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Dairy Cow Behavior andWelfare Implications of TimeWaiting Before Entry Into theMilking ParlorChristian Dijkstra a , Imbi Veermäe b , Jaan Praks b ,Väino Poikalainen b & David R. Arney ba Van Hall Instituut , Leeuwarden , The Netherlandsb Institute of Veterinary Medicine and AnimalSciences, Estonian University of Life Sciences ,Tartu , EstoniaPublished online: 25 Sep 2012.

To cite this article: Christian Dijkstra , Imbi Veermäe , Jaan Praks , Väino Poikalainen& David R. Arney (2012) Dairy Cow Behavior and Welfare Implications of Time WaitingBefore Entry Into the Milking Parlor, Journal of Applied Animal Welfare Science, 15:4,329-345, DOI: 10.1080/10888705.2012.709137

To link to this article: http://dx.doi.org/10.1080/10888705.2012.709137

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JOURNAL OF APPLIED ANIMAL WELFARE SCIENCE, 15:329–345, 2012Copyright © Taylor & Francis Group, LLCISSN: 1088-8705 print/1532-7604 onlineDOI: 10.1080/10888705.2012.709137

Dairy Cow Behavior and WelfareImplications of Time Waiting Before

Entry Into the Milking Parlor

Christian Dijkstra,1 Imbi Veermäe,2 Jaan Praks,2

Väino Poikalainen,2 and David R. Arney2

1Van Hall Instituut, Leeuwarden, The Netherlands2Institute of Veterinary Medicine and Animal Sciences, Estonian

University of Life Sciences, Tartu, Estonia

The objective of this study was to investigate dairy cows’ time spent in the possibly

stressful waiting area (WA) of the milking parlor (MP) and their behavioral patterns

while there and thereby investigate comparative effects on their welfare. The

experiments were carried out in 3 loose-housing cowsheds. The study consisted

of a total of 3,522 observations of individual dairy cows. Depending on the group

size and the number of places in the MP, cows’ waiting times in the WA were

as high as 1:42:22 (h:mm:ss). In Cowsheds I and II, only one third of cows were

observed ruminating in the WA, and up to 52% of cows were observed ruminating

in the WA of Cowshed III where the feeding group size was the smallest, waiting

time the shortest, and space per cow the largest. Cows spending more time in the

WA have limited opportunities to behave normally; therefore, the welfare of these

cows in particular is poor.

Current trends in intensive cattle production are toward higher milk production,larger dairy herds, the introduction of advanced and automated technical so-lutions, and a more business-oriented farm management style (Hultgren, 2003;Noordhuizen & Cannas da Silvia, 2007). These trends are extant in Estonia. Thedevelopment of the loose housing of large dairy cattle herds has increased rapidly

Correspondence should be sent to David R. Arney, Institute of Veterinary Medicine and AnimalSciences, Estonian University of Life Sciences, Kreutzwaldi 62, 51014 Tartu, Estonia. Email:david.arney@emu.ee

329

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330 DIJKSTRA ET AL.

in Estonia since the 1990s (Veermäe, Poikalainen, & Praks, 2001). The first largecowshed was introduced in 2002, and by 2010 one third of all dairy cows werekept in cowsheds with more than 300 dairy cows. There are several studies thatexamine the impacts on the welfare of the dairy cows under different housingtypes (Fregonesi & Leaver, 2001; Haley, Rushen, & de Passillé, 2000), but theeffect of enforced waiting times before entering the milking parlor (MP) hasbeen neglected. In these large loose-housing systems, cows often have to wait,standing for long periods of time in confined areas before entering the MP. This islikely to be a stressful environment for them; feeding and drinking behaviors areexcluded, cows cannot lie down, and locomotion activity is severely restricted.The environment is likely to be socially disruptive; the cows are forced intoclose proximity with each other, and there are no possibilities for low-rankingcows to avoid aggressive conspecifics or to leave the area. Indeed, Lexer, Hagen,Palme, Troxler, and Waiblinger (2009) surmised from their work that herdingand standing in the waiting area (WA) were responsible for the higher fecalcortisol levels collected in parlor-milked nonhuman animals than in robotic-milked animals. This waiting period can be in excess of 1 hr at each milking.If cows are being milked twice or even three times a day, this has a significantnegative impact on their daily budget of behavior; some behaviors (that the cowswould ordinarily express) may therefore be sacrificed from their daily repertoire.The frustration implicit in their inability to carry out these desired behaviors maybe considered a source of stress and therefore an impairment to their welfare(Veermäe, Kaihilahti, Praks, & Poikalainen, 2003), and it has been noted byCooper, Arney, and Phillips (2007) that cows experience discomfort when theyare forced to stand for long periods. The time that cows spend lying, as opposedto standing is of interest both from the cow’s and the dairy farmer’s points ofview (Österman & Redbo, 2001). High-producing dairy cows spend about 40%to 50% of the day lying down, and adequate rest is necessary to ensure highproduction (Rushen & Passillé, 1999). Blood flow to the udder doubles whencows are lying down, and because cows tend to ruminate for longer periodswhen lying down compared with when they are standing up, maximizing thetime spent lying down is important for optimizing rumination time (Rushen &Passillé, 1999). The time spent lying is normally approximately 7 to 10 hr a dayfor lactating dairy cows, in approximately five periods of 1.5 hr each (Arave& Walters, 1980). The preferred lying time for cattle is 10 hr per day (Cooperet al., 2007).

Extended periods without access to feed may reduce intakes and possiblyproduction. Housed cattle will typically eat forage (silage or hay) in bouts of 6to 12 meals per day for a total of 4 to 7 hr per day. However, providing onlythis amount of time for the cows to eat will reduce the intake by up to 20%,demonstrating the requirement to spread feeding bouts throughout the day forcattle (Campling & Morgan, 1981).

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IMPLICATIONS OF WAITING TIME BEFORE MILKING 331

A prominent feature of the social system of dairy cattle is the consistencyof order of entry into the MP (Grasso, De Rosa, Napolitano, Di Francia, &Bordi, 2007; Rathore, 1982). High-dominance animals tend to walk at the frontof the herd and get milked first, whereas more submissive animals tend towalk at the rear of the herd and get milked last. The dominance structureof dairy cows has been shown to remain stable throughout the course of alactation (Polikarpus, Kaart, Kokin, Veermäe, & Poikalainen, 2011; Sauter-Louis, Chesterton, & Pfeiffer, 2004). Submissive cows are therefore forced tospend more time waiting for milking. An uncharacteristically late entry into theparlor can also be related to health problems. Rathore (1982) reported that cowsentering the MP earlier had lower somatic cell counts than cows coming later.Grasso et al. (2007) observed a significant correlation between entrance orderand milk yield in primiparous animals. This result was attributed to the highersomatic cell counts observed in more productive subjects, which may determinestress during farming routines (Grasso et al., 2007). Juarez, Robinson, DePeters,and Price (2003) found that return time from MP (i.e., time after the first cowreturned from the MP) tended to increase linearly as the locomotion scores ofcows increased (a higher locomotion score represented increased severity oflameness). Based on the multivariate model, Sauter-Louis et al. (2004) found anincreased likelihood of lameness for cows who walked or were milked amongthe last quarter of the individuals of the herd (odds ratios D 1.8 and 1.5,respectively).

Individual cows may find milking either a positive or negative experience,but overall the motivation to be milked may be weak. Food is significantlymore rewarding than milking (Melin, Hermans, Pettersson, & Wiktorsson, 2006;Prescott, Mottram, & Webster, 1998). Gere and Hamar (2003) compared thebehaviors of Holstein-Friesian cows when entering the MP and at the feedingtrough; there was no correlation between the entrance order to the MP andthe dominance order at the feeding trough, but there is no reason to supposethat these two resources result in the same social hierarchical arrangement.Indeed, the competitiveness of individual cows in a herd will depend upon theirindividual motivation for a resource as well as their social position (Val-Laillet,Guesdon, von Keyserlingk, de Passillé, & Rushen, 2009; Val-Laillet, Veira, &von Keyserlingk, 2008).

This study was designed to observe the behavior of cows waiting to enter theMP and consider its implications for the welfare of the animals, particularly forthose cows who entered the parlor later than their herdmates and therefore spentthe longest time in enforced restrictive conditions in the WA. This study focusedon the time schedule of cows in the WA and MP, their behavioral patterns, andtheir actual and potential propensity to behave naturally, with the hypothesisbeing that dairy cows in the WA of the MP are likely to engage in abnormalbehavior.

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332 DIJKSTRA ET AL.

METHODS

Cowsheds and Animals

The experiments were carried out on three relatively newly constructed largeloose-housing cubicle cowsheds located in northern and central Estonia duringthe early winter period in October, November, and December 2004.

There were 519 dairy cows in Cowshed I, with a mean annual milk productionof 6,374 kg per cow. The lactating cows (Estonian Holstein breed) were dividedinto four feeding groups according to milk yield and milked in a 2 � 12 DeLavaltandem MP twice per day (milking periods from 05:00–12:00 and 17:00–24:00).The size of the WA for the MP was 172 m2, a mean initial space per cow of1.5 m2. The WA flooring was made of grooved concrete.

There were 561 dairy cows in Cowshed II, with a mean annual milk pro-duction of 7,916 kg per cow. Lactating cows (including individuals from bothEstonian Holstein and Estonian Red breeds) were divided into two feedinggroups (according to milk yields) and milked in a 2 � 20 Strankgo tandemMP three times per day (milking periods from 02:00–07:00, 11:00–16:00, and18:00–22:00). The size of the WA for the MP was 196 m2, a mean initial spaceper cow of 1.1 m2. The WA flooring was made of grooved concrete.

There were 693 dairy cows in Cowshed III (including individuals from bothEstonian Holstein and Estonian Red breeds) divided into five feeding groups(according to milk yield), with a mean annual milk production for the wholeherd of 7,675 kg per cow. Cows were milked in a 2 � 12 DeLaval tandemMP three times per day (milking periods from 03:00–09:00, 11:00–17:00, and19:00–24:00). The size of the WA for the MP was 140 m2, an initial mean spaceper cow of 1.9 m2. The WA flooring was made of grooved concrete.

An automated crowd gate was used to encourage cows to enter the MP fromthe WA in all farms.

Experiment Layout

In each cowshed, behavioral observations were carried out in the WA overthree milking periods on three consecutive days (Cowshed I during the morningmilking from 05:00–midday; Cowsheds II and III during the midday milkingfrom 11:00–16:00 and from 11:00–17:00, respectively; Table 1).

Cow groups were defined as follows (Figure 1):

Feeding group (FG)—this group has a fixed size and is housed and fedseparately in the cowshed. All of the members of an FG enter the waitingarea (WA) at the same time.

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IMPLICATIONS OF WAITING TIME BEFORE MILKING 333

TABLE 1

Experimental Layout

Observed Over

Three Observations

Cowshed Cows FGs

Mean

FG Size

MP

Size FGs WGs MGs Cows

Cowshed I 519 4 115 24 12 52 121 1,388Cowshed II 561 2 177 40 6 31 54 1,062Cowshed III 693 5 70 24 15 49 91 1,072

Total 33 132 266 3,522

Note. FG D feeding group; MP D milking parlor; WG D waiting group; MG D milking group.

Milking group (MG)—a group of cows on either the left or right side of themilking parlor (MP) during one milking session.

Milking session—time of milking each left and right MG in the MP in min,numbered consecutively.

FIGURE 1 Gray animals are from a single feeding group: waiting for milking (W),milking (M), and returning from the parlor to the feeding area (F). Black animals representthe following feeding groups, entering the waiting area (WA): (1) milking parlor, (2) WA,(3) alley to the cowshed, (4) alley to the WA, (5) area of WA left by movable barrier, (6) alleyto the waiting area, part II after turnout.

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334 DIJKSTRA ET AL.

FIGURE 2 (A) The number of cows in the waiting group (Cowshed I, milking four feedinggroups [FG]). (B) Cows’ waiting time in the waiting area (Cowshed I, milking four FG).

Waiting group (WG)—a group of cows in the WA during each milking. Thenumber of cows in the WA decreases at a regular time interval while thecows enter the MP from the WA. Different-size WGs are indicated byorder numbers (Figure 2).

Data Collection

Data collection took place during the daily milking management routine. Thefollowing data were recorded during investigation of the cows’ milking sched-ules:

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IMPLICATIONS OF WAITING TIME BEFORE MILKING 335

� Time when the first cow of each FG entered the WA (h:mm:ss);� Time when the last cow of each FG entered the WA (h:mm:ss);� Time when the first cow of the MG entered the MP, left and right side

separately (h:mm:ss);� Time when the last cow of the MG entered the MP, left and right side

separately (h:mm:ss);� Time when the cows left the MP, left and right side separately (h:mm:ss);� Number of cows in the WA during each milking session (size of WG); and� Number of cows in the MG.

Cow activities were defined as follows (according to Hurnik, Webster, & Siegel,1995):

Aggression: Any purposive action of an organism toward another organismwith the actual or potential result of harming, limiting, or depriving it.

Curiosity: A tendency to approach and investigate novel stimuli or situationsand become familiar with their attributes or implications.

Grooming: An act of integumentary care (e.g., licking, scratching) to removeparasites, smooth ruffled fur, remove dirt, and so on. Grooming is sub-divided into self-grooming (an animal grooming himself or herself) andallogrooming (an animal grooming another animal).

Mounting: The act of an animal raising the anterior part of his or her bodygenerally onto the posterior part of another animal.

Rumination: The process of digestion of ruminants whereby the animal swal-lows food quickly and then regurgitates and chews it more thoroughly ata later time until digestion is completed (Morris, 1992).

Vocalization: Production of sounds by the vibration of vocal cords in thelarynx.

Cows’ activities (aggression, curiosity, grooming and allogrooming, mounting,vocalizing, and falling over) were registered continuously from the time thefirst cow entered the WA. The number of ruminating cows was recorded every10 min. All observations were made by a single observer, observing the WAfrom a raised platform on the far side of the WA of the MP.

Statistical Analysis

The following data were collected for statistical analysis:

� WA entering time of the FG: (time when the last cow of the FG enteredthe WA) � (time when the first cow of the FG entered the WA), mm:ss;

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336 DIJKSTRA ET AL.

� Waiting time in the WA of the WG: [(time when the first cow of the leftside MG entered the MP) C (time when the first cow of the right side MGentered the MP)]/2 � (time when the first cow of the FG entered the WA),h:mm:ss;

� MP entering time of the MG: (time when the last cow of the MG enteredthe MP) � (time when the first cow of MG entered the MP), mm:ss;

� MP time of the MG: (time when cows leave the MP) � (time when thelast cow of MG entered the MP), mm:ss;

� Cows’ behaviors were calculated as a percentage of each behavior engagedin by all of the animals in each WG and FG; and

� Rumination was assessed as the percentage of ruminating animals in theWG.

Data were managed and descriptive statistics calculated with MS Excel andstatistical package SAS 9.1 for multiple comparison analysis. Behavioral datawere calculated for each WG—the cow group in the WA during a milkingsession. To compare different WG cows’ behaviors (percentages of cows en-gaged in a specific behavior), multiple comparisons were used. The referencemethod used was the Wilcoxon test, two-sided with a t distribution approx-imation.

RESULTS

As expected, the number of cows in the WA decreased with time in relation toMP size, whereas the waiting time increased according to the MP size (Figure 2).Statistical data on the cow groups’ time schedules are shown in Table 2.

The time schedule depended both on the FG and MG sizes. However, therewere also differences between the cowsheds. Mean WA entering time dependedon the group size and the distance between the FG location in the cowshedand the WA. FG entering time to the WA varied from 2:13 to 21:15 (mm:ss).The extent of the difference in waiting time varied greatly—from 01:01 (mm:ss)to 1:58:45 (h:mm:ss), depending on the milking session. MG entering time tothe MP ranged from 3 s (2 cows in the last MP group, Cowshed I) to 07:02(mm:ss)—for the first MG in Cowshed I.

The percentage of cows ruminating in the WA increased in all cowsheds asmilking proceeded. About one third of all cows were observed ruminating in theWA in Cowsheds I (32.1%; Figure 3) and II (36.7%) and 52.8% in Cowshed III.There were significant differences between rumination observations in differentWGs in all three cowsheds (p value of multiple comparisons of ruminationmeans <.05).

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TA

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mm

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0:21

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0:43

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1

No

te.

WA

Dw

aiti

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ea;

FG

Dfe

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ggr

oup;

WG

Dw

aiti

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MP

Dm

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GD

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p.

337

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338 DIJKSTRA ET AL.

FIGURE 3 (A) Total number and number of ruminating cows in the waiting area (WA)by waiting group (WG) number (Cowshed I). (B) Regression of percentage of ruminatingcows in the WA by WG (Cowshed I).

The activity of cows in the WA was low in all cowsheds. Less than 2% of allcows were engaged in any of the recorded activities except for curiosity, whichwas 8% in Cowshed III (Figure 4).

The mean numbers of cows in the WA and activities according to the WGnumber are shown in Table 3.

The number of aggressions was highest in Cowshed I where 1.4% of the cowsin the second WG acted aggressively toward another cow. Allogrooming wasnot observed in the last WG in each cowshed, and aggression was not observedin these final WGs. During the observation period, the only few incidents of

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IMPLICATIONS OF WAITING TIME BEFORE MILKING 339

FIGURE 4 Cow activities in the waiting area.

individuals falling over were observed in Cowshed III where the cows had beenhoused together for only 1 month.

The cows in the last WGs performed more curiosity (p D .02) and grooming(p D .04) activities. Mounting (p D .13) and vocalization (p D .13) activitieshad a tendency to decrease with time in the WA.

DISCUSSION

Being among the first cows to be milked gave certain advantages to the cows:In addition to spending less standing time in the WA, after returning to theempty cowshed, all cubicles and access to the feeding barrier were freelyavailable. Cows in the WA did not have opportunities to lie down, drink, oreat. Limited space per cow (at the beginning of milking a maximum of 3 m2 inthe WA) inhibited locomotion and social activity, as has been reported elsewhere(Dijkstra, Veermäe, Praks, & Poikalainen, 2007).

The cows’ opportunities for normal behavior in the WA were limited in allcowsheds (Table 3 and Figure 4). The most prevalent activity was rumination(Table 3 and Figure 3). According to Lidfors (1996), rumination accounts fora substantial part of a cow’s daily activities, altogether for about 6 to 8 hrperformed in about eight bouts of about 45 min each day. Rumination is oftenassociated with reduced alertness and its rhythmic action may induce a soporific

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TA

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Cow

Activitie

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IMPLICATIONS OF WAITING TIME BEFORE MILKING 341

or even hypnotic effect on the animal. Only healthy and unstressed cattle willruminate normally (Dado & Allen, 1994; Lidfors, 1996). In the current study,up to 52% of cows were observed ruminating in the WA of Cowshed III wherethe FG size was the smallest, waiting time the shortest, and space per cowthe largest. In Cowsheds I and II, only one third of cows ruminated in theWA. This low proportion of ruminating cows in the WA perhaps indicated anenvironment that was found to be stressful. The percentage of cows ruminatingin the WA increased in all cowsheds as milking proceeded. As the WG becamedepleted over time, the social environment changed, and it might therefore bethe case that as the WG becomes smaller, there are fewer stressor animals andthe remaining animals become less stressed. Indeed, the reduced number ofaggression events in the WA over time support this. Nevertheless, ruminationremained suboptimal, and having an extended period of time where the cowsremain in the constrictive and restrictive environment of the WA remains aconcern for good welfare. In this study, the cows were not identified individually.Therefore, it is not possible to say whether more cows started to ruminate inthe WA as time progressed or if the cows who ruminated were ruminatingthroughout the waiting period and were among those cows who happened toremain in the last MGs.

It is also not possible to distinguish between the cows from different MGsin the WA prior to the MG separating itself from the rest in the WA. We couldnot know which cows were leaving the WA for the MP until they actually didso. Therefore, the results of these observations represent a “substructed” image:the influence of an MG could only be estimated by observing the change inbehavior of the remaining cows once the MG had left the WA.

Despite some increase in space per cow (from 2–3 m2 to 4–5 m2), thecows’ activities remained low. The same behaviors and pattern of changes inbehaviors were observed in all cowsheds. The cows’ social activity (when twocows were involved) decreased. The number of aggressions and allogroomings(submissive cows’ behavior toward dominant cows) was reduced; there wereno allogroomings or aggressions among the final WGs. The same trend wasobserved for mounting and vocalization activities (except for mounting activityin Cowshed II, which remained unchanged). At the same time, curiosity andgrooming activities increased. Curiosity, or seeking behavior, has been identifiedpreviously from substantial neurological studies of mammals with a positiveemotional state (Panksepp, 2005). Grooming is a social behavior. It may bethat the first MGs were comprised of more socially extroverted animals andthat they were individuals who communicated more and also expressed moreof the other social behaviors. The last WA cows, who regularly had to wait formilking for several hours each day, were more intraverted animals. They engagedin less social behavior; rumination, curiosity, and self-grooming activities weredominant.

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In a previous study (Veermäe et al., 2003), cows entering the MP laterspent less time throughout the day feeding and less time lying. The cows whospend longer in the WA before milking therefore spend less time exhibitingnormal behavior. Production and welfare are impaired if they are sacrificingsome of their feeding time. The current study is limited in that behavior withoutthe MP was not considered. The experiment was designed with studying themilking parlor waiting area as the main objective, so predictions about conse-quences for intake and lying times upon returning to the cubicle areas are largelysurmise.

Haskell, Rennie, Bowell, Wemelsfelder, & Lawrence (2003) developed awelfare evaluation project that focused on younger cows: “Our main hypothesisis that the behavioral and physical responses of ‘at-risk’ younger cows providea sensitive indication of farm-level ‘stress’ ” (p. 554). However, our proposal isthat, in the evaluation of welfare, it is better to focus on the idea that the cowsin the last MGs are more at risk of suffering and are therefore more sensitiveindicators of farm-level stress for the following reasons:

� Milking order stability selects these cows into the last MG,� The last cows in the WA are often submissive cows,� Cows with health problems (lameness and udder diseases) tend to move

(or be forced) into later entry groups than their usual groups,� The cows’ possibilities to express normal behavior in the WA are very

limited,� Time in the WA is related to fewer possibilities for eating and lying in the

cowshed, and� Submissive cows are unable to avoid the stressful situation by rapidly

removing themselves from it.

It may therefore be concluded that cows in large groups perform “self-evaluation,” which occurs in the WA and is reflected in the milking order. Fromthe viewpoint of welfare, the WA is a critical factor in the management of largeloose-housing cowsheds. Cows who are more or less voluntarily joining thelast MG can be considered among the lowest social rank in the group. Theiropportunities to perform normal behavior are the most limited, and therefore itmay be better to focus welfare evaluations on this group of animals. Assessingthe welfare of the herd as a whole may discount the suffering of a significantportion of the herd. In the context of developments in the management of themilking process, and perhaps with particular reference to precision livestockfarming, efforts should be concentrated on the assessment of the welfare ofthese animals in particular and on reducing the period of waiting that cows mustendure prior to milking.

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CONCLUSIONS

Some cows spend long periods, up to 100 min at each milking, in the WAbefore entering the MP. The dairy cows’ time schedule in the WA depends onthe management of the milking process as well as the FG and MG sizes. Cowswere observed ruminating most frequently in the WA of Cowshed III where theFG size was the smallest, waiting time the shortest, and space per cow the largest.The percentage of cows ruminating in the WA increased in accordance with thedecrease in the WG size, whereas the percentages of vocalization, mounting,allogrooming, and aggression decreased, suggesting that as the WA lost somecows, the social environment became less of a source of stress for the remainingcows. Cows in the last MGs have fewer opportunities to express normal behaviorand are confined for longer periods each day, spending more of their time ina stressful environment. It is therefore reasonable to focus on these cows inwelfare evaluations of dairy cows in general but also in light of the introductionof new technologies in the milking process. If we assess the welfare of thisvulnerable group in a dairy management system positively, it may be sufficientto make an accurate positive assessment of the well being of the whole herdand likewise with a negative welfare assessment. If we make assessments on theobservations of the whole herd and use mean values for our assessments, wemay miss the hidden suffering of an overlooked portion of the herd.

ACKNOWLEDGMENTS

This research was supported by the Estonian Science Foundation Grant 7518and Interreg project Energy Positive Farm (ENPOS). We are most grateful forthe collaboration with owners and staff of the farms, who kindly permitted us tocarry out the experiments for this study. We also thank Mirjam Vallas for helpwith statistical analysis.

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