THERIOGENOLOGY

SEASONALEFFECTSON FEMALEREPRODUCTIVE FUNCTIONS

IN THE BOVINE (INDIAN BREEDS)

R. D. Randel
Texas A&MUniversity
Agricultural Research and Extension Center
Overton, TX 75684 USA

ABSTRACT

Reproductive function is mediated by season in the Indian breeds of

cattle (Bos indicus). The reproductive endocrinology of -Bos indicus
cattle differs from that of Bos taurus breeds; the estrus is shorter and
less intense and occurs late inrelation to an estrogen stimulus.
Moreover, the Bos indicus female has a smaller preovulatory surge of
luteinizing hormone (LH), which occurs earlier relative to the onset of
estrus, and she ovulates sooner after the onset of estrus. The corpus
luteum is smaller and contains less progesterone, and the serum
progesterone concentration is lower in Bos
- indicus
-_-- females.
Furthermore, they have fewer preovulatory LH surges than Bos taurus
females and their luteal cells are less responsive to LH in vitroduring
the winter. Their fertility is lower during the late fall and winter
months. For -Bos indicus cattle, recovery of transferable embryos and
survival of embryos in the recipient are at their maximum from July
through October.

INTRODUCTION

Seasonality of reproduction in the Indian breeds of cattle has been

reported by many authors in differing geographical locations. Anestrus
has been reported in Bos indicus cattle during unfavorable seasons (1,
2, j), as has frequency ofvulatory estrus in young Bos indicus
females (4, 5). During winter months, a high incidenceof quiet
ovulation has been reported in heifers of Indian breeds (5);
correspondingly, conception rates are higher during the summer months
(6).

Temperature may modify reproductive function in Bos indicus females

(1) as well as Bos
-- -taurus females (7). However, photoperiodappears to
be one primary stimulus for seasonal reproductive patterns in mammals
(8, 9).

This report will emphasize the endocrine relationships of -Bos

indicus females as they are modified by season.

170 JANUARY 1984 VOL. 21 NO. 1

 THERIOGENOLOGY

REPRODUCTIVE ENDOCRINOLOGY

Estrus
BOS indicus females have been reported to have a shorter period of
--
standing estrus than do --
Bos taurus females (5, 10, 111. Estrogen has
been shown to be the primary stimulus for estrus in ovariectomized cows
(12) and ewes (13) and for the preovulatory luteinizing hormone (LH)
surge in intact cows (14).

Ovariectomized Bos indicus females are less responsive to exogenous

estrogen than are ovxectomized BOS taurus females (15). Ovariectomized
BOS indicus females failed to act= heterosexual mount at any dose level
ofestradiol-178 (Table I). If homosexual activity is accepted as estrus
a lower response was found in --
Bos indicus compared to --
Bos taurus females
(Table II). The BOS indicus x Bos taurus females were intermediate in
heterosexual acti=yanaguarwithe BOS taurus in homosexual
--
activity.

Duration of estrus was shorter (P<.O5) in ovariectomized --

BOS indicus
females than in ovariectomized Bos taurus females. Bos indicus females
required a longer time (Pc.05) f= -ion of estraxl-176 to estrus
Bos indicus x BOS taurus or BOS taurus females (Table III).
than did the -~----

TABLE I. PROPORTIONS OF OVARIECTOMIZED COWS ACCEPTING HETEROSEXUAL MOUNT

AFTER INJECTION OF ESTRADIOL-17B.
Dosage Estradiol-17B
Breed 1 2mg 4mg 8

Brahman O/6** O/6** O/6** O/6**

Brahman x Hereford 2/6t 6/6 6/6 6/6
Hereford 5/6 6/6 5/6 6/6

+p<.10.
l *
P<.OO5.

TABLE II. PROPORTIONS OF OVARIECTOMIZED COWS ACCEPTING HOMOSEXUAL MOUNT

AFTER INJECTION OF ESTRADIOL-176.
Dosage Estradiol 17-8
Breed 1 2mg 4mg 8

Brahman 4/6+ S/6.+ 4/6+ S/6.+

Brahman x Hereford 5/6 6/6 6/6 6/6
Hereford 5/6 6/6 6/6 6/6
t
P<.lO.

JANUARY 1984 VOL. 21 NO. 1 171

THERIOGENOLOGY

TABLE III. RESPONSE TIME FOR THREE BREEDS AT FOUR LEVELS OF

ESTRADIOL-178.
Dosage Estradiol-170
Breeds 1 mg 2 mg 4 mg 8 mg

Brahman 19.59+1.4ea 16.7526.39 26.0 21.37, 20.2 25.88

Brahman x Hereford 16.19+3.05, 11.52f .98: 13.85k1.52, 10.22+2.16;
Hereford 5.49+ -99.. 10.81+1.48.. 12.75+3.70-. 10.61f1.03-

aMean hours + standard error.

*
PC.05.

The endogenous rise in serum estrogens has been found to occur 24 hr

before estrus in BOS indicus females, 16 hr before estrus in Bos indicus
x BOS taurus femalesand before estrus in --
Bos taurus ferna= (p<.o5;
165T- -

Bos indicus females differ in their response to either endogenous or

-~
exogenous estrogens in comparison with Bos taurus females. Bos indicus
females have a shorter, less intense est=whichccurs late inrelation
to the estrogen stimulus. The possibility exists that follicular growth
patterns and estrogen secretion or metabolism patterns are somewhat
different in BOS indicus females. Behavioral patterns in estrus
expression cert%ly differ between -___
BOS indicus and --
Bos taurus females.

Ovulation
Luteinizing hormone is responsible for ovulation in cattle and the
preovulatory LH surge occurs 20 to 22 hours prior to ovulation (17) or 3
to 6 hours after the onset of estrus (18) in Bos taurus cattle. Timing
of physiological events leading to ovulation havebeen reported in Bos
indicus, Bos indicus x Bos taurus and Bos taurus females (19). In this
report, Bos indicus females the Gozry LH surge earlier in
relationzeznd ovulated earlier after the onset of estrus than
did -~----
Bos indicus x Bos taurus or Bos taurus females (Table IV).

TABLE IV. TIMING

OF PHYSIOMGICAL EVENTS (Hr + SE).
Estrus to LH surge Estrus to
Breeds LH surge to ovulation ovulation
Brahman 0.4k3.4 18.5f3.1 18.9k2.2
Brahman x Hereford 6.8p2.1 22.2k2.6 29.0f1.3
Hereford 5.321.3 23.3f2.1 28.6f1.5

Comparative data has been reported on the preovulatory LH surge in

Bos indicus, Bos indicus x BOS taurus and Bos taurus heifers (19, 20).
In one experimx(19)e heiferswere treatedwithormones for estrus
synchronization and in the other the heifers were sampled under normal
estrous cycling conditions (20). The estrous synchronized Bos indicus
heifers had a significantly (P<.O5) lower preovulatory LH surgethan
crossbred or BOS taurus heifers (Figure 1). Under normal estrous cycling
conditions, themdicus heifers had the smallest preovulatory LH
surge with Bos indicus x Bos taurus heifers intermediate and --
Bos taurus
heifers beingh~st(P<.~igure 2).

172 JANUARY 1984 VOL. 21 NO. 1

 THERIOGENOLOGY

Fieure 1. The luteinizina hormone surge in estrous synchronized heifers.

m
32
STANDARD ERRQR

BRAHMAN
30

28
BRAHMAN X
HEREFORD
26

HEREFORD

s
=
24

21
I3
:
z 20

f 18

I
d 16

i
i 14

0
z 12

10

HOURS TO LH SURGE

JANUARY 1984 VOL. 21 NO. 1 173

THERIOGENOLOGY

Figure 2. The luteinizing hormone surge in normal cycling heifers.

STANDARD ERROR
I

m BRAHMAN

BRAHMAN X
E9 HEREFORD

HEREFORD

HOURS 10 LH SURGE

174 JANUARY 1984 VOL. 21 NO. 1

 THERIOGENOLOGY

These data indicate that the Bos indicus female has a smaller
preovulatory LH surge, which occurs earlierelation to the onset of
behavioral estrus compared with --.-
Bos indicus x --
BOS taurus or --
Bos taurus
females.

Corpus Luteum
Corpora lutea (CL) have been reported to be more difficult to detect
by palpation per rectum in BOS indicus females (3). The weight of CL
from Bos indicus heifers issignificantly (P<.Ol) less than CL from BOS
indicusxBosaurus or BOS taurus heifers (21). Weights of CL from
mature ferna= wassignifi~tlyO01) lower in BOS indicus compared
with Bos taurus females (Table V; 22). Content of progesterone in the CL
was l&&%??Bos indicus and BOS indicus cross heifers and highest in
BOS taurus hei?%m In matuZ CL progesterone content was
Gata.05) in --
Bos taurus compared with --
Bos indicus (Table VI; 22).

TABLE V. CORPUS LUTEXJMWEIGHTS (9).

Day of Cycle
Group 8 13 17

Brahman heifers 2.5+ 2.7+.<

-lb"
Brahman x Hereford heifers 4.0+1.5b 3.6+.3b
Hereford heifers 4.6f.4 3.82.3
Brahman cows 2.42.1'
Angus cows 4.1?.3d

"bValues with different superscripts differ (P<.O5).

"dValues with different superscripts differ (P<.OOl).

TABLE VI. PROGESTERONE CONTENT OF CL.

Group Irq/CL

Brahman heifers 216.9i45.0

Brahman x Hereford heifers 217.7f35.3
Hereford heifers 334.6287.8
Brahman cows 190.8f28.9;
Angus cows 266.3223.9

"bValues with different superscripts differ (Pc.05).

In these experiments the data indicate that BOS indicus females have
smaller CL with less total progesterone per -SeNm CL. levels of
progesterone also are lower in --
Bos indicus females compared with
Bos taurus females. Serum progesterone levels were lower (Pc.01) in Bos
indizand Bos indicus x BOS taurus compared with --Bos taurus heifers
(Table VII, 23) andwer(P<.025)in Bos indicus compared with Bos
taurus cows (22).

JANUARY 1984 VOL. 21 NO. 1 175

THERIOGENOLOGY

TABLE VII. SERUM PROGESTERONE LEVELS FOLLOWING ESTRUS (2 ng/ml?SE).

Day after estrus
-- Brahman Brahman x Hereford Hereford

2 1.0t0.3 0.7-fO.2 1.4f0.3

3 1.3f0.5 0.8?0.2 2.3kO.8
4 1.5ro.4 1.2tO.4 3.420.8
5 2.6tO.7 2.0+0.4 3.7fl.O
6 2.2tO.6 2.020.4 5.921.5
7 3.3t1.7 2.250.4 5.8f1.4
8 3.9+2-o 3.0f0.5 4.721.4
9 4.4T1.6 3.5kO.7 7.4t2.9
10 4.4t1.5 3.6tO.6 5.9+-2-o
11 4.at1.9 3.7fO.6 7.Ok2.4

BOS indicus females have substantial

_____ differences in pituitary and
ovarian endocrine function in comparison with Bos taurus females. They
are less responsive to estrogen, timing of physiologmndocrinological
events leading to ovulation is different, the preovulatory LH surge is
smaller, the resulting CL is smaller and contains less progesterone and
serum progesterone is lower during the estrous cycle.

SEASONAL EFFECTS

The major factor provoking the seasonal anestrus condition in ewes

has been reported to be the absence of an LH surge (24). In Texas, data
indicate that Bos indicus cows had a decreased (Pc.005) incidence of
preovulatory LHTrgesatestrus during the winter (1 of 5 cows) compared
with early spring (9 of 10 cows) and late spring (10 of 10 cows; 25).
When the serum LH profile was examined both early and late spring had
elevated (Pc.001) LH levels compared with cows in the winter (Figure 3).
These data support the previous reports of an increased frequency of
anovulatory estrus during unfavorable seasons in --
Bos indicus females (4,
5) -

In an experiment designed to test the effect of breed (Bos indicus

vs Bos taurus) and season (winter vs summer) Bos indicus hzfex
smaller m.001) than Bos taurus heifers and zendencywas found for
CL weights to be greaterduringe winter than during the summer (26).
Corpora lutea from Bos indicus heifers had a lower (Pc.01) content of
progesterone -----YES
compared to taurus heifers. Concentrations of
progesterone were lower (Pc.10) in summer compared with winter CL from
Bos indicus heifers with content being higher (Pc.01) in winter compared
with summer ~Bos ___
taurus CL (Table VIII). Although luteal progesterone
content increased from summer to winter in both breedtypes, this shift
was not reflected in systemic serum progesterone concentrations.

Luteal cells from Bos indicus and Bos taurus heifers were dispersed
and cultured with LH 76) The maximalprogesterone response was
consistently higher (Pc.001) in the Bos --taurus than in the Bos indicus
luteal cells and greater (Pc.001) dznq the summer than duri-
winter (Figure 4).

176 JANUARY 1984VOL. 21 NO. 1

 THERIOGENOLOGY

P/6”“(66 -Hl -INN) Hl WlllllS

JANUARY 1984 VOL. 21 NO. 1 177

 Figure 4. Effect of sea.son and breedtype on progesterone (P,) secretion by
luteal tissue challenged with luteinizing hormone (LH) in vitro.
Values adjusted for Pqconcentrations at 0 ng LH.

8C , 1 KEY: BREEDTYPE,SEASON

70 A- BRAHMAN,SUMMER
a- BRAHMAN,WINTER
O-HEREFORD xHOLSTEIN,SUMMER
8a O-HEREFORD x HOLSTEIN,WINTER

50

40

30

20

10

0 1 5 10 50 100 500 1000

DOSAGE LH CNIH-LH-893 ng
 THERIOGENOLOGY

These data indicate that seasonal changes occur in pituitary and CL

function in Bos indicus females with a lesser effect in Bos taurus
females. Thexanzfrom summer to winter reduced the occurrence
the preovulatory LH surge and the ability of the Bos indicus luteal cells
to respond to LH in vitro. These endocrine changesmediated by season
may affect subsequent fertility.

TABLE VIII. EFFECT OF BREED AND SEASON ON CL WEIGHT, PROGESTERONE

CONCENTRATION AND PROGESTERONE CONTENT (; + SE).
Brahman Hereford x Holstein
Parameter Summer Winter Summer Winter

Weight (g) 2.742 .lOa 3.01% .2ga 4.582 .44b 5.115 _4gb
Progesterone
concentration tug/g) 30.8 k2.8' 52.6 f 7.Sd 39.0 + 7.1e 40.4 +l.ge
Progesterone
content oJg/CL) 104.0 _+5.3f 153.2 k20.8' 174.1 +35.gh 201.9 +9.5i

a,b
Means ?r SE with different superscripts differ (P<.OOl .I -

c,d,e
Means + SE with different superscripts differ (Pc.10)

frg'h'lMeans + SE with different superscripts differ (P<.Ol)

EFFECT UPON CONCEPTION

Reports of a seasonal affect upon fertility in Bos indicus cattle

have been made from several areas of the world (6). Factorsclaimed to
be linked to fertility are temperature, nutrition and day length. Data
from Brahman cattle located in the Gulf Coast of Mexico shows the highest
fertility (65%) from June through October and the lowest fertility from
January through May (35%). This trend was also found in Guatemala,
Brazil and Florida. Data from Texas indicates that Brahman cattle have
higher (P<.OO5) first service conception rates in the summer (61.4%)
compared with the late fall (36.2%; 27). Fertility in Bos indicus cattle
appears to be altered by season with the seasonal maximumoccurring
during the period of warmest temperatures, longest days and most
available forage.

EFFECT UPON EMBRYO TRANSFER

The effect of season upon embryo transfer results in Bos indicus

cattle has been determined (Randel, unpublished data). Neitheryear
month of year affected (P>.lO) recovery of total numbers of ova and
embryos from Bos indicus donor cows. Month of year did alter (Pc.06)
number of tranzrableryos recovered (Figure 5). Maximum recovery of
transferable embryos occurred during April, July, August, September and
October. Pregnancys per donor cow flushed were highest (Pd.025) during
July, August, September and October (Figure 6).

Embryo transfer results rely upon the production of large numbers of

ova which become fertilized and are recovered as transferable embryos.
Total numbers of ovulations did not vary with season but the number of

JANUARY 1984 VOL. 21 NO. 1 179

THERIOGENOLOGY

Y
a

180 JANUARY 1984 VOL. 21 NO. 1

 THERIOGENOLOGY

JANUARY 1984 VOL. 21 NO. 1 181

THERIOGENOLOGY

182 JANUARY 1984 VOL. 21 NO. 1

 THERIOGENOLOGY

LITERATURE CITED

1. Dale, H. E., A. C. Ragsdale and C. S. Cheng. 1959. Effect of

constant environmental temperatures, 50° and 80' F., on
appearance of puberty in beef calves. J. Anim. Sci.
18:1363-1366.

2. Tomar, N. S. 1966. Effect of the season of insemination on

conception rates in Hariana cows and Murrah buffaloes. Indian
J. Dairy Sci. 19:14-17.

3. Plasse, D., A. L. Warnick and M. Koger. 1968. Reproductive

behavior of -~
BOS indicus females in a subtropical environment.
I. Puberty and ovulation frequency in Brahman and Brahman x
British females. J. Anim. sci. 27:94-100.

4. Luktuke, S. N. and P. Subramanian. 1961. Studies on certain

aspects of the oestrous phenomenon in Hariana cattle. J.
Reprod. and Fert. 2:199-200.

5. Plasse, D., A. C. Warnick and M. Koger. 1970. Reproductive

behavior of --
Bos indicus females in a subtropical environment.
IV. Length of estrous cycle, duration of estrus, time of
ovulation, fertilization and embryo survival in grade Brahman
heifers. J. Anim. Sci. 30:63-72.

6. Jochle, W. 1972. Seasonal fluctuations of reproductive functions

in Zebu cattle. Int. J. Biometerol. 16:131-144.

7. Tucker, H. A. 1982. Seasonality in cattle. Theriogenology

17:53-59.

8. Reiter, R. J. 1974. Circannual reproductive rhythms in mammals

related to photoperiod and pineal function: A review.
Chronobiologica:365-395.

9. Peters, R. R. and H. A. Tucker. 1978. Prolactin and growth hormone

response to photoperiod in heifers. Endocrinol. 103:229-234.

10. Anderson, J. 1944. The periodicity and duration of oestrus in Zebu

and grade cattle. J. Agri. Sci. 34:57-61.

11. DeAlba, J. E., Villa Corta and G. Ulloa. 1961. Influence of

natural service on length of oestrus in the cow. Anim. Prod.
3:327-330.

12. Short, R. E., B. E. Howland, R. D. Randel, D. W. Christensen

and R. A. Bellows. 1973. Induced LH release in spayed cows.
J. Anim. Sci. 37:551-557.

13. Scaramuzzi, R. J., S. A. Tillson, I. H. Thorneycroft and B. V.

Caldwell. 1971. Action of exogenous progesterone and estrogen
on behavioral estrus and luteinizing hormone levels in the
ovariectomized ewe. Endocrinol. 88:1184-1189.

JANUARY 1984VOL. 21 NO. 1 183

THERIOGENOLOGY

14. Chri-:<ensen, 9. S. , .J. N. :,!iltbank and M. L. iii>;:\ood. 1974. l>C~?ElS

of hcalrwr,es in the cc-rum of cycling beef #.:rws. J. Anim. Sci.
38:577-583.

75. '-'l,i,&s, R. C. III and R. D. pandel. 1978. Feproductive studies of

Sral.nnrY Cattle I. Hc.haviorsl effect of \?arious dose l,s\'elsof
c's!rndiol-17B uron uv*rii-i-: r:j ,,~j(i Fr,3i:man, Brahaan x Hereford
d ':ereford :‘ows.
a r\ T?;rri~,a<.nol> gy ?:429-435.

16. EznZi-1, R. D. 1980. ~rot*l i ,-i ,Lrn~~strc><rns hk?fC,lf and after estrus
1r, :; I a’i!;:ar 5.--.I-.pz.,
_CII. ,I_ i: ~~‘?.~;,,rd -,nd l'b,refc,rdheifers. J. Anim.
Fri. 51(S'_;:1-1.1):2 !?!litr.).

17. C,!io:rs, D., and H. Karg. !96,9. r;adioii-:?unologische L!<-Bestirmung

in Rlutserum vom Rind unter besonderer Berucksichtigung des
Srunst~~j~klus. Acta. 'ndocrinol. 61:96-103.

18. i:r,r,ricks,D. M., J. F. Dickey and G. D. I!iswender. 1970. Serllm

luteinizing hormone and plasma progesterone levels during the
estrous cycle and early pre';-ancy in COWS. Biol. Reprod.
2:?46-351.

19. Randel, R. D. 1976. LH and ovulation in Brahman, Brahman x

Hereford and Hereford heifers. J. knim. Sci. 43:300 (Abstr.1.

20. PaFidel, R. D. and W. M. Mcseley. 1977. Serum luteinizing hormone

surge and progesterone near cstrus in Brahman compared to
Erahman x Hereford and Hereford heifers. J. hnim. Sci.
45csupp1. 1):199 (.&hstr.).

21. Irvin, H. J., R. D. Randel, W. E. i:aensly and A. M. Sorensen.

1978. Reproductive studies of Arahrrjan cattle III. Comparison
of weight, progesterone content, histological characteristics,
and 3B-hydroxysteroid dehydrogenase activity isol-poration of
Erahman, Hereford and Brahman x Hereford heifers.
Therif_lgenology 10:417-427.

22. Hansen, T. R., R. D. Randel, D. W. I-ibby, E. C. Segerson and W. R.

Getz. 1982. A comparison of S~3llll estradiol-178 and
progesterone and ovarian characteristics of Angus and Brahman
cows. J. Anim. Sci. 55(Suppl. 1) :356 (Abstr).

23. Randel, R. D. 1974. Effect of Zebu genotype upon serum

progesterone during the estrous cycle. J. Anim. Sci. 45(Suppl.
1):411 (Abstr.).

24. Legan, S. J. and F. J. Karsch. 1979. Neuroendocrine regulation of

the estrous cycle and seasonal breeding in the ewe. Biol.
Reprod. 20:74-85.

25. Harrison, L. M., T. R. Hansen and R. D. Randel. 1982. Evidence for

seasonal and nutritional modification of ovarian and pituitary
function in crossbred heifers and Frahnan cows. J. .Anim. Sci.
55:649-656.

184 JANUARY 1984VOL. 21 NO. 1

 THERIOGENOLOGY

26. Rhodes, R. C. III, R. D. Randel and C. R. Long. 1982. corpus

luteum function in the bovine: In vivo and in vitro evidence
for both a seasonal and breedtype effect. J. Anim. Sci.
55:159-167.

27. Neuendorff, D. A., R. D. Randel and J. W. Lauderdale. 1984.

Efficacy of Lutalyse for estrous synchronization in Brahman
cattle. J. Anim. Sci. (Abstr.; submitted).

JANUARY 1984VOL. 21 NO. 1 185