Effect of temperature on fertility...
 Effect of temperature on fertility...
 Influence of temperature on endocrine...

Title: Influence of heat stress on reproductive performance
Full Citation
Permanent Link: http://ufdc.ufl.edu/UF00091684/00001
 Material Information
Title: Influence of heat stress on reproductive performance
Alternate Title: Dairy science mimeo report DY71-1 ; Florida Agricultural Experiment Station
Physical Description: Book
Language: English
Creator: Verde, Omar G.
Thatcher, W. W.
Wilcox, C. J.
Affiliation: Central University of Venezuela -- College of Verterinary Science
Publisher: Florida Agricultural Experiment Station, University of Florida
Place of Publication: Gainesville, Fla.
Publication Date: October 1, 1970
Copyright Date: 1970
 Record Information
Bibliographic ID: UF00091684
Volume ID: VID00001
Source Institution: University of Florida
Holding Location: University of Florida
Rights Management: All rights reserved by the source institution and holding location.
Resource Identifier: 313799756 - OCLC

Table of Contents
        Page 1
    Effect of temperature on fertility of the male
        Page 2
        Page 3
        Page 4
    Effect of temperature on fertility of the female
        Page 5
        Page 6
        Page 7
    Influence of temperature on endocrine balance
        Page 8
        Page 9
        Page 10
        Page 11
        Page 12
        Page 13
        Page 14
        Page 15
        Page 16
Full Text


HUME LIB Afi il e, Florida

APR 5 171 airy Science Mimeo Report DY71-11'
October 1, 1970

IFS.O Univ. of Florida
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
of Venezuela.
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.


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.


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.


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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cows and repeat breeders. Proceedings: Sixth International Congress
on Animal Reproduction and Artificial Insemination. Paris

2. Alliston, C. W., B. Howarth, Jr., and L. C. Ulberg. 1965. Embryonic
mortality following culture in vitro of one- and two-cell rabbit eggs
at elevated temperatures. J. Reprod. Fertil., 9:337.

3. Alliston, C. W. and L. C. Ulberg. 1961. Early pregnancy loss in sheep
at ambient temperatures of 70 and 90F. as determined by embryo transfer.
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4. Bearden, H. L., W. Hansel,.and R. W. Bratton. 1956. Fertilization
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