Part 3: You talkin' to me? How foxes use scent
We use scents for a host of applications. They can cover up offensive smells. They can be employed, in the form of candles and oils, as agents of relaxation. We use them as perfumes and aftershaves - many a teenage boy having covered themselves in a popular brand of body spray before a Saturday night in town. More subtly, they help control our own sexual and emotional behaviour, even if we're largely oblivious to it. It seems, for example, that we can smell an element of our immune systems called the Major Histocompatibility Complex. When someone has an MHC that's vastly different from ours, they smell nice to us, even after a sweaty session in the gym. The theory goes that parents with different MHCs offer an evolutionary advantage in terms of germ resistance to their kids.
Neurobiologists have found that information regarding smell is readily stored in long-term memory, with strong connections to what's known as emotional memory. In other words, as many of us will have experienced, scents have a powerful ability to evoke memory. Kenneth Grahame, in Chapter 5 of his timeless classic The Wind in the Willows, published in 1908, described with rich literary allusion the scent that stopped Mole in his tracks while walking home with Ratty:
“It was one of these mysterious fairy calls from out the void that suddenly reached Mole in the darkness, making him tingle through and through with its very familiar appeal, even while as yet he could not clearly remember what it was. He stopped dead in his tracks, his nose searching hither and thither in its effort to recapture the fine filament, the telegraphic current, that had so strongly moved him. A moment, and he had caught it again; and with it this time came recollection in fullest flood. Home!”
We don't yet have the breadth of understanding to know whether foxes can identify each other's immune profile from their scent marks, but, thanks to meticulous studies by the likes of David Macdonald and David Henry, we do know they use them to mark out their territories, leave information about their sexual state, and perhaps even to keep track of food caches.
It's important to recognise that “solitary” does not necessarily imply “asocial” and, while foxes live singly or in pairs throughout much of their range, scent plays an important role in fox society. Indeed, it is likely to be critical in helping to prevent unnecessary conflict. Clear perimeter scent messages communicate that the area is occupied, reducing the need for the territory holder to patrol borders and fight with neighbours over boundaries, and allowing more time for finding food and raising cubs. Good fences make good neighbours, even in vulpine society.
The application of aroma
Anyone who has spent time watching foxes will probably have seen them cock their leg or squat during their daily forays, or have come across a pile of fox poo, often in bizarre or infuriating places such as on garden gnomes, shoes, steps, gas cages in the case of one place I used to work, and even on ultrasonic fox repellents! This perhaps gives the impression that foxes just urinate and defecate whenever and wherever the urge takes them, but in fact there is considerable method in how and where they leave these “calling cards”.
Based on our review of the glands above, we know scent can be deposited by defecation, urination, squirting of anal sac secretion, rubbing of the backside along the ground, mouthing objects or scraping at the ground/vegetation with the feet. In some cases a single scent may suffice, while others call for several different ones. Urine marks may be associated with foot-scraping, for example, or faeces may be deposited with or without accompanying secretion from the anal glands. What's left where, and how, depends on the type of message being conveyed, its importance, and how long-lasting it needs to be.
In terms of where scent marks are deposited, they are invariably left on conspicuous objects in the environment - those likely to attract the attention of other passing foxes. A little elevation also helps to get the message at “nose height” where it's less likely to be overlooked. Jacek Goszczyński, working in the mosaic forest/field landscape of Rogów in central Poland, found that during the winter (1984-1988) some 80% of scent marks were left on raised objects and, in his 1980 paper to the Symposia of the Zoological Society of London, David Macdonald noted how foxes may go to extra effort to get their marks up high:
“I have seen a fox standing on its fore legs while defaecating onto a [gorse] shrub”
A study of fox population dynamics in Bristol during the autumn and winter of 1995, conducted by Phil Baker and colleagues, observed two dog foxes for 1,550 one-minute intervals, during which they scent-marked with urine on 361 occasions. The structures on which they left their mark were recorded on 302 occasions and revealed that conspicuous permanent vertical structures (e.g. walls, fences, gate, lampposts, telegraph poles, etc.) were the preferred recipients, the target for just over two-thirds (68%) of the marks. Hedges, trees and bushes were also frequently marked (26% of occasions), while other permanent (e.g. post boxes) and temporary structures (e.g. car tyres and rubbish sacks) were relatively unimportant signposts, accounting for only 3% of the urine marks each.
Francisco Javier de Miguel and colleagues at the Autonomous University of Madrid found that foxes in their study area of central Spain actively selected woody plants, particularly holm oak shrubs and rockroses, over grasses for faecal scent mark deposits. The authors stop short of linking their observations with a behavioural explanation, but the inference is that the pervasive scent of rockroses, which is clearly discernible to humans and thus (probably) also to foxes, could render it an attractive object to other animals, making it more likely their scent mark would be discovered. Scents may also persist for longer on woody species than on grasses. This ties in with personal observations that foxes may target specific woody bushes (e.g. Spirea) in gardens to vigorously scent mark, ignoring other plants and shrubs.
It makes sense that scent signposts remain in situ at least in the medium term (i.e. more than 24 hours), otherwise the fox would be forever patrolling its territory to reinforce the messages and would have no time to eat or sleep. It is therefore curious that Goszczyński found his foxes frequently marked “non-durable objects”, such as sticks/twigs and just the ground's surface. Presumably the choice of marking post at least partly reflects availability within the landscape, and urban foxes in Britain may be rather spoilt for choice. Of particular interest in Goszczyński's data set is that males appeared to more actively deposit scent on durable items (trunks, stumps, stones, burrows, etc.) than females, perhaps reflecting the observation by several authors that males perform the bulk of the territorial scent marking. Indeed, he noted that males scent marked more frequently than females (5.7 per km vs. 4.2 per km) and that 79% and 21% of urine marks were left on permanent and non-durable structures, respectively, compared with 15% and 85%, respectively, for vixens.
Before we look at urination and defaecation behaviour in more detail, it is also worth mentioning that scent marking is associated with the social and health status of the individual and the presence of potential predators. Foxes suffering from the brain parasite Toxoplasma gondii (toxoplasmosis), for example, do not appear to scent mark their home ranges. Viyanna Leo at the University of New South Wales and colleagues found that foxes behaved more apprehensively around feeding stations in the Strzelecki Desert, Australia, to which dingo scent had been applied, suggesting foxes can recognise predators by their scent alone. The response to a scent also appears to depend on age, and David Macdonald observed that his tame vixens would respond to wild fox urine with “overt submission” (the same behaviour they might use to greet an adult fox) until they were about 14 weeks old; by four months they merely stopped to sniff the mark briefly before carrying on.
Male foxes typically scent mark with urine by cocking their legs, that is, by lifting one or other back leg at an approximately 90-degree angle to the ground allowing a jet of urine to be projected at upright objects. This method of scent marking means that dog fox urine can be found 20-25cm (8-10 in.) above the ground. It should be noted, however, that while leg-cocking is typically dog fox behaviour, it cannot be taken for granted. David Henry, in his 1979 paper to Chemical Signals, described two males squat urinating; one juvenile did so for 81% of the scent marks he observed, while another of unspecified age squatted 56% of the time. Vixens rarely fully cock their legs, which David Macdonald suggested is possibly a reflection of their pelvic anatomy, and this means it is often possible to assign the sex of the fox leaving the mark. Henry, in his 1979 paper, explained:
“Field observations from this study support that a male red fox deposits urine in front of his hind paw marks, either directly in front if a squat posture is used, or laterally in front if a raised leg posture is used. The study agrees with Jorgenson's statement that a female red fox deposits urine either between or behind the hind paw marks.”
The above notwithstanding, vixens are sometimes observed partially raising a rear leg to urinate, although this is in a manner more akin to a limp than the leg-cocking of dogs. There's more to fox urination than simply the cocking of a leg, though. In a fascinating paper to Zeitschrift für Tierpsychologie, published in 1979, David Macdonald meticulously recounted his observations on the urine marking behaviour of his hand-reared foxes during leash walks, a captive family of foxes, and some of the local wild residents.
Macdonald described two distinct types of urination: squat urination, where the animal squatted and urinated in a single burst (lasting 7-25 seconds), which wasn't preceded by sniffing or directed at any particular structure; and token urination, which developed at 6-10 months old and consisted of the fox sprinkling a few drops of urine at different, usually visually conspicuous, sites and following up with a great deal of sniffing. Macdonald considered that squat urination was simply the voiding of urine, while token urination was intended to carry a specific message.
Urine marking seems to be concentrated along edge features, with marking rates depressed off regular paths. Macdonald found a strong correspondence between the number of token marks per site and the number of walks per path at the site. In other words, the more often a path was walked, the more scent marks there were per metre. Additionally, more 'tokens' were left on the outward walk than the return walk (about one-third as many) along the same path, and marking rates were higher within the vixen's range than during brief forays outside. A vixen walked for 4.5 hours one night marked 224 different sites. Marking rates were about one per 10 metres (33 ft.) in her home range to one per 40 m (131 ft.) on equivalent terrain outside her range; returning to her range, marking rate increased back to about one per 16 m (52 ft.). Macdonald wrote:
“Token marking involved continual 'topping up' of particular marking sites often through deliberate detours.”
Among both sexes, token marking was most prevalent during the winter breeding season, peaking for vixens in December and dogs during mid-January; the latter frequently “over-marking” (i.e. urinating on top of) scent marks left by the former, particularly when the vixen was dominant. Males continued to token mark throughout the year, but at a much lower rate than females. Vixens exhibited a sharp decline in token marking immediately after oestrous and this, coupled with observations by Macdonald of his captive group that dominant vixens token marked while subordinates squat urinated, suggests that this behaviour is associated with communicating breeding status as widely as possible. Indeed, it also aligns with an observation by Bridget MacCaskill who, in her 2001 book, The Blood is Wild, described the behaviour of her hand-reared vixen on a walk during her first breeding season:
“She pulled me along as if we could not get anywhere fast enough, leaving her mark everywhere, on pathways, patches of moss, flat-topped boulders, and generally making sure the fox world knew she wanted a mate.”
Urine marks aren't only reserved for geographic markers, however, and some intriguing observations suggest that they may also have more subtle social and gastronomic functions.
Allomarking is a behaviour whereby one member of a group scent marks another, and it's a well-documented behaviour among mammals. Rabbits squirt urine at each other during courtship, for example, while badgers frequently dab clan members with their subcaudal glands to help create a group scent, and there are a few observations suggesting foxes also engage in this behaviour. Dominant males in Macdonald's group were observed to token mark subordinate group members, typically on their heads and shoulders while they were lying down. Similarly, I have seen a dog fox (rather awkwardly, it must be said) allomark a vixen stood feeding. Unfortunately, this remains a poorly studied area of fox biology.
A slightly better-known aspect of fox urine marking is that associated with food. Of particular interest are the results of a series of ingenious experiments conducted by David Henry on 15 wild foxes in Canada's Prince Albert National Park in Saskatchewan during the early 1970s. Henry noted that foxes frequently urinated when scavenging, with marks deposited within 15cm (6 in.) of objects of interest, typically directly on them. Although brief, lasting only about two seconds on average, urine marks were manifold, with some foxes token marking up to 70 times per hour while scavenging. Henry wanted to understand the reason for such prolific scent marking and devised two experiments.
Henry presented his subjects with seven different substances, including dried and wet dog food, recording whether the fox ate and/or urine marked it. He found, after 30 runs with each substance, foxes ate the wet dog food and consistently (77% of the time) urine marked the spot where the food had been and thus left a greasy food residue. The dried dog food, which didn't leave a residue, was always eaten but only urine marked on four (0.13%) occasions. Additionally, the foxes retrieved buried wet food, ate it, smelt the hole and then urine marked it - in only 2 (0.9%) of 225 caching bouts observed did they urine mark a full cache, which piqued Henry's interest further. Could it be that the urine mark carried a message about the cache?
In the second experiment, Henry created some caches of dog food and waited for a fox to arrive and investigate. Over 15 days in October 1972, Henry found that once in the test area it took foxes, on average, about ten seconds to find the dog food buried 8cm (3 in.) below ground, and caches were investigated for about seven seconds at a time. Intriguingly, caches where a fox had urinated after eating the contents were investigated for only about a second, the same length of time they investigated random sites on the woodland floor where no food was present. In his paper to the journal Behaviour in 1977, Henry explained:
“Spots that had both the odor of food and urine were investigated as if no food stimuli were present. This suggests that the message content of a urine mark at a food remnant is equivalent to 'no edible food present'.”
In other words, the foxes appeared to be employing urine marking as a kind of “bookkeeping” system, alerting them to the fact that there was no food present even if the smell lingered. Moreover, Henry's stats suggest that this was potentially highly effective, improving their foraging efficiency by reducing investigation time by one-seventh (14%). Henry went on to establish that if the food odour was sufficiently strong (e.g. 30g vs. 3g of food in the cache) the fox would dig in spite of the urine mark.
The application of this bookkeeping system at a larger scale remains unclear. Polish biologist Lech Ryszkowski and colleagues, for example, found a very strong positive correlation between scent-marking behaviour and field vole (Microtus arvalis) density in western Poland's Wielkopolska region, but the majority of sites where hunting was successful were left unmarked. Similarly, Goszczyński found that the frequency of marking at carrion sites was not correlated with the amount of food it could provide.
Perhaps less well understood than the bookkeeping system postulated by Henry is the habit many foxes have of urinating on food and in water. Comments on social media platforms against trailcam videos of such behaviour imply that the meaning is straightforward: “This is mine”. While a claim of ownership is logical, it appears somewhat lacking in respect of water bowl urination, which seems most common during the late summer when cubs are becoming independent and ranging over the whole of their parents' territory. Similarly, urination in water bowls does not appear to prevent other foxes or species from drinking. One wonders whether this may be a method for subordinates or itinerants (i.e. those just passing through) to hide their scent from the territory owner by diluting it?
During his Rogów studies, Jacek Goszczyński noted that foxes mainly scent marked at sites with an attractive smell that might make other predators more likely to intensively search, which perhaps explains his observation that 34 (32%) of the carcasses he investigated had been marked with fox urine. This idea of a communal messageboard also makes more sense as an explanation for scent marking of food in gardens. If the aim was to ward off others, why leave it? Why not take it off and cache it somewhere? Henry's experiments suggest that, if the food were buried, a urine mark may fool other foxes into thinking there was no food left - but in most of the footage I have seen there is still food in plain sight. Perhaps a token mark on the food acts as a more subtle message to other passing foxes that the area is occupied and they stay/feed at their own risk. Additionally, a fascinating observation by West County-based naturalist Kelly Kilfeather suggests urine marking may help teach the cubs what's safe to eat. Kelly's observations are published below, with her consent:
“I've also seen adult foxes peeing ON food, which their cubs later came, sniffed, and then seemed to gain confidence about and ate… so I think in some contexts the cubs learn from these scent marks what to investigate and eat.
I saw different versions of similar occurrences but one very memorable one was when the mother vixen peed on a sausage… which she could have easily taken away with her (and I would have expected her to, since she had cubs in tow) but instead she just peed on it and went and sat on the lawn. The cubs took a few minutes approaching the patio, clearly nervous, doing the two steps forward, one step back nervous approach. One managed to get as far as the sausage, sniffed the yellow river that Mum had left, licked it (yuck!) and then noticeably relaxed and snaffled the sausage for itself… while Mama watched from the lawn.”
Finally, foxes show a propensity to urinate on unfamiliar objects in their environment. Goszczyński suggested that urination on gloves and plastic bags left by forestry workers as well as small mammal traps set in the woodland may have been the foxes familiarising themselves with new objects appearing in their territory.
It seems that David Macdonald summed urine marking behaviour up succinctly in 1979, when he wrote:
“… it is clear that urine marking communicates diverse messages within fox communities.”
To the frustration and horror of many a gardener and dog walker, foxes commonly employ their poo as a scent marking tool. Faeces are a more robust and visually conspicuous calling card than urine, remaining visible for days or weeks rather than hours. Their production is, however, directly proportional to the fox's food intake, accounting for the observation by Goszczyński that defaecation rates fell during the winter rut when food is more difficult to come by and males are preoccupied with finding mates.
During his Polish forestry study, Goszczyński found that droppings were most frequently deposited on the flat surface of snow (62% of those found in forests, 78% in fields), at hunting sites, and on or near carrion. Of the 105 carcasses he recorded during his study, 24 (23%) were marked with fox droppings, the number of droppings accumulating over successive feeding visits. More generally along fox trails, foxes defaecated at a rate of roughly one scat per three kilometres (2 mi.), with vixens marking at a slightly higher rate than males (again, possibly because dogs show less interest in food during the breeding season).
Similar to the urine marking of areas with high vole density, some data from Spain suggests that foxes may use productive feeding grounds to help intensify the messages in their droppings. On their study site, an oak-pine forest in Madrid, Raquel Monclús and colleagues at the Universidad Autónoma de Madrid investigated the scent marking behaviour of foxes in relation to the abundance of rabbits, their main prey in the region. They observed that foxes scent marked more frequently and were significantly more likely to use faeces than urine where rabbit density was high. Scent marks were typically placed in clearings, highly strategic places where several tracks intersect, and were accompanied by conspicuous environmental elements, such as tussocks, paw scrapes and latrines. The authors concluded that “… foxes used the remains of rabbit activity as amplifiers for their scent marks”. Additionally, several authors have observed foxes overmarking droppings with urine, or vice versa, which may similarly serve to amplify the mark. David Macdonald found, for example, that 70% of the droppings left during his leash walk experiments were deposited on sites previously marked with urine.
How often anal sac secretions are added to faeces remains largely unknown. Comparisons have been made with anal sac ejection in wolves, which happens on about 7% of defaecations and is most often applied by adult males, but there may not be a direct association between this behaviour in these socially different canids. Anal sac application may vary seasonally, as in her German paper to Forma et Functio in 1969, Berlin University anatomist Ingrid Spannhof described how the glandular epithelial activity of the anal gland in red foxes showed peaks during March/April, with smaller peaks in August/September and November. We also know that foxes find incubated anal sac extract very attractive, much more so than urine, suggesting that it has an important communication role.
Both Eric Albone and his colleagues in 1978 and Bristol University biologist Ruth Blizard and George Perry in 1979 found that foxes were more attracted to the bacterial metabolites of fox tissues than the same metabolites of other media. Albone found wild foxes spent longer sniffing at anal sac inoculum than that of meat broth or egg yolk. During their study in the Oxfordshire woodland in which David Macdonald conducted much of his Ph.D. research, they also found that these wild foxes were more interested in scent stations containing incubated fox extract than the alternatives. Interestingly, unfermented fox extract was no more attractive to the foxes than water. Blizard and Perry exposed their captive animals to two ports through which odours were blown and found that the one emitting incubated fox extract was visited more frequently and sniffed at for longer than the control port.
Finally, as with urine, foxes may allomark each other with faeces. In August 2015, veteran fox-watcher Maggie Bruce photographed a vixen defaecating on a related female in her garden in Yorkshire. This was the first time Maggie had observed this behaviour, and I have been unable to find anything about it in the literature. Nonetheless, it appears this wasn't unique. Panthera project's lead mammologist Mark Elbroch told me:
“We've caught the behavior on video several times at carcasses in the Northern Rockies, USA. A red fox will run backwards at a conspecific, or stand stationary, and shoot scats at another—with their tail curled safely to one side of them. The fox at the receiving end runs off in the encounters I remember… we didn't know what to make of it?”
Similarly, Janet Foley at the University of California, Davis' School of Veterinary Medicine mentioned that this behaviour has been seen in dogs kept in boarding kennels in the USA, although she'd never witnessed it personally. I would be very interested to hear from readers who have witnessed this behaviour in foxes.
Foxes have circumoral glands, enlarged integumentary glands embedded in section between the skin on their lips and that in their mouths (mucosa) known as the mucocutaneous junction. These glands have been poorly studied in foxes, but it seems likely they play a role in greeting and territorial behaviour as they do in cats and dogs. A fox may deploy scent from the glands by rubbing its chin on the ground or against tree trunks/saplings/shrubs, or by mouthing objects. Mouthing consists of wedging a branch or piece of vegetation in the corner of the mouth, often leaving a visible trail of saliva. David Macdonald notes that such mouthing may also be directed at other foxes within a family group, presumably helping to create a group scent. Mouthing of vegetation typically occurs during the winter breeding season (i.e. December and January), while food objects are mouthed throughout the year, reflecting how territorial behaviour and priorities change through the year.
Foxes may also scrape the ground or flattened vegetation with their feet, particularly their hind legs, following dominant encounters and/or scent marking. This activity may serve a dual function: applying additional scent from the sebaceous glands in the feet, and leaving an area of disturbed ground that may serve to draw the attention of any passing foxes, hence amplifying the message.
Let 'em have it - scent marking triggers
We're only just starting to recognise that foxes are more socially complex than we initially gave them credit for, and it's little surprise that several factors seem to affect when foxes scent mark. One of the most significant triggers appears to be the presence of another scent mark, typically urine and particularly the urine of an intruding animal (so-called “alien urine”).
In the mid-1970s, the late Jackson Laboratory biologist Melba Wilson and her colleagues found that synthetic urine, which included Δ3-isopentenyl methyl sulphide, one of the sulphur-based chemicals that appears to be specific to red foxes and present in higher concentrations in dog than vixen urine, triggered wild foxes in Maine's Acadia National Park to over-mark when placed along tracks. Moreover, they produced test mixtures with and without the sulphide and observed that they were over-marked while the sulphur-free ones were not. They suggest, therefore, that methyl sulphides present in fox urine is the principal attractant to foxes, causing them to over-mark.
Around the same time, Ruth Blizard and George Perry noted how their captive dog foxes over-marked 63% of alien male urine samples, while David Macdonald found that his leash-walked vixens would invariably urinate on unfamiliar scent marks. In his 1979 paper on fox scent marking behaviour, Macdonald described how the application of alien urine (collected from dead foxes submitted for post-mortem) to the vixen's regular territory resulted in her investigating and over-marking them. Over-marking was followed a minute or so later by the vixen excitedly running between this and her own nearby scent marks to sniff them and, despite not having marked these sites previously on the walk, all but one was remarked on subsequent walks. Macdonald explained:
“The intensive sniffing that the vixen typically showed as she approached these experimental sites, which began 2 m away, was accompanied by other changes in her behaviour; the area surrounding the experimental site was investigated, often with a slightly crouched body, tail curved and ears flicked backwards (postures associated with unease), and she might return to the site several times, sometimes urinating for a second or third time.”
Macdonald also observed that, during the pairing season (December and January in the northern hemisphere), dogs were seen to follow and over-mark the scent marks of dominant vixens only, suggesting that social status may also be an important trigger.
Wesley Whitten and his colleagues studied the marking behaviour of foxes living in two areas of Maine's Mount Desert Island during the breeding season. They found that a key indicator of whether a fox would scent mark a particular area was the presence and strength of existing scent, with foxes preferentially marking those mounds the researchers treated with a test solution (synthetic urine) at both sites. The biologists concluded, much as Blizard and Perry found, that the smell of urine, and particularly the presence of Δ3-isopentenyl methyl sulfide and 2-phenylethyl methyl sulfide, caused their foxes to scent mark.
More recently, experiments by researchers at Bristol University have added weight to the early observations on alien urine affecting territorial behaviour among foxes. In the late 1990s, a team led by Phil Baker, now at Reading University, found that when artificial scent was added to urban fox territories the residents responded:
“Thus both foxes responded to simulated intruder pressure by overmarking some of the simulated scent marks and by increasing both their scent-marking activity in the immediate vicinity of the simulated scent marks and their rate of marking.”
Similarly, while working on his Ph.D. in Bristol, Janosch Arnold found that application of synthetic urine into a fox territory caused males (but not females) to increase the amount of time they spent searching the area - the effect being stronger in larger males than smaller ones. It didn't cause a change in the overall amount of time the foxes were active for, or the size/shape/location of the territory, just the time spent in the scent-marked area. Vixens, by contrast, tended to avoid the area treated.
David Macdonald hypothesised that a combination of vegetation structure and the presence of an existing scent mark were triggers for urine marking. Concordant with Whitten and company, he considered that scent was “allowed” to decay to a certain point below which it needed “topping up”. Similarly, a tussock would be over-marked if alien urine was found on or near it.
During a six-year study of 14 fox cubs (4m, 10f) visiting John Fawcett's garden in the New Forest, Hampshire, he and Bristol University biologist Carl Soulsbury found that scent marking was an important component of family life for cubs; it changed according to sex and the likelihood of dispersal, and was involved in within-litter social interactions. It should be noted that the data presented by Soulsbury and Fawcett in their 2015 paper to Folia Zoologica are subject to substantial variability based on the error bars on the plots. Broadly, however, males scent-marked with urine more often than females in summer at 3-4 months old, declining rapidly as they aged; females also scent marked less as they grew older, but the decline began later and was more gradual. Philopatric vixens (i.e. those that remained on the family territory) had higher urine marking rates than those that dispersed. Soulsbury and Fawcett suggested:
“Our evidence indicates that this earlier lowering of social group affiliation, or increased within-group conflict among males, leads to earlier reductions in urine marking rates, compared to females.”
This study looked only at cubs, while an earlier paper reviewed the urine marking behaviour of 34 foxes (23f, 11m) visiting Fawcett's garden between 2007 and 2012, reinforcing the view that there are sex differences in territorial behaviour of foxes. Urine marking varied significantly across months, lower in June-August and with a strong interaction between month and sex. Marking rates were generally higher for males than females between August and November (the main juvenile dispersal period), but not significantly during the rest of the year, except in March when males urine marked significantly more frequently than females, which were presumably busy with cubs. In their paper to the Journal of Ethology, Fawcett and his coworkers explained:
“Urine marking is lowest during summer when territorial intrusions are least, whilst the higher male urine marking rate in March reflects the period when females are denning.”
In other words, maintaining urine marking rates in spring may reduce or discourage intruders that might threaten cubs.
In line with the suggestion that social status is a trigger for scent marking, in his 1979 Zeitschrift für Tierpsychologie paper, Macdonald noted that dominant males token marked much more frequently than subordinates, and victorious dog foxes often token marked at a high frequency for a minute or two after an aggressive encounter. Finally, Raquel Monclús and her team found that foxes scent marked more and increased the detectability of those marks in areas of high rabbit abundance at their study site in Madrid, suggesting prey resources may trigger scent marking as well as serving to amplify the marks.
Meaning in malodour
Konrad Lorenz, in his book Man Meets Dog, published in 1954, likened the idea of a dog cocking its leg to a nightingale singing, both species exhibiting equivalent territorial behaviour. The studies touched upon above lend support to this idea that scent marking is an important element of territorial delineation and defence, analogous to the fences and walls we put up around our property. Despite the countless hours spent watching foxes there's still more to understand about how the use of scent marks varies according to individual priorities. In his 1979 Zeitschrift für Tierpsychologie paper, for example, Macdonald noted how a dog fox accompanying a vixen marked ten times more frequently during the winter (February, the breeding season) than in spring (April), while another dog fox tracked across snow in April urinated 14 times in the space of 200m (220 yds). At other times, a fox may not urinate for hours on end.
That scent marks are left in conspicuous places tells us that they are meant to be “read” and their change of state (urine marks start off straw yellow and oxidise to an orange-brown within a few hours, for example) may allow their age to be inferred by the reader. Marking of home range borders and an increase in such behaviour during the breeding season suggests denotation of territory is a significant part of their application. Indeed, this is further supported by Macdonald's observations that foxes are reluctant to mark outside their home ranges and his subjects were more easily startled on walks away from their territory, and by Viyanna Leo and her coworkers’ findings that their subjects were nervous around stations and water sources containing unfamiliar fox scent, suggesting scent marks contain enough information to encode when strangers are about. That said, a team of biologists at the University of Sydney, led by Peter Banks, found that foxes were largely uninterested in scent stations treated with the scent of unfamiliar foxes, but were strongly attracted to those treated with wild dog and cat urine - potential predator and competitor, respectively. It may be that the response to scent marks varies with resource availability or some other ecological dynamic.
By digging up and transplanting urine marked sites, Macdonald also found that he could change the marking pattern of a vixen in her territory, causing her to abandon the previous sites she marked regularly and continue to mark at the translocated ones. Tussocks moved outside the vixen's range were always investigated, but never re-marked. He also observed that applying alien urine within the boundaries slightly reduced her range, causing her to turn back prematurely. Likewise, the presence of alien urine on the other side of the territory boundary made his tame vixen much more likely to turn around; she'd sometimes venture out her range if no alien urine was present. This suggests that the presence of their own scent marks may be as necessary for them knowing the limits of their territory as they are for letting potential interlopers know the area is occupied.
The observations of Sidney Bailey, Jacek Goszczyński, Eric Albone, Peter Flood and others that the components of these scent marks change over time, 3-methylbutyl methyl suphide peaking during the height of sperm production for example, indicate that scent marks carry information about breeding condition. This, coupled with behavioural observations of the frenzy with which individuals may scent mark during the breeding season, implies they can be used to signal sexual availability.
James Jorgenson and colleagues, in their 1978 paper to Science, reported that fox urine had a much more pungent smell during the breeding season. David Henry concurred, writing how, while tracking foxes in Canada's Prince Albert National Park, he was able to smell dog and vixen urine marks from significantly further away between December and February than in March or April. This would correspond with seasonal peaks in some urinary components found by Bailey and others.
Of 43 fresh urine marks examined in December, Henry found he could smell them from 30-60cm (1-2 ft.) away, while those of both sexes deposited from early January suddenly had a “strong musky odor” that meant he could smell them up to 5m (16 ft.) away. In contrast to the abrupt onset, this smell began diminishing slowly from the end of January until it approached pre-breeding levels, such that urine could only be smelt 25-45cm (10-18 in.) away come late March/early April. This perhaps corresponds to an increase in Δ3-isopentenyl methyl sulfide and 2-phenylthyl methyl sulfide production in January. Writing in his paper to Chemical Signals in 1979, Henry explained:
“… the odor of red fox urine abruptly intensifies at the beginning of the breeding season [in North America, most foxes mate in January or early February], stays at this intensity for approximately three weeks and then gradually diminishes over the next two months. The intensity of odor of both male and female scent marks appears to follow this pattern.”
As well as changes in urine components through the year, we know the activity of the violet gland changes seasonally, being much more active during the winter months when foxes are breeding.
The jury is still out on whether scent marks carry individual-specific information - i.e. whether a “reader” can tell not only that another fox is around, but who that other fox is. As we've seen, early work suggested dog fox urine contained a component (quinaldine) that vixen pee didn't, but that was subsequently proven incorrect. Similarly, Albone and Perry struggled to separate individual foxes based on their anal sac secretions, although they had more success looking at the ratio of putrescine to cadaverine. Likewise, Georges Ware and Pauline Gosden at Bristol University failed to find any correlation between the microbial flora in the anal sacs of the 24 foxes they studied over the two years of their experiment - different foxes sometimes produced identical strains, while the same fox also frequently yielded different strains. While working on his Ph.D. at Bristol University, however, Janosch Arnold found that nutritional condition and stress level affected the volatile compounds present in the urine of his foxes.
Whatever the final picture, the fact that foxes respond differently to unfamiliar scent marks suggests that they decode information our mass spectrometers do not and studies on other mammals have found individual differences in scent composition.
Tamako Miyazaki and colleagues at Iwate University in Japan found individual differences in the anal sac secretions of 13 domestic cats. Similarly, work by Christine Buesching and the WildCRU team at Oxford University has demonstrated that badgers (Meles meles) leave individually-specific scent marks, and Eleanor Kean has shown how the anal gland secretions of otters become darker with maturity, while the volatile composition changed with age and reproductive status. Jane Hurst and coworkers at the University of Liverpool demonstrated that major urinary proteins (MUPs) were important for individual recognition among house mice (Mus domesticus). MUPs are highly individual, being genome derived and having stable expression patterns, making them well adapted for communication of individual identity and status. Additionally, the researchers found that the MUPs of male mice bond to volatile signalling pheromones, causing them to be released slowly from urinary scent marks, presumably both prolonging the duration of the mark and also allowing other mice to ascertain how long ago it was left.
Finally, Gunter Tembrock at Humboldt-Universität zu Berlin noted that when foxes met, they sniffed each other's lips, ears, anogenital region and violet gland, hinting that different scent glands convey different messages. This may thus carry over to the scent marks left behind; a site marked with urine and faeces may tell a different story to one where the chin has been rubbed on the ground or where urine was applied in isolation. In ferrets, for example, Rachel Berzins and Remi Helder found neither sex was particularly interested in body or urogenital odour of the opposite sex, but both were engrossed by anal gland samples.
So, in short, foxes are smelly because scent forms an integral part of their social communication. It's the equivalent of our signposts, bulletin boards and social media, letting foxes know other foxes are around and, most probably, who those foxes are and how long ago they were there. It also serves to mark out territory ownership, akin to our walls and fences, and to play a role in helping teach cubs what to eat and perhaps even to keep track of caches.
To wrap up, I want to quote David Macdonald again, who summarises the use of scent by foxes very succinctly in his Running with the Fox:
“Not only should we expect each scent to convey a diversity of information - we should expect its context and function to vary between individuals. The selective forces acting on each individual within a society are different and these will be reflected in their scent marking behaviour, as in all other aspects of their social life.”