Dog foxes begin the entry to breeding condition in August, as the production of sperm resumes following a hiatus during the late spring and summer months—accordingly, the testes have increased in size by around six-fold come December (from 1-2 grams to 7-8 grams). The greatest quantities of mature sperm are produced during December and January, after which sperm production reduces; sperm may be present in the epididymis until April (some studies have found sperm in every month) but will have deteriorated to such an extent as to be largely useless. It seems that foxes undergo significant increases in testes size, and invest relatively more energy resources into producing sperm-making tissues, because there’s a high demand for sperm given the brief period during which this species can breed.
Like most mammals (including dogs, cats, hedgehogs, bats, rodents and non-human primates), dog foxes have a bony structure in the penis called a baculum (or “os penis” - left). The baculum is a heterotrophic skeletal element—in other words, it's not attached to the skeleton—that has a rough base and a deep groove giving it a V-shape in cross-section; it serves to maintain an erection during intercourse. The baculum bends down towards the tip by an angle of 10 to 30-degrees and grows as the fox matures, reaching its full length (4 or 5 cm / 2 in.) at just over a year old.
During mating, a bulb-like mass of tissue surrounding the baculum tip (called the bulbus glandis) swells as it engorges with blood and the pair may become locked (or tied) together - this is known as a copulatory tie or copulatory lock, and is present in most canids. While copulatory ties do not always occur, when they do they can last anywhere from a couple of minutes to more than an hour (90 minutes is the longest I have come across in the literature). A study of 524 matings in foxes kept on a fur farm in California during the late 1930s and early 40s found that the average lock time was 26 minutes, with some variation according to age (adults tending to remain coupled for several minutes longer than yearlings).
In a short note to the journal Lutra in 2014 Rob Bijlsma described a lock between two foxes that he witnessed one February morning during the same year in the Netherlands. Bijlsma described how the male closely trailed the female onto a small heathland at which point the vixen suddenly crouched and was immediately mounted by the male. The initial copulation took about 25 seconds of pelvic thrusting, after which the male lifted his right leg over the vixen's back and they remained locked, back-to-back but in various positions of standing and lying down, for 29 minutes. The pair tried to separate every minute or so, which resulted in:
“fight-like jumping and tugging behaviour, and the male biting the female, or vice versa, in leg, neck or face till calm was restored”.
Bijlsma's account described how the stalemate came to an abrupt end when another outburst of biting resulted in the male jumping and landing a metre (3 ft) away, while the female landed in a crouching position. Interestingly, Bijlsma noted how, for the duration of the tie it was the male who remained obviously alert (i.e., head up, scanning the environment) as the female was least attentive and often had her eyes half closed.
Standing back to back appears to be an anti-predator response that positions teeth at both ends. In a brief article to May 2008 issue of The Norfolk Natterjack, the bulletin of the Norfolk and Norwich Naturalists’ Society, John Hampshire described two foxes “stuck” together in the dunes between Horsey and Winterton in February 2008 that were being pestered by another fox. Hampshire observed the third fox, a male, stalk around the locked pair for some five minutes, attacking both individuals frequently. On most occasions the aggressor was met by the teeth of whichever of the pair he was facing up to at the time, but his attention seemed focused on the male. Hampshire wrote:
“The pair wheeled around and around so that one animal was always facing the aggressive male.”
After a particularly violent bout of fighting the pair separated and the vixen fled, leaving the two males to continue fighting for a minute or two. Hampshire noted that it was easy to tell the fighting males apart because the recently-mated animal had a very swollen penis and testicles. The aggressor eventually forced his rival to flee and there followed a period of ten minutes where the aggressor chased his rival around a large area of the marsh.
Studies on the sperm of the captive foxes by Russian researcher I.D. Starkov during the 1930s found that the average dog fox ejaculated 6 millilitres (mL) of semen each time and that this contained in excess of 300 million sperm (usually 200 to 500 million). There was some variation in volume, with immature males producing less semen (2.5 mL) than mature animals; the largest volume Starkov recorded was 22 mL. Subsequent studies by Finnish biologist Liisa Jalkanen showed that ejaculated semen is composed of three fractions, with sperm making up only one or two mL but containing 200-500 million spermatozoa. To give this some context, a teaspoon is 5 mL and an adult human will ejaculate up to about 10 mL, containing about 180 million (up to 400 million) spermatozoa.
In a 1993 paper, Jalkanen presented data on her analysis of 161 ejaculates from 36 adult silver foxes—she found that, on average, 88% of the sperm in an ejaculate were normal and, of the 12% that were in some way abnormal, more than half had a defective flagellum (tail). Jalkanen also found that dogs in their first breeding season had fewer sperm (more of which were defective) than mature males.
In another study, also on captive foxes but this time on a Polish farm during the late 1940s, Zbigniew Wolinski found that males were usually capable of inseminating vixens for between seven and 18 days (although some up to 48 days) per breeding season, with most matings occurring during mid-February. Research on farmed foxes by Russian biologist Ludmila Osadchuk has demonstrated that levels of plasma prolactin and luteinizing hormone drop as the days shorten, while follicle stimulating hormone increases, stimulating the reactivation of the testes. In pre-pubertal animals, Osadchuk's data show testosterone reaches its peak just prior to the breeding season getting underway, while mature males don't reach this zenith until much later in the season.
Sperm production begins just before the start of the breeding season, with peak sperm production about one month later, coinciding with the peak of vixen receptivity. Indeed, it seems that mating in the 24 hours after ova are shed by the female offers the highest chance of conception in the fox so peak sperm production must be closely tied with ovulation of the vixen.
Red fox vixens are monoestrous spontaneous ovulators; in other words, they come into season once a year and ovulation is triggered by changing season (in this case, by shortening days and, probably also a drop in temperature, making foxes short-day breeders), rather than by the presence of a male or the act of mating. In a minority of cases (about 1%) on some fur farms, vixens have apparently become sexually receptive twice in a single year, but there is no evidence of this from the wild. The ovaries of vixens increase in weight from the end of June until the end of November, although they can start coming into oestrous (or “season”) during October.
The oestrous lasts for around three weeks and during this time there is a critically important phase, lasting for about three days (ranging from one to six days), during which the vixen is receptive to fertilization: this period is called estrus (or “heat”), and is one of four phases that make up the oestrous cycle. Vladimir Heptner and Nikolai Naoumov, in their 1988 Mammals of the Soviet Union, note that strong frosts and snowstorms delay estrus and that there is a significant change in intensiveness of the “rut” in the forest zone of the former USSR. In favourable years, according to Heptner and Naoumov, concerted estrus took place in the course of one month while, during unfavourable years, it expanded to two-and-a-half months.
According to Lloyd, in the absence of a successful mating, the vixen will revert to nine-month anoestrus (i.e., will no longer be receptive to breeding) after a period of pseudo-pregnancy of up to 40 days, during which she may even lactate. Studies on captive vixens have demonstrated that older females come into estrus earlier (by around a week) than younger ones and Wolinski found that there was no decline in fertility until a vixen reached eight years old (an achievement few wild animals will see). Working in suburban London, however, Stephen Harris observed a decline in breeding performance in vixens by their fifth or six year.