Scrotal thermoregulation in the bull: The effect of surgery, body temperature and ambient temperature

The bull's scrotum and associated scrotal cord vasculature is traditionally regarded as a thermoregulatory device for maintaining the testis at an optimal temperature for sperm production. Most studies on this topic have focussed on the direct effects of applied heat on spermatogenesis and/or only considered static measurements of scrotal temperature (ST) of no more than a few days. Continual measurement of ST in a natural setting has not been documented and as such the dynamic relationship between ST, body temperature (BT) and ambient temperature (TA), if one exists, has not been clearly defined. Cattle possess a strong diurnal cycle for BT, so if ST is to remain at a constant temperature the difference between the two must vary throughout the day, which would explain the range in reported differences from the literature of 2 to 7 °C. The aim of this study was to determine whether ST does in fact remain at a constant temperature relative to BT and if it does, how this relationship changes over days and weeks.

Four Wagyu bulls (identified as B2 to B5) were surgically implanted with two implants, each containing a calibrated and wax coated temperature data-logging iButton (DS1922T, Maxim, California; 30 minute logging interval); one implant was sutured approximately 20 mm into the muscle layer on the right hand side flank and the other attached mid-testis to the parietal vaginal tunic within the scrotum. Post-surgery, all bulls were allowed to recover individually in a shaded pen (IP1 and IP2; 34 m²) and were then released into a nearby paddock (PAD; 1200 m²) with access to shade, where the bulls remained for 20 to 27 days and after which time they were then returned to the individual pens for implant removal (IP2). This study was conducted from mid-summer to early autumn. Half hourly climatic data was recorded using a weather station (Esidata MK-3; Environdata Australia Pty Ltd, Warwick, Australia). Photoperiod data was obtained from Bureau of Meteorology from the closest weather station (040082, 27.54°S, 152.34°E).

Pearson correlations (Minitab® 16.2.0, 2010 Minitab, Inc.) were used to identify the relationship between BT, ST, TA, and photoperiod for each bull. All relationships were significant and ranged from moderate to strong (r = 0.501 to 0.936, p < 0.001); however, the strongest relationship for every bull was between ST and photoperiod (r > 0.803, p < 0.001). As photoperiod is almost perfectly correlated with time, this correlation is likely to be a trend over time rather than an underlying relationship with photoperiod. A repeated measures analysis using the MIXED procedure with a first order auto-regressive error structure assumed, was completed in SAS to model the long term trend (Figure 1) (SAS Institute Inc., NC, USA); the individual animals were subjects and the date of observation included as a fixed effect. This same model was also used to examine the diurnal trend (Figure 2) with time of day added as a fixed factor and location (IP1, PAD and IP2) as a covariate as the different locations represented different periods of time.

During IP1, there was a small daily decline in mean ST (Figure 1); this increased to a steeper decline from 37 °C to around 35.7 °C during PAD, followed by a steady temperature for 5 days and then an increase in ST during IP2. The pattern of ST is not mirrored by BT suggesting a more complex relationship between the two. As time passes it can be seen that both the shape of the ST cycle and the temperature itself changes over time (Figure 2). ST appears to follow the BT diurnal cycle in IP1 indicating a possible breakdown or compromise in thermoregulation, before returning to a more steady temperature in PAD and IP2.

The lack of thermoregulation in IP1 is probably due to post-surgical recovery (inflammation) resulting in a compromised thermoregulatory ability, in combination with the fact that TA was highest during this period. Whilst any noticeable inflammation from the bull's scrota appeared resolved within 7 to 10 days, the data would suggest that the effect on thermoregulation ability is longer lasting. The steeper descent (> 1°C) in mean ST when the bulls were in the paddock is thereby likely due to “full” surgical recovery and resumption scrotal thermoregulation. Additionally, the PAD was an open environment where behavioural thermoregulation was an option and the authors believe that behaviour plays an important role in the control of ST. Finally, once returned to the confines of the pen (IP2) the opportunity for behavioural thermoregulation was reduced so that a slight increase in ST may have been associated with increased periods of time where the bull was lying down with the scrotum in direct contact with the body (Figure 1); this despite the fact that ST during the day remains at a relatively constant temperature (Figure 2 IP2). Additionally mean TA during this period is around 20 °C thus the animals would not be under a significant heat load. Given this dataset spans less than 3 months and behavioural observations were not a focus, conclusive long term trends and the effect of behaviour if they exist cannot be fully determined. A longer data set covering a larger portion of the year with more detailed behavioural observations would be required to separate the effects of behaviour and post-surgical recovery.

Figure 1: Means ± SEM for BT (filled circles) and ST (open circles) representing the long term trend. TA (crosses) is plotted on a secondary vertical axis. Vertical dashed lines indicate where animals moved location (IP1 to PAD to IP2).

Figure 2: Diurnal pattern of ST (Bottom line), BT (middle line) and TA (top line on secondary vertical axis) (Mean temperature, ^oC ± SEM) from the different locations (IP1, PAD and IP2).