Factors affecting the incidence of postpartum oestrus, ovarian

activity and reproductive performance in Thoroughbred mares

bred at foal heat under Indian subtropical conditions

Sumeet Sharma a,*, M.C.G. Davies Morel b, G.S. Dhaliwal c

a Civil Veterinary Hospital, Mahatam Nagar, Fazilka, Punjab 152123, Indiab Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth, Ceredigion SY23 3AL, UK

c Department of Teaching Veterinary Clinical Complex, Guru Angad Dev Veterinary and Animal Sciences University,

Ludhiana, Punjab 141004, India

Received 1 October 2009; received in revised form 26 November 2009; accepted 31 January 2010

Abstract

Decreased reproductive performance due to summer stress is a well known phenomenon in farm livestock. Whether this occurs in

the mare and specifically how this might affect postpartum reproductive activity and performance, especially at Foal Heat (FH), is

unknown. This study, therefore, aims to investigate this and the factors that might affect postpartum reproductive activity. Reproductive

records of 228 Thoroughbred mares (694 mare years) bred in subtropical north-western India were retrospectively analysed. Overt

oestrous activity occurred within 21 d postpartum in 92.94% (645/694) of mares. Significantly (p < 0.001) more April foaling mares

(97.37%, 185/190) expressed postpartum oestrous activity than those foaling in January (83.61%; 51/61) and February (88.49; 123/

139). Similarly significantly (p < 0.01) fewer multiparous mares failed to demonstrate oestrous activity than primiparous mares

(6.12% vs.15.07%; 38/621 vs. 11/73, respectively). 190 of these 694 mares were additionally monitored to confirm ovulation; in these

mares onset of FH (oestrus plus confirmed ovulation) occurred 8.42 � 0.17 d and first ovulation 13.64 � 0.20 d postpartum. Month,

stud farm, year, and parity did not affect interval from parturition to FH onset or to first ovulation; or FH onset to ovulation. In FH bred

mares Day 16 pregnancy rate and overall foaling rate were 53.76% (100/186) and 46.24% (86/186) respectively and were similar to

those of mares bred later postpartum. FH pregnancy rates were not affected by stud, season, month, year, number of matings, or day of

ovulation but were significantly (p < 0.008) lowered by increasing mare age. Significantly (p < 0.01) lower Day 16 pregnancy rates

were observed in uterine treated mares compared to untreated mares (31.09% vs. 57.96%; 9/29 vs. 91/157, respectively), this difference

was not evident during the rest of pregnancy. In conclusion, postpartum reproductive and ovarian activity appears to be affected by

environment, i.e., delayed in subtropical kept Thoroughbred mares compared to those kept in temperate climates. However, resulting

reproductive performance at FH and the factors affecting postpartum reproductive activity are similar.

# 2010 Elsevier Inc. All rights reserved.

Keywords: Mare; Postpartum; Ovarian activity; Reproductive performance; Foal heat; Subtropical climate

www.theriojournal.com

Available online at www.sciencedirect.com

Theriogenology 74 (2010) 90–99

1. Introduction

Reproductive competence, manifest as embryo

survival and production of a viable foal, is of

* Corresponding author. Tel.: +91 1638 263330.

E-mail address: sumeetsharmapau@yahoo.com (S. Sharma).

0093-691X/$ – see front matter # 2010 Elsevier Inc. All rights reserved.

doi:10.1016/j.theriogenology.2010.01.018

paramount importance in equine stud management

and is, therefore, of significant interest to breeders

and veterinarians throughout the world. Due to the

demand to produce one foal per mare per year

the majority of mares within a breeding program

are early lactating mares. For this reason the

optimum management of the postpartum period

S. Sharma et al. / Theriogenology 74 (2010) 90–99 91

is of paramount importance to economical stud

farming.

To realise the optimum economic return of

broodmares, the number of foals produced per dam

lifetime must be maximized. As pregnancy lasts an

average of 335–340 d, the goal of producing one foal/

mare/year is achievable only if broodmares conceive

within 25–30 d postpartum. This necessitates breeding

mares during the first postpartum oestrus, commonly

referred to as foal heat (FH). Although FH is a naturally

occurring event [1], resulting in good pregnancy rates in

feral pony populations [2], much controversy still exists

over the value of breeding intensively managed

domesticated mares at this time [3–12]. In particular

inconsistent results have been reported with respect to

pregnancy losses in FH bred mares and the various

factors that might affect FH pregnancy rates. Incon-

sistencies in previous studies may be due to: small

sample size [13,14]; use of mixed breed populations of

mares [6,9]; studies carried out under experimental

conditions [15,16]; various management systems

employed; or use of the relatively inaccurate technique

of transrectal palpation [5,17].

In Thoroughbred horses, pedigree and track records

take the highest priority when selecting the best of the

breed, but the effects of physiological and managerial

factors on reproductive performance are often not

appreciated, particularly those of environment.

Although from an evolutionary perspective, horses

are best adapted to temperate climates [18], many

horses are bred in the tropics and subtropics. One of the

consequences of subtropical/tropical environments in

other farm livestock species is the well known

phenomenon of summer stress, which causes depressed

reproductive activity, presumably due to elevated

environmental temperatures [19–21]. However it is

unclear how, and to what extent, such a phenomenon

may affect the reproductive activity of mares bred in

tropical and subtropical climates, in particular any

effect on postpartum reproductive characteristics and

performance in Thoroughbreds particularly at FH

breeding.

Thus, the aim of this study was to investigate, in

Thoroughbred mares bred under Indian subtropical

conditions:

i) the incidence of first postpartum oestrous activity

and the timing of first postpartum ovulation and true

FH (oestrus plus confirmed ovulation).

ii) the factors that might affect the incidence of first

postpartum oestrous activity and the timing of first

postpartum ovulation and true FH.

iii) reproductive performance at FH breeding.

iv) the factors that might affect reproductive perfor-

mance at FH breeding.

v) comparison of these indicators of postpartum

reproductive activity and performance with those

known to be typical of Thoroughbred mares bred in

temperate climates.

It is hoped that this study will help determine

whether summer stress is a phenomenon evident in

postpartum mares bred at FH under subtropical

environments and, if so, help in the identification of

mares at greatest risk of pregnancy loss.

2. Materials and methods

2.1. Database and management

Reproductive records were analysed for 228 mares

(694 mare years) aged between 4 and 19 years, recorded

over seven years (1998–2005) on nine commercial

Thoroughbred stud farms situated in the north-western

part of India (between latitude 288280 and 308 300N,

longitude 748310 and 778 020E). Since the majority of

mares remained on the same stud farm for several years

and were bred each year, many mares appear in the data

for more than one year, therefore for ‘‘mare’’ read

‘‘mare years’’. All the mares from which data was

collected were lactating, that is they had recently foaled

and were lactating throughout the season.

All stud farms had similar housing facilities and

management conditions and mares were fed a daily

ration according to their reproductive status in a

manner generally practiced in India (Lucerne/hay and

paddock grass ad-libitum plus approximately 5 kg of

concentrate fed twice or three times per day). As such,

all mares were in a body condition score 3–4 (on a

scale of 0–5). Teasing was carried out on a daily basis

from postpartum until the end of the first detected

oestrous period and at varying times thereafter

including Day 21. Day 21 was chosen as the cut-off

date as it was assumed that any oestrus displayed after

Day 21 could not be guaranteed to be the first

postpartum oestrus [7,22]. Mares were considered to

be in oestrus based on their behaviour at teasing as

determined by experienced stud farm managers. The

reproductive management decisions for all mares,

such as whether or not to monitor for ovulation, cover

on FH, uterine therapy, etc. were all made by, and

based on the experience of, stud managers and their

veterinarians with the ultimate aim of maximising

conception rates.

S. Sharma et al. / Theriogenology 74 (2010) 90–9992

2.2. The incidence of first postpartum oestrous

activity and the timing of first postpartum ovulation

and true FH (oestrus plus confirmed ovulation)

The onset of first postpartum oestrus was recorded in

all 694 mares from their teasing records up to Day 21

postpartum. As these mares were only teased to

determine oestrus, and ovulation was not confirmed in

all, their data can only be used to determine the incidence

of onset of first postpartum oestrous activity, which does

not necessarily mean true FH (oestrus plus ovulation).

Only 242 mares were monitored daily or on alternate

days to detect ovulation (via ultrasound and rectal

palpation). Of these, 190 spontaneously ovulated on or

before Day 21 postpartum and, therefore, were bred at

FH. As these mares were monitored for oestrus and

ovulation, those that did display both can be confirmed

as having experienced a true FH. These 190 were used

to determine the mean time of onset of FH period, first

postpartum ovulation, and the interval between onset of

FH oestrous activity and ovulation.

2.3. Factors affecting the incidence of first

postpartum oestrous activity and the timing of first

postpartum ovulation and true FH (oestrus plus

confirmed ovulation)

The 694 mares monitored only for postpartum

oestrous activity (via teasing) were divided into groups

according to: year, month of foaling, parity (primipar-

ous vs. multiparous), and stud farm. The incidence of

first postpartum oestrous activity was then calculated

for each group.

The 190 mares that were monitored for FH (both

oestrus and ovulation), were divided into the same

groupings as above and the mean time from parturition to

onset of FH, parturition to first postpartum ovulation, and

onset of FH to ovulation was calculated for each group.

Mares were allocated into groups according to parity

(primiparous mares aged 4–7 years and multiparous

mares aged 5–19 years) in preference to age as,

although there is an interaction between the two, parity

is reported to have the most significant effect on

postpartum reproductive activity [22].

2.4. Reproductive performance at FH breeding

All 190 mares in which FH (oestrus plus ovulation)

was determined were mated at FH period, however four

of these, as a result of manual reduction of a twin

pregnancy, lost both embryos within three days and so

were excluded from the study, leaving 186 mares which

were used to investigate reproductive performance at

FH breeding. In addition to these 186 mares, data from

another 278 spontaneously ovulating mares that were

first mated after FH and were carrying single

pregnancies, was used to provide comparative informa-

tion. All mares were first mated when follicle diameter

exceeded 35 mm and/or follicle consistency was

deemed, by an experienced veterinarian, to indicate

imminent ovulation (Day 0). All mares were mated

again at 48 h intervals until ovulation was confirmed. In

the small proportion of these mares where examination

only occurred on alternate days, ovulation was assumed

to have occurred on the day of last mating prior to

confirmation that ovulation had occurred. Pregnancy

diagnosis was first performed using ultrasonic scanning

at Day 16 post ovulation. All mares pregnant at this time

were then re-examined, via scanning or rectal palpation,

on average on Days 22, 28, 32, 41, 65, 85, 137, and 200

post ovulation in order to allow Day 16 and Day 41

pregnancy rates to be calculated, along with pregnancy

loss at various intervals from Day 41 to term (early

foetal losses Days 42–85; mid pregnancy foetal losses

Day 86–200; late pregnancy foetal losses Day 201-

foaling) as well as overall pregnancy losses between

Day 16 and term. All reproductive performance

parameters after Day 16 were expressed as percentages

of mares confirmed to be pregnant at Day 16. Stillborn

foals were also included as pregnancy losses. All

pregnancy rates were calculated per oestrus/FH.

2.5. Factors affecting reproductive performance in

mares bred at FH

The 186 mares bred at FH were divided into groups

according to year, month of FH breeding, stud farm,

number of matings per FH period, and use of uterine

treatment (saline lavage, infusion of antibiotics, and/or

administration of oxytocin as deemed appropriate by a

Veterinarian). In addition mares were grouped accord-

ing to age (4–7, 8–11, 12–15, and � 16 years) and time

interval to ovulation (�10, 11–15, and � 16 d post-

partum). Pregnancy rate and losses at the same intervals

as detailed above (section 2.4.) were again calculated

for each group.

2.6. Statistical analysis

To compare percentages, Chi-squared and Fisher’s

exact tests were used within groups of mares to

ascertain whether factors such as age, year, month, stud

farm, etc, had a significant effect on timing of FH,

timing of ovulation, pregnancy rate, pregnancy loss, etc.

S. Sharma et al. / Theriogenology 74 (2010) 90–99 93

Table 1

The timing of onset of FH, first post partum ovulation and the interval from onset of FH to ovulation in Thoroughbred mares.

Reproductive characteristics of mares bred on foal heat n

Month Day of onset of FH

(days post partum, mean � SEM)

First postpartum ovulation

(days post partum, mean � SEM)

Interval, onset of FH to

ovulation (days, mean � SEM)

January 8.25 � 0.48 14.25 � 1.03 6.00 � 0.71 4

February 7.96 � 0.43 13.73 � 0.45 5.77 � 0.45 26

March 8.31 � 0.27 13.81 � 0.31 5.50 � 0.24 74

April 8.89 � 0.34 13.62 � 0.37 4.73 � 0.28 63

May 7.81 � 0.48 12.75 � 0.70 4.94 � 0.64 16

June 8.57 � 0.53 13.29 � 0.36 4.71 � 0.36 7

Overall 8.42 � 0.17 13.64 � 0.20 5.22 � 0.16 190

No significant differences were observed.

If a significant (p < 0.05) effect was evident, multiple

comparisons were carried out and each comparison was

considered significant only after making the Bonferroni

adjustment [23]. To compare the mean values, one-way

univariate ANOVA test was used and the differences

were considered significant when p < 0.05. All

statistical comparisons were made with computer

software (State College, PA, Minitab Inc. USA).

3. Results

3.1. The incidence of first postpartum oestrous

activity and the timing of first postpartum ovulation

and true FH (oestrus plus confirmed ovulation)

Out of the total of the 694 mares analysed, overt

oestrous signs were observed in 92.94% (645/694) of

mares, within 21 d postpartum. In the 190 confirmed as

showing FH, the mean time of onset of FH was Day

8.42 � 0.17 (Day 5–18) postpartum and first postpartum

ovulation occurred on Day 13.64 � 0.20 (Day 8–21)

postpartum (Table 1). The mean interval between onset

of FH and first postpartum ovulation was 5.22 � 0.16 d

(1–12 d). Furthermore, 76.32% (145/190) of mares

expressed onset of FH between Day 6 and 9 postpartum

and 64.74% (123/190) of mares ovulated between Days

11 and 15 postpartum, the normal expected timings for

FH onset and ovulation in Thoroughbred mares. Mean

time to ovulation in the control group of mares bred after

FH was Day 35 � 0.13.

3.2. Factors affecting the incidence of first

postpartum oestrous activity and the timing of first

postpartum ovulation and true FH (oestrus plus

confirmed ovulation)

Significantly (p < 0.001) more April foaling mares

(97.37%, 185/190) exhibited oestrous activity within

21 d postpartum, when compared to those foaling

in January (83.61%, 51/61) or February (88.49%,

123/139). No significant difference was observed

across all the months when compared to mares that

foaled in March (92.79%, 206/222), May (97.10%,

65/67) and June (100%, 15/15). Significantly

(p < 0.01) more primiparous mares (15.07%, 11/73)

failed to exhibit oestrous activity within 21 d

postpartum than multiparous mares (6.12%, 38/

621). However, the percentage of the mares exhibiting

oestrous activity was not affected by the stud farm or

the year of the foaling.

In the 190 FH periods examined no significant effect

of year, month of foaling, parity, or stud farm was

evident on the mean intervals of parturition to the first

overt signs of FH, parturition to first postpartum

ovulation, and onset of FH to ovulation.

3.3. Reproductive performance at FH breeding

The reproductive performance parameters for FH

bred mares (186) and those bred after the FH (278) are

given in Table 2. No significant differences existed

between FH bred mares and those bred after FH in any

of the reproductive performance parameters measured.

Of the 186 mares mated at FH, 53.76% were pregnant at

Day 16 postpartum, this reduced to 49.75% at Day 41

(Table 2). Ultimately 46.24% of mares mated at FH

produced a live foal compared to 51.08% foaling rate

for 278 mares bred after FH. Of the initial 190 mares

mated at FH, 6.32% (12) produced a multiple

pregnancy. In 8 mares, manual reduction was successful

and they retained 1 embryo and so remained within the

investigation.

The overall foetal and pregnancy losses for FH bred

mares were 5.00% and 14.00%, respectively and did not

significantly differ from that seen in mares mated after

the FH (5.59% and 11.80% respectively).

S. Sharma et al. / Theriogenology 74 (2010) 90–9994

Table 2

Reproductive performance in Thoroughbred mares bred at FH compared to mares mated at a later post partum oestrus.

Reproductive performance parameters Postpartum mares first bred

Foal Heat (FH) Later postpartum oestrus

Management of oestrus

No. oestrus 186 278

No. matings 243 383

Average number of matings per oestrus 1.31 1.38

Pregnancy results- % (n)

Day 16 pregnancy rate per oestrus 53.76(100) 57.91(161)

Day 41 pregnancy rate per oestrus 48.92(91) 54.32(151)

Foaling rate per oestrus 46.24(86) 51.08(142)

*Multiple pregnancies evident at Day 16 8.00(8) 10.56(17)

*Embryonic losses (Day 16–41) 9.00(9) 6.21(10)

*Early foetal losses (Day 42–85) 1.00(1) 2.48(4)

*Mid foetal losses (Day 86–200) 2.00(2) 1.86(3)

*Late foetal losses (Day 201-term) 2.00(2) 1.24(2)

*Overall foetal losses (Day 42-term) 5.00(5) 5.59(9)

*Overall pregnancy losses (Day 16-term) 14.00(14) 11.80(19)

*Live foaling rate (Day 16-term) 86.00(86) 88.20(142)

No significant differences were observed.

* all expressed as a percentage of mares pregnant at Day 16.

3.4. Factors affecting reproductive performance in

mares bred at FH

Of the 186 FH bred mares, uterine treatment

was administered to 15.59% (29). Of these, 62.09%

Table 3

Effect of uterine treatment on reproductive performance in Thorough-

bred mares bred at FH.

Reproductive performance

parameters

Administration of

uterine treatment

Untreated Treated

Management of oestrus

No. oestrus 157 29

No. matings 204 39

Average number of matings

per oestrus

1.30 1.34

Pregnancy results- % (n)

Day 16 pregnancy rate per oestrus 57.96a(91) 31.03b(9)

Day 41 pregnancy rate per oestrus 52.23(82) 31.03(9)

Foaling rate per oestrus 49.68(78) 27.59(8)

*Multiple pregnancies evident at

Day 16

8.80(8) 0.00(0)

*Embryonic losses (Day 16-41) 8.80(8) 0.00(0)

*Early foetal losses (Day 42-85) 0.00(0) 11.11(1)

*Mid foetal losses (Day 86-200) 2.20(2) 0.00

*Late foetal losses (Day 201-term) 2.20(2) 0.00

*Overall foetal losses (Day 42-term) 4.39(4) 11.11(1)

*Overall pregnancy losses

(Day 16-term)

14.29(13) 11.11(1)

*Live foaling rate (Day 16-term) 85.71(78) 88.89(8)

a,bWithin rows, different superscripts differ significantly (P < 0.01).

*all expressed as a percentage of mares pregnant at Day 16.

(17) received post breeding therapy, 20.69% (6)

were treated during oestrus before mating, and

17.24% (5) were given both pre and post breeding

therapies. No significant effect of administering

uterine treatment was evident on any of the

reproductive performance parameters measured after

Day 16 (Table 3) though significantly (p < 0.01)

higher Day 16 pregnancy rates were evident in

mares receiving no treatment (57.96%) compared to

treated mares (31.03%). As such all subsequent

reproductive performance measures were calculated

as a percentage of mares pregnant at Day 16 when

investigating the effect of age, month, year,

etc, allowing all FH bred mares to be included,

regardless of whether or not they had received uterine

treatment.

The age of the mare affected reproductive

performance in mares aged 4–7 yr. Day 16 and

Day 41 pregnancy rates and the overall foaling rate

were 66.67%, 64.81%, and 61.11% respectively,

which were all significantly (p < 0.008) greater than

those evident in mares aged �16 yr (26.67%, 20.00%,

and 13.33% respectively) (Table 4). Additionally,

mares aged 4–7 yr had a significantly (p < 0.008)

higher Day 41 pregnancy rate than mares aged 12–15

yr (33.33%). No significant effect of mare age on any

of the other parameters measured was evident apart

from early foetal losses where mares aged 4–7 and

8–11 demonstrated significantly (p < 0.008) lower

incidence (0.00%) compared to mares aged � 16 yr

(25.0%).

S. Sharma et al. / Theriogenology 74 (2010) 90–99 95

Table 4

Effect of age on reproductive performance in Thoroughbred mares bred at FH.

Reproductive performance parameters Mare age (years)

4–7 8–11 12–15 �16

Management of oestrus

No. oestrus 54 81 36 15

No. matings 67 105 50 21

Average number of matings per oestrus 1.24 1.30 1.39 1.40

Pregnancy results- % (n)

Day 16 pregnancy rate per oestrus 66.67a(36) 55.56(45) 41.67(15) 26.67b(4)

Day 41 pregnancy rate per oestrus 64.81a(35) 50.62ab(41) 33.33b(12) 20.00b(3)

Foaling rate per oestrus 61.11a(33) 48.15(39) 33.33(12) 13.33b(2)

*Multiple pregnancies evident at Day 16 5.55(2) 8.89(4) 13.33(2) 0.00(0)

*Embryonic losses (Day 16–41) 2.78(1) 8.89(4) 20.00(3) 25.00(1)

*Early foetal losses (Day 42–85) 0.00a(0) 0.00a(0) 0.00(0) 25.00b(1)

*Mid foetal losses (Day 86–200) 2.78(1) 2.22(1) 0.00(0) 0.00(0)

*Late foetal losses (Day 201–term) 2.78(1) 2.22(1) 0.00(0) 0.00(0)

*Overall foetal losses (Day 42–term) 5.56(2) 4.44(2) 0.00(0) 25.00(1)

*Overall pregnancy losses (Day 16–term) 8.33(3) 13.33(6) 20.00(3) 50.00(2)

*Live foaling rate (Day 16–term) 91.67(33) 86.67(39) 80.00(12) 50.00(2)

a,bWithin rows, percentages with different superscripts differ significantly (P < 0.008).

*all expressed as a percentage of mares pregnant at Day 16.

Year, month of breeding, stud farm, and number of

matings per FH period did not significantly affect any of

the reproductive performance parameters measured.

Similarly, day of ovulation in relation to parturition had

no significant effect on the vast majority of reproductive

performance parameters except, unsurprisingly, the

number of times the mare was mated during her FH

period (Table 5).

Table 5

Effect of the interval from parturition to first post partum ovulation on rep

Reproductive performance parameters Interval

�10 d

Management of oestrus

No. oestrus 25

No. matings 28

Average number of matings per oestrus 1.12a

Pregnancy results- % (n)

Day 16 pregnancy rate per oestrus 36.00(9)

Day 41 pregnancy rate per oestrus 28.00(7)

Foaling rate per oestrus 28.00(7)

*Multiple pregnancies evident at Day 16 0.00(0)

*Embryonic losses (Day 16–41) 22.22(2)

*Early foetal losses (Day 42–85) 0.00(0)

*Mid foetal losses (Day 86–200) 0.00(0)

*Late foetal losses (Day 201–term) 0.00(0)

*Overall foetal losses (Day 42–term) 0.00(0)

*Overall pregnancy losses (Day 16–term) 22.22(2)

*Live foaling rate (Day 16–term) 77.78(7)

a,b Within rows, different superscripts differ significantly (P < 0.01).

*all expressed as a percentage of mares pregnant at Day 16.

4. Discussion

4.1. The incidence of first postpartum oestrous

activity and the timing of first postpartum ovulation

and true FH (oestrus plus confirmed ovulation)

In this survey, the vast majority of mares expressed

signs of overt oestrus and/or ovulated within 21 d

roductive performance in Thoroughbred mares bred at FH.

from parturition to ovulation

11–15 d �16 d

119 42

147 68

1.24a 1.62b

53.78(64) 64.29(27)

49.58(59) 59.52(25)

46.22(55) 57.14(24)

7.81(5) 11.11(3)

7.81(5) 7.41(2)

1.56(1) 0.00(0)

3.13(2) 0.00(0)

1.56(1) 3.70(1)

6.25(4) 3.70(1)

14.06(9) 11.11(3)

85.94(55) 88.89(24)

S. Sharma et al. / Theriogenology 74 (2010) 90–9996

postpartum a normal expectation for Thoroughbred

mares [17,24]. However, as not all mares were

ultrasonically scanned it is not possible to know how

many mares failed to show oestrous activity due to

behavioural anoestrus/silent heat or postpartum anoes-

trus. The incidence of behavioural anoestrus/silent heat

is reported to be as high as 44% [1], whereas postpartum

anoestrus occurs less (18%) frequently [9]. In the

current study the incidence of postpartum anoestrus

might be expected to be particularly low as Thor-

oughbred mares express oestrus less overtly than other

breeds [25] and the majority of mares foaled mid season

(the reproductively most optimum time), as such sexual

inactivity is most likely to be due to behavioural

anoestrus.

In temperate climates, the normal expectation is that

Thoroughbred mares will show FH within 10 d and

ovulate on average 12 d after parturition [7,26]. In the

current study mean onset of FH was 8.42 d postpartum,

which lies within the expected range for temperate

mares, however, the mean time to ovulation was 13.64

d. This is somewhat longer than observed in temperate

mares but agrees with other work on mares in

subtropical environments. Malschitzky [27] and Winter

et al. [28], working in Brazil, reported mean intervals to

ovulation of 13.2 and 14.2 d for Thoroughbred and

Criollo mares, respectively. Similarly, Blanchard et al.

[9], working in Texas, reported 13.0 d for a mixed

population of mares and Panasophonkul et al. [1]

reported 13.4 d for Thai crossbred mares in Thailand.

Even longer intervals of 17 d have been reported by

others [29]. As a result, this study supports the

conclusion that environment (photoperiod) affects

postpartum ovarian activity and the speculation that

differences reported between breeds might in fact be

due to environmental conditions/climate rather than

breed per se [22].

The expectation is that ovulation will occur on the

last day of FH period, which lasts 4–5 d in most breeds

[1,10,13,14,30]. Although the timing of the end of FH

was not determined in this study, the mean interval from

onset of oestrus to ovulation was 5.22 d, the mean FH

length is likely, therefore, to have fallen outside the

expected 4–5 d range. Hence, although it cannot be

certain, this indicates that FH is longer in Thorough-

breds, at least those kept in sub-tropical environments,

than other breeds.

In addition to any breed/climate effect, other factors,

such as nutrition, may affect postpartum reproductive

activity. Any nutritional effect in the current study is

likely to be minimal as all mares were kept on well

managed stud farms with good nutritional management

and were in good body condition. However, other

factors were seen in this study to have an effect.

Primiparous mares were less likely to show postpartum

oestrous activity within 21 d than multiparous mares.

This agrees with Nagy et al. [22] and is somewhat to be

expected as primiparous mares are particularly protec-

tive of their foals and more nervous than multiparous

mares [31,32], masking oestrous signs in the presence

of a stallion. However, parity had no effect on true FH

(oestrus and confirmed ovulation). In practice, parity is

a function of age plus number of previous foaling

[22,33]. However in tropical climates, no effect of age

on interval between foaling and FH ovulation has been

reported [28] and a major temperate region study

reported only a parity effect on postpartum oestrous

activity [22]. It is likely, therefore, that any effect seen

in the present study is a true effect of parity rather than

age.

The current study suggests that season may have

some effect on oestrus. A significantly higher propor-

tion of April foaling mares showed oestrous activity

than those foaling in January and February, although no

significant effect was observed on ovulation or on

oestrus when oestrous activity was further defined as

true FH. This limited effect may be simply a reflection

of transitional anoestrus [34], however, an interaction

with age/parity cannot be ruled out. As reported in other

studies [22,35], in the current work primiparous mares

are generally younger than multiparous mares, hence

reproductively more efficient [35] and so conceive

earlier in the year. Consequently, mares foaling in

January are more likely to be young primiparous mares

and, as discussed previously, are less likely to show

oestrus. This, plus previous reports of no effect of

season on timing of FH in subtropical kept mares

[24,28] suggest that season has, at most, a small effect

on postpartum reproductive activity in subtropical/

tropical mares. This differs from that reported for

temperate kept mares [17,26,36]. Presumably the

reduced seasonal effect evident in subtropical/tropical

kept mares is due to the reduced monthly variation in

day-length. Additionally the issue of evolutionary

biology should not be ignored. The seasonality of

animals is the result of their adaptation to local

environmental conditions [37]. The horse evolved in

temperate climates and reproductive activity is geared

towards producing foals at the most optimum time for

survival [38]. Hence the reproductive activity of mares

kept in temperate climates (providing pharmacological

intervention is not used) is under greater photoperiodic/

climatic control than tropical/subtropical kept mares. It

might, therefore, be expected, as indicated in the current

S. Sharma et al. / Theriogenology 74 (2010) 90–99 97

study, that season would have less of an effect on

reproductive efficiency and activity in tropical/sub-

tropical kept mares than those kept under temperate

conditions. The existence of strong genetic bases for

seasonality of reproductive activity in equines should be

further explored to propose selection criteria and/or

gene markers accessible to breeders wishing to reduce

seasonality in their stock.

4.2. Reproductive performance at FH breeding

To the best of our knowledge, this is the first

extensive report on reproductive performance of

Thoroughbred mares kept in a subtropical environment

and bred at FH. Day 16 pregnancy rates (53.76%) fall

within the range (37–57%) previously reported for

Thoroughbreds [5,7,11,15,39], though lower than the

range, (57.5–82%) reported for most other breeds

[6,9,13,16,40]. No significant difference was apparent

in the reproductive performance of FH bred mares

compared to those bred later postpartum. This, again, is

in agreement with several previous studies in Thor-

oughbreds [8,41] and in other breeds [8,9,40,42] and

agrees with the conclusions of Sharma et al. [12] that

FH bred mares are perfectly capable of maintaining a

pregnancy once successful fertilization has been

achieved. It is noteworthy that reproductive efficiency

appears little improved by domestication irrespective of

climatic conditions, as evidenced by the high post-

partum reproductive success in feral horse populations

around the world [2] compared to those reported here

and elsewhere for intensively managed mares such as

Thoroughbreds. These observations suggest further

work is justified to investigate possible positive effects

of, for example, locomotor activity on involution and

postpartum fertility.

Despite overall reproductive performance being

unaffected by breeding at FH, it is possible that this

may not be true for all categories of mares. Indeed this

study shows that older mares had significantly poorer

pregnancy rates, foaling rates, and higher early foetal

losses after FH breeding. This age effect is generally

reported for mares [9,40] and specifically for Thor-

oughbreds [7,35] regardless of breeding time. This

decline has been attributed to a host of factors such as

uterine and/or ovarian aging [43,44–47] including

uterine fluid [48]. All these will impact on FH breeding

success. This association between uterine fluid and

subfertility makes it surprising that in this study uterine

treatment was not associated with an improvement in

Day 16 pregnancy rates, this has also been reported by

others [9,49]. However, in the current study this

association between treatment and reduced reproduc-

tive performance at Day 16 is not evident in live foaling

rates, due to higher pregnancy losses in untreated mares.

It is difficult to draw concrete conclusions from this

work due to low mare numbers and the involvement of

several different veterinarians hence uniform criteria

were not used to determine which mares required

treatment. However, it would be expected that the

experienced veterinarians in this study would make

sound clinical and managerial decisions based on mare

uterine health, such as to ensure that mares with severe

cases of uterine incompetence were not bred at FH even

with treatment. Thus it may be reasonable to assume

that the mares which received uterine treatment and

were bred at FH would have had minimal compromised

uterine health which would be expected to be resolved

with uterine therapy. However, it appears that uterine

treatment during FH does not necessarily improve Day

16 pregnancy rates, but might improve live foaling

rates.

Somewhat surprisingly, this study failed to indicate a

significant effect of interval from parturition to

ovulation, on reproductive performance, though a trend

was evident. This supports the observations of

Blanchard et al. [9], but contradicts others

[3,6,17,50]. Involution occurs rapidly after foaling,

both physically [3,51] and histopathologically [52–54]

and may take 31 d [55]. Hence by the time a FH embryo

enters the uterus it is unlikely that uterine involution

will be complete, especially in the previously gravid

horn [3,55]. This may account for poorer reproductive

performance in early ovulating mares at FH mating

[3,6,56] although this may be compensated for by the

preferential establishment of pregnancies in the pre-

viously non gravid horn [12,57].

Reproductive performance as evident in the sub-

tropical mares of this study and the effect of factors

upon this performance all conform to the normal

expectations for temperate kept Thoroughbred mares.

This may be considered surprising as reduced repro-

ductive performance due to summer stress is a well

documented phenomenon in other farm species [19–

21]. Additionally, this study indicates that this lack of an

effect at FH breeding is evident despite environmental

temperatures of 35–45 8C, characteristic of mid-April,

the peak breeding season in north-western India.

5. Conclusion

It is apparent that the incidence of postpartum

oestrous activity, the timing of first postpartum

ovulation, and the timing of FH in Thoroughbred

S. Sharma et al. / Theriogenology 74 (2010) 90–9998

mares may be affected by the subtropical climate of

India when compared to temperate climates, however,

resulting reproductive performance is not affected. In

common with mares bred in temperate climates, parity

and month of foaling had a limited but significant effect

on the incidence of oestrous activity, however, when

oestrous activity was further defined as true FH (oestrus

plus confirmed ovulation) no effect of month, parity,

year, or stud farm was evident. Additionally, reproduc-

tive performance at FH was not different to that

observed in mares bred later postpartum, however, in

mares bred at FH, advancing age and administration of

uterine treatment had an adverse effect on reproductive

performance. It can be concluded, therefore, that

breeding mares in a subtropical environment may

affect postpartum reproductive and ovarian activity but

is not detrimental to reproductive performance in FH

bred mares, unlike in other farm animals.

Acknowledgments

The authors are grateful to the veterinarians, owners,

staff, and management of the surveyed stud farms for

access to their records and help with extraction of

relevant information.

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