SFLRIDA 7A'Tr'TUPnA EXPERIMENT STATION
HUME LIB Afi il e, Florida
APR 5 171 airy Science Mimeo Report DY71-11'
October 1, 1970
IFS.O Univ. of Florida
INFLUENCE -' RJLSS. o ri rUCTIVE PERFORMANCE: A REVIEW
0. G. Verde,2. 3. Wilcox3.
O. G. Verde, 'W. W. Thatcher and C. J. Wilcox
The term embryo death is used by most researchers to describe prenatal
mortality occurring at any time during the period of the zygote and of the
embryo. Fertility losses in clinically normal dairy cattle of low fertility
(repeat breeders) are considered to be due mainly to fertilization failure
and early embryonic mortality (14, 23, 46). Fertilization rates of 55.8%
and 66.1% of recovered ova, and embryo mortality ranging from 40 to 70%,
have been reported in repeat breeder cows (13, 23, 33, 45, 46). Estimates
of embryo mortality in animals without histories of infertility are approx-
imately 20% (4, 17, 24, 32, 33). Ayalon and co-workers (1) reported that
the major portion of embryo losses in repeat breeders is already apparent
by no later than 13 days post-insemination. This is in conflict with the
work of Hawk et al. (25) in which most of the embryonic losses occurred
A joint publication of the University of Florida Department of Dairy
Science and the Facultad de Ciencias Veterinarias de la Universidad
Central de Venezuela, Maracay; Spanish translation also available.
Assistant Professor, College of Veterinary Science, Central University
Assistant Physiologist and Associate Geneticist, respectively,
University of Florida.
later than 16 days post-estrus. Bishop (5) stated that some embryonic
loss is necessary in order to eliminate certain genotypes from each
generation. However, this factor would account for just a small portion
of the total losses. One important conclusion can be drawn from these
studies: embryonic death is a major factor in the reduction of reproductive
efficiency in cows.
Several environmental components are recognized as exerting an adverse
effect on the reproductive process. Of major concern to the subtropical
and tropical regions is the pronounced influence of temperature on embryo
survival. An offspring at term represents the successful function of a
series of sequential physiological events. The stress of heat could act
by either affecting the spermatozoa prior to fertilization, the ova after
fertilization, or a specific response by the dam that could perhaps affect
the embryo's environment and well being.
EFFECT OF TEMPERATURE ON FERTILITY OF THE MALE
Considerable work has been conducted regarding the effect of elevated
temperatures on the reproductive system of the male. A cryptorchid male
produces no sperm, and it is possible to produce this condition experi-
mentally by placing the testis in the abdominal cavity. These observations
led to the thesis that higher temperatures in the abdominal cavity caused
degeneration of the germinal epithelium. Moore (34) reported that
application of 470C heat to the testicles of the guinea pig for 10 minutes
resulted in degenerated tubules 12 days after heat exposure. Guinea pig
epididymal spermatozoa subjected to elevated temperatures resulted in an
increase in the number of stillbirths and abortions (57). Litter size in
rabbits inseminated with spermatozoa maintained at 40*C was decreased
compared with the 370C control (51).
Seasonal differences in spermatogenic activity and fertility in dairy
cattle have been observed and explained on the basis of higher summer
environmental temperatures. Erb et al. (18) found that maximum breeding
efficiency of the Purdue Station herd was in May with a 74.3% pregnancy
rate as compared to a low of only 58.2% in August. Subsequent studies with
the same herd demonstrated that semen of inferior quality was produced during
the months of July, August and September. Semen of superior quality was
obtained during April, May and June. Similar results were reported by
Johnston and Branton (30), Branton et al. (7), and Fryer et al. (22). In
addition, Johnston and Branton evaluated fertility based on 60-90 day non-
returns to first service. No differences in the percentage of non-returns
was detected (about 70% in all cases). Exposure of bulls to increasing
temperature in climatic control chambers resulted in decreased motility,
sperm concentration and total sperm count (12).
Howarth et al. (27) capacitated sperm for 6 hours in uteri of rabbits
kept at two different air temperatures (320C and 210C). The sperm were
recovered and used to inseminate females maintained at 210C. The rate of
fertilization was the same. However, the ability of the resulting embryo
to survive and form an implantation site was significantly reduced in
rabbits fertilized by heat stressed sperm. Most implantation sites
contained normal embryos indicating that death had occurred prior to im-
Burfening and Ulberg (11) studied the direct effect of high temperature
on rabbit sperm in vitro. Each ejaculate was split and cultured for 3 hours
at either 38C or 40C and placed in opposite uterine horns of females pre-
vivously mated to vasectomized males. There was no significant effect of
temperature on either semen quality or fertilizing capacity. However, the
rate of continued embryonic development to the point of implantation was
greatly reduced for those ova fertilized by sperm cultured at the higher
temperature. These data suggested that spermatozoa could be influenced
before fertilization by a 20C increase in temperature which decreased
subsequent pre-implantation embryo survival.
Burfening et al. (10) exposed male mice to 32C ambient temperature
for 24 hours and evaluated subsequent fertility (rate of fertilization,
implantation and fetal survival) from matings during the 30 day period
following heat stress. A decrease in early embryo survival from matings
soon after heat stress indicated mature spermatozoa and late spermatid
sensitivity. Fertilization rates were the lowest 18 days after stress
indicating that heat stress possibly interfered with or terminated the
process of spermatid maturation to form the mature spermatozoa.
First et al. (21) postulated that embryo loss, as a result of elevated
ambient temperatures on sperm via the uterine environment, may be related
to the aging of sperm. Perhaps the elevated ambient temperature speeds up
the sperm aging process. Salisbury and co-workers (39, 40, 41, 42)
demonstrated that the aging of bovine spermatozoa affects their ability to
fertilize ova and also impairs the ability of some of the zygotes formed
to complete normal embryogenesis. Alterations in the integrity of the
genome (DNA) may be such that the resulting concepts is incapable of sus-
tained life. Burfening (9) reported that heat-stressed rabbit spermatozoa
had a decreased DNA content and an increased embryo death rate. However,
no significant correlation was detected between the loss of DNA and embryo
death. Possibly the genetic material in the haploid state may be extremely
susceptible to damage. A recessive lethal mutation in a diploid organism
necessitates a gene change in the homozygous condition to render a nonviable
organism. Therefore, genetic damage to sperm resulting from higher
temperature would more likely be associated with dominant: 3ethals. Con-
ceivably, early death of an embryo might be due to loss or malfunction of
part of the genome.
EFFECT OF TEMPERATURE ON FERTILITY OF THE FEMALE
High temperature does not have a very marked effect on ovarian f-nction
(36, 38, 52, 56) but rather on the uterus during the preparatory stagnr. of
pregnancy as well as during the initial development of the embryo. Veates
(56) studied the effect of high environmental temperatures (/40.60C) on
reproduction of ewes Ewes showed no adverse effects of temperature on
occurrence of estrus but there was a significant ro1luction in the n 11,liner
of young produced.
Dutt et al. (16) reported that ewes subjected to high ambient
temperature (32.20C) at about the time of mating reiulted in lower ferti-
lization rates and increased early embryonic death. Ewes; exposed to high
temperatures beginning on the 12th day of the cycle .rior to broedi.ng: showed
approximately one-half the fertilization rate of control ewes. Embryo loss
was estimated to be 92%. When ewes were not exposed to the treatment room
until 8 days postbreeding, embryo losses were not significantly different
from control ewes.
Warnick et al. (52) compared ovulation rate, conception rate and
embryonic survival up to 25 days of pregnancy in five groups of gilts main-
tained under different environmental conditions of ]5.60C, 32.20C or
atmospheric conditions with shade. No significant differences were detected
in ovulation rate, conception rate or number of live embryos at 25.days
postbreeding. Gilts maintained continuously at 32.20C averaged 10.9 embryos
compared to 13.5 embryos for gilts at 15.6C. High temperature up to 3
days postbreeding had no effect on number of embryos, whereas, gilts
maintained at 32.20C from 3 days postbreeding had 11.3 embryos compared
to 13.6 for gilts at 15.6C. Tompkins et al. (48) found that exposure of
sows to 350C for 24 hours on day 1 of gestation significantly reduced embryo
survival at 27 to 51 days of gestation. The difference in results between
these two studies in swine could have been due to higher temperature stress
used by Tompkins et al.
Stott (43) and Stott and Williams (44) observed that a lowered seasonal
breeding efficiency was associated with high ambient temperature and
humidity in lactating dairy cows. Only 17.1% of the animals inseminated
during the month of August were carrying viable embryos at 35 to 41 days
post-insemination. This value increased to 61.5% during May and started to
decrease afterwards (44). Fallon (19) found no relationship between rectal
temperature at time of insemination and conception rate based on 60-90 day
non-return to service.
There are many physiological events associated with reproduction which
occur in a precise sequence during the period of the embryo's development
and could be influenced by the stress of high temperature. Thesperm,
immediately after mating, are subjected to the environment of the female
reproductive tract; ova leave the ovary and come under the influence of the
environment of the oviduct; final maturation of the egg occurs at the time
of the union of sperm and ovum in the oviduct; first development of the
concepts occurs in the oviduct followed by implantation in the uterus.
Consequently, there are numerous events related to the sequence of embryo
development in which heat stress could exert a deleterious effect.
Alliston and Ulberg (3), using embryo transfers, studied the time
during which the detrimental effects of high temperature were exerted upon
the sheep embryo. Transfers were performed approximately 72 hours after
onset of estrus and successful transfers were verified by a laparotomy
performed 25-30 days later. Where both donor and recipient were maintained
at 21.2C, 56.6% of the transfers were successful compared to 9.5% in which
donors were maintained at 32.20C and recipients at 21.2C. They concluded
that some detrimental action had occurred by 3 days after onset of estrus
in ewes at 32.2C. It was also observed that embryonic death occurred at a
later stage of development in uteri. When donors were maintained at 21.10C
and recipients at 32.20C, 24% of the transfers were successful.
Dutt (15) exposed ewes to high temperatures at the time of breeding
and at 1, 3 and 5 days after breeding. Results showed no significant
differences in fertility rate in the different groups. Exposure to heat
resulted in an increase in morphologically abnormal ova; and embryo loss,
estimated as the percentage of fertilized ova that failed to survive, was
significantly higher in all the treated groups. Embryo loss for the combined
0- and 1-day groups was significantly higher than in the 3- and 5-day ewes.
They concluded that the sheep zygote is most sensitive to the harmful
effects of high ambient temperatures during the initial stages of cleavage
while in the oviduct. Eighty-five percent of the control ewes lambed,
compared to 10% for the ewes in the 0- and 1-day groups, 35% for the 3-day
group and 40% in the 5-day group.
Observations by Woody and Ulberg (55) suggested that high air temperature
did not adversely affect the ovum prior to fertilization. Sheep ova were
recovered from donors at 21C or 32C shortly after ovulation and trans-
ferred to mated recipients. There were just as many embryos 30 days post-
mating in those recipients which received ova from animals maintained at 320C
as there were in those which received ova from animals maintained at 210C.
Fertilized rabbit ova can be grown through any one cell division, in
vitro, and development continued after transfer into a normal reproductive
system (29). In that way, the direct effect of temperature at specific
developmental stages on embryo survival could be tested. Alliston et al. (2)
demonstrated that fertilized ova grown in vitro through the first cell
division at 400C had a lower rate of embryo survival than those grown at 380C.
As the period of culture at 400C was delayed to either the second, third or
fourth cell division, differences in post-implantation death losses dis-
Since an increase in temperature surrounding the embryo at the time
of first cell divisions reduces survival, body temperatures of females
following insemination should be associated with conception rates. Ulberg
and Burfening (49) reported a decline in pregnancy rates in dairy cattle
(based on 35 to 42 day pregnancy diagnoses) from approximately 61% to 45%
as rectal temperatures increased from 37.5*C to 38.50C 12 hours after insem-
These studies in the female indicate that a temperature stress of the
ovum immediately after fertilization causes the resulting concepts to
perish some time later in its development.
INFLUENCE OF TEMPERATURE ON ENDOCRINE BALANCE
The physiological mechanisms through which heat stress produces its
effects are unknown, but there is some evidence that endocrine imbalances
may be involved.
The thyroid gland has been studied extensively regarding its response
and involvement in heat stressed animals. Bogart and Mayer (6) demonstrated
that administration of thyroxine reversed "summer sterility" in rams.
Johnson and Ragsdale (31) found a decline in thyroid activity on exposure
of heifers to high temperature. Ryle (37) found that the proportion of
ewes at 400C with live embryos was increased when thyroxine injections
were given. She concluded that thyroid hypofunction was the most critical
factor causing embryo loss in ewes acclimated to high temperature. In
contrast, Howarth and Hawk (28) reported that L-thyroxine had no effect on
embryo survival either during the period of August through September, or
November through January. Brooks and Ross (8) reported that daily injections
of either 0.2, 0.3, or 0.4 mg of thyroxine per 45.4 kg body weight had no
beneficial effect upon semen quality in rams kept at normal or high
environmental temperatures. Ambient temperatures of approximately 26.7C
constituted a critical point above which semen quality declined.
Elevated body temperatures reduced embryo survival in intact rats but
not in adrenalectomized rats maintained on cortical implants (20). Rats
were exposed to temperatures of 39.40C for 5 hours on each of two consecutive
days after mating. Embryo survival, at 15 days after mating, was 98% for
controls, 36% for rats treated on days 1 and 2, and 69% for those treated
on days 3 and 4. Adrenalectomized rats treated with high temperature on
days 3 and 4 had 94% survival, which was the same as controls. Thus,
removal of the adrenal gland permitted normal embryo survival in animals
heat stressed at this time. However, the effect of adrenalectomy during
the critical period of days 1 and 2 was not evaluated.
Adrenalectomy did not improve fertility in female rabbits exposed
to thermal stress (26). In contrast, adrenalectomy altered the point in
the reproductive process where fertility was affected. A reduction in
fertilization rate and an increase in the production of morphologically
abnormal eggs was observed. A higher increase in rectal temperatures,
accompany thermal stress of adrenalectomized does, may have been
responsible for altering the point in the reproductive process that was
Adrenocorticotrophic hormone increased embryonic mortality in intact
rats but not in adrenalectomized rats (50). Likewise, adrenocorticotrophic
hormone and cortisone interrupted pregnancy when administered to rabbits
and mice (35). Results by Howarth and Hawk (28) suggested that adrenal
hyperactivity could be a contributory factor to the adverse effects of
stressful environmental conditions on reproduction. Injections of hydro-
cortisone acetate for 4 days beginning at estrus had no effect on
fertilization but it significantly reduced embryonic survival during late
summer and early autumn. Comparable experiments during the winter months
had no effect on fertility. Thwaites (47) reported that neither progesterone,
thyroxine or cortisol therapy affected embryo survival in heat stressed ewes.
Arizona workers (53, 54) determined that the first 4 to 6 days after
a cow was bred constituted the critical period when the animal was sensitive
to heat stress. Exposure to thermal stress after this period did not result
in pregnancy losses. Refrigerated confinement during the critical period
failed to improve reproductive performance. However, the length and con-
ditions of confinement were not conducive for good management practices
and animal comfort. Evaporative cooled shade units were constructed to cool
a larger number of animals for longer periods of time under a more routine
pattern of operation at the dairy unit. Cows having access to the cooled
shades had markedly higher breeding efficiencies than those provided with
conventional shades through the months of June through October. In
addition, milk production was maintained at a higher level in the group
provided with cooled shade.
Lactating cows appear to be more sensitive to thermal stress than
nonlactating animals. It is reasonable to assume that lactating cows have
higher body temperatures due to higher metabolic rates. However, increasing
the severity of thermal stress during the critical period failed to impair
reproductive performance in nonlactating cows. It was concluded that
increased body temperature does not affect the ovum, spermatozoa or the
developing concepts directly, but that reproductive efficiency is reduced
by some indirect means. Lactating cows are subjected to readjustments in
endocrine function following parturition due to lactation, insufficient
energy intake and infection. Consequently, adverse climatic temperatures
may indirectly affect reproductive efficiency by further altering the
endocrine balance of the lactating cow.
The corpus luteum is the usual site of ovarian progesterone secretion.
Luteal tissue progesterone concentrations of thermal stressed cows were no
different than concentrations from control animals taken at the same time.
However, adrenal progesterone concentrations were significantly greater in
treated cows. Subsequent studies revealed that ovariectomized cows exposed
to high ambient temperatures for only 24 hours exhibited an immediate
increase in blood progesterone which presisted up to 30 days. Additional
studies revealed that cows having access to cooled shades during the
summer months had blood progesterone levels about one-tenth that of control
animals. Associated with the lower progesterone levels was a higher
breeding efficiency in the cooled cows. Secretion of excessive or insufficient
amounts of progesterone could result in an incompatibility of the uterus
and embryo, embryonic mortality and prolonged estrus cycles observed in
animals bred but not pregnant.
Heat stress is a major factor causing a reduction of reproductive
performance. Increased economic losses are incurred due to costs of
repeated inseminations, prolonged dry periods, replacement costs for cows
culled due to poor reproductive performance and losses in total milk
production per cow. Reductions in embryo survival due to heat stress
appear to result from the direct effects of high temperature on sperma-
tozoa and the fertilized ova in the early cleavage divisions. Additional
evidence suggests that alterations in maternal hormonal balance, in
response to heat stress, may be associated with reduced embryo survival.
Specifically, thermal stress to the lactating dairy cow mav predispose
the animal to an adrenal progesterone hormonal imbalance that may alter
reproductive performance. The exact physiological mechanisms which cause
embryo death have not been fully elucidated.
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