Introduction

Since one bull may be responsible for breeding 20 (natural service) to thousands (artificial insemination) of females, bull fertility is critically important. Although sterile bulls (total inability to reproduce) are uncommon, there can be a wide range in bull fertility, particularly in the absence of selection for fertility.¹ It is well established that a bull’s testes must be 2–6 °C cooler than core body temperature for fertile sperm to be produced; consequently, increased testicular temperature, regardless of cause, reduces semen quality.² Although the underlying cause of infertility in bulls is frequently unknown, I speculate that it is often increased testicular temperature.

Anatomy and physiology

Regulation of testicular temperature is dependent on several features. Scrotal skin is typically thin, with minimal hair and an extensive subcutaneous vasculature, facilitating heat loss by radiation.³ The scrotal neck is the warmest part of the scrotum; a long distinct scrotal neck (and pendulous scrotum) reduces testicular temperature by increasing the area for radiation and enabling the testes to move away from the body. The tunica dartos, a thin sheet of smooth muscle under the scrotal skin, is controlled by sympathetic nerves and contracts and relaxes in cold and warm environments, respectively.⁴ The cremaster muscle also contracts to draw the testes closer to the body under cold ambient conditions.⁴ Dorsal to the testis is the testicular vascular cone,⁵ comprising the highly coiled testicular artery surrounded by the pampiniform plexus, a complex venous network. The testicular vascular cone functions as a classic counter-current heat exchanger, transferring heat from the artery to the vein, contributing to testicular cooling. Characteristics of scrotal surface temperatures and the testicular vascular cone in bulls aged 0.5–3 years have been reported.⁶ In a recent study in bulls,⁷ testicular vascular cone diameter increased with age; furthermore, increased testicular vascular cone diameter and a decreased distance between arterial and venous blood in this structure were associated with increased percentage of normal sperm and fewer sperm with defects.⁷ In a comparative study of semen quality and scrotal/testicular thermoregulation in Bos indicus, Bos taurus, and B. indicus/B. taurus crossbred bulls, there were significant differences among these three genotypes in the vascular arrangement, characteristics of the testicular artery (e.g., wall thickness), and thickness of the tunica albuginea; overall, B. indicus bulls had the best thermoregulatory capacity whereas B. taurus bulls had the worst, with crossbred bulls intermediate.⁸

Sweating and whole-body responses also contribute to testicular cooling. In bulls, sweat gland density is highest in the scrotal skin.⁹ In rams, apocrine sweat glands in the scrotum discharge simultaneously (up to 10 times per hour) when scrotal surface temperature is about 35.5 °C.¹⁰ In these animals, respiration rate increases in association with scrotal surface temperature, reaching 200 breaths per minute when scrotal surface temperature is 38–40 °C.¹¹

Surface and internal temperatures

In beef bulls, average temperatures at the top, middle, and bottom were 30.4, 29.8, and 28.8 °C (scrotal surface); 33.3, 33.0, and 32.9 °C (scrotal subcutaneous); and 34.3, 34.3, and 34.5 °C (intratesticular).¹² Therefore, top-to-bottom differences (gradients) in temperature were 1.6, 0.4, and –0.2 °C for scrotal surface, scrotal subcutaneous, and intratesticular temperatures, respectively. Moving dorsal to ventral, the scrotum gets cooler, whereas the testis (independent of the scrotum) gets warmer. These temperature gradients are consistent with their vasculature, as the scrotum is vascularized from top to bottom, whereas the testis is essentially vascularized from bottom to top. In that regard, the testicular artery exits the bottom of the testicular vascular cone, courses the length of the testis (under the corpus epididymis), and at the bottom of the testis ramifies into multiple branches that spread dorsally and laterally across the surface of the testis before entering the testicular parenchyma.¹³ Blood within the testicular artery was a similar temperature at the top of the testis compared with the bottom of the testis, but was significantly cooler at the point of entry into the testicular parenchyma (intra-arterial temperatures at these locations were 34.3, 33.4, and 31.7 °C, respectively¹⁴). Therefore, both the scrotum and the testis are warmest at the origin of their blood supply (top of scrotum and bottom of testis), but they both get cooler distal to that point (i.e., bottom of scrotum, top of testis). Remarkably, these opposing temperature gradients collectively result in a nearly uniform intratesticular temperature in situ.¹⁵

In beef bulls, internal temperatures of the caput, corpus, and cauda epididymis averaged 35.6, 34.6, and 33.1 °C (gradient, 2.5 °C).¹² That the caput was warmer than the testicular parenchyma at the top of the testis was attributed to the proximity of the caput to the testicular vascular cone. Furthermore, it was noteworthy that the cauda, critical in sperm storage and maturation, was cooler than the testicular parenchyma.

It has been well established that bulls fed moderate-energy diets after weaning have better semen quality than those fed high-energy diets. In one study, beef bulls fed a moderate- versus high-energy diet for 168 days after weaning had a larger scrotal surface temperature gradient (3.9 vs. 3.4 °C, P < 0.02), more morphologically normal sperm (68.8% vs. 62.5%, P < 0.01), and a higher proportion of progressively motile sperm (53.4% vs. 44.5%, P < 0.006).¹⁶ Perhaps increased dietary energy reduced heat loss, thereby increasing the temperature of the testes and scrotum.

Sources of testicular heat

Testicular blood flow and oxygen uptake were measured in eight Angus bulls to determine the relative importance of blood flow versus metabolism as sources of testicular heat.¹⁷ Blood flow in the testicular artery averaged 12.4 mL/min. Arterial blood was warmer (39.2 vs. 36.9 °C, P < 0.001) and had more hemoglobin saturated with oxygen than blood in the testicular vein (95.3 vs. 42.0%, P < 0.001). Based on blood flow and hemoglobin saturation, the oxygen used by one testis (1.2 mL/min) was calculated to produce 5.8 calories of heat per minute, compared with 28.3 calories per minute attributed to blood flow. Therefore, the major source of testicular heat is blood flow not metabolism.

The testis usually operates on the brink of hypoxia.⁴ Increased temperature increases metabolism, with a concurrent need for increased oxygen to sustain aerobic metabolism. However, in rams,⁴ blood flow changes little in response to increases in testicular temperature and consequently the testes become hypoxic. Increasing blood oxygen saturation is not practical, since the blood is nearly completely saturated under normal conditions. Although increasing blood flow would increase the delivery of oxygen, it would also bring considerable additional heat into the testes. Therefore, increasing heat loss from the scrotum would appear to be the most appropriate response to increased testicular temperature.