|
|
||||||||
USDA-ARS, Livestock Behavior Research Unit, 125 S. Russell St., 216 Poultry, Purdue University, West Lafayette, IN 47907
| ABSTRACT |
|---|
|
|
|---|
1 acid-glycoprotein, were not different at any time. In this study, calves that were banded at 3-wk-of-age showed behaviors indicative of discomfort for 2 h, were attacked by more flies, and showed increased fly avoidance behaviors when docked.
Key Words: pain flies behavior
| INTRODUCTION |
|---|
|
|
|---|
The stable fly (Stomoxys calcitrans L.) is one of the most common types of disruptive flies in the United States (Dougherty et al., 1995). These flies are the most bothersome when they are biting, which occurs when flies feed as temperatures become warm. The feeding lasts from 2 to 5 min, then the flies remain on the animal to either rest or seek a new feeding station. Cattle attempt to escape this annoyance by taking flight, stomping, kicking their trunk, tail swishing, skin twitching, and head or ear movements. Flies become an economic liability because of disruption and alterations of eating patterns and increased energy expenditure in avoidance behaviors. Biting flies have been linked to disrupted grazing, slower growth (Campbell and Berry, 1989), reduced milk production and weight gain, and increased stress (Jonsson and Mayer, 1999). Campbell and Berry (1989) established an economic threshold of two stable flies per foreleg. New Zealand studies showed that at low (zero) fly numbers in the morning, there were no differences in frequencies of fly-avoidance behaviors (such as stomping, ear twitching, and tail swings) between intact and docked cows. However, at later times of the day (1200 and 1500 h) fly counts increased (more than 20 per side per 6 min), and docked cows had more avoidance behaviors that relieved the rear of the cow from flies than did the control cows (Phipps et al., 1995). Fly numbers were greater on docked cows (Wilson, 1972; Matthews et al., 1995), and fly counts were greater on rear legs of cows with trimmed switches and docked cows (Matthews et al., 1995; Eicher et al., 2001). Concurrent data showed an increase in fly avoidance behaviors in docked cows. Interestingly, cows in New Zealand that had switches trimmed but not docked were similar to controls for tail flicks, but similar to docked cows for foot stomps. All of these studies were conducted on mature animals in free-stalls, tie-stalls, or on pasture setting. Calf hutches are a good breeding ground for flies causing young calves to be more prone to fly pestering than mature animals housed in most confined housing systems or on pastures. No studies to date have addressed the impact of tail docking on calves while housed in hutches.
Cortisol is released in response to both tail docking and fly irritants. Cortisol briefly increased after tail docking in neonatal calves (Tom et al., 2001). With increased fly bites, cortisol concentrations and heart and respiration rates increased in mature animals (Schwinghammer et al., 1987). Acute phase proteins are proteins released from the liver following pathogenic infections, tissue damage, and to some stressors such as withholding of feed. Since increased plasma cortisol can exacerbate concentrations and duration of acute phase proteins (Baumann and Gauldie, 1994; Gabay et al., 1995), it follows that plasma acute phase proteins may increase with fly bites, which may be more numerous following tail docking. Previous studies have shown increased haptoglobin in response to removal of the tail of mature dairy cattle (Eicher et al., 2000). Some calf acute phase proteins are greatest at birth and decrease over time to near the concentrations of nonstressed mature cattle by 4 wk-of-age (
1-acid glycoprotein, Eicher, unpublished data), but haptoglobin begins and remains at nondetectable concentrations (Alsemgeest et al., 1993). Besides the immune system of the neonatal calf that is still developing, neurological mechanisms may still be developing as in other species.
Recent evidence shows that for procedures considered painful, some neurological maturation is beneficial (Narsinghani et al., 2000). Some pain damping mechanisms are not fully developed in fetus and neonates; including diffuse noxious inhibitory controls (Ren et al., 1997; Boucher et al., 1998), delayed maturation of interneurons, or the excitory role of neurotransmitters (Bicknell and Beal, 1984; Wang et al., 1994). But the behavioral indicators of pain have not been assessed for young dairy cattle in response to tail docking.
Our objectives in this study were to determine 1) behavioral indicators of acute pain after tail banding and 2) fly avoidance behaviors and fly counts on docked and intact Holstein heifer calves.
| MATERIALS AND METHODS |
|---|
|
|
|---|
Maintenance behaviors (Table 1
) were observed for 2 h postbanding in 72 h mode (1.2 s per frame) of a time-lapse video recorder (Panasonic AG-6540, Mipitas, CA) at the Purdue location only (n = 10 per treatment). A BP70 Panasonic camera (Mipitas, CA, outfitted with a wide-angle lens) was housed in a protective weather resistant cover, mounted on a tripod at approximately 71 cm high, and placed 2 m from the front of the calf hutch. Two hutches were viewed with one camera. These behaviors were analyzed by 5 min instantaneous scan sampling (Noldus Observer, Wagegingen, Norway).
|
1 acid-glycoprotein). Radial immunodiffusion assays were used to determine haptoglobin and
1 acid-glycoprotein concentrations (Saikin Kagaku Institute Co., Sendai, Japan).
Tests and Assays
The haptoglobin agar gel plates each were loaded with two standards, 25 and 750 µg/ml and eight test samples per plate using standards, L-cysteine reducing reagent, and solvent provided (Morimatsu et al., 1992). The
1 acid-glycoprotein only required the addition of 5 µl of standard (50 and 1500 µg/ml) or sample per well in a 10 well plate. Previous work in our laboratory, established a coefficient of variation that corresponded to the kit description (< 4%). We have also validated the haptoglobin and
1 acid-glycoprotein kits for effect of serum compared to plasma, and fresh compared to frozen samples.
In the Purdue herd, a heat sensitivity test (Zenor, 1997; Fender et al., 2000) was administered to control and banded calves (n = 10 per treatment). The heat sensitivity test was performed on the tail end at 15 min intervals for two h postbanding. Heat sensitivity testing began by clipping the lower 15 cm of control and docked calves tails a day prior to the testing. Water was heated to 60 ± 2.5°C. The heated water was taken to the hutch and the test performed in an insulated cooler. This resulted in less than 1°C drop in temperature during the testing. The shaved 15 cm of the calfs tail was inserted into the water. The time it took the calf to move the tail was recorded if less than 30 s. As in Fender et al. (2000), timing was stopped and the tail removed from the water at 30 s. When two successive tests resulted in the researcher removing the tail at 30 s, the test was discontinued for that calf. The time that the calf first left the tail in the heated water for 30 s to meet the criteria for discontinued testing was recorded, indicating no sensitivity to heat in the tail below the banding site. All testing was discontinued at 120 min postbanding, the time at which none of the control calves but all banded calves had met the criteria.
Fly Counts and Fly Avoidance Behaviors
Beginning in July (fly season), the control and docked calves in both herds were observed for fly avoidance behaviors for a 1-h time period at 0800, 1200, and 1600 using 5 min focal animal sampling on 3 consecutive d. Feeding occurred after the observation period. Flies were counted the hour preceding the behavior observations.
Fly counting procedures: calves were marked at the beginning of the stifle on the back leg and at the joint at the joining of the front leg to the body. Calves were brought to a standing position, and fly counts began after 30 s. Each leg was counted for 2 min, counting two legs simultaneously (McNeal and Campbell, 1981). An average (number per leg) was calculated for the front legs, back legs, and a total.
Behaviors (Table 1
) were defined and calves were observed for fly avoidance behaviors. Fly avoidance behaviors were recorded with direct observation by interval time sampling. One focal calf was observed continuously for 5 min, then the next calf was observed for 5 min, until all calves in that block had been observed once between 0800 to 0900, 1200 to 1300, and 1600 to 1700 h. This was repeated for 3 consecutive d. The mean of the 3 d was used as the response of each calf for each of the 0800, 1200, or 1600 h observation.
All animal care was within the Guide for the Care and Use of Agricultural Animals in Agricultural Research and Teaching (1999), and animal use was approved by the Purdue Animal Care and Use Committee and the University of Wisconsin Animal Care and Use Committee.
Statistical Methods
The Mixed model program of SAS (SAS, 2000; Littell et al., 1996) was used to analyze data as a repeated measures design (compound symmetry and ante-dependency structure used as appropriate for each variable). The fixed effect was treatment (docked or intact) and the random effect was block. Behavior data was normalized using a square root transformation.
| RESULTS |
|---|
|
|
|---|
Behavior at Banding
Behaviors of docked calves were different than for control calves following banding (Figure 1
). Lying decreased (P < 0.05; 62.5 and 31.2 mean percentage of observations) and walking (or running) was greater (P < 0.05, 7.0 and 20.0 mean percentage of observations) for the banded calves in the 2 h observation period following banding. The percentage of observations with standing was not different (P > 0.05) between control (29.1) and banded (45.1) calves. Feeding and grooming, both of which occurred infrequently, were not different between the treatments. Mean percentage of observations were 1.9 and 2.1 for feeding, and 0.1 and 0 for grooming, for control and banded calves, respectively. The specific pain indicator movement, the head-to-tail movement, differed between treated and control calves (P < 0.05) being almost eight times more frequent in the banded calves (0.97 and 7.76 occurrences per observation). Seventy five percent of the calves in the study (n = 40) lost their tails without cutting by 3 wk postbanding, leaving four calves at the Indiana location that needed cutting and six at the Wisconsin site.
|
|
|
1-acid glycoprotein (383 and 395 before treatments, 367 and 406 at 72 h postbanding, and 272 and 320 at 4 wk postbanding for control and docked calves, respectively) and haptoglobin ( 31, and 0 before treatments, 0 and 11.1 at 72 h postbanding, and 0 for both at 4 wk postbanding for control and docked calves, respectively). Haptoglobin and
1-acid glycoprotein concentrations were within normal ranges and none of the haptoglobin concentrations reached the concentration that is considered to be a response to a stressor (200 µg/ml) in mature cattle.
|
| DISCUSSION |
|---|
|
|
|---|
The heat sensitivity test showed that the tails of docked calves were insensitive 2 h after banding. Five of the banded calves (half of those tested) were insensitive to hot water at 75 min postbanding and the other five were sensitive to the hot water until 105 min postbanding. Therefore pain experienced by the calves after that 2 h period postbanding, must be originating proximal to the banding site. Tom et al., (2001) observed cortisol increased after banding at 1 h postbanding, but not at 30 min postbanding or at any of their time points after 120 min postbanding. This suggests that a moderate acute pain is experienced for about 1 h after the initial cessation of feeling in the tail. Our data only reflect the loss of sensitivity below the banding site. The tail that is above the band may become more sensitive to stimulus as inflammation and swelling occurs. Wilson (1972) noted that mature cows, exhibited swelling at the banding site at 6 h postbanding, increased tail movement 6 h postbanding, and decreased tail movement from those of control cows by 24 and 48 h postbanding. However, our data did not encompass alterations in behavior or sensitivity that develop after the initial 2 h postbanding. Other painful management procedures result in greater increases in cortisol and behavioral indicators of pain. For example, dehorning causes a much greater cortisol increase which lasts for a longer period of time (Sylvester et al., 1998), and increased vocalization is a significant behavioral indicator of pain (Watts and Stookey, 1999). Studies of 4 to 6-wk-old calves demonstrated anesthetic was useful to reduce pain during dehorning. Decreased head and leg movements, plasma cortisol, and duration of increased heart rates were used as indicators of pain reduction (Grondahl-Nielsen et al., 1999). The area around the horn bud of newborn to 3 to 4 mo-old calves was well innervated regardless of age (Taschke and Folsch, 1997).
In other species, pain control mechanisms are still developing in the neonate (Narsinghani et al., 2000). Specific pain behaviors increase and nonspecific behaviors decrease with advancing neonatal age (Guy and Abbott, 1992). Additionally, mechanisms such as diffuse noxious inhibitory controls follow a rostrocaudal pattern, resulting in higher pain threshold in the forelimbs compared to the hind limbs (Ren et al., 1997). The greater sensitivity of neonates to noxious stimuli and the rostrocaudal pattern of some of the inhibitory controls, may explain the differences in calves and cows responses to tail banding. However, at this time, no published studies are available on the development of pain damping mechanisms in neonatal cattle.
Acute Phase Protein Response
Acute phase proteins are released from the liver in response to cytokine stimulus (Interleukin-1 or -6) and cortisol enhances that response. Infections or tissue damage are two conditions that lead to the release of acute phase proteins. Because of the tissue damage that occurs during banding, acute phase protein release may occur as the tails became necrotic over the 3 wk before the tails were removed. However, acute phase protein concentrations were not greater in the docked calves after banding or after the removal of the necrotic tail. In contrast, this was not true in mature heifer cattle (Eicher et al., 2000). Haptoglobin increased slightly near the end of 1 wk after banding and then concentrations increased dramatically after cutting off the necrotic tail. In the present study, tails were not removed until 3 wk postbanding and most had fallen off by 3 wk postbanding with no further intervention. The difference in acute phase protein response between neonatal and mature heifers may have been caused by sample timing (our sampling time points were based on mature cattle acute phase protein responses to the tissue damage caused by banding and cutting off of the tail), less tissue that is becoming necrotic (calf tails have a much smaller circumference), or removal of the tail before all of it was necrotic in the mature heifers (cows tails were removed at 1 wk postbanding compared to 3 wk postbanding in the young calf).
Fly Counts and Fly Avoidance Behaviors
Both fly avoidance behaviors and fly counts required direct, live observations. The size of the fly, the frequency of fly landings, and the speed of the fly avoidance behaviors studied precluded the use of video recording. Observations were conducted at three times during the day to allow for known times of day effects (Phipps et al., 1995). Behavior was not sampled more intensively due to personal constraints and the study design.
Fly counts were numerous at both locations in this study, as we expected. This was particularly true by the afternoon counts. The significantly greater fly numbers on the calves with docked tails support the need for the tail at least through the period the calf is in the hutch. Flies can be controlled somewhat by spraying the hutches and frequent cleaning, but during the height of fly season flies are difficult to control in the hutch environment. Most older heifers are either pastured or raised in feed lot situations, but the effect of no tail on fly avoidance responses has not been assessed for this age of dairy heifer in the United States. However, flies become an economic liability because of disruption and alterations of eating patterns and increased energy expenditure in avoidance behaviors. Several studies have demonstrated that biting flies are linked to disrupted grazing and slower growth (Campbell and Berry, 1989), reduced milk production and weight gain and increased stress (Jonsson and Mayer, 1999). Jonsson and Mayer (1999) examined available literature to predict a lower threshold number of flies (n = 30) where adverse effects on milk yield or weight gain could be detected. It could be postulated from our data that without tails, calves would fall into the category above the threshold sooner and remain there longer resulting in decreased gain and greater fly annoyance.
It was surprising to find that tail swings were greater for control calves at both afternoon observations. This raises the possibility of learned helplessness (Ukai, M., 2000; Ronan et al., 2000). Learned helplessness is the lack of behavioral responses seen in animals after being exposed to inescapable aversive stimulus. The calves having not experienced a benefit of tail swings, may have quit trying to use the tail. In contrast, the mature heifers that had used their tails for 2 yr continued to try to use the tail to dislodge flies (Phipps et al., 1995; Eicher et al., 2001).
An interesting phenomenon was the use of licking, subjectively seen as a final effort to alleviate the fly annoyance. This behavior was increased in the docked calves, so was probably a behavior that replaced the use of the tail. Foot stomps and skin twitching were not different between treatments. The foot stomp counts were predictably affected by the increased lying time of the docked calves. Skin twitching is similar between treatments probably because it is useful to dislodge flies from areas that would not be moved by tail swings.
| CONCLUSIONS |
|---|
|
|
|---|
| ACKNOWLEDGEMENTS |
|---|
|
|
|---|
Received for publication December 11, 2001. Accepted for publication May 8, 2002.
| REFERENCES |
|---|
|
|
|---|
This article has been cited by other articles:
![]() |
W. K. Fulwider, T. Grandin, B. E. Rollin, T. E. Engle, N. L. Dalsted, and W. D. Lamm Survey of Dairy Management Practices on One Hundred Thirteen North Central and Northeastern United States Dairies J Dairy Sci, April 1, 2008; 91(4): 1686 - 1692. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. D. Eicher, H. W. Cheng, A. D. Sorrells, and M. M. Schutz Short communication: behavioral and physiological indicators of sensitivity or chronic pain following tail docking. J Dairy Sci, August 1, 2006; 89(8): 3047 - 3051. [Abstract] [Full Text] [PDF] |
||||
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |