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The Effect of Heat Stress and Lameness on Time Budgets of Lactating Dairy Cows

N. B. Cook^*,1, R. L. Mentink^*, T. B. Bennett^* and K. Burgi

^* School of Veterinary Medicine, University of Wisconsin–Madison, Madison 53706-1102
Comfort Hoof-Care Inc., Baraboo, WI 53913

¹ Corresponding author: nbcook{at}wisc.edu

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

 
Time budgets for 14 cows housed in a 3-row free-stall pen were obtained for 4 filming sessions timed to capture different climatic conditions, with a range in mean pen temperature-humidity index from 56.2 to 73.8. Mean lying time decreased from 10.9 to 7.9 h/d from the coolest to the hottest session filmed. This change in behavior occurred predominantly between 0600 h and 1800 h. Time spent standing in the alley increased from 2.6 to 4.5 h/d from the coolest to the hottest session filmed, with changes occurring between 1200 h and 1800 h. There was a negative effect of increasing locomotion score over the summer with higher locomotion scores associated with less time spent standing up in the alley. Time spent drinking increased from 0.3 to 0.5 h/d across the range in temperature-humidity index. Filming session alone did not affect time spent standing in the stall, but the effect of locomotion score was significant, with score 2 and score 3 cows standing in the stall longer than score 1 cows (4.0 and 4.4 compared with 2.9 h/d respectively). Behavioral changes observed and traditionally associated with heat stress were confounded by changes in locomotion score. Increases in claw horn lesion development reported in the late summer may be associated with an increase in total standing time per day. The changes in behavior described were because of mild to moderate heat stress. The finding that activity shifts occur around a temperature-humidity index of 68 supports the use of more aggressive heat-abatement strategies implemented at an activation temperature of around 21°C.

Key Words: heat stress • lameness • time budget

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

 
The dramatic impact of heat stress on dairy cow milk production has been the primary focus of climate research in recent years (West, 2003). Under conditions of heat stress, dairy cattle develop respiratory alkalosis as a consequence of thermal panting and attempts to use evaporative heat loss (Benjamin, 1981). Dry matter intake is reduced; thus, blood flow to the mammary gland and the portal plasma flow are lowered, which in turn reduce milk yield (McGuire et al., 1989; Lough et al., 1990). In addition, heat stress affects reproductive performance through reduced viability of the spermatozoa and ova, via a negative effect on the intensity and duration of estrus, and through delayed or inhibited ovulation (Ravagnolo and Misztal, 2002).

The temperature-humidity index (THI) has been commonly used to estimate the effect of heat stress on production and reproduction (Ravagnolo et al., 2000; West et al., 2003). There is general agreement that significant effects are observed at a mean daily THI of around 72 (Johnson, 1987; Igono et al., 1992; Armstrong, 1994). Such combinations of temperature and humidity are seen during the summer across North America and in many other parts of the world. Most heat stress research has focused on conditions of sustained moderate to severe heat stress in locations such as the southeastern and southwestern United States, whereas information on the effects of episodic mild to moderate heat stress typical of the upper Midwest has not been readily available (Ominski et al., 2002). Episodic periods of heat stress may present the cow with greater challenges in the short-term because physiological homeorhetic adaptations take weeks rather than days to occur (Beede and Collier, 1986; Collier et al., 2006).

There has been little work on behavioral adaptations to sustained or episodic heat stress. Shultz (1984) studied cow responses to weather types in corrals in the southwestern United States. An almost linear relationship between ambient temperature and the proportion of cows standing was demonstrated. More recently, Overton et al. (2002) documented temporal cyclicity in lying behavior in a freestall pen and noted an inverse relationship between the proportion of cows lying down and ambient temperature. This association, however, was confounded by time after milking. In a study conducted in 4 Swiss dairy herds, lying behavior of sentinel animals was tracked under different climatic conditions (Zahner et al., 2004). The authors noted that the duration of lying behavior decreased during the day with increasing THI, but lying duration during the night was unaffected. Although it is generally accepted that cows stand more in alleys and stalls during periods of heat stress, no previous study has followed a group of cows through different climatic conditions and reported changes in daily time budgets for lying, standing, drinking, milking, and feeding activity.

Claw horn lesions, such as sole ulcer, are believed to develop from increased pedal bone mobility induced by changes in the corium at calving (Lischer et al., 2002) and potentially from nutritional insults such as subacute ruminal acidosis (Cook et al., 2004a; Stone, 2004). Factors that contribute to an increase in time spent standing may exacerbate these changes by further compromising the structure of the claw. Reductions in lying activity per day have been associated with lameness in dairy cows (Leonard et al., 1996; Cook et al., 2004a). Poor stall design and excessively long milking times also have a negative effect on hoof health (Cook et al., 2004b; Espejo and Endres, 2007). Behavioral adaptations to heat stress may be another potential risk factor for reduced lying times and associated lameness. An increase in the rate of claw horn lesion associated lameness in the late summer has been reported and associated with periods of heat stress in Wisconsin dairy herds (Cook, 2004). This may be because of increased susceptibility to subacute ruminal acidosis or because of an increase in standing activity or a combination of the two.

This study documented the degree of change in daily activity time budgets in a group of lactating dairy cows between filming sessions that targeted different THI on a commercial free-stall dairy farm. In addition, changes in activity during 4 specified periods of the day between filming sessions were recorded.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

 
Cow Selection
Twenty multiparous Holstein cows were randomly selected from a subset of cows less than 150 DIM, within a single pen of a commercial freestall-housed dairy herd. Each cow was given a unique identification number using black hair dye, visible from both flanks and the head. Three weeks before the start of filming, the feet of each cow were trimmed and balanced. Cows identified as clinically lame by the herdsman during the filming period were treated within 7 d.

The pen was monitored for a total of 4 filming sessions under different weather conditions. At a single milking during each filming session, the cows were scored for locomotion on a flat and level surface when returning from milking using a 4-point scoring system where 1 = nonlame, 2 = slightly lame, 3 = moderately lame, and 4 = severely lame (Nordlund et al., 2004). Parity, locomotion score, current DIM, and most recent DHIA-recorded daily milk weight at each filming session were used as covariates in the statistical modeling.

Animal Housing
Study animals were housed with a group of multiparous cows in an east–west oriented pen with curtain sidewalls and 3 rows of freestalls bedded with sawdust on top of a rubber crumb-filled geotextile mattress. Group size was maintained between 100 and 105 cows with access to 92 stalls that measured 1.19 m wide and 2.49 m long against the side wall (2.21 m long for the head-to-head stalls), 1.68 m from curb to brisket locator, with a neck rail 1.14 m above the stall surface and 1.68 m from the rear curb. Pen flooring was grooved concrete, with a 1.8-m wide rubber surface in the feed alley, adjacent to the feed bunk that consisted of 65- x 0.61-m wide headlocks. Water troughs were located at the ends of the pen and at the single cross alley in the middle of the pen.

Heat abatement was provided by 3 recirculation fans (1.22 m diameter) spaced at 12-m intervals and located over the feed bunk. No fans were located over the stalls. The fans were activated above a temperature of 21.1°C. In addition, water soakers were located along the feed bunk at 1.98-m intervals. The soaker cycle was activated above a temperature of 25.6°C and cycled through 1.5-min periods on and 11-min periods off.

Cows were milked 3 times daily. Fans and water soakers were present in the holding area. A TMR was fed once a day at approximately 0900 h and pushed up 6 times per day. Cows were added to and removed from the pen at weekly intervals. Filming was timed to avoid periods within 48 h of new pen additions.

Choice of Filming Times
Weather forecasts were used to predict local weather conditions for 4 filming sessions between early June and the beginning of September 2004. The aim was to film 2 sessions with a predicted maximum outside ambient temperature less than 23.9°C and 2 sessions with a predicted minimum outside ambient temperature greater than 18.3°C. The pen was filmed over a 3-d period when weather predictions were favorable. The dates of filming for each of 4 sessions (S1 to S4) were June 22 to 24, July 12 to 14, August 10 to 12, and August 25 to 27, 2004.

Climate Monitoring
Two calibrated temperature and humidity data loggers (Dickson TR320 Pro Series; Dickson, Addison, IL) were located at the east and west end of the pen and taped to a pole protected from direct sunlight and slightly above cow level. Temperature and relative humidity data were downloaded for each minute of each filming session and the THI was calculated for each location in the pen. A value for THI was obtained by averaging the data obtained from each end of the pen at each minute for the entire filming session and for distinct time periods within each session. The equation used to calculate THI was: THI = T – (0.55 – 0.55 x RH) x (T – 58), where T is the pen ambient temperature in °F, and RH is relative humidity expressed as a decimal (NOAA, 1976).

Filming Methodology
Methodology for video capture and tracking of individual marked cows has been described (Cook et al., 2004b). Digital camcorders (Sony DCRTRV900 miniDV video cameras; Sony Corporation, New York, NY) were used to record 1 s of activity every 30 s on the long-play setting. Activity was captured between 1407 h on d 1 and 0700 h on d 3, resulting in 40.9 continuous hours comparable across 4 sessions.

Time spent feeding (head over the feed curb), drinking (head over the water trough), standing in an alley, standing in a stall (standing with all 4 feet in the stall or perching with front 2 feet in the stall), lying down in a stall, and time spent out of the pen while milking was recorded for each cow at each session. Time budgets were created for 4 periods during the middle 24 h of the filming of each session, where period A (PA) was from 00:00 (h:min elapsed) to 05:59, period B (PB) was from 06:00 to 11:59, period C (PC) was from 12:00 to 17:59, and period D (PD) was from 18:00 to 23:59. Period X (PX) was the combined total from 00:00 to 23:59 h (where PX = PA + PB + PC + PD), and period Y (PY) was the time budget for the whole 40.9-h period, converted to a 24-h day by proportion.

Statistical Analysis
Mixed effect models were created to investigate the differences in cow behavior (time spent lying down in the stall, standing in the stall, standing in the alley, standing drinking, standing feeding, and standing milking) between different filming sessions (S1 to S4) at different mean THI. Plots of residuals were used to ensure an approximate normal distribution and determine whether transformations of the data were required. Where log transformations were used, back transformed values of the least squares mean along with 95% confidence limits are given in the data tables.

For the entire filming session, analysis of covariance was performed for each behavior using PROC MIXED in SAS version 9.1 (SAS Institute, Inc., Cary, NC), with filming session and locomotion score for each individual cow at each session forced into all models. Other covariates were parity, most recent DHIA-recorded milk yield, and DIM at each filming session. Session, parity, locomotion score, and cow identification were included in the class statement along with a random effect for cow. Nonsignificant fixed effects (P > 0.05) were removed by the process of stepwise backwards elimination. Biologically plausible 2-way interactions were examined from the resultant model and retained if P < 0.05. Differences recorded between least squares mean activities for each session were tested using Fisher’s protected least significant difference with P < 0.05.

For the analysis of behavior by period (PA to PD) and between each session (S1 to S4), a repeated measures mixed model was used with cow as the repeated subject. The Akaike information criterion was used to test 2 different covariance structures. Compound symmetry provided the best model fit, compared with the first-order autoregressive covariance structure, suggesting that the correlation within a cow was relatively constant across periods, rather than becoming weaker over time. The compound symmetry covariance structure was identical to fitting cow as a random effect, as the random effect assumes equal correlation across periods (Littell et al., 1998). Fixed effects of session, period, and the interaction between session and period were forced into all models. Other covariates were parity, most recent DHIA recorded milk yield, locomotion score at each session, and DIM. Nonsignificant fixed effects (P > 0.05) were removed by the process of stepwise backwards elimination. Biologically plausible 2-way (other than session by period) and 3-way interactions were examined from the resultant model and retained if P < 0.05. Differences between least squares means activities for each period between sessions were tested using Fisher’s protected least significant difference. Tukey’s method was used to allow for multiple comparisons, with significance determined at P < 0.05.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

 
Cow Background Information
Time budgets for the 4 filming sessions were obtained for 14 out of 20 cows with a mean parity of 2.6 (range 2 to 5). Three cows were removed from the pen during at least one of the filming sessions because of illness, and 3 cows could not be tracked because of indistinct coloring. Between cows and sessions, DIM ranged from 53 to 195 and milk yield ranged from 22.8 to 52.5 kg/d (Table 1). Mean locomotion score for the 14 cows filmed varied from 1.6 to 1.8 between sessions, with the proportion of cows scoring 3 or more (clinically lame) increasing to 21.4% for S3 and S4. The proportion of cows with a locomotion score of 2 or more was greatest for S1.

There was no effect of session on time spent standing in the stall but the effect of locomotion score was significant (P = 0.02). Least squares mean (±SE) time standing in the stall at locomotion scores 1, 2, and 3 were 2.91 ± 0.35, 4.00 ± 0.34, and 4.41 ± 0.57 h/d, respectively, with the difference between scores 1 and 2 (P = 0.015) and 1 and 3 (P = 0.023) being significant.

Changes in Behavior Within Periods Between Filming Sessions
Session by period interactions were detected for time lying, time standing in the stall, time standing in the alley, time drinking, and time milking, but not for time feeding. The period effect on time milking was explained by the absence of milking in PB and was not examined further. Behavioral changes within periods and between sessions are shown in Table 4.

There was a session by period interaction for time spent standing up in a stall, but the only significant contrast was within PA between S3 and S4. Locomotion score was also significant alone (P = 0.021) and as part of a 3-way interaction with both session and period (P = 0.046). Effect of locomotion score within period followed a similar pattern to that described previously for the entire PX, with greater locomotion scores tending to increase time spent standing in the stall.

The session by period interaction was significant for time spent standing in the alley, with significant contrasts occurring within PC between S1 and S3 and between S3 and S4, with an increase of over 1 h/d standing between extremes of THI (57.2 to 78.3). There was also an effect of locomotion score alone (P = 0.039), but no interaction with session and period, with the trend of spending less time standing in the alley at higher locomotion scores mirroring that found for the entire PX.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

 
Weather changes during the summer of 2004 enabled a comparison of behavioral time budgets in 14 high-yielding dairy cows housed in a single freestall pen between filming sessions with different THI. The mean THI was highest during PC and lowest for PA or PB for each filming session. The final range between filming sessions was typical of the variation observed over the summer in the upper Midwest, with relatively short episodes of mild to moderate heat stress.

The effect of filming session was complicated by the potential influences of change in DIM, milk yield, and locomotion score throughout the summer. The weather changes that occurred naturally in 2004 allowed for a "cool" session to be filmed in between 2 "hot" sessions. This created a switchback-like study design for the effect of session and THI on activity.

The covariates milk yield and DIM were not significant in our statistical models. Locomotion score of each individual cow at each session, however, was a significant covariate for time spent standing in the stall and time spent standing in the alley. The influence of locomotion score on stall use behavior has been previously described (Cook et al., 2004b). The finding that time spent standing in the stall increased and time standing in the alley decreased with increasing locomotion score complements the previous work. The importance of locomotion score in understanding the effects of heat stress in the current study lends support to the idea that behavioral studies on individual cows should include locomotion score as a covariate in statistical analyses (Cook et al., 2004b).

Changes in locomotion score during the summer influenced the change in behavior between sessions. Although the proportion of cows with a locomotion score of 3 increased toward the end of the summer, the proportion of abnormal scores (2 and 3) was highest during the first session filmed. This may have been related to the fact that all cows had their feet trimmed immediately before the study, which contributed to some of the differences observed between sessions and was accounted for in the modeling procedure.

Healthy dairy cattle maintain 12 to 13 h/d of lying time (Cook et al., 2004b; Jensen et al., 2005) and this amount of time is a target resting period for the high-producing dairy cow housed in a freestall barn. In the study herd, the maximum observed mean lying time was only 10.9 h/d during S3, the coolest session filmed. This resting time is typical of that found in similar mattress freestall herds under thermoneutral conditions (Cook et al., 2004b) and may be indicative of stall designs that have lunge obstructions, high brisket locators, and smaller resting areas than those currently recommended (Cook and Nordlund, 2005).

There was a reduction in lying time of 3 h/d over a range of mean THI from 56.2 to 73.8, resulting in resting times of less than 8 h/d for the warmest session filmed. Reduced lying time of this magnitude is a suggested risk factor for claw horn lesion development (Leonard et al., 1996) and may contribute to the increased rates of claw horn lesions observed in lactating dairy cows in Wisconsin in the late summer (Cook, 2004). Indeed, more cows with locomotion score 3 were observed at the end of the summer in this study herd.

Time spent standing when the cow would rather be lying down may stress the bond between the third phalanx and the claw horn capsule, a bond that is already weakened around calving (Tarlton et al., 2002) and by feeding disorders such as subacute ruminal acidosis (Thoefner et al., 2004). Heat stress behavior, poor stall design and comfort, overstocking, and prolonged milking times are the 4 major situations in modern dairy herds that cause this increase in daily standing time.

The behavioral component changes that result in changes in standing time across session (lowest to highest THI) are summarized in Figure 1. The most significant changes are increases in time spent standing in the alley and time spent standing in the stall, with a small but significant change in time spent drinking. The perception is that cows are standing in the stalls trying to cool off and spending time standing in the alleys beneath the water soakers and the fans. The data presented here suggest that this observation may be only partly true. Increased time spent standing in stalls was largely a result of changes in locomotion score rather than THI over the summer. Lame cows struggle to rise and lie down in mattress stalls and this leads to prolonged periods standing in the stall between periods of lying down (Cook et al., 2004b). There tend to be more lame cows at the end of the summer than at the start of the summer so more cows were seen standing in the stall. Increases in time spent in the alley are associated with increases in mean THI between sessions, but they were also influenced negatively by locomotion score, which tended to reduce time spent standing in the alley. Thus, it would appear that although nonlame cows attempt to cool off by standing beneath soakers and fans in the alley, lame cows may prefer to stand on the more cushioned surface of the stall and spend less time in the alley. This choice may compromise the ability of lame cows to cool when heat-stressed.

View larger version (32K): [in this window] [in a new window]   Figure 1. Time budgets (h/d) for 14 cows across 4 filming sessions (S1 to S4) in order of lowest (S3) to highest mean temperature-humidity index (S4) demonstrating the change in activity components that make up total daily standing time. Activity: TUM = time milking, TUW = time drinking, TUF = time feeding, TUIS = time standing up in the stall, TUIA = time standing up in the alley, and TDIS = time lying down in the stall.

Comparison of activity during separate periods within a day and between filming sessions identified the specific times of the day during which cows were most affected by heat stress. There were differences observed between 0600 h and 1800 h. Lying time was reduced between 0600 h and 1200 h and between 1200 h and 1800 h between the extremes of THI (54.0 to 70.5). In addition, from 1200 h to 1800 h lying times were reduced for THI 57.2 to 68.5. A change in time standing in the alley between these periods was explained by the interaction between session and period.

There was no evidence for a shift in time of feeding in the study herd. This may have been because of the use of water soakers and fans over the feedbunk that allowed heat-stressed cows to maintain normal patterns of feeding behavior. The heat abatement strategies used may have persuaded cows to spend increased time feeding in one of the warmer filming sessions (S2).

Effects on production, reproduction, and bovine physiology are typically associated with a THI of 72 or greater (Johnson, 1987; Igono et al., 1992; Armstrong, 1994). In this behavioral study, we found subtle, but significant, changes in behavior at a THI of 68. To minimize the extent and impact of these changes, a more aggressive approach to cooling cattle, even under climates of only mild to moderate heat stress, may be necessary. The study herd was typical of many herds in the upper Midwest that activate recirculation fans at around 21°C and use water soakers at a temperature of 23.9 to 26.7°C. This study would lend support to the use of both fans and soakers at barn temperatures of around 21°C to limit heat-associated changes in behavior. The study herd did not have fans located over the stalls in the pen. Placing additional fans over the stalls may help further reduce the effects of heat stress but stall-standing behavior in this study was largely related to changes in locomotion score.

	CONCLUSIONS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

 
Dairy cows had a reduction in lying time of 3 h/d across the range of THI typically experienced in the upper Midwest during the summer. In addition, behavioral changes observed and traditionally associated with heat stress are confounded by changes in locomotion score that typically occur over the late summer months. Increases in claw horn lesion development in the late summer may be associated with the increase in total standing time per day. The changes in behavior described were due to mild to moderate heat stress (THI of 68). The use of more aggressive heat abatement strategies implemented at activation temperatures of around 21°C is recommended. The study did not measure the effects of the prolonged periods of moderate to severe heat stress seen elsewhere in North America. However, the findings may be useful in predicting behavioral outcomes in these more extreme environments.

	ACKNOWLEDGEMENTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

 
The authors would like to acknowledge the assistance of Tim Evert, the herd owner, for his patience and time. We would also like to thank Nicholas Keuler of the College of Agriculture and Life Sciences Statistical Consulting Service for advice on analyzing the data. This study was funded by the UW Cow Comfort and Well-being Consortium, which consists of Zinpro Performance Minerals, Pfizer Animal Health, Vitaplus Corporation, AgSource Cooperative Services, Promat Ltd., Artex Fabricators Ltd., and L and L, Inc., and a UW School of Veterinary Medicine Food Animal Grant. R. L. Mentink was funded by a Merck Merial Summer Training Scholarship in 2004.

Received for publication October 5, 2006. Accepted for publication December 13, 2006.

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TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

 


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