Advertisement
Review| Volume 104, ISSUE 1, P20-46, January 2021

Invited review: Lying time and the welfare of dairy cows

Open AccessPublished:November 05, 2020DOI:https://doi.org/10.3168/jds.2019-18074

      ABSTRACT

      Adequate time lying down is often considered an important aspect of dairy cow welfare. We examine what is known about cows' motivation to lie down and the consequences for health and other indicators of biological function when this behavior is thwarted. We review the environmental and animal-based factors that affect lying time in the context of animal welfare. Our objective is to review the research into the time that dairy cows spend lying down and to critically examine the evidence for the link with animal welfare. Cows can be highly motivated to lie down. They show rebound lying behavior after periods of forced standing and will sacrifice other activities, such as feeding, to lie down for an adequate amount of time. They will work, by pushing levers or weighted gates, to lie down and show possible indicators of frustration when lying behavior is thwarted. Some evidence suggests that risk of lameness is increased in environments that provide unfavorable conditions for cows to lie down and where cows are forced to stand. Lameness itself can result in longer lying times, whereas mastitis reduces it. Cow-based factors such as reproductive status, age, and milk production influence lying time, but the welfare implications of these differences are unknown. Lower lying times are reported in pasture-based systems, dry lots, and bedded packs (9 h/d) compared with tiestalls and freestalls (10 to 12 h/d) in cross-farm research. Unfavorable conditions, including too few lying stalls for the number of cows, hard or wet lying surfaces, inadequate bedding, stalls that are too small or poorly designed, heat, and rain all reduce lying time. Time constraints, such as feeding or milking, can influence lying time. However, more information is needed about the implications of mediating factors such as the effect of the standing surface (concrete, pasture, or other surfaces) and cow behavior while standing (e.g., being restrained, walking, grazing) to understand the effect of low lying times on animal welfare. Many factors contribute to the difficulty of finding a valid threshold for daily lying time to use in the assessment of animal welfare. Although higher lying times often correspond with cow comfort, and lower lying times are seen in unfavorable conditions, exceptions occur, namely when cows lie down for longer because of disease or when they spend more time standing because of estrus or parturition, or to engage in other behaviors. In conclusion, lying behavior is important to dairy cattle, but caution and a full understanding of the context and the character of the animals in question is needed before drawing firm conclusions about animal welfare from measures of lying time.

      Key words

      INTRODUCTION

      Growing interest in the welfare of dairy cattle (
      • von Keyserlingk M.A.G.
      • Martin N.P.
      • Kebreab E.
      • Knowlton K.F.
      • Grant R.J.
      • Stephenson M.
      • Sniffen C.J.
      • Harner III, J.P.
      • Wright A.D.
      • Smith S.I.
      Invited review: Sustainability of the US dairy industry.
      ) has resulted in scientific research, animal welfare legislation, and nonregulatory animal welfare assurance schemes (
      • Veissier I.
      • Butterworth A.
      • Bock B.
      • Roe E.
      European approaches to ensure good animal welfare.
      ;
      • Hoenig D.E.
      • Coetzee J.F.
      Perspectives on the emerging role of US veterinarians in education, policy, politics, and research.
      ). Earlier legislation and guidelines focused on “input-based” standards, which prescribed the particular housing or management methods that must be used. More recent on-farm animal welfare assessment protocols include animal-based welfare measures (
      • Fraser D.
      Animal welfare: Translating science into practice.
      ), of which the European Welfare Quality program is the best known (
      • Blokhuis H.J.
      • Veissier I.
      • Miele M.
      • Jones B.
      The Welfare Quality project and beyond: Safeguarding farm animal well-being.
      ). However, the costs of carrying out on-farm welfare assessments on commercial farms limit the time available to take animal-based measures, especially behavioral ones (
      • Sørensen J.T.
      • Rousing T.
      • Møller S.H.
      • Bonde M.
      • Hegelund L.
      On-farm welfare assessment systems: What are the recording costs?.
      ). Consequently, there is considerable interest in automatic recording of behaviors relevant to animal welfare in a time-efficient manner (
      • European Food Safety Authority Panel on Animal Health and Welfare
      Scientific opinion on the use of animal-based measures to assess welfare of dairy cow.
      ;
      • Rushen J.
      • Chapinal N.
      • de Passillé A.M.
      Automated monitoring of behavioural-based animal welfare indicators.
      ).
      The time cows spend lying down may reflect their welfare (
      • European Food Safety Authority Panel on Animal Health and Welfare
      Scientific report on the effects of farming systems on dairy cow welfare and disease. EFSA-Q-2006-113. Parma, Italy.
      ), and some animal welfare standards make recommendations about how much time cows should lie down (e.g., Canadian
      • National Farm Animal Care Council
      Code of Practice for the Care and Handling of Dairy Cattle.
      ; New Zealand ). Measuring this behavior has become easier through use of various automated loggers (e.g.,
      • Borchers M.R.
      • Chang Y.M.
      • Tsai I.C.
      • Wadsworth B.A.
      • Bewley J.M.
      A validation of technologies monitoring dairy cow feeding, ruminating, and lying behaviors.
      ), and measurement of lying behavior has become more common in research and in large-scale on-farm assessments of dairy welfare (e.g.,
      • O'Driscoll K.
      • Boyle L.
      • Hanlon A.
      A brief note on the validation of a system for recording lying behaviour in dairy cows.
      ;
      • Ito K.
      • Weary D.M.
      • von Keyserlingk M.A.G.
      Lying behavior: Assessing within- and between-herd variation in free-stall-housed dairy cows.
      ;
      • Ledgerwood D.N.
      • Winckler C.
      • Tucker C.B.
      Evaluation of data loggers, sampling intervals, and editing techniques for measuring the lying behavior of dairy cattle.
      ).
      Our objective is to review the research into the time that dairy cows spend lying down and to critically examine the evidence for the link with animal welfare. We focus on adult cows and refer to other classes of cattle only when research on this group is lacking. Many aspects of the lying behavior of cattle may provide information about their welfare status—for example, the time spent in the process of lying down or getting up (e.g.,
      • Dippel S.
      • Dolezal M.
      • Brenninkmeyer C.
      • Brinkmann J.
      • March S.
      • Knierim U.
      • Winckler C.
      Risk factors for lameness in freestall-housed dairy cows across two breeds, farming systems, and countries.
      ;
      • Plesch G.
      • Broerkens N.
      • Laister S.
      • Winckler C.
      • Knierim U.
      Reliability and feasibility of selected measures concerning resting behaviour for the on-farm welfare assessment in dairy cows.
      ;
      • Zambelis A.
      • Gagnon-Barbin M.
      • St John J.
      • Vasseur E.
      Development of scoring systems for abnormal rising and lying down by dairy cattle, and their relationship with other welfare outcome measures.
      ) and lying in various lying postures (e.g.,
      • Haley D.B.
      • de Passillé A.M.
      • Rushen J.
      Assessing cow comfort: Effects of two floor types and two tie stall designs on the behaviour of lactating dairy cows.
      ). However, to date, the time cows spend lying down represents the bulk of investigation in this area and is our focus. After an overview of the characteristics of lying behavior, we examine the direct evidence related to animal welfare: cows' motivation to lie down and the consequences for health and other indicators of biological function when this behavior is thwarted. We then review the environmental and animal-based factors that affect lying time and end by placing these in the context of the animal welfare.

      THE BEHAVIOR OF LYING DOWN

      Before diving into the animal welfare implications of lying behavior, we provide an overview of what is known about the amount of time cows engage in this behavior, how these patterns are structured within and between days, and how they get up and down as well as postures assumed while lying.

      Time Spent Lying Down

      On average, lactating cows lie down for 8 to 13 h/d, with the most commonly reported averages between 10 and 12 h/d (Table 1). However, large differences exist among cows. For example, Figure 1 shows the distribution of daily lying time for 3,122 cows in tiestall and freestall herds in Canada and the United States (data combined from
      • Charlton G.L.
      • Haley D.B.
      • Rushen J.
      • de Passillé A.M.
      Stocking density, milking duration, and lying times of lactating cows on Canadian freestall dairy farms.
      ;
      • Solano L.
      • Barkema H.W.
      • Pajor E.A.
      • Mason S.
      • LeBlanc S.J.
      • Nash C.G.R.
      • Haley D.B.
      • Pellerin D.
      • Rushen J.
      • de Passillé A.M.
      • Vasseur E.
      • Orsel K.
      Associations between lying behavior and lameness in Canadian Holstein-Friesian cows housed in freestall barns.
      ;
      • Westin R.
      • Vaughan A.
      • de Passillé A.M.
      • DeVries T.J.
      • Pajor E.A.
      • Pellerin D.
      • Siegford J.M.
      • Vasseur E.
      • Rushen J.
      Lying times of lactating cows on dairy farms with automatic milking systems and the relation to lameness, leg lesions, and body condition score.
      ). The mean daily duration of time spent lying down is around 11 h/d but varies among cows from less than 6 h/d to more than 16 h/d (Figure 1).
      Table 1Mean daily duration of lying time (and range) reported for lactating dairy cows in different types of housing systems
      Reference
      Only includes studies that examined multiple farms.
      LocationFarmsCowsMean duration (h/d)Range (h/d)
      Freestall with parlor
      • Ito K.
      • Chapinal N.
      • Weary D.M.
      • von Keyserlingk M.A.G.
      Associations between herd-level factors and lying behavior of freestall-housed dairy cows.
      US7940/farm10.5
      • Ito K.
      • Weary D.M.
      • von Keyserlingk M.A.G.
      Lying behavior: Assessing within- and between-herd variation in free-stall-housed dairy cows.
      Canada432,03311.09.5–12.9
      • Thomsen P.T.
      • Munksgaard L.
      • Sørensen J.T.
      Locomotion scores and lying behaviour are indicators of hoof lesions in dairy cows.
      Denmark391,23310.7
      • Wechsler B.
      • Schaub J.
      • Friedli K.
      • Hauser R.
      Behaviour and leg injuries in dairy cows kept in cubicle systems with straw bedding or soft lying mats.
      Switzerland1810/farm11.3
      • Gomez A.
      • Cook N.B.
      Time budgets of lactating dairy cattle in commercial freestall herds.
      US16~13/farm11.9
      • Yunta C.
      • Guasch I.
      • Bach A.
      Short communication: Lying behavior of lactating dairy cows is influenced by lameness especially around feeding time.
      Spain1040/farm12.0
      • Thorup V.M.
      • Munksgaard L.
      • Robert P.E.
      • Erhard H.W.
      • Thomsen P.T.
      • Friggens N.C.
      Lameness detection via leg-mounted accelerometers on dairy cows on four commercial farms.
      Denmark4200/farm11.4
      • Solano L.
      • Barkema H.W.
      • Pajor E.A.
      • Mason S.
      • LeBlanc S.J.
      • Nash C.G.R.
      • Haley D.B.
      • Pellerin D.
      • Rushen J.
      • de Passillé A.M.
      • Vasseur E.
      • Orsel K.
      Associations between lying behavior and lameness in Canadian Holstein-Friesian cows housed in freestall barns.
      Canada14140/farm10.68.2–13.2
      Freestall with AMS
      AMS = automatic milking system
      • Westin R.
      • Vaughan A.
      • de Passillé A.M.
      • DeVries T.J.
      • Pajor E.A.
      • Pellerin D.
      • Siegford J.M.
      • Vasseur E.
      • Rushen J.
      Lying times of lactating cows on dairy farms with automatic milking systems and the relation to lameness, leg lesions, and body condition score.
      Canada3640/farm11.39.7–13.5
      • Deming J.A.
      • Bergeron R.
      • Leslie K.E.
      • DeVries T.J.
      Associations of housing, management, milking activity, and standing and lying behavior of dairy cows milked in automatic systems.
      Canada1330/farm10.8
      • Helmreich S.
      • Hauser R.
      • Jungbluth T.
      • Wechsler B.
      • Gygax L.
      Time-budget constraints for cows with high milking frequency on farms with automatic milking systems.
      Switzerland413810.69.4–11.5
      • King M.T.M.
      • Pajor E.A.
      • LeBlanc S.J.
      • DeVries T.J.
      Associations of herd-level housing, management, and lameness prevalence with productivity and cow behavior in herds with automated milking systems.
      Canada4130/farm11.510.1–11.7
      Tiestall
      • Charlton G.L.
      • Bouffard V.
      • Gibbons J.
      • Vasseur E.
      • Haley D.B.
      • Pellerin D.
      • Rushen J.
      • de Passillé A.M.
      Can automated measures of lying time help assess lameness and leg lesions on tie-stall dairy farms?.
      Canada10040/farm12.510.0–15.0
      Dry lots
      • Steensels M.
      • Bahr C.
      • Berckmans D.
      • Halachmi I.
      • Antler A.
      • Maltz E.
      Lying patterns of high producing healthy dairy cows after calving in commercial herds as affected by age, environmental conditions and production.
      Israel32108.9
      • Tresoldi G.
      • Schütz K.E.
      • Tucker C.B.
      Cow cooling on commercial drylot dairies: A description of 10 farms in California.
      US1010–15/farm9.07.4–10.6
      Deep-bedded pack
      • Endres M.I.
      • Barberg A.E.
      Behavior of dairy cows in an alternative bedded-pack housing system.
      US121479.36.1–11.4
      Pasture
      • Sepúlveda-Varas P.
      • Weary D.M.
      • von Keyserlingk M.A.G.
      Lying behavior and postpartum health status in grazing dairy cows.
      Chile62748.5
      • Beggs D.S.
      • Jongman E.C.
      • Hemsworth P.E.
      • Fisher A.D.
      Implications of prolonged milking time on time budgets and lying behavior of cows in large pasture-based dairy herds.
      Australia1030/farm9.5
      1 Only includes studies that examined multiple farms.
      2 AMS = automatic milking system
      Figure thumbnail gr1
      Figure 1Percent distribution of daily lying times for 3,122 individual cows in tiestalls and freestalls, both with a conventional milking parlor and with an automated milking system, in Canada and the US. Based on averages for 4 d. Data combined from 3 studies (
      • Charlton G.L.
      • Haley D.B.
      • Rushen J.
      • de Passillé A.M.
      Stocking density, milking duration, and lying times of lactating cows on Canadian freestall dairy farms.
      ;
      • Solano L.
      • Barkema H.W.
      • Pajor E.A.
      • Mason S.
      • LeBlanc S.J.
      • Nash C.G.R.
      • Haley D.B.
      • Pellerin D.
      • Rushen J.
      • de Passillé A.M.
      • Vasseur E.
      • Orsel K.
      Associations between lying behavior and lameness in Canadian Holstein-Friesian cows housed in freestall barns.
      ;
      • Westin R.
      • Vaughan A.
      • de Passillé A.M.
      • DeVries T.J.
      • Pajor E.A.
      • Pellerin D.
      • Siegford J.M.
      • Vasseur E.
      • Rushen J.
      Lying times of lactating cows on dairy farms with automatic milking systems and the relation to lameness, leg lesions, and body condition score.
      ).
      A change in total lying time can come about as a result of a changed frequency of bouts, a change in bout duration, or both. The average bout frequency is typically between 9 to 11 bouts/d, with mean bout duration varying from 60 to 99 min (
      • Ito K.
      • Weary D.M.
      • von Keyserlingk M.A.G.
      Lying behavior: Assessing within- and between-herd variation in free-stall-housed dairy cows.
      ;
      • Thomsen P.T.
      • Munksgaard L.
      • Sørensen J.T.
      Locomotion scores and lying behaviour are indicators of hoof lesions in dairy cows.
      ;
      • Charlton G.L.
      • Haley D.B.
      • Rushen J.
      • de Passillé A.M.
      Stocking density, milking duration, and lying times of lactating cows on Canadian freestall dairy farms.
      ;
      • Westin R.
      • Vaughan A.
      • de Passillé A.M.
      • DeVries T.J.
      • Pajor E.A.
      • Pellerin D.
      • Siegford J.M.
      • Vasseur E.
      • Rushen J.
      Lying times of lactating cows on dairy farms with automatic milking systems and the relation to lameness, leg lesions, and body condition score.
      ). However, again, there are large difference among cows in bout frequency and mean bout duration. For example,
      • Westin R.
      • Vaughan A.
      • de Passillé A.M.
      • DeVries T.J.
      • Pajor E.A.
      • Pellerin D.
      • Siegford J.M.
      • Vasseur E.
      • Rushen J.
      Lying times of lactating cows on dairy farms with automatic milking systems and the relation to lameness, leg lesions, and body condition score.
      reported that daily bout frequency varied among cows from less than 5/d to more than 20/d, and mean bout duration varied from less than 20 min to more than 150 min. The duration of a single bout of lying down can also vary greatly for an individual cow, the shortest bouts being a few minutes, whereas the longest can be up to several hours (
      • Tucker C.B.
      • Cox N.R.
      • Weary D.M.
      • Špinka M.
      Laterality of lying behaviour in dairy cattle.
      ;
      • Silper B.F.
      • Polsky L.
      • Luu J.
      • Burnett T.A.
      • Rushen J.
      • de Passillé A.M.
      • Cerri R.L.A.
      Automated and visual measurements of estrous behavior and their sources of variation in Holstein heifers. II: Standing and lying patterns.
      ), although evidence suggests that cattle are more willing to work for lying bouts that last at least 30 min (
      • Jensen M.B.
      • Pedersen L.J.
      • Munksgaard L.
      The effect of reward duration on demand functions for rest in dairy heifers and lying requirements as measured by demand functions.
      ).
      The most common measures of lying behavior include the total duration of time spent lying down within a period of time (usually a day), the frequency of bouts of lying down, and the bout duration (usually the mean bout duration), all of which can be automatically measured (
      • Ledgerwood D.N.
      • Winckler C.
      • Tucker C.B.
      Evaluation of data loggers, sampling intervals, and editing techniques for measuring the lying behavior of dairy cattle.
      ;
      • Kok A.
      • van Knegsel A.T.M.
      • van Middelaar C.E.
      • Hogeveen H.
      • Kemp B.
      • de Boer I.J.M.
      Technical note: Validation of sensor-recorded lying bouts in lactating dairy cows using a 2-sensor approach.
      ). Bout frequency and mean bout duration can be differentially affected by various factors: for example, cow parity is positively correlated with bout duration but negatively correlated with bout frequency (
      • Vasseur E.
      • Rushen J.
      • Haley D.B.
      • de Passillé A.M.
      Sampling cows to assess lying time for on-farm animal welfare assessment.
      ), a hard lying surface results in longer bout duration but lower bout frequency and total lying time compared with softer surfaces (
      • Rushen J.
      • Haley D.
      • de Passillé A.M.
      Effect of softer flooring in tie stalls on resting behavior and leg injuries of lactating cows.
      ), and wet bedding results in fewer bouts but does not affect bout duration (
      • Schütz K.E.
      • Cave V.M.
      • Cox N.R.
      • Huddart F.J.
      • Tucker C.B.
      Effects of 3 surface types on dairy cattle behavior, preference, and hygiene.
      ). We recommend that all 3 measures, over 24 h, should be taken to capture the lying behavior of cows.

      How Do Cows Lie Down?

      Cattle begin lying down by searching for an appropriate resting location (
      • Krohn C.C.
      • Munksgaard L.
      Behaviour of dairy cows kept in extensive (loose housing/pasture) or intensive (tie stall) environments II. Lying and lying-down behaviour.
      ). They then show intention movements, characterized by sniffing the surface and swinging the head from side to side close to the ground (
      • Lidfors L.
      The use of getting up and lying down movements in the evaluation of cattle environments.
      ;
      • Müller C.
      • Ladewig J.
      • Thielscher H.H.
      • Smidt D.
      Behavior and heart-rate of heifers housed in tether stanchions without straw.
      ;
      • Krohn C.C.
      • Munksgaard L.
      Behaviour of dairy cows kept in extensive (loose housing/pasture) or intensive (tie stall) environments II. Lying and lying-down behaviour.
      ;
      • Tucker C.B.
      • Weary D.M.
      Bedding on geotextile mattresses: How much is needed to improve cow comfort?.
      ;
      • Bak A.S.
      • Herskin M.S.
      • Jensen M.B.
      Effect of sand and rubber surface on the lying behavior of lame dairy cows in hospital pens.
      ). Keeping the head close to the surface, the animal bends one front leg, descends onto its carpal joints (one after the other) and places the hind leg of the intended lying side behind the opposite forelimb and underneath the body. The head is stretched forward and downward while the animal lowers the body to rest first on the brisket and then, after bending the hind legs, on the lower hind leg, thigh, and abdomen. During both standing up and lying down, both the horizontal and lateral movements of the animal's body can be sizable:
      • Ceballos A.
      • Sanderson D.
      • Rushen J.
      • Weary D.M.
      Improving stall design: Use of 3-D kinematics to measure space use by dairy cows when lying down.
      estimated that a mature cow required 300 cm of longitudinal space and 109 cm of lateral space to complete the lying-down sequence.
      While lying down, cattle assume a range of positions, which can be described by whether the animal is resting on the side or sternum, whether the front or back legs, or both, are folded under the body or extended, and whether or not the head is supported by the neck (e.g.,
      • Haley D.B.
      • de Passillé A.M.
      • Rushen J.
      Assessing cow comfort: Effects of two floor types and two tie stall designs on the behaviour of lactating dairy cows.
      ;
      • Tucker C.B.
      • Rogers A.R.
      • Verkerk G.A.
      • Kendall P.E.
      • Webster J.R.
      • Matthews L.R.
      Effects of shelter and body condition on the behaviour and physiology of dairy cattle in winter.
      ). These particular postures have been related to the phase of sleep in calves (
      • Hänninen L.
      • Mäkelä J.P.
      • Rushen J.
      • de Passillé A.M.
      • Saloniemi H.
      Assessing sleep state in calves through electrophysiological and behavioural recordings: A preliminary study.
      ), but more studies are needed among adult cattle (
      • Ternman E.
      • Pastell M.
      • Agenäs S.
      • Strasser C.
      • Winckler C.
      • Nielsen P.P.
      • Hänninen L.
      Agreement between different sleep states and behaviour indicators in dairy cows.
      ). Lying postures may also relate to the fullness and size of the udder or to thermoregulatory responses, but we have little comprehensive data on this for lactating cows.
      The way that cows lie down and the postures they adopt can explain some of the effects of housing on their lying time. For example, the fact that a large proportion of the weight is placed on the carpal joints when both standing up and lying down may explain some of the effects of carpal injury and stall flooring on lying time (e.g.,
      • Rushen J.
      • Haley D.
      • de Passillé A.M.
      Effect of softer flooring in tie stalls on resting behavior and leg injuries of lactating cows.
      ), and space requirements may explain the effects of stall dimensions on lying behavior.

      When Do Cows Lie Down?

      Several studies have examined the times of day that cows lie down and have found clear evidence of diurnal rhythms. Although they do lie down during the day as well as during the night, the majority of their time lying down occurs during the latter (
      • Winckler C.
      • Tucker C.B.
      • Weary D.M.
      Effects of under-and overstocking freestalls on dairy cattle behaviour.
      ). However, this is less evident when cows are housed indoors, rather than at pasture (
      • O'Connell J.
      • Giller P.S.
      • Meaney W.
      A comparison of dairy cattle behavioural patterns at pasture and during confinement.
      ;
      • Ketelaar-de Lauwere C.C.
      • Ipema A.H.
      • van Ouwerkerk E.N.J.
      • Hendriks M.M. W.B.
      • Metz J.H.M.
      • Noordhuizen J.P. T.M.
      • Schouten W.G.P.
      Voluntary automatic milking in combination with grazing of dairy cows: Milking frequency and effects on behaviour.
      ).

      MOTIVATION

      Problems of animal welfare often occur when an animal is highly motivated to perform a particular behavior but is unable to do so because of the husbandry environment (
      • Dawkins M.S.
      Using behaviour to assess animal welfare.
      ). Research into this aspect of behavioral deprivation has focused on the extent that motivation to perform the behavior increases when the animal is unable to perform the behavior so that compensatory behavior (a “rebound”) is shown. One possibility (which is often assumed) is that cows are motivated to lie down for a certain amount of time per day. Another possibility is that cows attempt to limit the length of time they spend standing at a single time. These questions of motivation have been examined using several approaches.

      Evidence of Rebound or Compensatory Responses Associated with Lying Behavior

      The literature provides 3 primary forms of evidence about this. The first form examines how cows make tradeoffs between bouts of lying and standing behavior, of their own accord, and involves analysis of lying and standing bouts within a day. The second examines how lying behavior changes following thwarting, and the third quantified changes over days in response to unfavorable conditions or forced standing.
      How cows make tradeoffs in the decision to stand up or lie down within a day can provide insight into their motivation for these behaviors. Good evidence exists that the probability of a cow standing up increases with the time spent lying down in a given bout (
      • Jensen M.B.
      • Pedersen L.J.
      • Munksgaard L.
      The effect of reward duration on demand functions for rest in dairy heifers and lying requirements as measured by demand functions.
      ;
      • Tucker C.B.
      • Cox N.R.
      • Weary D.M.
      • Špinka M.
      Laterality of lying behaviour in dairy cattle.
      ;
      • Tolkamp B.J.
      • Haskell M.J.
      • Langford F.M.
      • Roberts D.J.
      • Morgan C.A.
      Are cows more likely to lie down the longer they stand?.
      ). Similarly, we would expect the reverse effect: the probability of lying down should increase the longer the cow has been standing. Surprisingly,
      • Tolkamp B.J.
      • Haskell M.J.
      • Langford F.M.
      • Roberts D.J.
      • Morgan C.A.
      Are cows more likely to lie down the longer they stand?.
      found no relationship between the duration of the standing bout and the probability that the cow would lie down. However, we find several problems with this analysis. First, standing bouts over 4 h were rare, and standing bouts less than 4 min in length were not recorded. This may obscure any nonlinear relationships where both very long and very short standing bouts affected the motivation to lie down, for which some evidence does exist (e.g.,
      • Tucker C.B.
      • Cox N.R.
      • Weary D.M.
      • Špinka M.
      Laterality of lying behaviour in dairy cattle.
      ). In addition, the
      • Tolkamp B.J.
      • Haskell M.J.
      • Langford F.M.
      • Roberts D.J.
      • Morgan C.A.
      Are cows more likely to lie down the longer they stand?.
      analysis ignores the fact that some standing or lying bouts would have been affected by milking or feeding times. Consequently, we cannot conclude much about the motivation to lie down from this particular study, but the approach has value, in principle, without these methodological limitations.
      Other research has examined how forced, prolonged standing affects cows' motivation to lie down afterward. When both dairy cows (
      • Munksgaard L.
      • Simonsen H.B.
      Behavioral and pituitary adrenal-axis responses of dairy cows to social isolation and deprivation of lying down.
      ) and young bulls (
      • Munksgaard L.
      • Ingvartsen K.L.
      • Pedersen L.J.
      • Nielsen V.K.M.
      Deprivation of lying down affects behaviour and pituitary-adrenal axis responses in young bulls.
      ) were forced to stand for 7 h twice a day by physical restraint, they spent almost all of the remaining time (93% and 95%) lying down. Cows forced to stand for 4 h spent more time lying down in the following 4 h (
      • Norring M.
      • Valros A.
      The effect of lying motivation on cow behaviour.
      ) or 20 h (
      • Bolinger D.J.
      • Albright J.L.
      • Morrow-Tesch J.
      • Kenyon S.J.
      • Cunningham M.D.
      The effects of restraint using self-locking stanchions on dairy cows in relation to behavior, feed intake, physiological parameters, health, and milk yield.
      ) than those that were not. In addition, the latency to lie down can be short, 4 to 7 min, after 4 h of forced standing (
      • Krebs N.
      • Berry S.L.
      • Tucker C.B.
      Restless behavior increases over time, but not with compressibility of the flooring surface, during forced standing at the feed bunk.
      ;
      • Norring M.
      • Valros A.
      The effect of lying motivation on cow behaviour.
      ) and is over an hour sooner than cows that have not been standing for 4 h (
      • Tucker C.B.
      • Munksgaard L.
      • Mintline E.M.
      • Jensen M.B.
      Use of a pneumatic push gate to measure dairy cattle motivation to lie down in a deep-bedded area.
      ). Quickly engaging in lying behavior (short latency to lie), once provided the opportunity, indicates that the cows are motivated to do so.
      Cows have also been forced to stand, not by being physically restrained, but as a result of inappropriate surfaces or lack of space. These “environmentally imposed” standing periods also result in a rebound in lying behavior. For example, being kept temporarily on hard, wet, or muddy surfaces (
      • Fisher A.D.
      • Stewart M.
      • Verkerk G.A.
      • Morrow C.J.
      • Matthews L.R.
      The effects of surface type on lying behaviour and stress responses of dairy cows during periodic weather-induced removal from pasture.
      ;
      • Schütz K.E.
      • Cox N.R.
      Effects of short-term repeated exposure to different flooring surfaces on the behavior and physiology of dairy cattle.
      ;
      • Schütz K.E.
      • Cave V.M.
      • Cox N.R.
      • Huddart F.J.
      • Tucker C.B.
      Effects of 3 surface types on dairy cattle behavior, preference, and hygiene.
      ) or rubber mats at high stocking densities (
      • Schütz K.E.
      • Huddart F.J.
      • Sutherland M.A.
      • Stewart M.
      • Cox N.R.
      Effects of space allowance on the behavior and physiology of cattle temporarily managed on rubber mats.
      ) resulted in a total reduction in time spent lying down in the 18 to 21 h/d they were kept in these unfavorable conditions and a subsequent rebound lying behavior when released onto pasture each day. In contrast, in these studies, cows kept on comfortable surfaces, or with more space, spent the time on pasture grazing and showed little evidence of a rebound in lying behavior (quickly lying down upon release, spending more lying) during this time away from the experimental treatments. Others have also found that thwarting the ability to access a comfortable surface is followed by a compensatory increase in lying time, which could be substantial:
      • Tucker C.B.
      • Munksgaard L.
      • Mintline E.M.
      • Jensen M.B.
      Use of a pneumatic push gate to measure dairy cattle motivation to lie down in a deep-bedded area.
      reported that cows that were unable to lie down for an average of about 14 consecutive hours spent close to 18 h lying down once they were able to access a deep-bedding area again. In light of these studies, we can conclude that the motivation to lie down is increased after 4 or more consecutive hours of forced standing.
      The final line of evidence about motivation growing over time comes from experiments that exposed cows to unfavorable conditions or forced standing and quantified lying time over days and in comparison with controls kept in better conditions. Using this approach,
      • Chen J.M.
      • Stull C.L.
      • Ledgerwood D.N.
      • Tucker C.B.
      Muddy conditions reduce hygiene and lying time in dairy cattle and increase time spent on concrete.
      found that heifers and cows reduced their lying time when exposed to very muddy conditions for 3 to 5 h/d. However after 2 d of exposure to mud, cattle spent between 8 and 10 h/d lying, compared with a consistent 12+ h/d over the same period on dry soil.
      • Schütz K.E.
      • Cox N.R.
      Effects of short-term repeated exposure to different flooring surfaces on the behavior and physiology of dairy cattle.
      also found that over a series of 4-d exposures to concrete, cows initially reduced their lying time dramatically (less than 6 out of 18 h) but gradually began to spend more time lying (up to 8 out of 18 h) over the 4 d. Contemporary controls kept on softer wood chips maintain higher lying times, always more than 8 out of 18 h. Finally,
      • Cooper M.D.
      • Arney D.R.
      • Phillips C.J.C.
      Two- or four-hour lying deprivation on the behavior of lactating dairy cows.
      forced cows to stand for 2 or 4 h and then monitored whether they could recover this lost lying time over the following 40 h; they found that cattle never fully recovered, compared with unrestricted controls. Taken together, these studies indicate that cows make some cumulative attempts to recover or maintain lying time, under unfavorable conditions or following forced standing.

      Tradeoffs Between Lying Down and Other Behaviors

      Studies have investigated cows' motivation to lie down by examining what they will forgo to lie down. The clear pattern is that cattle prioritize lying down over feeding, following deprivation of both or when time budgets are restricted in some way to make them choose one over the other.
      • Metz J.H.M.
      The reaction of cows to a short-term deprivation of lying.
      found that, following 3 h of deprivation of both lying and feeding, cattle chose to lie down instead of eating when opportunities to engage in both behaviors were presented.
      • Munksgaard L.
      • Jensen M.B.
      • Pedersen L.J.
      • Hansen S.W.
      • Matthews L.
      Quantifying behavioural priorities—Effects of time constraints on behaviour of dairy cows, Bos taurus..
      reduced the time available for lying down and feeding, as well as social activity. With 23 h available for all 3 activities, the dairy cows lay down for approximately 13 h per 24 h, but when time available was reduced to either 12 or 15 h, lying time was reduced to 8.5 and 9.7 h. However, in both treatments the feeding time was reduced relatively more, and feed intake was reduced, to the extent that the cows lost weight (
      • Munksgaard L.
      • Jensen M.B.
      • Pedersen L.J.
      • Hansen S.W.
      • Matthews L.
      Quantifying behavioural priorities—Effects of time constraints on behaviour of dairy cows, Bos taurus..
      ).
      • Tucker C.B.
      • Munksgaard L.
      • Mintline E.M.
      • Jensen M.B.
      Use of a pneumatic push gate to measure dairy cattle motivation to lie down in a deep-bedded area.
      found a 32% reduction in feeding time due to a compensatory increase in lying time. Finally, several studies in New Zealand found that, when released onto pasture to eat for a limited number of hours each day, cows otherwise kept in unfavorable lying conditions opted to lie down during this time (
      • Fisher A.D.
      • Stewart M.
      • Verkerk G.A.
      • Morrow C.J.
      • Matthews L.R.
      The effects of surface type on lying behaviour and stress responses of dairy cows during periodic weather-induced removal from pasture.
      ;
      • Schütz K.E.
      • Cox N.R.
      Effects of short-term repeated exposure to different flooring surfaces on the behavior and physiology of dairy cattle.
      ;
      • Schütz K.E.
      • Huddart F.J.
      • Sutherland M.A.
      • Stewart M.
      • Cox N.R.
      Effects of space allowance on the behavior and physiology of cattle temporarily managed on rubber mats.
      ,
      • Schütz K.E.
      • Cave V.M.
      • Cox N.R.
      • Huddart F.J.
      • Tucker C.B.
      Effects of 3 surface types on dairy cattle behavior, preference, and hygiene.
      ), whereas contemporary controls that had more comfortable conditions for the nonpastured portion of the day did not make this sacrifice.

      Operant Conditioning and Consumer Demand Approaches

      Another way of assessing the importance of lying down to cows is to examine whether the opportunity to lie down can act as a reward in operant conditioning. This method can be extended by varying the “cost” that the cow must pay to lie down, an approach inspired by economic theory and often termed “consumer demand.” The elasticity of a demand function is the percentage change in behavior as a function of the percentage change in price. If the behavior drops off steeply when the price is raised, then the behavior is evaluated to be less important than if the behavior had remained higher. This measures how sensitive to increasing cost a given behavior is; the less elastic, the more important the behavior (
      • Jensen M.B.
      • Pedersen L.J.
      Using motivation tests to assess ethological needs and preferences.
      ).
      • Jensen M.B.
      • Munksgaard L.
      • Pedersen L.J.
      • Ladewig J.
      • Matthews L.
      Prior deprivation and reward duration affect the demand function for rest in dairy heifers.
      ,
      • Jensen M.B.
      • Pedersen L.J.
      • Munksgaard L.
      The effect of reward duration on demand functions for rest in dairy heifers and lying requirements as measured by demand functions.
      housed pregnant heifers in tiestalls and prevented them from lying down twice daily, using a girth strap that forced the animals to remain standing. Following varying periods of deprivation, the heifers could press a panel to release the girth strap and have the opportunity to lie down. The heifers rapidly learned to do this, showing that the opportunity to lie down was reinforcing to the animals. The “cost” of lying down was varied by varying the number of times the animals had to press the panel to release the strap for each lying bout. In accordance with research showing that prolonged standing results in a rebound, pregnant heifers increased their work at a higher rate with increasing price following 6 h of forced standing versus following 3 h (
      • Jensen M.B.
      • Munksgaard L.
      • Pedersen L.J.
      • Ladewig J.
      • Matthews L.
      Prior deprivation and reward duration affect the demand function for rest in dairy heifers.
      ), indicating a higher willingness to work following the longer forced standing. Heifers also increased their work at a higher rate with increasing price when they had access to longer lying bouts (20 vs. 30, 50, and 80 min), indicating that, once lying, they want at least a certain amount of rest (
      • Jensen M.B.
      • Pedersen L.J.
      • Munksgaard L.
      The effect of reward duration on demand functions for rest in dairy heifers and lying requirements as measured by demand functions.
      ). The results also identified the daily duration pregnant heifers want to lie down, as they increased their worked at increasing price to maintain approximately 13 h of lying overall (
      • Jensen M.B.
      • Pedersen L.J.
      • Munksgaard L.
      The effect of reward duration on demand functions for rest in dairy heifers and lying requirements as measured by demand functions.
      ).
      Another approach is to measure the cost the animal will pay for the largest meaningful reward (maximum price paid;
      • Kirkden R.D.
      • Edwards J.S.S.
      • Broom D.M.
      A theoretical comparison of the consumer surplus and the elasticities of demand as measures of motivational strength.
      ;
      • Hovland A.L.
      • Mason G.
      • Bøe K.E.
      • Steinheim G.
      • Bakken M.
      Evaluation of the 'maximum price paid’ as an index of motivational strength for farmed silver foxes (Vulpes vulpes).
      ). Cows have been asked about the maximum price they are willing to pay for access to a lying area by requiring them to push through a gate that required increasing force to open. Dairy cows maintained 13 h of lying until they either no longer pushed through the gate (on average, 36% of BW) or reached the maximum force of the apparatus (258 kgf;
      • Tucker C.B.
      • Munksgaard L.
      • Mintline E.M.
      • Jensen M.B.
      Use of a pneumatic push gate to measure dairy cattle motivation to lie down in a deep-bedded area.
      ). This approach likely underestimates how much cows will work for a comfortable lying area, because when the gate became too heavy to open, cows would unsuccessfully try to open it, as many as 39 times in a single day (
      • Tucker C.B.
      • Munksgaard L.
      • Mintline E.M.
      • Jensen M.B.
      Use of a pneumatic push gate to measure dairy cattle motivation to lie down in a deep-bedded area.
      ). These numerous attempts indicate that they had reached their physical limit, and not that their motivation had subsided.

      Possible Indicators of Frustration: Behavioral Changes When Lying Is Thwarted

      When cows are prevented from lying down, they often perform more intention movements (i.e., repeatedly sniffing the surface, often accompanied by swinging the head from side to side close to the surface or bending one front leg without lying down) as well as lying attempts—that is, placing one or both carpal joints on the surface, followed by standing up again (reviewed by
      • Lidfors L.
      The use of getting up and lying down movements in the evaluation of cattle environments.
      ). Most of the experiments that have documented this response have examined unfavorable lying conditions such as little bedding (
      • Tucker C.B.
      • Cox N.R.
      • Weary D.M.
      • Špinka M.
      Laterality of lying behaviour in dairy cattle.
      ) or hard surfaces (
      • Haley D.B.
      • de Passillé A.M.
      • Rushen J.
      Assessing cow comfort: Effects of two floor types and two tie stall designs on the behaviour of lactating dairy cows.
      ), or these features of the lying surface combined with confinement (
      • Müller C.
      • Ladewig J.
      • Thielscher H.H.
      • Smidt D.
      Behavior and heart-rate of heifers housed in tether stanchions without straw.
      ;
      • Krohn C.C.
      • Munksgaard L.
      Behaviour of dairy cows kept in extensive (loose housing/pasture) or intensive (tie stall) environments II. Lying and lying-down behaviour.
      ), compared with cow behavior in environments that are known to be more comfortable.
      Behavioral indicators of restlessness have been examined in experiments that have forced cattle to stand. These experiments report less feeding and more leaning (
      • Norring M.
      • Valros A.
      The effect of lying motivation on cow behaviour.
      ) and more transitions between behaviors (
      • Munksgaard L.
      • Simonsen H.B.
      Behavioral and pituitary adrenal-axis responses of dairy cows to social isolation and deprivation of lying down.
      ;
      • Munksgaard L.
      • Ingvartsen K.L.
      • Pedersen L.J.
      • Nielsen V.K.M.
      Deprivation of lying down affects behaviour and pituitary-adrenal axis responses in young bulls.
      ) when cows are prevented from lying down. Cows show more stepping and shifting weight from one limb to the other the longer they are forced to stand (
      • Cooper M.D.
      • Arney D.R.
      • Phillips C.J.C.
      Two- or four-hour lying deprivation on the behavior of lactating dairy cows.
      ;
      • Chapinal N.
      • de Passillé A.M.
      • Rushen J.
      • Tucker C.B.
      Short communication: Measures of weight distribution and frequency of steps as indicators of restless behavior.
      ;
      • Krebs N.
      • Berry S.L.
      • Tucker C.B.
      Restless behavior increases over time, but not with compressibility of the flooring surface, during forced standing at the feed bunk.
      ;
      • Rajapaksha E.
      • Tucker C.B.
      How do cattle respond to sloped floors? An investigation using behavior and electromyograms.
      ,
      • Rajapaksha E.
      • Tucker C.B.
      Stepping behavior and muscle activity of dairy cows on uncomfortable standing surfaces presented under 1 or 4 legs.
      ;
      • Rajapaksha E.
      • Winkler C.
      • Tucker C.B.
      Effect of rubber flooring on dairy cattle stepping behavior and muscle activity.
      ;
      • Schütz K.E.
      • Rajapaksha E.
      • Mintline E.M.
      • Cox N.R.
      • Tucker C.B.
      Stepping behavior and muscle activity of dairy cattle standing on concrete or rubber flooring for 1 or 3 hours.
      ). Interpreting what this restlessness means in terms of animal welfare is complicated. On one hand, more restless behavior is shown by lame animals than by sound ones (
      • Neveux S.
      • Weary D.M.
      • Rushen J.
      • von Keyserlingk M.A.G.
      • de Passillé A.M.
      Hoof discomfort changes how dairy cattle distribute their body weight.
      ;
      • Chapinal N.
      • Tucker C.B.
      Validation of an automated method to count steps while cows stand on a weighing platform and its application as a measure to detect lameness.
      ), which would imply that it indicates pain. However, it is also possible that restless behavior could function as a means to avoid fatigue through more blood circulation to the limbs. Further research is required to determine whether or not restlessness is associated with frustration.

      Motivation—Summary and Conclusions

      Overwhelming evidence confirms the importance of lying behavior for cows. Forcing cows to stand results in a higher motivation and compensatory lying (“rebound”) when the opportunity arises. This can be sufficiently high as to result in a substantially reduced time spent feeding and, sometimes, reduced feed intake. The increase in motivation can occur when cows are prevented from lying down for as little as 3 to 4 h, and cows show several behavioral changes that may indicate frustration when they are forced to stand.

      HEALTH AND BIOLOGICAL FUNCTION

      Problems of animal welfare occur when health is compromised (
      • Dawkins M.S.
      Using behaviour to assess animal welfare.
      ). We review what is known about the implications of reduced time spent lying down in terms of health, as well as other aspects of biological function that may be affected, namely indicators of stress response, milk production, and the ability to sleep and ruminate.

      Increased Risk of Lameness and Illness

      Several authors suggest that the risk of lameness is greater when lying areas are uncomfortable (
      • Cook N.B.
      • Mentink R.L.
      • Bennett T.B.
      • Burgi K.
      The effect of heat stress and lameness on time budgets of lactating dairy cows.
      ;
      • Bell N.J.
      • Bell M.J.
      • Knowles T.G.
      • Whay H.R.
      • Main D.J.
      • Webster A.J.F.
      The development, implementation and testing of a lameness control programme based on HACCP principles and designed for heifers on dairy farms.
      ;
      • Dippel S.
      • Dolezal M.
      • Brenninkmeyer C.
      • Brinkmann J.
      • March S.
      • Knierim U.
      • Winckler C.
      Risk factors for lameness in freestall-housed dairy cows across two breeds, farming systems, and countries.
      ;
      • Rouha-Mülleder C.
      • Iben C.
      • Wagner E.
      • Laaha G.
      • Troxler J.
      • Waiblinger S.
      Relative importance of factors influencing the prevalence of lameness in Austrian cubicle loose-housed dairy cows.
      ), and higher risk of lameness may be one of the most serious welfare consequences of reduced lying time. Some studies have shown an association between short lying time and the occurrence of lameness (
      • Leonard F.C.
      • O'Connell J.
      • O'Farrell K.
      Effect of different housing conditions on behaviour and foot lesions in Friesian heifers.
      ;
      • Galindo F.
      • Broom D.M.
      The relationships between social behaviour of dairy cows and the occurrence of lameness in three herds.
      ;
      • Thomsen P.T.
      • Munksgaard L.
      • Sørensen J.T.
      Locomotion scores and lying behaviour are indicators of hoof lesions in dairy cows.
      ), and some aspects of stall design appear to be a risk factor for both lower lying time and more lameness (
      • Bouffard V.
      • de Passillé A.M.
      • Rushen J.
      • Vasseur E.
      • Nash C.G.R.
      • Haley D.B.
      • Pellerin D.
      Effect of following recommendations for tiestall configuration on neck and leg lesions, lameness, cleanliness, and lying time in dairy cows.
      ). However, housing conditions that differ in the prevalence of lameness do not always differ in the time that the cows spend lying down (
      • Cook N.B.
      • Bennett T.B.
      • Nordlund K.V.
      Effect of free stall surface on daily activity patterns in dairy cows with relevance to lameness prevalence.
      ;
      • Ito K.
      • von Keyserlingk M.A.G.
      • LeBlanc S.J.
      • Weary D.M.
      Lying behavior as an indicator of lameness in dairy cows.
      ). Such studies, however, are complicated by the possibility that, once cows become lame, they spend more time lying down. No studies have experimentally reduced lying time and examined consequent changes in lameness, so the best evidence that reduced lying time increases risk of lameness is limited to correlational studies that have found reduced lying time preceding the onset of lameness (
      • Cook N.B.
      The impact of management and facilities on cow culling rates.
      ).
      Of these,
      • Leonard F.C.
      • O'Connell J.M.
      • O'Farrell K.J.
      Effect of overcrowding on claw health in first-calved Friesian heifers.
      found lower lying times in heifers 1 mo before claw lesions were measured, in populations where there was sufficient variation in lying time. Three (
      • Chapinal N.
      • de Passillé A.M.
      • Weary D.M.
      • von Keyserlingk M.A.G.
      • Rushen J.
      Using gait score, walking speed, and lying behavior to detect hoof lesions in dairy cows.
      ;
      • Proudfoot K.L.
      • Weary D.M.
      • von Keyserlingk M.A.G.
      Behavior during transition differs for cows diagnosed with claw horn lesions in mid lactation.
      ;
      • Sepúlveda-Varas P.
      • Weary D.M.
      • von Keyserlingk M.A.G.
      Lying behavior and postpartum health status in grazing dairy cows.
      ) of 4 more recent studies documented reduced time spent lying down before calving in cows that became lame or developed claw lesions after calving (10.6 vs. 12.2 h/d, 10.1 vs. 12.1 h/d, and 7.3 vs. 8.5 h/d, respectively). In contrast,
      • Dippel S.
      • Tucker C.B.
      • Winckler C.
      • Weary D.M.
      Effects of behaviour on the development of claw lesions in early lactation dairy cows.
      found no differences in lying behavior of freestall-housed dairy cows (all about 11 h/d) in the weeks before claw lesions were visible. Rather, these authors and
      • Proudfoot K.L.
      • Weary D.M.
      • von Keyserlingk M.A.G.
      Behavior during transition differs for cows diagnosed with claw horn lesions in mid lactation.
      reported that spending more time standing partially in the stall, with the hind hooves in the alleyway, was associated with subsequent hoof health pathology.
      Two other studies found that environmental conditions that led to cows becoming lame also led to reduced time spent lying down beforehand. An early study (
      • Leach K.A.
      • Offer J.E.
      • Svoboda I.
      • Logue D.N.
      Effects of type of forage fed to dairy heifers: Associations between claw characteristics, clinical lameness, environment and behaviour.
      ) noticed that feeding cows wet fermented grass silage resulted in cows spending less time lying down (11.1 vs. 13.0 h/d) before calving, and this increased the prevalence of claw lesions 18 to 24 mo after calving.
      • Olmos G.
      • Boyle L.
      • Hanlon A.
      • Patton J.
      • Murphy J.J.
      • Mee J.F.
      Hoof disorders, locomotion ability and lying times of cubicle-housed compared to pasture-based dairy cows.
      compared cows kept at pasture or housed indoors in a freestall barn. Cows at pasture had healthier claws than the cows housed indoors, and the difference was significant 85 d after calving. The cows at pasture also spent more time lying (12.2 vs. 8.1 h/d) 33 d after calving and before the differences in claw lesion scores became apparent.
      Changes in lying behavior may also increase the risk for other disease. For example, changes in post-milking standing time may affect the risk of mastitis if the cow does not remain standing for long enough to ensure that the teat canal closes before they come in contact with the lying surface.
      • DeVries T.J.
      • Dufour S.
      • Scholl D.T.
      Relationship between feeding strategy, lying behavior patterns, and incidence of intramammary infection in dairy cows.
      found that cows kept in tiestalls had lower odds of getting a new udder infection if they lay down 40 to 60 min after milking compared with within the first 40 min after milking. However, in a study in a loose-housing barn with an automatic milking system, standing for long (>2.5 h) rather than short periods after milking increased the risk of infection (
      • DeVries T.J.
      • Aarnoudse M.G.
      • Barkema H.W.
      • Leslie K.E.
      • von Keyserlingk M.A.G.
      Associations of dairy cow behavior, barn hygiene, cow hygiene, and risk of elevated somatic cell count.
      ).
      Considerable circumstantial evidence indicates that lying times less than 11 h, especially around or before parturition, are associated with subsequent development of lameness and claw lesions. However, much of this evidence is longitudinal in nature, and, in some cases, lower lying times were confounded with other aspects of the animals' management (e.g., wet vs. dry fermented feed; pasture vs. freestall housing). Some of these confounding factors are also risk factors in their own right; for example, lameness tends to be lower when cows are kept on pasture (e.g.,
      • Hernandez-Mendo O.
      • von Keyserlingk M.A.G.
      • Veira D.M.
      • Weary D.M.
      Effects of pasture on lameness in dairy cows.
      ), further complicating our ability to draw conclusions about lying time, lameness, and causation.

      Physiological Indicators of the Stress Response

      Several studies have examined whether forcing cows to stand or keeping them in unfavorable conditions for lying down affects the hypothalamo-pituitary-adrenal (HPA) axis. Among studies, HPA axis responses vary. Inclement weather can result in more HPA activity and reduced lying time (
      • Tucker C.B.
      • Rogers A.R.
      • Verkerk G.A.
      • Kendall P.E.
      • Webster J.R.
      • Matthews L.R.
      Effects of shelter and body condition on the behaviour and physiology of dairy cattle in winter.
      ;
      • Webster J.R.
      • Stewart M.
      • Rogers A.R.
      • Verkerk G.A.
      Assessment of welfare from physiological and behavioural responses of New Zealand dairy cows exposed to cold and wet conditions.
      ), but the causal relationships are unknown. Overstocking cows has been found to either increase cortisol concentrations (
      • Friend T.H.
      • Gwazdauskas F.G.
      • Polan C.E.
      Change in adrenal response from free stall competition.
      ) or have no effect (
      • Krawczel P.D.
      • Klaiber L.B.
      • Butzler R.E.
      • Klaiber L.M.
      • Dann H.M.
      • Mooney C.S.
      • Grant R.J.
      Short-term increases in stocking density affect the lying and social behavior, but not the productivity, of lactating Holstein dairy cows.
      ;
      • Schütz K.E.
      • Huddart F.J.
      • Sutherland M.A.
      • Stewart M.
      • Cox N.R.
      Effects of space allowance on the behavior and physiology of cattle temporarily managed on rubber mats.
      ). Similarly, cows kept in a concrete yard for 4 d had a shorter lying time (7.0 h/d) and a higher fecal glucocorticoid metabolite concentration than cows kept on a wood chip pad with a much longer lying time (11.9 h/d). However, in the same experiment, cows kept on either a farm lane or in a small paddock had a severe reduction in lying time (5.7 vs. 6.9 h/d) but did not differ in fecal glucocorticoid metabolite concentration (
      • Fisher A.D.
      • Stewart M.
      • Verkerk G.A.
      • Morrow C.J.
      • Matthews L.R.
      The effects of surface type on lying behaviour and stress responses of dairy cows during periodic weather-induced removal from pasture.
      ). Studies that have forced cows to stand for 14.8 consecutive hours for 7 d report higher baseline cortisol compared with controls (
      • Fisher A.D.
      • Verkerk G.A.
      • Morrow C.J.
      • Matthews L.R.
      The effects of feed restriction and lying deprivation on pituitary-adrenal axis regulation in lactating cows.
      ), whereas others that forced cows to stand for 14 h (divided into two 7-h sessions) for 24 d found no differences in plasma cortisol (
      • Munksgaard L.
      • Simonsen H.B.
      Behavioral and pituitary adrenal-axis responses of dairy cows to social isolation and deprivation of lying down.
      ). A complication with the forced standing experimental model is that the method used to keep the cow upright—for example, an electrified girth strap (
      • Fisher A.D.
      • Verkerk G.A.
      • Morrow C.J.
      • Matthews L.R.
      The effects of feed restriction and lying deprivation on pituitary-adrenal axis regulation in lactating cows.
      )—itself may be painful.
      Forced standing and unfavorable lying conditions can also affect the reactivity of the HPA axis (
      • Friend T.H.
      • Gwazdauskas F.G.
      • Polan C.E.
      Change in adrenal response from free stall competition.
      ;
      • Munksgaard L.
      • Simonsen H.B.
      Behavioral and pituitary adrenal-axis responses of dairy cows to social isolation and deprivation of lying down.
      ;
      • Fisher A.D.
      • Verkerk G.A.
      • Morrow C.J.
      • Matthews L.R.
      The effects of feed restriction and lying deprivation on pituitary-adrenal axis regulation in lactating cows.
      ), but the response depends upon the duration of the treatment and the timing of blood sampling. For example, in a study with bulls,
      • Munksgaard L.
      • Ingvartsen K.L.
      • Pedersen L.J.
      • Nielsen V.K.M.
      Deprivation of lying down affects behaviour and pituitary-adrenal axis responses in young bulls.
      found a decrease in cortisol response to CRF and ACTH following forced standing on d 3 after treatment, which was not apparent on d 22 and 49. The behavioral responses to forced standing were apparent on all 3 d, showing that the change in HPA response was not due to general adaptation to the deprivation of lying down.
      The hormonal responses to forced standing is not limited to the HPA axis. For example,
      • Munksgaard L.
      • Løvendahl P.
      Effects of social and physical stressors on growth hormone levels in dairy cows.
      showed that forcing cows to stand for 14 h/d (divided into two 7-h sessions) appeared to be associated with a reduction in growth hormone.
      Taken together, the results suggest that forced standing and unfavorable lying conditions can induce physiological stress responses indicating reduced welfare. However, the changes are not simple or consistent. We do not yet know whether these changes result from the length of time that cows remained standing at one time, the reduction in overall daily lying time, or the methods used to prevent them from lying down. Nor do we yet know whether these effects occur following the shorter periods of forced standing thought to be more typical on commercial farms. We need to examine a broader range of hormonal systems and use a wider range of experimental models to manipulate when and how cows lie down, to better understand the physiological effects of lying and the consequences for the animals' welfare.

      Changes in Milk Production

      Changes in milk production do not necessarily indicate a change in animal welfare. However, when this change is result of stress, such as those previously discussed, or illness or a reduction in feed intake, then concern about animal welfare is justified.
      Reductions in lying time have been experimentally induced by unfavorable lying conditions such as overstocking (
      • Krawczel P.D.
      • Klaiber L.B.
      • Butzler R.E.
      • Klaiber L.M.
      • Dann H.M.
      • Mooney C.S.
      • Grant R.J.
      Short-term increases in stocking density affect the lying and social behavior, but not the productivity, of lactating Holstein dairy cows.
      ), manipulating the stall width (
      • Tucker C.B.
      • Weary D.M.
      • Fraser D.
      Free-stall dimensions: Effects on preference and stall usage.
      ), or manipulating the comfort of stalls (
      • Haley D.B.
      • Rushen J.
      • de Passillé A.M.
      Behavioural indicators of cow comfort: Activity and resting behaviour of dairy cows in two types of housing.
      ;
      • Tucker C.B.
      • Weary D.M.
      • von Keyserlingk M.A.G.
      • Beauchemin K.A.
      Cow comfort in tie-stalls: Increased depth of shavings or straw bedding increases lying time.
      ), and none of these found any change in the milk yield associated with these treatments. Thus, a direct and simple effect of altered lying time on milk yield seems unlikely (
      • Cook N.B.
      The impact of management and facilities on cow culling rates.
      ); however, we note that the average lying times were all above 10 h/d in these experiments. When cows had less time to both lie down and feed, they produced less milk, most likely due to a drop in feed intake (
      • Munksgaard L.
      • Jensen M.B.
      • Pedersen L.J.
      • Hansen S.W.
      • Matthews L.
      Quantifying behavioural priorities—Effects of time constraints on behaviour of dairy cows, Bos taurus..
      ). Thus, the effects on milk production of preventing cows from lying down may depend on whether or not a resultant reduction in feed intake occurs as a result of competition for time spent lying down.

      Sleep

      An obvious biologically important behavior that occurs when cattle are lying down is sleep. Research in this area is affected and limited by our ability to quantify different types of sleep. Using electroencephalography (EEG), sleep can be subdivided into non-rapid eye movement (NREM) and rapid eye movement (REM). However, we lack a reliable noninvasive method to measure sleep in adult cows, as rumination causes disturbance to the EEG signal and makes it difficult to interpret the vigilance state while cows are chewing their cud (
      • Hänninen L.
      • Mäkelä J.P.
      • Rushen J.
      • de Passillé A.M.
      • Saloniemi H.
      Assessing sleep state in calves through electrophysiological and behavioural recordings: A preliminary study.
      ;
      • Ternman E.
      • Hänninen L.
      • Pastell M.
      • Agenäs S.
      • Nielsen P.P.
      Sleep in dairy cows recorded with a non-invasive EEG technique.
      ). However, to date, these methods do generate reliable estimates of REM sleep (
      • Ruckebusch Y.
      The relevance of drowsiness in the circadian cycle of farm animals.
      ). In addition, NREM sleep and total time spent sleeping in adult cattle are possible to measure when the animals are not ruminating (
      • Ternman E.
      • Hänninen L.
      • Pastell M.
      • Agenäs S.
      • Nielsen P.P.
      Sleep in dairy cows recorded with a non-invasive EEG technique.
      ,
      • Ternman E.
      • Pastell M.
      • Agenäs S.
      • Strasser C.
      • Winckler C.
      • Nielsen P.P.
      • Hänninen L.
      Agreement between different sleep states and behaviour indicators in dairy cows.
      ,
      • Ternman E.
      • Pastell M.
      • Hänninen L.
      • Agenäs S.
      • Nielsen P.P.
      First-night effect on sleep time in dairy cows.
      ,
      • Ternman E.
      • Nilsson E.
      • Nielsen P.P.
      • Pastell M.
      • Hänninen L.
      • Agenäs S.
      Rapid eye movement sleep time in dairy cows changes during the lactation cycle.
      ;
      • Kull J.A.
      • Proudfoot K.L.
      • Pighetti G.M.
      • Bewley J.M.
      • O'Hara B.F.
      • Donohue K.D.
      • Krawczel P.D.
      Effects of acute lying and sleep deprivation on the behavior of lactating dairy cows.
      ), and the following results are limited by these constraints.
      Cattle must lie down to have REM sleep, but they can have NREM sleep when standing if forced (
      • Ruckebusch Y.
      Sleep deprivation in cattle.
      ). Adult cattle sleep for considerably less time than they lie down: only 4 h/d, of which less than an hour is REM sleep (
      • Ruckebusch Y.
      The relevance of drowsiness in the circadian cycle of farm animals.
      ;
      • Ternman E.
      • Pastell M.
      • Hänninen L.
      • Agenäs S.
      • Nielsen P.P.
      First-night effect on sleep time in dairy cows.
      ,
      • Ternman E.
      • Nilsson E.
      • Nielsen P.P.
      • Pastell M.
      • Hänninen L.
      • Agenäs S.
      Rapid eye movement sleep time in dairy cows changes during the lactation cycle.
      ). The measurement method affects the amounts of NREM sleep recorded: studies using implanted electrodes reported 3 h of NREM sleep (
      • Ruckebusch Y.
      The relevance of drowsiness in the circadian cycle of farm animals.
      ), whereas noninvasive techniques report only around 1 h (
      • Ternman E.
      • Pastell M.
      • Hänninen L.
      • Agenäs S.
      • Nielsen P.P.
      First-night effect on sleep time in dairy cows.
      ,
      • Ternman E.
      • Nilsson E.
      • Nielsen P.P.
      • Pastell M.
      • Hänninen L.
      • Agenäs S.
      Rapid eye movement sleep time in dairy cows changes during the lactation cycle.
      ;
      • Kull J.A.
      • Proudfoot K.L.
      • Pighetti G.M.
      • Bewley J.M.
      • O'Hara B.F.
      • Donohue K.D.
      • Krawczel P.D.
      Effects of acute lying and sleep deprivation on the behavior of lactating dairy cows.
      ). The sleep cycle of adult dairy cows typically consists of 1 NREM bout lasting 5 ± 3 min and 1 REM bout lasting 3 ± 1 min, followed by the cow waking up (
      • Ternman E.
      • Hänninen L.
      • Pastell M.
      • Agenäs S.
      • Nielsen P.P.
      Sleep in dairy cows recorded with a non-invasive EEG technique.
      ).
      In one of the few sleep deprivation studies in cattle (
      • Ruckebusch Y.
      Sleep deprivation in cattle.
      ), cows were prevented from lying down for 14 to 22 h/d for 2 mo. During periods of forced standing, cows increased their NREM sleep and markedly reduced REM sleep. Rebound effects were observed as a doubled amount of NREM and REM sleep during 4 d after deprivation, compared with beforehand (
      • Ruckebusch Y.
      Sleep deprivation in cattle.
      ). In more recent work, cows deprived for 24 h of either sleep or lying took between 2 and 4 d to recover their lying time, respectively (
      • Kull J.A.
      • Proudfoot K.L.
      • Pighetti G.M.
      • Bewley J.M.
      • O'Hara B.F.
      • Donohue K.D.
      • Krawczel P.D.
      Effects of acute lying and sleep deprivation on the behavior of lactating dairy cows.
      ). Unfortunately, very little is known about how changes in lying time affect time sleeping or the consequences of reduced sleep for cattle, and this clearly requires further research.

      Rumination

      The other main activity that cows engage in while lying down is rumination. Research is fairly consistent in finding that lactating cows ruminate, on average, between 7 and 9 h/d, for example, in freestalls with a milking parlor (
      • Schirmann K.
      • Chapinal N.
      • Weary D.M.
      • Heuwieser W.
      • von Keyserlingk M.A.G.
      Rumination and its relationship to feeding and lying behavior in Holstein dairy cows.
      ) or with an automatic milking system (
      • Reith S.
      • Hoy S.
      Relationship between daily rumination time and estrus of dairy cows.
      ), in tiestalls (
      • Munksgaard L.
      • Simonsen H.B.
      Behavioral and pituitary adrenal-axis responses of dairy cows to social isolation and deprivation of lying down.
      ), and at pasture (
      • Kilgour R.J.
      In pursuit of “normal”: A review of the behaviour of cattle at pasture.
      ). More rumination occurs at nighttime, at the time when cows are often lying down (
      • Gregorini P.
      • DelaRue B.
      • McLeod K.
      • Clark C.E.F.
      • Glassey C.B.
      • Jago J.
      Rumination behavior of grazing dairy cows in response to restricted time at pasture.
      ;
      • Kilgour R.J.
      In pursuit of “normal”: A review of the behaviour of cattle at pasture.
      ;
      • Schirmann K.
      • Chapinal N.
      • Weary D.M.
      • Heuwieser W.
      • von Keyserlingk M.A.G.
      Rumination and its relationship to feeding and lying behavior in Holstein dairy cows.
      ;
      • Gregorini P.
      • Dela Rue B.
      • Pourau M.
      • Glassey C.
      • Jago J.
      A note on rumination behavior of dairy cows under intensive grazing systems.
      ). When explicitly examining the relationship between rumination and lying time, some studies found no correlation (
      • Schirmann K.
      • Chapinal N.
      • Weary D.M.
      • Heuwieser W.
      • von Keyserlingk M.A.G.
      Rumination and its relationship to feeding and lying behavior in Holstein dairy cows.
      ), but others reported a negative correlation (
      • Stone A.E.
      • Jones B.W.
      • Becker C.A.
      • Bewley J.M.
      Influence of breed, milk yield, and temperature-humidity index on dairy cow lying time, neck activity, reticulorumen temperature, and rumination behavior.
      ). Indeed, rumination time seems best explained by the physical and chemical composition of the diet and NDF intake (
      • Beauchemin K.A.
      Invited review: Current perspectives on eating and rumination activity in dairy cows.
      ).
      Although cows often ruminate while resting (e.g.,
      • Walker S.L.
      • Smith R.F.
      • Routly J.E.
      • Jones D.N.
      • Morris M.J.
      • Dobson H.
      Lameness, activity time-budgets, and estrus expression in dairy cattle.
      ), when lying time is experimentally restricted, a larger proportion of the rumination then occurs while standing (
      • Munksgaard L.
      • Simonsen H.B.
      Behavioral and pituitary adrenal-axis responses of dairy cows to social isolation and deprivation of lying down.
      ). Similarly,
      • Cooper M.D.
      • Arney D.R.
      • Phillips C.J.C.
      Two- or four-hour lying deprivation on the behavior of lactating dairy cows.
      prevented cows lying down for a 2- or 4-h period and also observed that cows switched to ruminating while standing, but found that the duration of rumination was reduced. Three other studies have either forced cows to stand or overstocked the freestalls; none found significant changes in rumination time, although all report a numerical reduction in this behavior (
      • Munksgaard L.
      • Simonsen H.B.
      Behavioral and pituitary adrenal-axis responses of dairy cows to social isolation and deprivation of lying down.
      ;
      • Krawczel P.D.
      • Klaiber L.B.
      • Butzler R.E.
      • Klaiber L.M.
      • Dann H.M.
      • Mooney C.S.
      • Grant R.J.
      Short-term increases in stocking density affect the lying and social behavior, but not the productivity, of lactating Holstein dairy cows.
      ,
      • Krawczel P.D.
      • Mooney C.S.
      • Dann H.M.
      • Carter M.P.
      • Butzler R.E.
      • Ballard C.S.
      • Grant R.J.
      Effect of alternative models for increasing stocking density on the short-term behavior and hygiene of Holstein dairy cows.
      ). Taken together, studies suggest that, although cows mainly ruminate while lying down, they can ruminate standing up, and when lying time is reduced rumination time is not reduced to nearly the same extent, if at all. However, we have no information as to whether the effectiveness of rumination is the same when cows are lying or standing.

      Health and Biological Function—Summary and Conclusions

      The risk of lameness and hoof lesions increases with reduced lying time, but this likely depends upon the surface on which the cows are standing. Reduced time lying down can result in some changes in the endocrine systems that often respond to stress, but the effects are complex and we do not yet know the consequences of this for the welfare of the animals. There is little evidence that reduced lying time reduces milk yield or rumination, or whether this is an animal welfare issue. Based on other species, reduced lying time may have further substantial effects on animal welfare if sleep is also reduced, and we need more evidence as to whether this occurs for cows.

      ENVIRONMENTAL INFLUENCES ON LYING TIME

      The lying time of cows is affected by many housing and management factors. Given the likelihood that forced reductions in lying time can have deleterious consequences for animal welfare, aspects of farm design and management that reduce lying time should be viewed with concern.

      Type of Housing System

      Cows in tiestall and freestall systems lie down, on average, between 10 and 12 h/d, whereas cows in bedded packs, dry lots, and pasture lie for about 9 h/d (Table 1). However, the range in average lying times between individual farms that have the same type of housing system are large (e.g., 8.7 to 13.5 h/d in freestalls and 6.1 to 12.1 h/d at pasture; from Table 1). This suggests that measures of lying time on commercial farms depend greatly on management and the details of the housing system.

      Time Constraints Due to Feeding and Milking

      The extent that farm management affects the time that cows must spend in competing activities may be a considerable risk factor for reduced lying times. Feeding, milking, and waiting for access to milking can take a large amount of time (
      • Charlton G.L.
      • Haley D.B.
      • Rushen J.
      • de Passillé A.M.
      Stocking density, milking duration, and lying times of lactating cows on Canadian freestall dairy farms.
      ;
      • Beauchemin K.A.
      Invited review: Current perspectives on eating and rumination activity in dairy cows.
      ), so that the time spent in these 2 activities will likely influence lying time. Social behavior, drinking, and grooming take less time (<1 h/d;
      • Dado R.G.
      • Allen M.S.
      Variation in and relationships among feeding, chewing and drinking variables for lactating dairy cows.
      ;
      • Krohn C.C.
      Behaviour of dairy cows kept in extensive (loose housing/pasture) or intensive (tie stall) environments. III. Grooming, exploration and abnormal behaviour.
      ;
      • Huzzey J.M.
      • Von Keyserlingk M.A.G.
      • Weary D.M.
      Changes in feeding, drinking, and standing behavior of dairy cows during the transition period.
      ;
      • Cook N.B.
      • Mentink R.L.
      • Bennett T.B.
      • Burgi K.
      The effect of heat stress and lameness on time budgets of lactating dairy cows.
      ;
      • DeVries T.J.
      • Vankova M.
      • Veira D.M.
      • von Keyserlingk M.A.G.
      Short communication: Usage of mechanical brushes by lactating dairy cows.
      ;
      • Val-Laillet D.
      • Guesdon V.
      • von Keyserlingk M.A.G.
      • de Passillé A.M.
      • Rushen J.
      Allogrooming in cattle: Relationships between social preferences, feeding displacements and social dominance.
      ), and therefore we do not expect these activities to have a large effect on lying time. In addition, in some systems, cows are also restrained in headlocks while waiting for herd health checks or as part of breeding protocols, but few data are available about the variation in this practice, so although it may be a considerable time constraint for some cows, where they also have little choice in the matter, these are not well studied. Thus, we will focus on milking and feeding in our review of time constraints.
      • Friend T.H.
      • Polan C.E.
      • McGilliard M.L.
      Free stall and feed bunk requirements relative to behavior, production and individual feed intake in dairy cows.
      reported sizable negative correlations (ranging from −0.61 to −0.85) between the daily durations of feeding and lying down for cows in freestall systems, but small increases in feeding time (<1 h/d) do not result in changes in lying time (
      • Henriksen J.C.S.
      • Weisbjerg M.R.
      • Løvendahl P.
      • Kristensen T.
      • Munksgaard L.
      Effects of an individual cow concentrate strategy on production and behavior.
      ). As expected, larger increases in feeding time lead to a reduced time spent lying down.
      • Munksgaard L.
      • Herskin M.S.
      • Løvendahl P.
      • Andersen J.B.
      Effects of nutrition on stress reactivity.
      reported that cows in tiestalls fed a low-energy diet spent 6.4 h/d feeding and only 11.1 h/d lying down, whereas cows fed a high-energy diet spent 4.8 h/d feeding and 12.3 h/d lying down. The similar size changes in feeding and lying times suggest a substitution of the two.
      • Dohme-Meier F.
      • Kaufmann L.D.
      • Görs S.
      • Junghans P.
      • Metges C.C.
      • van Dorland H.A.
      • Bruckmaier R.M.
      • Münger A.
      Comparison of energy expenditure, eating pattern and physical activity of grazing and zero-grazing dairy cows at different time points during lactation.
      increased feeding time of cows from 6.6 to 8.8 h/d by placing cows on pasture for 16 to 18.5 h/d, where they had to graze rather than eat TMR. The time spent lying down was reduced, but the change (10.3 to 9.7 h/d) was much smaller than for feeding time. This may reflect the relatively low time spent lying down in this study. In some cases, the relationships between lying and feeding time can be more complex:
      • Crossley R.E.
      • Harlander-Matauschek A.
      • DeVries T.J.
      Variability in behavior and production among dairy cows fed under differing levels of competition.
      increased competition for feed by increasing the number of cows per feed bin. Increased competition reduced both feeding times and lying times, probably because the cows were spending more time waiting to get access to the feeders. Waiting to feed or searching for free space at the feed bunk is an activity that can be time-consuming, but relatively little is known about this (
      • Olofsson J.
      • Wiktorsson H.
      Competition for total mixed diets fed restrictively using one or four cows per feeding station.
      ;
      • Huzzey J.M.
      • DeVries T.J.
      • Valois P.
      • von Keyserlingk M.A.G.
      Stocking density and feed barrier design affect the feeding and social behavior of dairy cattle.
      ).
      Changing when feed is delivered can also change cow lying time. When twice-daily feeding was delayed by 6 h relative to milking,
      • DeVries T.J.
      • von Keyserlingk M.A.G.
      Time of feed delivery affects the feeding and lying patterns of dairy cows.
      found that cows spent 12.5% more time feeding in total. Delayed feeding reduced the latency to lie down after milking by 20 min, but it did not change the daily lying time.
      No studies appear to have examined the relationship between average feeding time and lying time at the farm level. We examined the relationship across different research studies that report measures of both lying time and feeding time over 24 h. Figure 2 shows the relationship between the average time cows spent lying down and the average time the cows spent feeding in both freestall and tiestall housing and at pasture.
      Figure thumbnail gr2
      Figure 2Relationship between time spent lying down and feeding for studies of cows in freestalls, in tiestalls, and at pasture (
      • Wales W.J.
      • Dellow D.W.
      • Doyle P.T.
      Protein supplementation of cows grazing limited amounts of paspalum (Paspalum dilatatum Poir.)-dominant irrigated pasture in mid lactation.
      ,
      • Wales W.J.
      • Dellow D.W.
      • Doyle P.T.
      • Egan A.R.
      Effects of feeding additional pasture hay in autumn to dairy cows grazing irrigated perennial ryegrass-white clover pasture and supplemented with barley grain.
      ;
      • Haley D.B.
      • de Passillé A.M.
      • Rushen J.
      Assessing cow comfort: Effects of two floor types and two tie stall designs on the behaviour of lactating dairy cows.
      ;
      • Fregonesi J.A.
      • Leaver J.D.
      Influence of space allowance and milk yield level on behaviour, performance and health of dairy cows housed in strawyard and cubicle systems.
      ;
      • González M.
      • Yabuta A.K.
      • Galindo F.
      Behaviour and adrenal activity of first parturition and multiparous cows under a competitive situation.
      ;
      • Thorne P.L.
      • Jago J.G.
      • Kolver E.S.
      • Roche J.R.
      Diet and genotype affect feeding behaviour of Holstein-Friesian dairy cows during late lactation.
      ;
      • Fregonesi J.A.
      • Tucker C.B.
      • Weary D.M.
      • Flower F.C.
      • Vittie T.
      Effect of rubber flooring in front of the feed bunk on the time budgets of dairy cattle.
      ;
      • DeVries T.J.
      • von Keyserlingk M.A.G.
      Time of feed delivery affects the feeding and lying patterns of dairy cows.
      ;
      • Munksgaard L.
      • Jensen M.B.
      • Pedersen L.J.
      • Hansen S.W.
      • Matthews L.
      Quantifying behavioural priorities—Effects of time constraints on behaviour of dairy cows, Bos taurus..
      ,
      • Munksgaard L.
      • Rushen J.
      • de Passillé A.M.
      • Krohn C.C.
      Forced versus free traffic in an automated milking system.
      ;
      • Kendall P.E.
      • Nielsen P.P.
      • Webster J.R.
      • Verkerk G.A.
      • Littlejohn R.P.
      • Matthews L.R.
      The effects of providing shade to lactating dairy cows in a temperate climate.
      ;
      • Tucker C.B.
      • Weary D.M.
      • de Passillé A.M.
      • Campbell B.
      • Rushen J.
      Flooring in front of the feed bunk affects feeding behavior and use of freestalls by dairy cows.
      ,
      • Tucker C.B.
      • Dalley D.E.
      • Burke J.L.K.
      • Clark D.A.
      Milking cows once daily influences behavior and udder firmness at peak and mid lactation.
      ,
      • Tucker C.B.
      • Rogers A.R.
      • Verkerk G.A.
      • Kendall P.E.
      • Webster J.R.
      • Matthews L.R.
      Effects of shelter and body condition on the behaviour and physiology of dairy cattle in winter.
      ,
      • Tucker C.B.
      • Rogers A.R.
      • Schütz K.E.
      Effect of solar radiation on dairy cattle behaviour, use of shade and body temperature in a pasture-based system.
      ,
      • Tucker C.B.
      • Lacy-Hulbert S.J.
      • Webster J.R.
      Effect of milking frequency and feeding level before and after dry off on dairy cattle behavior and udder characteristics.
      ;
      • Cook N.B.
      • Mentink R.L.
      • Bennett T.B.
      • Burgi K.
      The effect of heat stress and lameness on time budgets of lactating dairy cows.
      ;
      • Rushen J.
      • Haley D.
      • de Passillé A.M.
      Effect of softer flooring in tie stalls on resting behavior and leg injuries of lactating cows.
      ;
      • Fisher A.D.
      • Roberts N.
      • Bluett S.J.
      • Verkerk G.A.
      • Matthews L.R.
      Effects of shade provision on the behaviour, body temperature and milk production of grazing dairy cows during a New Zealand summer.
      ;
      • O'Driscoll K.
      • Boyle L.
      • Hanlon A.
      The effect of breed and housing system on dairy cow feeding and lying behaviour.
      ;
      • Collings L.K.M.
      • Weary D.M.
      • Chapinal N.
      • von Keyserlingk M.A.G.
      Temporal feed restriction and overstocking increase competition for feed by dairy cattle.
      ;
      • Schirmann K.
      • Chapinal N.
      • Weary D.M.
      • Heuwieser W.
      • von Keyserlingk M.A.G.
      Short-term effects of regrouping on behavior of prepartum dairy cows.
      ;
      • Siivonen J.
      • Taponen S.
      • Hovinen M.
      • Pastell M.
      • Lensink B.J.
      • Pyörälä S.
      • Hänninen L.
      Impact of acute clinical mastitis on cow behaviour.
      ;
      • Fogsgaard K.K.
      • Røntved C.M.
      • Sørensen P.
      • Herskin M.S.
      Sickness behavior in dairy cows during Escherichia coli mastitis.
      ;
      • Krawczel P.D.
      • Klaiber L.B.
      • Butzler R.E.
      • Klaiber L.M.
      • Dann H.M.
      • Mooney C.S.
      • Grant R.J.
      Short-term increases in stocking density affect the lying and social behavior, but not the productivity, of lactating Holstein dairy cows.
      ,
      • Krawczel P.D.
      • Mooney C.S.
      • Dann H.M.
      • Carter M.P.
      • Butzler R.E.
      • Ballard C.S.
      • Grant R.J.
      Effect of alternative models for increasing stocking density on the short-term behavior and hygiene of Holstein dairy cows.
      ;
      • Matthews L.R.
      • Cameron C.
      • Sheahan A.J.
      • Kolver E.S.
      • Roche J.R.
      Associations among dairy cow body condition and welfare-associated behavioral traits.
      ;
      • Hart K.D.
      • McBride B.W.
      • Duffield T.F.
      • DeVries T.J.
      Effect of milking frequency on the behavior and productivity of lactating dairy cows.
      ;
      • Hetti Arachchige A.D.
      • Fisher A.D.
      • Auldist M.J.
      • Wales W.J.
      • Jongman E.C.
      Effects of different systems of feeding supplements on time budgets of cows grazing restricted pasture allowances.
      ;
      • Schütz K.E.
      • Cox N.R.
      • Macdonald K.A.
      • Roche J.R.
      • Verkerk G.A.
      • Rogers A.R.
      • Tucker C.B.
      • Matthews L.R.
      • Meier S.
      • Webster J.R.
      Behavioral and physiological effects of a short-term feed restriction in lactating dairy cattle with different body condition scores at calving.
      ;
      • Dohme-Meier F.
      • Kaufmann L.D.
      • Görs S.
      • Junghans P.
      • Metges C.C.
      • van Dorland H.A.
      • Bruckmaier R.M.
      • Münger A.
      Comparison of energy expenditure, eating pattern and physical activity of grazing and zero-grazing dairy cows at different time points during lactation.
      ;
      • Kanjanapruthipong J.
      • Junlapho W.
      • Karnjanasirm K.
      Feeding and lying behavior of heat-stressed early lactation cows fed low fiber diets containing roughage and nonforage fiber sources.
      ;
      • Chen J.M.
      • Schütz K.E.
      • Tucker C.B.
      Technical note: Comparison of instantaneous sampling and continuous observation of dairy cattle behavior in freestall housing.
      ;
      • Løvendahl P.
      • Munksgaard L.
      An investigation into genetic and phenotypic variation in time budgets and yield of dairy cows.
      ;
      • Wang F.X.
      • Shao D.F.
      • Li S.L.
      • Wang Y.J.
      • Azarfar A.
      • Cao Z.J.
      Effects of stocking density on behavior, productivity, and comfort indices of lactating dairy cows.
      ;
      • Crossley R.E.
      • Harlander-Matauschek A.
      • DeVries T.J.
      Variability in behavior and production among dairy cows fed under differing levels of competition.
      ). To be included in this comparison, these 39 studies had to have measured lying and feeding time over 24 h simultaneously in the same animals.
      It is apparent from Figure 2 that grazing time of cows at pasture is more variable among studies than is feeding time of cows in either freestall or tiestall housing, and that the lowest lying times found at pasture (<9.3 h/d) occur when grazing times are longest (>7.9 h/d). Where grazing times for cows at pasture are within the range found for feeding times in tiestall and freestall housing (3.1 to 7.7 h/d), then the times spent lying down (10.4 to 12.1 h/d) are also in the same range as cows in freestalls and tiestalls (10 to 12 h/d). In support of this interpretation,
      • O'Driscoll K.
      • Gleeson D.
      • O'Brien B.
      • Boyle L.
      Effect of milking frequency and nutritional level on hoof health, locomotion score and lying behaviour of dairy cows.
      ,
      • O'Driscoll K.
      • Lewis E.
      • Kennedy E.
      Effect of feed allowance at pasture on the lying behaviour of dairy cows.
      ) report that lowering the quantity of pasture increased grazing time and reduced lying time after the morning milking. Similarly, when grazing and eating times overlap with values in tiestalls and freestalls, lying time is consistent, even if the overall feed availability spans a considerable range, between 8 and 16 kg of DM/d (
      • Hetti Arachchige A.D.
      • Fisher A.D.
      • Auldist M.J.
      • Wales W.J.
      • Jongman E.C.
      Effects of different systems of feeding supplements on time budgets of cows grazing restricted pasture allowances.
      ). Overall, these data suggest that the lower average lying times reported for cows at pasture compared with those in freestalls or tiestalls are associated with greater time spent grazing than feeding indoors.
      Less research has examined the effect of milking time.
      • Charlton G.L.
      • Haley D.B.
      • Rushen J.
      • de Passillé A.M.
      Stocking density, milking duration, and lying times of lactating cows on Canadian freestall dairy farms.
      reported that the time that cows were away from the home pen for milking differed greatly between the 111 freestall farms visited, varying from less than 1 to more than 8 h/d. Although no overall correlation was detectable between time away for milking and the daily duration of lying time, no farm with a milking time greater than 3.7 h/d had a lying time of 12 h/d or greater. Up to a milking time of 3.3 h/d, no relationship occurred between milking and lying time. However, increased milking times above 3.3 h/d were associated with a reduction in lying time, with the milking times accounting for 27% of the differences between farms in average lying time. Thus, the relationship between milking and lying time is likely to be nonlinear.
      Research that has examined patterns of individual cows also provide insight into the effects of milking time.
      • Gomez A.
      • Cook N.B.
      Time budgets of lactating dairy cattle in commercial freestall herds.
      examined the association between milking times (time away from the pen for milking) and lying times for 205 lactating cows in 16 commercial freestall herds in the US but, unlike
      • Charlton G.L.
      • Haley D.B.
      • Rushen J.
      • de Passillé A.M.
      Stocking density, milking duration, and lying times of lactating cows on Canadian freestall dairy farms.
      , reported results for individual cows. Milking time varied from 0.5 to 6.0 h/d, and an increase in milking time was associated with a 2- to 4-h/d decrease in lying time. In contrast, cows early or late in the milking order within 10 herds in Australia differed in the amount of time away from the paddock (1.4 vs. 4.5 h/d, on average), but every hour away reduced lying time by only 14 min/d (
      • Beggs D.S.
      • Jongman E.C.
      • Hemsworth P.E.
      • Fisher A.D.
      Implications of prolonged milking time on time budgets and lying behavior of cows in large pasture-based dairy herds.
      ). Time away for milking explained only 14% of the variation in lying time in this study (
      • Beggs D.S.
      • Jongman E.C.
      • Hemsworth P.E.
      • Fisher A.D.
      Implications of prolonged milking time on time budgets and lying behavior of cows in large pasture-based dairy herds.
      ). These mixed results highlight the complexity of these interactions, and other factors, such as what the cows do while standing, likely also play a role.
      Experiments that either remove or add a milking also have the potential to inform how milking influences lying time. Some experiments find that eliminating a milking—for example, from twice to once a day at peak lactation—tends to result in higher lying times at pasture (1×: 9.8, vs. 2×: 8.3 h/d;
      • Tucker C.B.
      • Dalley D.E.
      • Burke J.L.K.
      • Clark D.A.
      Milking cows once daily influences behavior and udder firmness at peak and mid lactation.
      ), but others find that this transition has no consistent effect (
      • O'Driscoll K.
      • O'Brien B.
      • Gleeson D.
      • Boyle L.
      Milking frequency and nutritional level affect grazing behaviour of dairy cows: A case study.
      ,
      • O'Driscoll K.
      • Gleeson D.
      • O'Brien B.
      • Boyle L.
      Does omission of a regular milking event affect cow comfort?.
      ). Interpretation of research that reduces milking frequency is also confounded by complications associated with changes in udder fill. When a milking is added,
      • Hart K.D.
      • McBride B.W.
      • Duffield T.F.
      • DeVries T.J.
      Effect of milking frequency on the behavior and productivity of lactating dairy cows.
      reported that cows milked 2 or 3× daily spent 11.5 to 11.7 h lying down, regardless of this management difference. These authors report that the additional third milking took only 15 min/d, so perhaps it is not unexpected that the effect on the animals' time budget was minimal.
      The animal welfare implications of these behavioral tradeoffs are dependent on (1) the degree of choice the cow has and (2) the biological implications of reduced lying time. If cows are willing to spend more time grazing and relatively less time lying, and their need to perform both behaviors is fulfilled, then there is little cause for concern. However, if cows would rather spend more time lying, if given the opportunity, if they experience hunger, or evidence indicates that their biological function is impaired (e.g., weight loss, greater risk for disease), then the lower lying times are problematic. Milking times that result in lower lying times are more problematic than tradeoffs with feeding, given that cows often do not have much choice in the matter and are standing on concrete during all (freestall, dry lots, bedded packs) or part of this time (pasture). There are likely detrimental health implications of the additional time spent standing on concrete, regardless of the reason (
      • Cook N.B.
      The impact of management and facilities on cow culling rates.
      ).

      Stall Stocking Density

      One factor that could affect the lying time of cows is the availability of a lying area (
      • Krawczel P.D.
      • Lee A.R.
      Lying time and its importance to the dairy cow impact of stocking density and time budget stresses.
      ). One controversial practice in freestall housing is overstocking, where more cows than lying stalls are present: some animal welfare standards for dairy cattle use a cutoff value of 1.2 cows per stall (
      • National Farm Animal Care Council
      Code of Practice for the Care and Handling of Dairy Cattle.
      ), and others require enough stalls for all individuals (
      • OIE
      Animal Welfare and Dairy Cattle Production Systems in the Terrestrial Animal Health Code.
      ). In several studies, the stocking density of lactating cows has been manipulated experimentally in small groups, either by preventing access to some stalls or by increasing the number of cows and keeping the number of stalls constant; the methods used achieve a similar outcome in these conditions (
      • Krawczel P.D.
      • Mooney C.S.
      • Dann H.M.
      • Carter M.P.
      • Butzler R.E.
      • Ballard C.S.
      • Grant R.J.
      Effect of alternative models for increasing stocking density on the short-term behavior and hygiene of Holstein dairy cows.
      ). These studies show that with increasing stocking density (cows per lying stall), the total lying time decreases, although the level of the effect varies from study to study (mean values from available experimental studies on lactating cows are summarized in Figure 3).
      Figure thumbnail gr3
      Figure 3Relationship between stocking density (number of cows per freestall) and lying time (ratio of time relative to a 1:1 cow-to-stall control) relative to values when there was a 1:1 ratio of cows to stalls. Eight studies focused on lactating dairy cows, stocking density of freestalls, and lying behavior are shown; values from the same citation represent treatments within each.
      All studies find that average lying time within the herd is reduced when stocking density is above 1.2 cows per lying stall, but in the studies that have looked at stocking densities between 1.0 and 1.2 cows per stall, conflicting results are reported: most report no reduction in lying time (
      • Friend T.H.
      • Polan C.E.
      • McGilliard M.L.
      Free stall and feed bunk requirements relative to behavior, production and individual feed intake in dairy cows.
      ;
      • Hill C.T.
      • Krawczel P.D.
      • Dann H.M.
      • Ballard C.S.
      • Hovey R.C.
      • Falls W.A.
      • Grant R.J.
      Effect of stocking density on the short-term behavioural responses of dairy cows.
      ;
      • Krawczel P.D.
      • Klaiber L.B.
      • Butzler R.E.
      • Klaiber L.M.
      • Dann H.M.
      • Mooney C.S.
      • Grant R.J.
      Short-term increases in stocking density affect the lying and social behavior, but not the productivity, of lactating Holstein dairy cows.
      ), but others (
      • Fregonesi J.A.
      • Tucker C.B.
      • Weary D.M.
      Overstocking reduces lying time in dairy cows.
      ) do find one. However, some studies have found that lying time continues to increase with understocking, or less than 1.0 cow per lying stall (
      • Telezhenko E.
      • von Keyserlingk M.A.G.
      • Talebi A.
      • Weary D.M.
      Effect of pen size, group size, and stocking density on activity in freestall-housed dairy cows.
      ;
      • Lobeck-Luchterhand K.M.
      • Silva P.R.B.
      • Chebel R.C.
      • Endres M.I.
      Effect of stocking density on social, feeding, and lying behavior of prepartum dairy animals.
      ;
      • Winckler C.
      • Tucker C.B.
      • Weary D.M.
      Effects of under-and overstocking freestalls on dairy cattle behaviour.
      ;
      • Cortés Fernández de Arcipreste N.
      • Mancera K.F.
      • Miguel-Pacheco G.G.
      • Galindo F.
      Plasticity and consistency of lying and ruminating behaviours of heifers exposed to different cubicle availability: A glance at individuality.
      ), so we find reasons to be skeptical of the assumption that stocking density can be increased to 1.2 cows per stall without negative effects on lying time.
      We note several caveats in interpreting the results of these studies. First, the average lying times of the entire herd may not give the whole picture of the effects of overstocking: lying times of subordinate cows may be most reduced, because they are more likely to be displaced from stalls (
      • Friend T.H.
      • Polan C.E.
      • McGilliard M.L.
      Free stall and feed bunk requirements relative to behavior, production and individual feed intake in dairy cows.
      ;
      • Fregonesi J.A.
      • Tucker C.B.
      • Weary D.M.
      Overstocking reduces lying time in dairy cows.
      ).
      • Friend T.H.
      • Polan C.E.
      • McGilliard M.L.
      Free stall and feed bunk requirements relative to behavior, production and individual feed intake in dairy cows.
      reported more variability in lying time as stocking density increased (≥1.2) and found a positive correlation between lying time and social dominance. Furthermore, cows were displaced from stalls more at high stocking densities. It may also be misleading to look only at total lying time over 24 h. For example,
      • Hill C.T.
      • Krawczel P.D.
      • Dann H.M.
      • Ballard C.S.
      • Hovey R.C.
      • Falls W.A.
      • Grant R.J.
      Effect of stocking density on the short-term behavioural responses of dairy cows.
      reported that lying at certain times of the day was reduced by overstocking, even if average daily lying times was not affected. Similarly,
      • Winckler C.
      • Tucker C.B.
      • Weary D.M.
      Effects of under-and overstocking freestalls on dairy cattle behaviour.
      found that cows that were less successful in gaining access to stalls used them more during the day, compared with more successful cows, indicating that they shifted how they used this resource. Although the direct effect of stocking density on sleep is not known, a greater proportion of cattle sleep occurs at night (
      • Ruckebusch Y.
      Feeding and sleep patterns of cows prior to and post parturition.
      ;
      • Ternman E.
      • Pastell M.
      • Agenäs S.
      • Strasser C.
      • Winckler C.
      • Nielsen P.P.
      • Hänninen L.
      Agreement between different sleep states and behaviour indicators in dairy cows.
      ,
      • Ternman E.
      • Pastell M.
      • Hänninen L.
      • Agenäs S.
      • Nielsen P.P.
      First-night effect on sleep time in dairy cows.
      ,
      • Ternman E.
      • Nilsson E.
      • Nielsen P.P.
      • Pastell M.
      • Hänninen L.
      • Agenäs S.
      Rapid eye movement sleep time in dairy cows changes during the lactation cycle.
      ) and could be disproportionally affected if lying time at this time was displaced. Finally, the way that stall stocking density is manipulated may also have an effect. Most researchers increased stocking density by blocking access to certain stalls, which means the results are not affected by group size or by changes in stocking rate at the feed bunk. However, in reality, higher stocking density on commercial farms is likely to be achieved by adding more cows to large groups, which involves changes in space availability, not only in the stalls but also in the alleyways and at the feed bunk.
      Comparisons among farms in stocking density do not find the relationship with average lying time seen in the experimental studies.
      • Deming J.A.
      • Bergeron R.
      • Leslie K.E.
      • DeVries T.J.
      Associations of housing, management, milking activity, and standing and lying behavior of dairy cows milked in automatic systems.
      report no relationship between stocking density and lying time on 13 Canadian herds using automatic milking systems.
      • Charlton G.L.
      • Haley D.B.
      • Rushen J.
      • de Passillé A.M.
      Stocking density, milking duration, and lying times of lactating cows on Canadian freestall dairy farms.