M.A.G. von Keyserlingk

BOARD-INVITED REVIEW: Using behavior to predict and identify ill health in animals1

We review recent research in one of the oldest and most important applications of ethology: evaluating animal health. Traditionally, such evaluations have been based on subjective assessments of debilitative signs; animals are judged ill when they appear depressed or off feed. Such assessments are prone to error but can be dramatically improved with training using well-defined clinical criteria. The availability of new technology to automatically record behaviors allows for increased use of objective measures; automated measures of feeding behavior and intake are increasingly available in commercial agriculture, and recent work has shown these to be valuable indicators of illness. Research has also identified behaviors indicative of risk of disease or injury. For example, the time spent standing on wet, concrete surfaces can be used to predict susceptibility to hoof injuries in dairy cattle, and time spent nuzzling the udder of the sow can predict the risk of crushing in piglets. One conceptual advance has been to view decreased exploration, feeding, social, sexual, and other behaviors as a coordinated response that helps afflicted individuals recover from illness. We argue that the sickness behaviors most likely to decline are those that provide longer-term fitness benefits (such as play), as animals divert resources to those functions of critical short-term value such as maintaining body temperature. We urge future research assessing the strength of motivation to express sickness behaviors, allowing for quantitative estimates of how sick an animal feels. Finally, we call for new theoretical and empirical work on behaviors that may act to signal health status, including behaviors that have evolved as honest (i.e., reliable) signals of condition for offspring-parent, inter- and intra-sexual, and predator-prey communication.

Invited review: The welfare of dairy cattle--key concepts and the role of science.

Concerns about the welfare of animals typically include 3 questions: is the animal functioning well (e.g., good health, productivity, etc.), is the animal feeling well (e.g., absence of pain, etc.), and is the animal able to live according to its nature (e.g., perform natural behaviors that are thought to be important to it, such as grazing)? We review examples, primarily from our own research, showing how all 3 questions can be addressed using science. For example, we review work showing 1) how common diseases such as lameness can be better identified and prevented through improvements in the ways cows are housed and managed, 2) how pain caused by dehorning of dairy calves can be reduced, and 3) how environmental conditions affect cow preferences for indoor housing versus pasture. Disagreements about animal welfare can occur when different measures are used. For example, management systems that favor production may restrict natural behavior or can even lead to higher rates of disease. The best approaches are those that address all 3 types of concerns, for example, feeding systems for calves that allow expression of key behaviors (i.e., sucking on a teat), that avoid negative affect (i.e., hunger), and that allow for improved functioning (i.e., higher rates of body weight gain, and ultimately higher milk production).

Invited review: Effects of milk ration on solid feed intake, weaning, and performance in dairy heifers

A feeding regimen that allows a smooth transition from milk to solid feed is vital for successful heifer-rearing programs. In the past, research efforts have focused on the development of feeding methods that allow early weaning, perhaps because the risk of disease is highest during the milk feeding stage. To encourage early intake of calf starter, conventional feeding programs have limited the supply of milk (often to 10% of BW at birth). However, dairy calves provided free access to milk will typically consume more than twice this amount. We critically review the available literature examining the relationship between milk feeding method, solid feed consumption, and rumen development in young dairy calves and identify areas where new work is required. We conclude that milk-fed dairy calves can safely ingest milk at approximately 20% of body weight (BW)/d, and greater milk consumption supports greater BW gain, improved feed efficiency, reduced incidence of disease, and greater opportunity to express natural behaviors, which in combination suggest improved welfare. Method of weaning greatly influences feed consumption, rumen development, and growth check in calves provided higher amounts of milk. Gradual weaning encourages starter intake during the preweaning period, and both weaning age and duration of weaning influence this consumption. Increased solid feed consumption during the weaning process contributes to rumen development, permitting higher starter intake and BW gain after weaning. Growth factors in milk may also enhance the growth and maturation of the gastrointestinal tract, but more research is required to understand the role of these factors. Greater nutrient supply through increased amount of milk appears to improve immune function and long-term performance of heifer calves; for example, reducing the age at first breeding and increasing first-lactation milk yield, but more research is needed to confirm these effects.

Lying behavior as an indicator of lameness in dairy cows

Lameness is widely recognized as one of the most serious welfare and production concerns in the dairy industry. Our objectives were to evaluate the associations between lying behavior and lameness, and to determine whether lying behavior can be used as a diagnostic tool for lameness. Electronic data loggers recorded lying behavior of 1,319 cows from 28 farms at 1-min intervals for 5 d. These cows were gait scored according to a 5-point Numerical Rating System (NRS), and categorized as NRS <or=2, NRS=3, or NRS=4; no cow was scored as NRS=5. Lameness was dichotomized twice: LAME (NRS >or=3) and SEVLAME (NRS=4). Data were divided into 2 groups: 11 farms using deep-bedded stalls (DB) and 17 farms using mattress stalls (MAT). Differences in the daily lying time (h/d), frequency of lying bouts (n/d), duration of lying bouts (min/bout), and the standard deviation of bout duration (min/bout) between LAME or SEVLAME cows and those that were not were tested using mixed models. Receiver operating characteristic curves were constructed to identify behavioral thresholds to distinguish SEVLAME cows from the rest. Odds ratios for SEVLAME were estimated using logistic regression. Overall, 28.5% of cows were LAME including 7.3% that were SEVLAME. The prevalence of SEVLAME was higher on MAT farms than on DB farms (9.3+/-1.3 vs. 4.4+/-1.2%, respectively). SEVLAME cows on DB farms spent 12.8 [confidence interval (CI): 12.0 to 13.7] h/d lying down compared with 11.2 (CI: 10.7 to 11.8) h/d for cows that were not SEVLAME. These cows had longer duration of lying bouts [95.3 (CI: 84.6 to 107.3) vs. 80.3 (CI: 74.9 to 86.1) min/bout] and greater SD of bout duration [44.4 (CI: 41.1 to 48.0) vs. 50.7 (CI: 44.1 to 58.3) min/bout]. There were no behavioral differences among lameness categories on MAT farms. Within DB farms, cows with lying times >14.5 h/d had 16.2 (5.8 to 45.2) times higher odds of being SEVLAME. Cows with average lying bouts >90 min/bout were at 3.0 (1.2 to 7.4) times higher odds of being SEVLAME, and cows with average SD of bout duration >55 min/bout were at 4.1 (1.7 to 9.9) times higher odds of being SEVLAME. These results show that high lying times, long lying bouts, and variability in the duration of lying bouts were associated with lameness, and that stall surface influenced the behavioral responses of lame cows.

Lying behavior: Assessing within- and between-herd variation in free-stall-housed dairy cows

One of the most important design criteria for dairy cow housing is access to a comfortable lying area. Behaviors such as the time cows spend lying down and how often they lie down can be used to evaluate the quality of stalls; however, assessing lying behavior on farms can be challenging. Indices such as the cow comfort index (CCI) and stall use index (SUI) have been widely used in on-farm assessments. The aims were to establish reliable sampling and recording methods for measuring lying behavior, to evaluate the adequacy of the CCI and SUI as estimates of lying behavior, and to describe variation in the lying behaviors of free-stall-housed dairy cows. The time spent lying down and the number of lying bouts for 2,033 cows on 43 farms were recorded for 5 d using electronic data loggers sampling at 1-min intervals. The CCI and SUI were calculated based on a single observation taken 2 h before the afternoon milking on each farm. Subsets of data were created, including 4, 3, 2, or 1 d per cow and 40, 30, 20, 10, 5, or 1 cow(s) per farm. The estimates derived from each sample size were compared with the overall means (based on 5 d and 44 cows per farm) for lying time and number of lying bouts, and the CCI and SUI were compared with the farm means of lying time, number of lying bouts, and bout duration using linear regression. Recording 30 or more cows for 3 d or more represented the overall means with high accuracy (R(2) > 0.9), but using fewer cows or fewer days per cow resulted in poorer estimates of the farm mean. The CCI and SUI showed no association with the daily lying time (h/d; R(2) < 0.01), and CCI was only weakly associated with the number of lying bouts per day (R(2) = 0.16) and bout duration (min/bout; R(2) = 0.09). Cows lay down 11.0 +/- 2.1 h/d in 9 +/- 3 bouts/d, with a bout duration of 88 +/- 30 min/bout. These values ranged from 9.5 to 12.9 h/d, 7 to 10 bouts/d, and 65 to 112 min/bout across farm means, and 4.2 to 19.5 h/d, 1 to 28 bouts/d, and 22 to 342 min/bout across individuals, showing that variation in lying behavior among individual cows within farm was greater than differences among farms.

Benchmarking cow comfort on North American freestall dairies: lameness, leg injuries, lying time, facility design, and management for high-producing Holstein dairy cows.

In this paper, we describe a novel approach to corporate involvement in on-farm assessment, driven by the desire to provide a service for dairy producers and to create a vehicle for engagement on issues of dairy cow welfare. This program provides producers with feedback on animal-based (including gait score, leg injuries, and lying time) and facility-based (including freestall design, bedding practices, feed bunk design and management, and stocking density) measures that can be used to better address their management goals. The aim of this paper is to describe variation in the prevalence of lameness and leg injuries, lying behavior, facility design, and management practices for high-producing cows on freestall dairy farms in 3 regions of North America: British Columbia (BC; n=42); California (CA; n=39); and the northeastern United States (NE-US; n=40). Prevalence of clinical lameness averaged (mean ± SD) 27.9±14.1% in BC, 30.8±15.5% in CA, and 54.8±16.7% in NE-US; prevalence of severe lameness averaged 7.1±5.4% in BC, 3.6±4.2% in CA, and 8.2±5.6% in NE-US. Overall prevalence of hock injuries was 42.3±26.2% in BC, 56.2±21.6% in CA, and 81.2±22.5% in NE-US; prevalence of severe injuries was 3.7±5.2% in BC, 1.8±3.1% in CA, 5.4±5.9% in NE-US. Prevalence of swollen knees was minimal in CA (0.3±0.6%) but high (23.1±16.3%) in NE-US (not scored in BC). Lying times were similar across regions (11.0±0.7h/d in BC, 10.4±0.8h/d in CA, 10.6±0.9h/d in NE-US), but individual lying times among cows assessed varied (4.2 to 19.5h/d, 3.7 to 17.5h/d, and 2.8 to 20.5h/d in BC, CA, and NE-US, respectively). These results showed considerable variation in lameness and leg injury prevalence as well as facility design and management among freestall farms in North America. Each of the 3 regions had farms with a very low prevalence of lameness and injuries, suggesting great opportunities for improvement on other farms within the region.

Short communication: Haptoglobin as an early indicator of metritis

The purpose of this study was to determine whether haptoglobin (Hp) could be used as a predictive measure for metritis. Cattle were grouped into 3 health categories based on the condition of vaginal discharge and body temperature after calving: severe metritis (n = 12), mild metritis (n = 32), and healthy (n = 23). Blood was collected and analyzed for Hp concentration on d -20 +/- 5, -6 +/- 2, -2 +/- 1, and d 0 relative to calving, and then every 3 d after calving until d +21. Cows with mild and severe metritis had greater Hp concentrations than healthy cows between d 0 and d +12. Mean (+/-SE) Hp concentrations peaked on d +3 in the cows with mild metritis (1.06 +/- 0.15 g/L) and on d +6 in cows with severe metritis (1.62 +/- 0.47 g/L). Mean concentrations for the healthy group were 0.58 +/- 0.12 g/L and 0.31 +/- 0.08 g/L on d +3 and d +6, respectively. Clinical signs of pathological discharge for the mildly and severely metritic cows did not occur until, on average, 8.6 +/- 3.9 d and 5.3 +/- 1.9 d after calving, respectively. Cows with Hp concentrations >or=1 g/L on d +3 were 6.7 times more likely to develop severe or mild metritis; this predictive threshold has a sensitivity of 50% and specificity of 87%. These results indicate that an acute phase inflammatory response precedes clinical metritis and that Hp screening may assist in the early detection of metritis, providing increased opportunities for early treatment and prevention.

Using gait score, walking speed, and lying behavior to detect hoof lesions in dairy cows

The objective was to determine whether changes in the different components of gait, walking speed, and lying behavior were associated with hoof pathologies in lactating Holstein cows. In experiment 1, 53 cows had their gait scored, their walking speed estimated, and their lying behavior monitored before clinical assessment of the hooves. Multiparous cows with ulcers scored higher than cows without ulcers for overall gait score [numerical rating score (NRS); 3.3 +/- 0.2 vs. 2.8 +/- 0.2], back arch, joint flexion, asymmetric steps, and reluctance to bear weight. Although cows with ulcers did not walk more slowly than cows without ulcers (1.4 m/s), they spent more time lying down (827.8 +/- 29.1 vs. 738.2 +/- 15.5 min/d) because of longer lying bouts (93.3 +/- 5.9 vs. 79.7 +/- 3.4 min). In experiment 2, 47 cows were monitored for hoof health and changes in gait score from 4 wk before to 24 wk after calving. Differences were found after calving between cows that developed an ulcer and cows that did not for NRS (3.1 +/- 0.1 vs. 2.35 +/- 0.1), back arch, joint flexion, asymmetric steps, and reluctance to bear weight. Numerical rating score, back arch, and asymmetric steps were able to discriminate cows with ulcers at least 4 wk before the diagnosis. Cows that developed a sole ulcer had a faster decline in lying time during the periparturient period and a faster increase beginning in wk 2 after calving. The NRS was a more consistent predictor of sole ulcers than lying behavior or speed. The NRS was able to discriminate cows with ulcers across studies at a high intraobserver accuracy and reasonable specificity and was able to predict the presence of ulcers at least 4 wk before diagnosis. Abduction/adduction of the rear legs, head bob, and tracking-up did not consistently discriminate cows with ulcers, and we suggest that these measures are less useful for on farm gait assessment. Compared with the other gait attributes, back arch, joint flexion, asymmetric steps, and reluctance to bear weight best predicted the presence of sole ulcers.

Hay intake improves performance and rumen development of calves fed higher quantities of milk.

Research to date has suggested that access to forage before weaning can limit rumen development in calves, but no research has yet addressed the role of forage for calves fed higher quantities of milk. This study compared performance and rumen development of calves provided high volumes (equivalent to approximately 20% of calf birth weight) of milk with and without access to hay. At d 3 of age, individually housed calves were randomly assigned to treatment (either ad libitum access to chopped grass hay or no forage; n=15 calves per treatment, 10 heifers, and 5 bulls). All calves were provided ad libitum access to water and starter throughout the study. All calves were offered 8L of milk/d from a nipple bottle from d 3 to 35, 4 L/d from d 36 to 53, and 2L/d until weaning at d 56. Solid feed intake and growth parameters were monitored from d 3 to 70. At d 70, males from both treatments were slaughtered to measure rumen development parameters. Overall dry matter (DM) intake from solid feed did not differ between treatments before wk 5. However, during wk 6 to 10, calves fed forage consumed more total DM (starter plus hay) than did calves fed no forage. Hip and wither height, heart girth, and body barrel at d 3, 56, and 70 did not differ between treatments. Reticulorumen weight was heavier in calves fed hay versus those fed only starter (12.77±1.29 vs. 7.99±0.69 kg with digesta; 1.89±0.05 vs.1.60±0.09 kg without digesta). Body weight without digesta was similar in calves fed forage or no forage. Mean rumen pH was higher in calves fed hay compared with those fed no forage (5.49±0.08 vs. 5.06±0.04). In conclusion, provision of chopped hay to calves fed high volumes of milk can promote solid feed DM intake and rumen development without affecting BW gain.

Acute Behavioral Effects of Regrouping Dairy Cows

Regrouping is a common management practice on commercial dairy farms. The objectives of this study were to examine the effects of regrouping on feeding behavior, social behavior, and milk production. Eleven mid-lactation Holstein cows were individually introduced into previously established social groups. Behavior and milk production were monitored from 3 d before until 3 d after regrouping. Cows were fed a total mixed ration ad libitum twice daily. Time-lapse video was used to quantify feeding and social behavior. Cows spent approximately 15 min less time eating in the first hour following regrouping compared with the 3 d before regrouping. Cows were displaced from the feeding area on average 10 times/d before regrouping, but this value increased to more than 25 times ( +/- 2.6) on the day of mixing and gradually declined on the days following. The number of lying bouts declined from 12.2 +/- 0.9 to 10.5 +/- 0.9 on the day of regrouping; lying time showed a similar tendency. Cows initiated, on average, 7.5 +/- 1.3 allogrooming events/d over the 3 d before regrouping but this declined to 1.3 +/- 1.3 events on the day of mixing and remained lower than baseline for the following 3 d. Milk production declined from 43.4 +/- 1.5 kg/d to 39.7 +/- 1.5 kg/d on the day of regrouping, but did not differ from premixing levels on subsequent days. This study shows that regrouping can disrupt behavior and production in the hours and days following regrouping and suggests the need for future research to identify management changes that reduce these effects.