of neuromata indicate the potential for chronic pain (phantom limb syndrome) in this area long after docking. However, if cortisol levels indicate level of distress, then chronic pain was not apparent in the docked lambs in experiment 2; cortisol levels had returned to baseline within 3 days of docking. Although the elaboration of adrenal steroids assists the animal in coping with stress, the effects elicited by the corticosteroids can have a detrimental effect on the organism. In domestic animals, stressors have been implicated in the onset of pathological lesions (eg. gastric ulcers, coliform enteritis) and death (Fraser et al., 1975; Dantzer and Mormede, 1983). The precise immunosuppressive effect of stressors has not been elucidated, however, the role of glucocorticoids as modulators of immunity has been known for over three decades. In laboratory animals, short-term exposure to noxious stimuli suppresses humoral immunity (Rasmussen et al., 1959). Furthermore, stress-induced levels of corticoids have been demonstrated to suppress cellular immunity (Gisler et al., 1971; Gisler and Schenkel-Hulliger, 1971; Folch and Waksman, 1974; Monjan and Collector, 1977). Similarly, administration of ACTH, cortisol or dexamethasone, the synthetic corticoid analogue, altered leukocyte number and immune function in domestic animals, although the action of exogenous cortisol appears to be more severe than similar levels of endogenous cortisol (Gwazdauskas et al., 1980; Roth and Kaeberle, 1981, 1983; Roth et al., 1982; Collins and Suarez-Guemes, 1985; Martin, 1985; Yang and Schultz, 1986, McGlone er al., 1990). Endogenous increases in cortisol due to stress have been reported to inhibit lymphocyte responses in shipped calves (Blecha et al., 1984) and restrained pigs (Westly and Kelley, 1984).
184
R. C. Rhodes III er al.
Alternatively, Minton and Blecha (1990) reported that heat stress and restraint of yearling lambs significantly increased cortisol, but did not alter the ability of lymphocytes to respond to mitogens. These researchers suggested that acute stressors might not be of sticient duration or intensity to alter immune func~on in sheep. Whether subjecting IamPS to other stressors, such as those commonly encountered in production contexts would be of sufficient duration and intensity to limit immune function, remains to be determined. Acknowledgements-This research is Contribution # 2820 of the College of Resource Development, University of Rhode Island, with support from the Rhode Island Agricultural Experiment Station. We thank Drs M. W. Fleming and U. G. Whitworth for critical review of the manuscript.
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