Male involvement in fertility and factors
affecting semen quality in bulls
John P. Kastelic
Department of Production Animal Health, University of Calgary, Faculty of Veterinary Medicine, Calgary, AB, Canada
Implications
• Fertility varies substantially among bulls. In general, methods to
predict fertility are better for identifying bulls with low fertility
than for ranking bulls with good to excellent fertility.
• Compensable sperm abnormalities can be overcome by increasing the dose used for artificial insemination; these are attributed
to sperm reaching and penetrating the zona pellucida. In contrast,
increasing the insemination dose does not improve fertility for
uncompensable defects, implying that the sperm are able to cause
fertilization and initiate development, but they do not sustain embryogenesis.
• Bull testes must be 2 to 6°C cooler than core body temperature
for fertile sperm; consequently, increased testicular temperature
reduces semen quality.
• Increased nutrition before 30 weeks of age increased luteinizing hormone pulse frequency, hastened puberty, and increased
testicular size at maturity in bulls. However, attempts to correct
nutritional deficiencies present during calfhood by supplemental
nutrition later in life were unsuccessful.
Key words: breeding soundness evaluation, bull fertility, scrotal/testicular thermoregulation, sperm defects
Introduction
There is no doubt that there are substantial differences in fertility among
individual bulls. In a recent review (Flowers, 2013), normal ranges in reproductive performance from entire herds were compared to those reported
for males. For beef cattle, maximum fertility was similar for herds versus
males. However, since minimum fertility was less for the latter, it was concluded that beef bulls contribute significantly to fertility failures, as bulls
with reduced fertility are frequently used. However, for dairy cattle, there
were similar minimums for herds and bulls, yet maximum fertility for bulls
exceeded that of the herd. Therefore, it was concluded that reproductive
failure in dairy cattle was due more to the cow than to the bull.
In general, fertility is more important in an individual bull than an individual cow, as one bull may be used to breed up to 40 females with natural
service, or potentially hundreds of thousands via artificial insemination.
Although 20 to 40% of bulls may have reduced fertility, few are complete© Kastelic
doi:10.2527/af.2013-0029
20 ly sterile (Coulter and Kastelic, 1999). Subfertile bulls delay conception,
prolong the calving season, reduce calf weaning weights, and increase the
numbers of females culled, thereby resulting in economic losses and threatening sustainability of a livestock operation. Furthermore, infertile bulls
can have adverse effects of animal welfare, due to repeated breedings and
delayed calving. Whereas some management practices such as multiplesire breeding groups, low breeding pressure, and extended breeding seasons make identification of subfertile bulls difficult, other strategies such as
single-sire mating groups, short breeding seasons, and artificial insemination highlight the need to critically evaluate bull fertility.
Evaluation of Breeding Soundness
The two general methods of evaluating the breeding soundness potential of bulls are either breeding a large number of normal, fertile females
and determining pregnancy/calving rates or conducting a breeding soundness evaluation. Although a breeding trial is the ultimate test of fertility,
it is expensive, particularly if reproductive performance is poor. Therefore, it is strongly recommended to conduct a standard breeding soundness
evaluation before the breeding season. These evaluations identify bulls
with substantial deficits in fertility, but they do not consistently identify
subfertile bulls. In that regard, the use of frozen-thawed semen from bulls
in commercial artificial insemination centers that meets minimum quality
standards can result in pregnancy rates that differ by 20 to 25% points
(Larson and Miller, 2000), as standard semen end points identify grossly
abnormal semen but do not consistently identify subfertile bulls with apparently normal semen (Gadea et al., 2004). Since bull fertility is influenced by a wide range of factors, no single diagnostic test can accurately
predict fertility, although an appropriate combination of tests can be more
informative (Kastelic and Thundathil, 2008). Based on work in boars, perhaps a means of assessing the post-insemination sperm-oviduct interaction
would substantially increase the ability to predict fertility (Flowers, 2013).
Seminal plasma proteins apparently have potential as fertility predictors
(Flowers, 2013), and more than 400 proteins have been identified in a bull
sperm plasma membrane fraction (Byrne et al., 2012).
The standards of the Society for Theriogenology (www.therio.org) are
intended to assess the likelihood of a bull establishing pregnancy in ≥ 25
healthy, cycling females in a 65- to 70-day breeding season. The classification is based on the bull meeting minimum standards for health and
structural soundness, sperm motility ( ≥ 30% progressively motile sperm),
sperm morphology ( ≥ 70% normal and ≤ 20% defective heads), and scrotal circumference. The latter is highly correlated with paired testis weight,
which is, in turn, positively correlated with daily sperm production and
semen quality (reviewed by Barth, 2007). In that regard, bulls with larger
testes produce more and better quality sperm, in general. Furthermore,
Animal Frontiers
Flickr/tausend und eins, fotografik
bulls with large testes have female siblings and daughters with earlier puberty and better fertility (reviewed by Barth, 2007). Since the heritability of
scrotal circumference in young bulls is ~0.5, it responds well to selection
(reviewed by Barth, 2007).
Compensable versus Uncompensable
Sperm Defects
There are several systems of classifying sperm abnormalities, and dividing them into compensable and uncompensable defects is a practical
approach that is gaining popularity (reviewed in Amann and DeJarnette,
2012). Compensable abnormalities can be overcome by increasing the
dose used for artificial insemination. Therefore, these abnormalities are
generally believed to be associated with sperm reaching and penetrating
the zona pellucida, and as such, are associated with sperm viability measures such as motility, acrosome integrity, and cell membrane integrity. For
example, sperm with knobbed acrosomes or bent tails are unlikely to fertilize an ovum. In contrast, uncompensable defects are defined as fertility of a
male or an insemination dose that does not improve with an increased number of sperm, implying that the sperm are able to cause fertilization and
initiate development but are unable to sustain embryogenesis, with most
failures occurring before day 8 post breeding. Chromosomal abnormalities, protamine status, and perhaps abnormalities of mRNA are believed
to be uncompensable defects, as these sperm would be expected to initiate
fertilization but not sustain development. Furthermore, laboratory processing such as flow-sorting sperm for sex selection can increase the number of
uncompensable sperm defects (DeJarnette, 2005).
The “threshold” in sperm numbers is the limit beyond which further
increases in sperm numbers per insemination dose fails to further increase
fertility, which can be due to reaching the limit of female fertility, or a
value below the level of female fertility, due to the presence of uncompensable sperm defects (Amann and DeJarnette, 2012). Consequently, the
threshold for a particular bull or ejaculate can vary widely and depends on
the severity and ratio of compensable and uncompensable sperm defects.
Males that have a prolonged linear increase in fertility with increasing
numbers of sperm are considered to have primarily compensable sperm
defects, whereas those that quickly reach a plateau are considered to have
a large proportion of uncompensable sperm defects. Regardless, it appears
that most fertility curves reach their threshold when 70% of sperm have a
compensable trait (Flowers, 2013).
Compensable sperm quality attributes are those that affect the ability
of a sperm to access and fertilize an ovum. Therefore, measurements of
motility, viability, and membrane function are commonly used to estimate
compensable sperm quality. However, given that they do not assess uncompensable semen traits, they are most appropriate to determine the number of sperm per insemination dose to reach maximal fertility rather than to
predict absolute fertility (Amann and DeJarnette, 2012).
Visual assessment of sperm motility is quick and inexpensive. However, it is highly subjective and often has limited repeatability (DeJarnette,
2005). There are numerous computer-assisted sperm analyzer (CASA)
machines that are commercially available. These provide an objective and
much more repeatable method of assessing sperm motility, yielding numerous end points that characterize sperm motion (Kathiravan et al., 2011).
Acrosomal integrity and sperm viability are commonly measured to
predict fertility. The acrosome can be stained using a number of live/dead
stains such as eosin/nigrosin or assessed without staining with appropriate
optical systems such as differential interference contrast microscopy. Furthermore, there are several stains that enable assessments to be made with
flow cytometry, allowing rapid and objective evaluation of large numbers
of sperm. In addition, sperm from neat semen often is subjected to additional manipulations that provide more information with regards to its
fertilizing potential. Frozen-thawed sperm are often maintained at 37°C
for 2 to 4 hours after thawing and then evaluated; this mimics exposure to
the female reproductive tract and facilitates detection of latent sperm abnormalities that may not be apparent immediately post-thaw (DeJarnette,
2005). Furthermore, the hypo-osmotic swelling test (HOST) can be used
to determine membrane viability.
Testicular Temperature
It is well established that bull testes must be 2 to 6°C cooler than
core body temperature for fertile sperm to be produced. Consequently,
increased testicular temperature, regardless of the cause, reduces semen
quality (Waites, 1970). Furthermore, increased testicular temperature is a
common underlying cause of infertility in bulls (Kastelic, 2013).
October 2013, Vol. 3, No. 4
21
Figure 1. Left: Vascular cast of the spermatic cord, testis, and epididymis in a
two-year-old beef bull. The cast was prepared by flushing the testicular artery and
vein and injecting them with red and blue latex, respectively; allowing latex to
harden; and placing the structure in sodium hydroxide (to digest the tissues and
liberate the cast). The testicular vascular cone, consisting of the coiled testicular
artery surrounded by the venous pampiniform plexus, is above the testis. Note that
the testicular artery exits the bottom of the testicular vascular cone, passes to the
bottom of the testis (underneath the corpus epididymis), and then is readily visible
on the posterior surface of the testis, as it branches and spreads upward, before
entering the testicular parenchyma. Right: Vascular casts of the testicular artery
(within the testicular vascular cone) of six-month and two-year-old (left and right,
respectively) beef bulls.
parenchyma (Kastelic et al., 1996, 1997; Figure 1). Blood within the
testicular artery has a similar temperature at the top of the testis compared
to the bottom of the testis, but is significantly cooler at the point of entry
into the testicular parenchyma. Therefore, both the scrotum and the testis
are warmest at the origin of their blood supply (top of scrotum and bottom
of testis) and get cooler distal to that point (Kastelic et al., 1996, 1997).
Remarkably, these opposing temperature gradients collectively result in a
nearly uniform intratesticular temperature in situ.
Increased Ambient Temperature
The effect of increased ambient temperature on semen quality has
been widely reported. In one study, ambient temperatures of 40°C at a
relative humidity of 35 to 45% for as little as 12 hours reduced semen
quality (Skinner and Louw, 1966). Furthermore, Bos taurus bulls are
more susceptible than Bos indicus bulls to high ambient temperatures
(Skinner and Louw, 1966). In that regard, decreases in semen quality
were less severe, occurred later, and recovered more rapidly in crossbred
(Bos indicus x Bos taurus) bulls than in purebred Bos taurus bulls
exposed to high ambient temperatures (Johnston et al., 1963).
Sources of Testicular Heat
There are several features involved in regulation of testicular
temperature. Scrotal skin is typically thin, with minimal hair and an
extensive subcutaneous vasculature that promotes heat loss by radiation.
The scrotal neck is the warmest part of the scrotum; a long, distinct scrotal
neck and pendulous scrotum reduce testicular temperature by increasing
the area for radiation, and enabling the testes to move away from the body
when ambient temperatures are increased. Immediately above each testis is
its “testicular vascular cone” (Cook et al., 1994), comprised of the highly
coiled testicular artery surrounded by the pampiniform plexus, a complex
venous network (Figure 1). There is a classical counter-current heat
exchanger in the testicular vascular cone, transferring heat from the artery
to the vein, thereby reducing the heat that is carried into the testes. The
scrotum has very high sweat gland density, so sweating and other wholebody responses such as panting keep testes cooler than body temperature.
Scrotal and testicular temperatures, and the role of blood vessels in
achieving these temperatures, have been described. Temperature gradients
were 1.6, 0.4, and -0.2°C for scrotal surface, scrotal subcutaneous, and
intratesticular temperatures, respectively (Kastelic et al., 1995). Therefore,
moving from the top to the bottom anatomically, the scrotum gets cooler,
whereas the testis get warmer. These temperature gradients were consistent
with the associated vasculature network of the testes. The scrotum is
vascularized from top to bottom. In contrast, the testis is essentially
vascularized from the bottom to the top; the testicular artery exits the
bottom of the testicular vascular cone, courses the length of the testis, and at
the bottom of the testis, divides into multiple branches that spread upward
and sideways across the surface of the testis before entering the testicular
22 Testicular blood flow and oxygen uptake were measured in eight
Angus bulls to determine the importance of blood flow versus normal
daily metabolism as sources of testicular heat (Barros et al., 1999). Blood
flow in the testicular artery averaged 12.4 mL per minute. Arterial blood
was warmer (39.2 versus 36.9°C, P < 0.001) and had more hemoglobin
saturated with oxygen than blood in the testicular vein (95.3 versus
42.0% P < 0.001). Based on blood flow and hemoglobin saturation, the
oxygen used by one testis (1.2 mL per minute) was calculated to produce
5.8 calories of heat per minute compared to 28.3 calories per minute
attributed to blood flow. Therefore, the major source of testicular heat is
blood flow, not the basal metabolism of the male (Barros et al., 1999).
Pathogenesis of Heat-induced Changes in
Sperm Morphology
The testis operates on the brink of hypoxia under physiological conditions (Kastelic, 2013), whereas in situations of increased scrotal/testicular
temperatures, metabolism and oxygen utilization increase, but blood flow
to the testis remains constant, resulting in frank hypoxia (Kastelic, 2013).
To determine the relative contributions of hyperthermia and hypoxia to
heat-induced changes in sperm morphology, mice were subjected to ambient temperatures of 20 and 36°C and concurrently exposed to hyperoxic
conditions to prevent the hypoxia induced by elevated testicular temperature (Kastelic et al., 2008). It was noteworthy that hyperoxia, which
increases testicular oxygen saturation, did not protect against hyperthermia-induced deterioration in sperm quality. Furthermore, since sperm
characteristics were not significantly different between mice exposed to
hypoxic versus normoxic or hyperoxic conditions at 20°C, it appeared that
the effects of increased testicular temperature on semen quality were due to
hyperthermia per se and not hypoxia (Kastelic et al., 2008). Similar results
were obtained with a scrotal insulation model in rams (Kastelic et al., unpublished). Although further work is needed to verify these findings, they
Animal Frontiers
do call into question the long-standing dogma that the effects of increased
testicular temperature on sperm morphology are due to hypoxia.
Effects of Increased Temperature on
Testicular Cells
Although heating seems to affect Sertoli and Leydig cell function, germ
cells are the most sensitive to heat (Waites and Setchell, 1990). All stages
of spermatogenesis are susceptible, with the degree of damage related to
the extent and duration of the increased temperature (Waites and Setchell,
1990). Spermatocytes in meiotic prophase are killed by heat, whereas spermatozoa that are more mature usually have metabolic and structural abnormalities (Setchell et al., 1971). Heating the testis usually decreases the proportion of progressively motile and live sperm and increases the incidence
of morphologically abnormal sperm, especially those with defective heads
(Barth and Oko, 1989). Although there is considerable variation among
bulls in the nature and proportion of defective sperm, the order of appearance of specific defects is relatively consistent (Barth and Bowman, 1994).
Unless spermatogonia are affected, the interval from cessation of heating
to restoration of normal spermatozoa in the ejaculate corresponds to the
interval from the beginning of differentiation to ejaculation (Waites and
Setchell, 1990). Even though sperm morphology has returned to normal,
their utilization may decrease fertilization rates and increase the incidence
of embryonic death (Burfening and Ulberg, 1968).
Summary of Increased Testicular Temperature
When scrotal/testicular temperature is increased, sperm morphology is
generally unaffected initially (for an interval corresponding to epididymal
transit time) but subsequently declines (Barth and Oko, 1989). However,
in some studies, sperm in the epididymis at the time of scrotal heating were
morphologically abnormal when collected soon after heating (Wildeus and
Entwistle, 1983). In another study, changes in these sperm were manifest
only after they were frozen, thawed, and incubated. Sperm morphology
usually returns to pre-treatment values within approximately six weeks after the thermal insult (Vogler et al., 1991). However, a prolonged or severe
increase in testicular temperature will increase the interval for recovery.
In general, the decrease in semen quality following increased testicular
temperature is related to the severity and the duration of the thermal insult.
Evaluation of Scrotal Surface Temperature with
Infrared Thermography
Infrared thermography is a technique that measures the surface temperature of the testes and, thus, can be used to assess whether bulls are being
exposed to heat stress. White and red regions are areas of elevated temperatures, whereas green and blue indicate reduced temperatures. Color patterns from bulls with normal scrotal thermoregulation were symmetrical
left to right, with the temperature at the top being 4 to 6°C warmer than at
the bottom (Kastelic et al., 2012; Figure 2). Random temperature patterns,
including a lack of horizontal symmetry and areas of increased scrotal surface temperature, were interpreted as abnormal thermoregulation of the
testes or epididymides. Nearly every bull with an abnormal thermogram
had reduced semen quality (Kastelic et al., 2012); however, it is noteworthy that not every bull with poor quality semen had an abnormal thermogram. As a consequence, although infrared thermography is a useful tool
for breeding soundness evaluation of bulls, it does not replace collection
and evaluation of semen. In one study, 30 yearling beef bulls, all deemed
Figure 2. Infrared thermograms of the posterior aspects of the scrotum in two beef bulls. Left: This bull has a normal temperature pattern; decreasing temperatures from
top to bottom and left to right symmetry. Right: This bull has a grossly abnormal temperature pattern, characterized by large areas of uniform temperature.
October 2013, Vol. 3, No. 4
23
An Angus calf. A series of experiments showed that increased nutrition during calfhood resulted in a more sustained luteinizing hormone pulse frequency increase
early in life, as well as improved testicular development and maturity (photo credit:
Wikipedia commons).
sound for breeding via a standard soundness examination, were individually exposed to ~18 heifers for 45 days. Pregnancy rates 80 days after the
end of the breeding season were similar (83 versus 85%) for bulls with a
normal or questionable scrotal surface temperature pattern, respectively,
but were greater (P < 0.01) than pregnancy rates for bulls with an abnormal
scrotal surface temperature pattern (68%; Lunstra and Coulter, 1997).
Effects of Nutrition on Male Reproductive
Development
In a series of experiments, Angus, Hereford, and Simmental bulls
were fed high or medium nutrition from weaning, which occurred at 6 to
7 months of age until they were 12 to 24 months old (reviewed in Coulter
and Kastelic, 1999). In general, bulls receiving high nutrition had greater
body weight and backfat, but paired testes weight was not affected by diet.
Moreover, bulls receiving high nutrition had less daily sperm production
and epididymal sperm reserves and greater proportion of sperm abnormalities. It was speculated that increased dietary energy may adversely affect
sperm production and semen quality due to fat deposition in the scrotum,
thereby reducing heat radiated from the scrotal skin and increasing scrotal
and testicular temperatures (reviewed in Coulter and Kastelic, 1999). In
another study, bulls fed high-nutrition diets had greater scrotal circumference than those fed medium-nutrition diets, but paired testes weights were
the same (Coulter and Kastelic, 1999). Since scrotal weight was greater in
bulls fed high nutrition, perhaps fat deposition in the scrotum increased
scrotal circumference in these bulls. In addition to the deleterious effects
of high-energy diets on reproductive function, these diets may also result
in abnormal foot growth due to laminitis, as well as adverse effects on bone
and cartilage growth, and may increase the risk of rumen inflammation,
liver abscess, and vesicular adenitis (Coulter and Kastelic, 1999).
A series of four experiments were conducted to evaluate the effects of
nutrition during calfhood (6 to 8 to 26 to 30 weeks of age) and the subsequent peripubertal period from approximately 30 to 70 weeks of age, on
sexual development and reproductive function in beef bulls (reviewed by
24 Barth et al., 2008). In these studies, increased nutrition during calfhood
resulted in a more sustained increase in luteinizing hormone (LH) pulse
frequency early in life (before 25 weeks) and greater testicular development at maturity. Conversely, low nutrition during calfhood suppressed LH
secretion before 25 weeks, delayed puberty, and reduced testicular development at maturity. For example, for bulls fed low, medium, or high nutrition from 10 to 70 weeks of age, age at puberty was 326.9 ± 5.5, 304.7 ±
7.4, and 292.3 ± 4.6 days respectively, and paired testis weights were 523.9
± 25.8, 552.4 ± 21.1, and 655.2 ± 21.2 g (mean ± SEM). Furthermore, the
initial suppression of testicular development and delayed puberty was not
corrected in bulls fed reduced nutrition before approximately 26 weeks of
age and subsequently placed on the high-nutrition regimen. Therefore, it is
not possible to compensate for the effects of low nutrition early in life by
subsequently giving supplemental feed.
When low nutrition was accomplished by restricted feed intake, hypothalamic and pituitary function were suppressed, with LH secretion most
severely affected (Brito, 2006). It appeared that insulin-like growth factor I
(IGF-I) was a possible signal to the central “metabolic sensor” involved in
translating body nutritional status to the gonadotropin releasing hormone
(GnRH) pulse generator (Brito, 2006). Nutrition also affected blood testosterone concentrations, indicating effects on the number and/or function
of Leydig cells. Age-related increases in physiological and GnRH-stimulated serum testosterone concentrations occurred earlier in bulls receiving
high nutrition but were delayed in bulls receiving low nutrition; these effects were probably mediated by both LH and IGF-I (Brito, 2006). Circulating leptin and insulin apparently have only permissive roles on GnRH
secretion but may enhance testicular development. Growth hormone concentrations decreased concomitantly with increasing IGF-I concentrations
during sexual development in bulls, suggesting the testes could contribute
considerable amounts of circulating IGF-I (Brito, 2006).
Sexual development and reproductive function were studied from 6 to
16 months of age in 22 Angus x Charolais and 17 Angus bulls (Brito et al.,
2012). Associations of average daily gain (ADG) and body weight with
ages at puberty and at maturity, scrotal circumference, paired-testes volume and weight, testicular vascular cone diameter and fat thickness, scrotal
temperature, sperm production and morphology, and testicular histology
were determined. There were no significant correlations between cumulative ADG and any of the end points investigated. Body weight at various
ages was negatively correlated with ages at puberty and maturity in Angus
x Charolais bulls, positively correlated with paired-testes weight in Angus
x Charolais and Angus bulls, and positively correlated with seminiferous
tubule volume in Angus bulls (P < 0.05). Semen quality improved gradually with age, and the interval between puberty (mean ± SD; 309.4 ± 29.7
and 357 ± 42 days of age) and maturity was approximately 50 days. Age,
body weight, scrotal circumference, and paired-testes volume were all
good predictors of pubertal and mature status, with moderate to high sensitivity and specificity (71.6 to 92.4%). In summary, growth rate between 6
and 16 months of age did not affect sexual development and reproductive
function in beef bulls. However, greater body weight at various ages was
associated with reduced ages at puberty and maturity and with larger testes
at 16 months of age. Therefore, improved nutrition might be beneficial, but
only when offered before 6 months of age. Average daily gains of approximately 1.0 to 1.6 kg/day did not result in excessive fat accumulation in the
scrotum, increased scrotal temperature, or reduction in sperm production
and semen quality and could be considered “safe” targets for growing beef
bulls.
Animal Frontiers
Conclusions and Future Directions
Bull fertility remains critically important for sustainable cattle production. Although considerable progress has been made in our understanding
of factors affecting bull fertility, and our ability to identify subfertile bulls,
there are still considerable gaps in knowledge. For example, there is a
need for reliable methods to accurately rank bulls as having good to excellent fertility. Increased testicular temperature interferes with production of
morphologically normal sperm and decreases fertility; although the pathogenesis has been classically attributed to hypoxia, recent evidence was
consistent with a direct effect of increased testicular temperature.
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About the Author
Dr. John Kastelic holds a DVM with distinction from the University of Saskatchewan (1982); a Ph.D. from the University
of Wisconsin–Madison (1990), and a Professor of Honorary Cause from Szent István University (2007). He is a diplomate
of the American College of Theriogenologists and a former Theriogenologist of the
Year (2009). He spent two years in private
veterinary practice, 22 years as a research
scientist, and recently joined the University of Calgary where he is a Professor of
Cattle Reproductive Health-Theriogenology and Head of the Department of Production Animal Health. For 10 years,
Dr. Kastelic was the Co-Editor-in-Chief of the journal Theriogenology. He
has published extensively on various aspects of reproduction, primarily in
bulls and cows, and has given numerous presentations on animal reproduction and scientific writing around the world.
Correspondence: [email protected]
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