Dairy cows seek isolation at calving and when ill

Abstract

Dairy cows are typically gregarious, but isolate themselves in the hours before calving when kept on pasture. Self-isolation is also a common behavior of ill animals. The objectives of this study were to determine if dairy cows would (1) isolate to calve when housed indoors in an individual maternity pen and (2) continue to isolate when ill after calving. We selected individuals from a pool of 79 multiparous Holstein dairy cows based on inclusion criteria created to address each objective. Cows were moved from a group pen to 1 of 10 adjacent maternity pens. Half of these individual pens were partially covered with plywood, creating a secluded corner as well as a window that provided visual access to the group pen. The other individual pens were uncovered on all sides. For our first objective, we selected 39 cows that were moved into the maternity pens >8 h before calving (partially covered: n = 19; uncovered: n = 20). For our second objective, we selected 18 cows housed in the partially covered pens: 9 cows with high rectal temperature after calving and signs of an infectious disease (mastitis, metritis, pneumonia, or some combination), and 9 healthy cows paired with ill cows based on the amount of time they spent in the maternity pen before calving. Ten-minute scan sampling was used to record the location and lying time from 6 h before to 72 h after calving. Individual feed intake was measured after calving. Binomial tests were used to determine if cows in both pen types were more likely to calve in the corner or window side of the pen. Repeated-measures ANOVA were used to determine if cows used the corner more as calving approached and if ill cows spent more time lying or more time in the corner compared with healthy cows in the 72 h after calving. Cows in the uncovered pens were equally likely to calve on both sides of the pen (10 vs. 10), but 79% of cows in the partially covered pens calved on the corner side of the pen (15 vs. 4). Cows in the partially covered pens used the corner side of the pen more in the 1 h before and after calving compared with those housed in the uncovered pens. Ill cows housed in the partially covered pens ate less, tended to spend more time lying down, and spent more time in the corner of the pen compared with healthy cows. These results indicate that periparturient dairy cows seek seclusion to calve and when ill, which suggests that adding a secluded area to maternity and hospital pens may be beneficial.

Full text

2731
J. Dairy Sci. 97 :2731–2739
http://dx.doi.org/ 10.3168/jds.2013-7274
© American Dairy Science Association®, 2014 .
ABSTRACT
Dairy cows are typically gregarious, but isolate them-
selves in the hours before calving when kept on pasture.
Self-isolation is also a common behavior of ill animals.
The objectives of this study were to determine if dairy
cows would (1) isolate to calve when housed indoors in
an individual maternity pen and (2) continue to isolate
when ill after calving. We selected individuals from a
pool of 79 multiparous Holstein dairy cows based on
inclusion criteria created to address each objective.
Cows were moved from a group pen to 1 of 10 adjacent
maternity pens. Half of these individual pens were par-
tially covered with plywood, creating a secluded corner
as well as a window that provided visual access to the
group pen. The other individual pens were uncovered
on all sides. For our first objective, we selected 39 cows
that were moved into the maternity pens >8 h before
calving (partially covered: n = 19; uncovered: n = 20).
For our second objective, we selected 18 cows housed
in the partially covered pens: 9 cows with high rectal
temperature after calving and signs of an infectious
disease (mastitis, metritis, pneumonia, or some combi-
nation), and 9 healthy cows paired with ill cows based
on the amount of time they spent in the maternity pen
before calving. Ten-minute scan sampling was used to
record the location and lying time from 6 h before to
72 h after calving. Individual feed intake was measured
after calving. Binomial tests were used to determine if
cows in both pen types were more likely to calve in the
corner or window side of the pen. Repeated-measures
ANOVA were used to determine if cows used the corner
more as calving approached and if ill cows spent more
time lying or more time in the corner compared with
healthy cows in the 72 h after calving. Cows in the
uncovered pens were equally likely to calve on both
sides of the pen (10 vs. 10), but 79% of cows in the
partially covered pens calved on the corner side of the
pen (15 vs. 4). Cows in the partially covered pens used
the corner side of the pen more in the 1 h before and
after calving compared with those housed in the uncov-
ered pens. Ill cows housed in the partially covered pens
ate less, tended to spend more time lying down, and
spent more time in the corner of the pen compared with
healthy cows. These results indicate that periparturient
dairy cows seek seclusion to calve and when ill, which
suggests that adding a secluded area to maternity and
hospital pens may be beneficial.
Key words: transition , sickness behavior , parturition
INTRODUCTION
As herd animals, dairy cows typically synchronize
their behaviors and rarely stray from the protection
of the group (Miller and Wood-Gush, 1991). However,
this behavior can change as the time of calving ap-
proaches. Domesticated cows kept on pasture often
leave the herd to calve (Lidfors et al., 1994), and at
least some wild ungulates (e.g., bison: Lott and Gal-
land, 1985; elk: Barbknecht et al., 2011) show similar
self-isolation behavior.
Self-isolation in cattle may not be unique to parturi-
tion. In laboratory rodents, isolation is a common sign
of illness (Crestani et al., 1991; Arakawa et al., 2010).
Dairy cows are at high risk of disease after calving (In-
gvartsen, 2006) and behavior is becoming increasingly
recognized as useful for identifying ill animals (reviewed
by Weary et al., 2009). Recent studies have determined
that feeding and standing behaviors can identify cows
at risk for postpartum disease (reviewed by Sepúlveda-
Varas et al., 2013). To our knowledge, no research has
determined whether cows will isolate themselves when
ill.
On many commercial dairy farms cows are given
little opportunity to isolate when calving or when ill.
Management and housing of cows at calving and dur-
ing illness is highly variable; cows are typically either
housed in group pens or individual maternity or hos-
pital pens (e.g., Fogsgaard et al., 2012a). Individual
pens are often in high-traffic areas, allowing producers
easy access to monitor ill and calving cows. In the cur-
rent study, we modified an individual pen to allow cows
Dairy cows seek isolation at calving and when ill
K. L. Proudfoot ,*† M. B. Jensen ,‡ D. M. Weary ,* and M. A. G. von Keyserlingk *1
* Animal Welfare Program, Faculty of Land and Food Systems, University of British Columbia, 2357 Main Mall, Vancouver, British Columbia,
V6T 1Z4, Canada
† Department of Veterinary Preventive Medicine, College of Veterinary Medicine, The Ohio State University, Columbus 43210
‡ Department of Animal Science, Aarhus University, Blichers Allé 20, PO Box 50, DK-8830 Tjele, Denmark
Received July 21, 2013.
Accepted January 22, 2014.
1
Corresponding author: nina@mail.ubc.ca

2732 PROUDFOOT ET AL.
Journal of Dairy Science Vol. 97 No. 5, 2014
some visual isolation from herd mates during calving
and the first few days after calving. Our objectives were
to determine if (1) cows were more likely to calve in a
secluded area and (2) cows that became ill after calving
would spend more time in the secluded area.
MATERIALS AND METHODS
The experiment took place at the Aarhus University
cattle research facility (Foulum, Denmark) between
September 2011 and February 2012. Cows were cared
for according to a protocol approved by the Danish
Animal Experiments Inspectorate, Ministry of Justice
(Copenhagen, Denmark) and the University of British
Columbia Animal Care Committee (Vancouver, BC,
Canada; CCAC, 2009).
Animals and Housing
The experiment began with 79 multiparous Danish
Holstein dairy cows. Before calving, cows were grouped
based on expected calving date into 6 blocks with a
mean of 14.7 cows each (SD = 1.5; minimum = 12,
maximum = 16). The entire block was moved into 1 of
2 group pens (each 9 × 15 m; Figure 1) approximately 2
wk before the first expected calving date of cows within
that block. Group pens had deep straw bedding and 12
individual feeding bins (each 75 cm wide).
Individual cows were moved into maternity pens
either before or during signs of labor. Cows were al-
ternately moved into uncovered and partially covered
pens, starting with the pen nearest to the feeding
troughs. The time at which cows were moved into the
individual pen was based upon treatments assigned to
them to address a separate research question: the effect
of time of movement into the individual pen on labor
progress and behavior (see Proudfoot et al., 2013 for a
description). To ensure that these treatments did not
affect our results, we considered the variation in time
that cows spent in the individual pen for both hypoth-
eses tested in this experiment.
The size of each group decreased as cows were moved
into maternity pens. Each block consisted of experi-
mental cows as well as nonexperimental cows or heifers
with expected calving dates later than the experimen-
tal cows. No cows were added to each block, but we
ensured that at least 1 nonexperimental cow was in the
group pen while the last experimental cow was in the
maternity pen.
Figure 2 shows the design of the individual pens. All
individual pens were surrounded by 1.3 m-high tubular
metal bars on 3 sides and a feed bunk on the fourth
side. In half of the pens, a 1.8-m-high plywood barrier
fully covered 2 pen sides, and the side facing the group
pen was half covered to create one secluded corner and
one 1.5-m-wide window that allowed visual contact
Figure 1. Floor plan of the experimental area. Dashed lines represent tubular metal bars separating group and individual pens, and thick
black lines around pens represent plywood used for the partially covered pens.

Journal of Dairy Science Vol. 97 No. 5, 2014
ISOLATION BEHAVIOR OF DAIRY COWS 2733
with the group (partially covered). Each individual pen
had a door that opened into the group pen so that
cows could easily be moved between them. The side
of the corner was always the side without the door, as
the plywood would have obstructed door movement.
For each group pen, 8 pens had the corner on the right
side and 2 had the corner on the left side. To account
for any side bias in the location of cows within the pen
(i.e., one of our main measurements), we created an
equal number of uncovered individual pens to act as
controls. These pens were exposed on all sides, allowing
visual and head-to-head contact with the cows of the
same block in the group pen and adjacent individual
pens. Cows and their calves remained in the individual
pens for 3 d after calving.
Cows were fed a TMR ad libitum with a forage-to-
concentrate ratio of 79:21 (%, DM basis) before calving
and 60:40 (%, DM basis) after calving. Feed was al-
located twice daily at 1000 and 1700 h. After calving,
cows were milked twice daily at 0600 and 1800 h using
a manual milking machine. Water was available ad libi-
tum in the group and maternity pens via water bowls.
Inclusion and Exclusion Criteria
Inclusion criteria for each objective were defined sep-
arately. For both objectives, cows were excluded from
the experiment if they had calved in the group pen (n
= 10), experienced a difficult calving or had twins (n =
7), were disturbed by human activity during labor (i.e.,
straw added to her pen; n = 1), or had milk fever on
the day of calving (n = 2). Of the 59 remaining cows,
34 were in the partially covered pens and 25 were in the
uncovered pens.
Location Before and at Calving. To minimize the
effects of novelty, we excluded cows that calved within
8 h of being moved from the group into the individual
pen (n = 18). Two cows were also excluded because
they were housed in an uncovered pen with a plywood
barrier on one side (both calved next to the barrier).
Thus, the final number of cows included to address this
research question was 39 (partially covered: n = 19;
uncovered: n = 20).
Location and Health Status Postpartum. To
determine the effect of illness on the use of the corner
side of the pen, we included all cows that were housed
in the partially covered pens (n = 34). Some of these
cows were also included in the first objective (ill: n =
5; healthy: n = 5).
To determine health status, rectal body temperature
was taken twice daily at milking for the first 3 d after
calving. A health examination was performed 3 and 9 d
after calving by an experienced researcher and techni-
cian, or as needed by the herd veterinarian. Cows were
checked for signs of metritis using a vaginal exam and
a 4-point scoring system (see Huzzey et al., 2007 for a
description of this scoring system), and signs of ketosis
using a small blood sample from the tail vein [Precision
Xtra Ketone Glucose and Ketone Monitoring System
(Abbott Laboratories, Abbott Park, IL), validated by
Iwersen et al., 2009]. Signs of mastitis were recorded by
the milker daily based on the color and consistency of
the milk.
Cows were considered ill if they had at least 2 consec-
utive body temperatures >39.0°C and showed signs of
metritis (n = 2; a score of 2 or higher, all diagnosed on
d 3 after calving), mastitis (n = 5; 3 diagnosed on d 2
after calving and 2 diagnosed on d 3 after calving), pneu-
Figure 2. Design of (A) uncovered and (B) partially covered individual maternity pens. Gray squares indicate plywood barriers and black
lines indicate tubular metal bars separating pens. Pens were separated into a corner or window half to assign cow location. The side of the corner
for each uncovered pen was determined by matching these to partially covered pens.

2734 PROUDFOOT ET AL.
Journal of Dairy Science Vol. 97 No. 5, 2014
monia (n = 1; diagnosed by a veterinarian on d 2 after
calving), or a combination of mastitis and metritis (n
= 1; diagnosed on d 2 and 3 after calving, respectively).
Cows with mastitis or pneumonia were treated on the
day of diagnosis with an injectable antibiotic given by
the herd veterinarian according to standard veterinary
procedures [pneumonia: Alamycin 300 mg/mL, 100 mL
dosage (Norbrook Laboratories Ltd., Corby, UK); mas-
titis: 1 of the following 3 treatments: penicillin, 100 mL
dosage (Penovet; Boehringer Ingelheim Pharma GmbH
& Co. KG, Ingelheim, Germany); amoxicillin, 150 mL
dosage (150 mg/mL Curamox; Boehringer Ingelheim
Denmark A/S, Copenhagen, Denmark); or sulfadiazine
200 mg and trimethoprim 40 mg, 150 mL dosage (Noro-
dine 24%; Norbrook Laboratories Ltd.)]. Treatments
were repeated by farm staff for 3 d after diagnosis. The
cow with pneumonia and 4 cows with mastitis were also
given a nonsteroidal antiinflammatory drug (NSAID)
on the day after diagnosis [either flunixin meglumine,
50 mg/mL, 20 mL dosage (Finadyne Solution; MSD
Animal Health, Milton Keynes, UK) or Metacam, 20
mg/mL solution, 15 mL dosage (Boehringer Ingelheim
Pharma GmbH & Co. KG)].
Considerable variation existed in the time the 9 ill
cows were kept in the maternity pen before calving
(minimum = 0.8 h, maximum = 120 h). To determine
if time in the maternity pen affected behavior after
calving, we ran a preliminary regression between time
in the maternity pen and time spent in the corner after
calving. A negative relationship was detected, whereby
cows that spent more time in maternity pen before
calving used the corner less (R2 = 0.13; slope = −2.4;
P = 0.04). To avoid any bias in our final analysis, we
paired the 9 ill cows with 9 healthy cows (i.e., no clini-
cal signs of infectious or metabolic disease up to 9 d
after calving) by time spent in the maternity pen before
calving and included pair in the model.
Behavioral Data Collection
Behaviors were monitored using digital video camer-
as (TVCCD-140IR; Monacor UK Ltd., Milton Keynes,
UK) mounted above each pen. One experienced ob-
server collected all data from video. The video was
used to determine the time and location of the cow at
the moment of calving (i.e., when the calf’s hips were
fully expelled from the dam). Behavior was measured
from 6 h before to 72 h after calving using 10-min scan
sampling. During each scan, the location of the cow in
the pen, the posture of the cow (standing or lying), and
the proximity of the calf and the cow (i.e., within or
greater than 1 calf-length apart) were recorded.
Figure 2 shows the 2 options for cow location: (1) the
corner where the plywood barrier prevented visual and
physical contact to the cows housed in the group pen
and (2) the window where cows could have visual and
head-to-head contact with the cows in the group pen. A
cow was considered to be in the corner or window when
the majority of her body was contained within the area.
In the few exceptions where she was positioned directly
in the center of the pen and it was difficult to distin-
guish which side of the pen she was on, we recorded this
as center [cows spent 11.0 ± 7.8 (mean ± SD) min/h
in the center of the pen]. If a cow was categorized in
the center of the pen at the moment of calving, we
measured how much of their body was on each side of
the pen and reassigned her to be in either the corner
or window side (partially covered: n = 1; uncovered: n
= 3). We matched each partially covered pen with an
uncovered pen to determine the side of the window and
corner for the uncovered pens.
For ill and healthy cows, feed intake was measured
before morning delivery at 1000 h and any feed refus-
als were weighed and removed the next morning before
fresh feed was delivered. Daily feed intake (on a % DM
basis) was calculated as the difference between feed
delivery and feed refusals. If a cow calved before fresh
feed delivery at 1000 h, DMI on the day of calving
and the 2 following days were included in the analysis
(healthy: n = 4; ill: n = 5). If cows calved after fresh
feed delivery, DMI on the day after calving and the 2
following days were included in the analysis (healthy: n
= 5; ill: n = 4).
Statistical Analysis
All statistical analyses were performed with SAS soft-
ware (version 9.2; SAS Institute Inc., Cary, NC) using
the cow as the experimental unit. To test if the number
of cows in the pen affected behavioral responses, our
preliminary analysis including the number of cows in
the group pen as a covariate; no effect of this variable
was observed on any measure, so this variable will not
be discussed further. Two-tailed binomial tests were
used to determine if cows were more likely to calve
on one side or the other when housed in the partially
covered or uncovered pens (with a reference of 50%).
To determine if cows changed their use of the corner
in the hours around calving, video data were summed
by hour for the 6 h before calving until the 4 h after
calving. Data were analyzed with repeated-measures
ANOVA (PROC MIXED); the model included pen
type (uncovered or covered), hour, and a pen type ×
hour interaction. Cow was included as a random effect
and the correlation between repeated hourly measures
was modeled with compound symmetry. After visual
inspection of the graph, specific contrasts were made
between treatments in the 1 h before and 1 h after calv-

Journal of Dairy Science Vol. 97 No. 5, 2014
ISOLATION BEHAVIOR OF DAIRY COWS 2735
ing using the ESTIMATE statement of PROC MIXED.
For calf location, data after calving were analyzed us-
ing repeated-measures ANOVA (PROC MIXED); the
model included pen type (uncovered or covered), hour,
and a pen type × hour interaction. The correlation
between repeated hourly measures was modeled with
compound symmetry and the cow-calf pair was con-
sidered the random effect. We observed a clear linear
reduction in time that cows and calves spent near each
other over the 4 h after calving, so hour was modeled as
a continuous variable to determine the rate of change
(slope).
To determine if ill cows spent more time lying and
more time in the corner during the 72 h after calving
compared with healthy cows, data were first summed
per 24-h period (0 to 23 h = 24 h, 24 to 47 h = 48 h,
and 48 to 71 h = 72 h). Video data were missing for 1
ill cow during the 48- and 72-h periods and for 1 ill cow
during the 72-h period after calving. Data were analyzed
with repeated-measures ANOVA (PROC MIXED);
the model included pair, health (ill or healthy), 24-h
period, and a health × period interaction. Cow was
included as a random effect, and the correlation be-
tween repeated hourly measurements was modeled with
autoregressive covariance. For calf location, data after
calving were analyzed using repeated-measures ANO-
VA (PROC MIXED); the model included pair, health
(ill or healthy), 24-h period, and a health × period
interaction. The correlation between repeated hourly
measures was modeled with compound symmetry and
the cow-calf pair was considered the random effect.
Specific contrasts were made between the first 24-h
period versus the subsequent 2 periods (48 and 72 h).
To determine if ill cows ate less than healthy cows
in the first 3 d after calving, data were analyzed with
repeated-measures ANOVA (PROC MIXED). These
3 d differed from the 72 h after calving used above,
as day here represents a 24-h clock, whereas the 24-h
periods after calving were based on actual calving time.
The model included pair, health (ill or healthy), day,
period × health interaction, and cow as a random ef-
fect. After visual inspection of the graph and a period
× health interaction (P = 0.01), specific contrasts were
made between health categories using the ESTIMATE
statement of PROC MIXED.
RESULTS
Location of Cows at Calving
Figure 3 shows the calving location of cows housed
in uncovered and partially covered pens. Cows in the
uncovered pen showed no side preference; 10 calved on
the corner side and the other 10 calved on the window
side of the pen. Cows housed in the partially covered
pens preferred to calve in the corner, with 15 of 19 cows
calving on this side (P = 0.01).
Location of Cow and Calf Around Calving
A pen type × hour interaction was detected for the
time spent in the corner (Figure 4; P = 0.04). Cows
housed in the partially covered pen used the corner
more in the 1 h before (−1 h; P = 0.003) and 1 h after
(0 h; P = 0.02) calving compared with those housed in
the uncovered pens.
No effect of pen type on calf location existed, but a
linear reduction was observed in the time that calves
spent within one-calf length of the cow over the 4 h
after calving (Slope = −4.2, P < 0.01). Calves were
near the cow for almost the full hour in the first hour
after calving (56.4 ± 1.8 min/h), and this was reduced
to 43.6 ± 1.8 min/h by 4 h after calving.
DMI, Location of Ill and Healthy Cows,
and Location of Calves After Calving
For DMI, a day × health interaction (P = 0.02) was
detected; ill cows ate less than healthy cows on the first
day after calving (13.4 vs. 20.4 ± 1.1 kg of DM/d; P <
0.001), but not on d 2 (18.5 vs. 20.1 ± 1.1 kg of DM/d;
P = 0.32) or d 3 (19.5 vs. 19.6 ± 1.2 kg of DM/d; P
= 0.95).
Figure 5 shows the lying time and time spent in the
corner for ill and healthy cows. Ill cows tended to spend
more time lying (P = 0.08) and spent more time in the
corner compared with healthy cows during the 3 d after
Figure 3. Percentage of cows that calved in the corner and window
sides of partially covered (n = 19) and uncovered (n = 20) individual
maternity pens.

2736 PROUDFOOT ET AL.
Journal of Dairy Science Vol. 97 No. 5, 2014
calving (P < 0.001). No interactions between period
and health were detected for lying time or time spent
in the corner.
No effect of illness on calf location was observed, but
cows and calves spent the most time near each other in
the first 24 h after calving compared with the next 2
periods (24 h: 16.0 ± 0.6 h/24 h; 48 h: 12.0 ± 0.7 h/24
h; 72 h: 12.3 ± 0.7 h/24 h; 24 vs. 48 h: P < 0.0001; 24
vs. 72 h: P < 0.001).
DISCUSSION
The objectives of this study were to determine if
cows sought seclusion during calving and illness. We
provided cows a pen that allowed them to spend time
in a secluded area or an open area with visual access
and head-to-head contact with cows in a group pen.
Cows preferred to use a secluded area for calving and
began to use this area more in the 1 h before calving.
After calving, cows that became ill continued to use the
secluded area more than healthy cows.
Our finding that cows used a secluded area to calve
agrees with an earlier study using domesticated cows
kept on pasture (Lidfors et al., 1994) and a study us-
ing indoor-housed cows (Proudfoot et al., 2014). On
pasture, cows distanced themselves from the herd on
the day of calving, choosing to calve in a dry area sur-
rounded by tree or bush cover (Lidfors et al., 1994).
Similar to other “hider” species, calves spent the first
few days of life hidden in brush or tree cover in a
similar location to where they were born while the dam
grazed nearby (Vitale et al., 1986). If no suitable cover
was available, cows calved within close proximity of the
herd (Lidfors et al., 1994). When housed indoors, cows
sought the seclusion of a large shelter at calving if they
calved in the daytime (Proudfoot et al., 2014), but not
if they calved at night.
Cows in the current study secluded themselves for
a short time period around calving (1 h before to 1 h
after). In other studies, cows were reported to begin to
isolate much earlier, including 24 and 8 h before calving
(Lidfors et al., 1994; Proudfoot et al., 2014, respec-
tively). The difference between our results and those
of previous studies could be partially due to sampling
technique. Lidfors et al. (1994) averaged data over
24-h periods, limiting the sensitivity to detect when
the behavior started. However, Proudfoot et al. (2014)
recorded behavior hourly using the same method as
in the current study. The difference between studies
may also be due to the size of the secluded area in the
maternity pen. As cows approach calving, they become
Figure 4. Least squares means ± SE of time spent in the corner
side of the pen from 6 h before calving until 4 h after calving (0 h refers
to the first hour after calving) for cows housed in partially covered (n
= 19) and uncovered (n = 20) individual maternity pens (min/h). *P
< 0.05; **P < 0.01.
Figure 5. Least squares means ± SE for (A) lying time and (B)
time spent in the corner for ill (n = 9) and healthy (n = 9) cows
housed in the partially covered pens during the 72 h after calving
(h/24-h period).

Journal of Dairy Science Vol. 97 No. 5, 2014
ISOLATION BEHAVIOR OF DAIRY COWS 2737
restless, characterized by increased postural transitions
from standing to lying (Huzzey et al., 2005; Jensen,
2012). The small size of our pens (4.5 × 3 m) did not
allow us to determine if a cow was switching sides of
the pen or was simply restless, as cows changed their
location within the pen (from the corner to the window
side and vice versa) when they transitioned between
lying and standing. Cows increased their use of the se-
cluded area in the hour before calving when restlessness
is known to be high, suggesting that the motivation to
hide may have increased as calving became imminent.
Cows in the partially covered pens also spent more
time in the secluded area in the hour after calving. This
behavior is likely due to the position of the calf at calv-
ing, as most cows in the partially covered pens calved
in the secluded area, and regardless of pen type, cows
spent most of this hour near the calf. Cows spend the
first few hours after calving licking the calf (Edwards
and Broom, 1982; Jensen, 2012); licking is thought to
be essential for the development of the dam-calf bond
(Hudson and Mullord, 1977). Our results showed that
cows spent a relatively short time in seclusion after
calving. This could be due to the small size of the pen
and potential soiling in the secluded corner due to calv-
ing, or could suggest that the cow is ready to re-enter
the herd soon after calving.
For our second research question, we hypothesized
that cows would also seek seclusion as a result of illness.
When an animal becomes ill with an infectious disease,
2 key changes occur to help the animal fight the in-
fection: (1) a febrile (fever) response and (2) strategic
behavioral changes that conserve and redirect energy
to the immune system (Hart, 1988). Sickness behaviors
are driven by signals from the immune system in the
brain (e.g., cytokines such as IL-1; Kelley et al., 2003),
are generally nonspecific, and include a reduction in
feed intake and feeding behavior as well as a general
reduction in activity and social behaviors (Dantzer,
2001).
Cows with signs of infectious disease and a febrile
response ate less than healthy cows on the first day af-
ter calving. A similar response has been found in other
studies using cows with metritis (Huzzey et al., 2007)
and mastitis (Fogsgaard et al., 2012b) in early lacta-
tion. This difference disappeared in the following 2 d,
likely because 7 of the 9 ill cows were treated for their
illnesses (5 on d 2 and 2 on d 3). Ill cows also tended
to spend more time lying down, also a common sick-
ness behavior. However, this result differs from that in
previous work, which showed that mastitic cows spent
less time lying compared with healthy cows as a means
to avoid pressure and pain from the udder (Siivonen et
al., 2011; Cyples et al., 2012; Fogsgaard et al., 2012b).
Cows with metritis and pneumonia likely accounted
for the tendency for higher lying time of ill animals
reported here.
A novel finding from the current study was that ill
cows spent more time in the secluded area compared
with healthy cows. Although this is the first evidence
for isolation behavior in ill dairy cows, reduced social
exploration has been found in studies of sickness be-
havior in laboratory animals (e.g., Crestani et al., 1991;
Bluthé et al., 1999). In those studies, sickness behavior
was caused by injecting the animals with either LPS
(an endotoxin) or IL-1 to mimic an infectious disease.
Animals infected with LPS or IL-1 reduced social explo-
ration when presented with a conspecific (e.g., sniffing,
grooming, and chasing; Crestani et al., 1991; Bluthé
et al., 1999). In addition to reduced social exploration,
evidence also exists that mice reduce maternal behav-
iors when ill (Aubert et al., 1997). We did not find
any effects of illness on the time that the cow and calf
spent near each other, but did not specifically measure
maternal behavior. Further studies are encouraged to
determine the effects of illness on maternal behaviors
in cattle, such as allowing the calf to nurse or initiat-
ing contact with the calf. One limitation of the current
study was the small number of ill cows affected with
3 different diseases. Although sickness behaviors are
normally generalized across infectious diseases when a
fever is present (Hart, 1988), it would be useful to con-
duct a larger study to reduce some of the variation due
to illness type and severity as well as day of diagnosis
and treatment.
The reasons for isolation during calving and illness
remain unknown. In wild ungulates, it is thought that
cows hide during calving as an anti-predator strategy
or to facilitate the dam-calf bond by preventing distur-
bance from other cows (Leuthold, 1977). In our case,
the partially covered maternity pen allowed cows to
isolate from the adjacent group pen of familiar cows (as
they had been housed with them before calving), while
allowing some head-to-head contact via the window.
Before calving, cows may have been using the secluded
area to avoid attention from cows in the group pen
drawn to odors associated with calving (see Proudfoot
et al., 2013 for an example of this behavior). It is un-
clear how behavior may have been affected by the pres-
ence of unfamiliar cows (as would be the case for heifers
introduced to the lactating herd for the first time). Ill
animals may also benefit from avoiding others, in part
to reduce the risk of secondary infection (Loehle, 1995).
However, evidence also exists that support from social
partners may have health benefits (reviewed by Rault,
2012).
Cows may also hide to avoid noise and activity in the
barn. In our previous study (Proudfoot et al., 2014),
indoor-housed cows used a shelter to calve during the

2738 PROUDFOOT ET AL.
Journal of Dairy Science Vol. 97 No. 5, 2014
daytime; we speculated that this behavior may have
been partly driven by the high traffic of people and
cows in the barn during that time, as the study was
conducted on a busy research farm. A wide range in the
activity around maternity and hospital pens in com-
mercial herds likely exists, as this is influenced by farm
size and location of the pens relative to high-activity
areas such as the milking parlor. In the present study,
we did not have a large enough sample of cows that
calved on each side of the partially covered pen to as-
sess how time of day influenced the cows’ choice, but
the 4 cows that calved in the window side did so during
the daytime. It should also be noted that human activ-
ity in the barn was minimal; activity was limited to
feeding and milking, or when cows were inspected for
signs of labor.
Cows may use a secluded area to be protected from
drafts in the barn. Although no evidence exists that
cows seek warmth during calving, evidence exists that
wild ungulates will seek warm areas when ill (Hetem
et al., 2008) and Holstein steers housed outdoors will
increase use of a shelter when ill (White et al., 2012).
In our case, the barn was naturally ventilated with
windows, and the maternity pens were situated against
walls with windows so any air coming into the barn
would move through the maternity pens. However, the
plywood barrier may have created a favorable microcli-
mate in the secluded corner.
These ideas are not mutually exclusive; a combina-
tion of factors likely influences the decision to seek a se-
cluded area around calving and during illness. Further
research is encouraged to determine the mechanisms
that motivate isolation seeking. The mechanisms of
sickness behavior are becoming relatively well known,
including the role of proinflammatory cytokines
(Dantzer, 2001). Similar mechanisms may contribute to
seclusion at calving (e.g., Sordillo et al., 1995), but this
remains unknown.
CONCLUSIONS
When given the opportunity, cows housed in indi-
vidual maternity pens preferentially used a secluded
area to calve. Cows began using the secluded area more
in the hour before calving and continued to use it more
for the hour after calving. Ill cows ate less, tended to
spend more time lying, and spent more time using the
secluded area compared with healthy cows.
ACKNOWLEDGMENTS
We gratefully acknowledge the barn staff of the cattle
facility at Aarhus University Research Centre Foulum
(Tjele, Denmark). We also thank John Misa Obidah
and Erik Luc Decker of Aarhus University for their help
with data collection and handling. K. L. Proudfoot was
funded in part by The Aarhus University Research
Foundation as a visiting PhD student and a Natural
Sciences and Engineering Research Council of Canada
(NSERC, Ottawa, ON, Canada) Discovery Grant
awarded to M. A. G. von Keyserlingk. The research was
funded by the Danish Ministry of Food, Agriculture
and Fisheries (Copenhagen, Denmark).
REFERENCES
Arakawa, H., K. Arakawa, and T. Deak. 2010. Sickness-related odor
communication signals as determinants of social behavior in rat: A
role for inflammatory processes. Horm. Behav. 57:330–341.
Aubert, A., G. Goodall, R. Dantzer, and G. Gheusi. 1997. Differential
effects of lipopolysaccharide on pup retrieving and nest building in
lactating mice. Brain Behav. Immun. 11:107–118.
Barbknecht, A. E., W. S. Fairbanks, J. D. Rogerson, E. J. Maichak, B.
M. Scurlock, and L. L. Meadows. 2011. Elk parturition site selec-
tion at local and landscape scales. J. Wildl. Manage. 75:646–654.
Bluthé, R.-M., N. Castanon, F. Pousset, A. Bristow, C. Ball, J. Le-
stage, B. Michaud, K. W. Kelley, and R. Dantzer. 1999. Central
injection of IL-10 antagonizes the behavioural effects of lipopoly-
saccharide in rats. Psychoneuroendocrinology 24:301–311.
CCAC (Canadian Council on Animal Care). 2009. CCAC Guidelines
on: The Care and use of Farm Animals in Research, Teaching and
Testing. CCAC, Ottawa, ON, Canada.
Crestani, F., F. Seguy, and R. Dantzer. 1991. Behavioural effects of
peripherally injected interleukin-1: Role of prostaglandins. Brain
Res. 542:330–335.
Cyples, J. A., C. E. Fitzpatrick, K. E. Leslie, T. J. DeVries, D. B.
Haley, and N. Chapinal. 2012. Short communication: The effects of
experimentally induced Escherichia coli clinical mastitis on lying
behavior of dairy cows. J. Dairy Sci. 95:2571–2575.
Dantzer, R. 2001. Cytokine-induced sickness behavior: Where do we
stand? Brain Behav. Immun. 15:7–24.
Edwards, S. A., and D. M. Broom. 1982. Behavioural interactions of
dairy cows with their newborn calves and the effects of parity.
Anim. Behav. 30:525–535.
Fogsgaard, K. K., M. S. Herskin, P. J. Gorden, A. M. O’Connor, L.
L. Timms, and S. T. Millman. 2012a. Survey of management and
design of hospital pens at Iowa dairy farms. Pages 40–41 in Proc.
Dairy Cattle Welf. Symp., Guelph, ON, Canada. Univ. Guelph,
Guelph, ON, Canada.
Fogsgaard, K. K., C. M. Røntved, P. Sørensen, and M. S. Herskin.
2012b. Sickness behavior in dairy cows during Escherichia coli
mastitis. J. Dairy Sci. 95:630–638.
Hart, B. L. 1988. Biological basis of the behavior of sick animals. Neu-
rosci. Biobehav. Rev. 12:123–137.
Hetem, R. S., D. Mitchell, S. K. Maloney, L. C. R. Meyer, L. G. Fick,
G. I. H. Kerley, and A. Fuller. 2008. Fever and sickness behav-
ior during an opportunistic infection in a free-living antelope, the
greater kudu (Tragelaphus strepsiceros). Am. J. Physiol. Regul.
Integr. Comp. Physiol. 294:R246–R254.
Hudson, S. J., and M. M. Mullord. 1977. Investigations of maternal
bonding in dairy cattle. Appl. Anim. Ethol. 3:271–276.
Huzzey, J. M., D. M. Veira, D. M. Weary, and M. A. G. von Keyser-
lingk. 2007. Prepartum behavior and dry matter intake identify
dairy cows at risk for metritis. J. Dairy Sci. 90:3220–3233.
Huzzey, J. M., M. A. G. von Keyserlingk, and D. M. Weary. 2005.
Changes in feeding, drinking, and standing behavior of dairy cows
during the transition period. J. Dairy Sci. 88:2454–2461.
Ingvartsen, K. L. 2006. Feeding- and management-related diseases
in the transition cow: Physiological adaptations around calving
and strategies to reduce feeding-related diseases. Anim. Feed Sci.
Technol. 126:175–213.

Journal of Dairy Science Vol. 97 No. 5, 2014
ISOLATION BEHAVIOR OF DAIRY COWS 2739
Iwersen, M., U. Falkenberg, R. Voigtsberger, D. Forderung, and W.
Heuwieser. 2009. Evaluation of an electronic cowside test to detect
subclinical ketosis in dairy cows. J. Dairy Sci. 92:2618–2624.
Jensen, M. B. 2012. Behaviour around the time of calving in dairy
cows. Appl. Anim. Behav. Sci. 139:195–202.
Kelley, K. W., R.-M. Bluthé, R. Dantzer, J.-H. Zhou, W.-H. Shen, R.
W. Johnson, and S. R. Broussard. 2003. Cytokine-induced sickness
behavior. Brain Behav. Immun. 17(Suppl. 1):S112–S118.
Leuthold, W. 1977. African Ungulates. Springer, Berlin, Germany.
Lidfors, L. M., D. Moran, J. Jung, P. Jensen, and H. Castren. 1994.
Behaviour at calving and choice of calving place in cattle kept in
different environments. Appl. Anim. Behav. Sci. 42:11–28.
Loehle, C. 1995. Social barriers to pathogen transmission in wild ani-
mal populations. Ecology 76:326–335.
Lott, D. F., and J. C. Galland. 1985. Parturition in American bison:
Precocity and systematic variation in cow isolation. Z. Tierpsy-
chol. 69:66–71.
Miller, K., and D. G. M. Wood-Gush. 1991. Some effects of housing
on the social behaviour of dairy cows. Anim. Prod. 53:271–278.
Proudfoot, K. L., M. B. Jensen, P. M. H. Heegaard, and M. A. G. von
Keyserlingk. 2013. Effect of moving dairy cows at different stages
of labor on behavior during parturition. J. Dairy Sci. 96:1638–
1646.
Proudfoot, K. L., D. M. Weary, and M. A. G. von Keyserlingk. 2014.
Maternal isolation behavior of Holstein dairy cows kept indoors.
J. Anim. Sci. 92:277–281.
Rault, J.-L. 2012. Friends with benefits: Social support and its rele-
vance for farm animal welfare. Appl. Anim. Behav. Sci. 136:1–14.
Sepúlveda-Varas, P., J. M. Huzzey, D. M. Weary, and M. A. G. von
Keyserlingk. 2013. Behaviour, illness and management during the
periparturient period in dairy cows. Anim. Prod. Sci. 53:988–999.
Siivonen, J., S. Taponen, M. Hovinen, M. Pastell, B. J. Lensink, S.
Pyörälä, and L. Hänninen. 2011. Impact of acute clinical mastitis
on cow behaviour. Appl. Anim. Behav. Sci. 132:101–106.
Sordillo, L. M., G. M. Pighetti, and M. R. Davis. 1995. Enhanced pro-
duction of bovine tumor necrosis factor-α during the periparturi-
ent period. Vet. Immunol. Immunopathol. 49:263–270.
Vitale, A. F., M. Tenucci, M. Papini, and S. Lovari. 1986. Social be-
haviour of the calves of semi-wild Maremma cattle, Bos primige-
nius taurus. Appl. Anim. Behav. Sci. 16:217–231.
Weary, D. M., J. M. Huzzey, and M. A. G. von Keyserlingk. 2009.
Board-Invited Review: Using behavior to predict and identify ill
health in animals. J. Anim. Sci. 87:770–777.
White, B. J., D. E. Anderson, D. G. Renter, R. L. Larson, D. A. Mosi-
er, L. L. Kelly, M. E. Theurer, B. D. Robert, and M. L. Walz. 2012.
Clinical, behavioral, and pulmonary changes in calves following
inoculation with Mycoplasma bovis. Am. J. Vet. Res. 73:490–497.