1. Introduction
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Summer heat stress HS is a major contributing factor in low fertility among
lactating dairy cows. It is a worldwide problem, which inflicts heavy economic losses and affects about 60 of the world cattle population. Conception rates drop from about
40–60 in cooler months to 10–20 or lower in summer, depending on the severity of Ž
. the thermal stress Cavestany et al., 1985 . The most prominent characteristic of summer
infertility is its multifactorial nature, since hyperthermia directly alters and impairs the cellular functions of various partsrtissues of the reproductive system. Furthermore,
exposure of cattle to thermal stress elicits indirect responses, which may also have an impact on reproductive processes. Such responses include redistribution of blood flow
among body organs, reduction in food intake, respiratory alkalosis, etc. Although the impact of the various direct and indirect effects of HS on reproductive processes has
never been quantified, it is believed that the direct effect of hyperthermia in impairing cellular functions is the predominant one. The substantial rise in milk yield in recent
years has aggravated the low summer fertility syndrome, because of the concurrent rise in metabolic heat production. The various cooling procedures used on farms have not
been able to improve fertility substantially, and the conception rate of lactating cows in the summer, even in farms equipped with cooling systems, is still pronouncedly below
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that in the winter Hansen, 1997 . Traditionally, low summer fertility is associated mainly with the warm months of the
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year usually June, July, August and September in the northern hemisphere . However, Ž
. fertility remains lower in autumn October and November , than in winter, although
ambient temperatures drop and the cows are no longer exposed to HS. A delayed effect of summer HS on autumn fertility is evident, and it accounts for about one-third or more
of the low summer fertility syndrome.
In the last decade, considerable efforts have been dedicated to shedding light on the HS-induced impairment of processes in the reproductive system, and of the functioning
of various parts of it. Ultrasonography, cell culture, in vitro oocyte maturation and fertilization are among the means of achieving improved understanding of mechanisms
by which thermal stress negatively influences bovine fertility. This review focuses basically on immediate and delayed effects of HS on follicular development, dynamics
of follicular waves, steroidogenic capacity of theca and granulosa cells, corpus luteum Ž
. CL development and function, and secretion of progesterone and gonadotrophins, and
briefly reviews oocyte quality, embryonic development and uterine function under HS. In the second part of the review, several hormonal strategies are discussed, which aim to
optimize reproductive functioning and to improve fertility of cattle under HS conditions.
2. Follicular dynamics
HS-induced alterations in follicular dynamics have been monitored by ultrasonogra- phy. Heat exposure of lactating cows during the entire estrous cycle induced a 50
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increase in the number of large 10 mm follicles during the first follicular wave Ž
. Wolfenson et al., 1995 . A similar response was monitored during the follicular phase
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in lactating cows Roth, 1998 , and a similar tendency was also recorded in HS heifers
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during days 17–21 of the cycle Wilson et al., 1998b . This response resulted from HS-induced reduction in the dominance of the large follicle, which permitted the growth
of an additional large follicle, and it provides at least a partial explanation of the marked rise in twinning in cows calving during May–July in hot countries such as Saudi Arabia
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. Ryan and Boland, 1991 , or of the 50 rise in the twinning rate of mature cows during
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May–July in Israel Herd Book data . This rise is probably due to insemination of cows, which had double ovulations during the hot months of August and September.
Another sensitive indication of HS-induced attenuation of dominance is the lack of a decline in the number of medium-size follicles during the period of dominance of the
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first-wave Badinga et al., 1993 or preovulatory follicle Wolfenson et al., 1995 . Similarly, in a seasonal study in which follicular dynamics was studied in April, June,
Ž August and November, a larger first-wave dominant follicle in April non-heat-stressed
. season was associated with an earlier regression of the largest subordinate follicle and a
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sharper decrease in the number of medium-size follicles Badinga et al., 1994 . A slower decline in size of the second-largest, subordinate follicle was also found in studies of
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acute HS in cows and heifers Roth et al., 1997; Wilson et al., 1998b . HS-induced depression of dominance was also found to be associated with a 2–3-day
Ž earlier emergence of the second-wave dominantrpreovulatory follicle Wolfenson et al.,
. 1995 . This may have an important physiological significance, because earlier emer-
gence of the preovulatory follicle may result in ovulation of older follicles. The duration of dominance of the preovulatory follicle was found to be negatively correlated with
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fertility of cattle Mihm et al., 1994 . It is worth noting, however, that the day of the cycle on which the second-wave dominant follicle was first detected did not differ
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between replicate months in a seasonal study Badinga et al., 1994 . Earlier emergence of the second follicular wave was also detected, in terms of number of medium-size
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follicles, in HS lactating cows Roth et al., 1997 . Emergence was noted a day earlier and the number of follicles declined 2 days later than in control cows. This was
associated with the earlier appearance of a wider surge in plasma FSH concentration Ž
. Roth, 1998 . Moreover, plasma FSH concentrations were also higher during the
periovulatory period in HS cows; this rise in FSH was associated with a pronounced Ž
. decrease in the concentration of immunoreactive inhibin in plasma Roth, 1998 . In
agreement with these findings, a reduction of plasma inhibin concentration in summer Ž
. was found in cyclic buffaloes in India Palta et al., 1997 and a tendency for reduction in
Ž plasma concentration of the hormone was also noted in HS cows Wolfenson et al.,
. 1995 . The latter findings suggest that depression of dominance during HS involves
suppression of inhibin secretion by granulosa cells and subsequent alterations in FSH secretion.
Ž Conflicting findings on the effect of HS on the development of small follicles class
. 1; 2–5 mm are evident. A reduction in the number of small follicles was documented
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by Wolfenson et al. 1995 and Wilson et al. 1998a,b ; whereas an increase in the Ž
. number of small follicles was found by Trout et al. 1998 . Discrepancies between
studies could be related to differences in experimental design, or in the severity of the HS.
In summary, exposure of cattle to thermal stress does not suppress the overall pattern of follicular wave dynamics in cattle. However, HS does suppress follicular dominance,
resulting in a number of changes in follicular growth. Among them, at least two Ž .
responses standout in their physiological importance: 1
development of a larger number of large follicles probably increases the rate of double ovulation and hence of
Ž . twin calving; and
2 early emergence of the preovulatory follicle lengthens the
dominance period, and this has been shown to be associated with lower fertility in Ž
. spontaneously cyclic dairy cows Bleach et al., 1998 or in heifers induced to ovulate
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persistent dominant follicles Mihm et al., 1994; Austin et al., 1999 .
3. Steroidogenic capacity
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