Charlotte Nevison and Rosie Barclay
Are you embarrassed when your dog thrusts its nose into the groin of a visitor to the household? Has your usually obedient canine ever been known to run off apparently oblivious to your calls then stop and roll delightedly in the remains of a long dead creature or fox scat? Do you have to wait because your dog has refused to move until he has checked out and cocked his leg at every lamppost, or seen your otherwise placid pooch turn into a master escape artist when the bitch next door is in heat? Yes? Then you are not alone. To us these behaviours can be inexplicable, confusing, inconvenient and possibly repulsive, but these behaviours indicate that our canine companions are motivated to respond to scents that we are either unaware of, or do not appreciate! In this chapter we will unravel some of the mysteries of the sensory world of dogs by illustrating how their sense of smell differs from ours, why scents are important to them and how misunderstandings about scent relate to some of the common ‘problems’ we experience with our canine companions.
Before discussing what important information is conveyed in scents we need to think about what scents are and how animals’ gain information from them. You will be aware that objects may smell, as may liquids and that some smell more than others. You may also become aware of an odour without deliberately sniffing at something. To this end all animals are basically alike but what is your brain actually responding to?
Scents are airborne molecules (volatiles) that have typically been released from a solid or liquid source. They may consist of a variety of volatiles released at different rates depending on factors such as the weather and whether or not they are being sniffed! When inhaled volatiles are detected by specialised cells which send signals to the brain. These signals may then elicit a behavioural response if the volatiles convey information that is relevant to the animal at that particular time.
Although we detect odours in the same way, in comparison with most other mammals humans are pretty poor at detecting scent. It is estimated that dogs have a 100-1000 times greater potential to detect odours than us because they possess more receptors for scent. This allows them to detect volatiles at a lower concentration in the atmosphere; they can more easily detect sources which release volatiles slowly or that are further away.
Scientists have demonstrated that dogs and other mammals have a much superior sense of smell to us and are better detectors than any machines (‘artificial noses’) that have been developed to date. Such research is largely driven by the fact that detecting scents can be of considerable use in human society. Dogs are trained to detect drugs, firearms and distinguish human scents during search and rescue operations and even detect cancer from human urine samples. However, though these skills are remarkable, they are learned responses acquired through the process of training. They reflect how amazing the canine sense of smell is but they do not tell us why it has evolved to be so special. Put simply, dogs are excellent scent detectors because this skill was of use to their wild ancestors.
Although dogs have been domesticated for centuries, scents that were naturally motivating and reinforcing to their ancestors are likely to still influence the untrained behaviour of the domestic dog, though responses may be tempered by breeding, training and whether their needs are fulfilled in the domestic environment.
Two of the key objectives for ancestral dogs was to locate food and defend physical resources as part of a cohesive social group, all within a complex and possibly large area. Scents played a key role in achieving these objectives.
For a dog 15,000 years ago there were no easy meals and no bins containing tasty scraps! Potential prey would have been scattered and constantly moving over rough terrain, not neatly penned up in fields. In short, the chances of seeing potential meals from a distance were slim.
Hearing would have been of limited use because a dog’s hearing extends to ultrasonic frequencies, which are easily obstructed by objects including hilly terrain and trees which may have been more important when dogs were evolving.
Fortunately for ancestral dogs (and other predators) potential prey species, or their waste products or scent marks, would have smelt as they released volatiles. Carcasses also smell. Such scents would travel through the atmosphere, around potential obstacles, and would become stronger as they were approached (thus indicating where the source was). Once the food was located the remaining problem to ancestral dogs was acquiring it. The ease at which this was achieved would depend on factors such as its abundance, size and the environment but evidence suggests that much of the time they would have needed a little help from other group members, which in turn required an efficient means of communicating with each other.
As discussed elsewhere in this book, much of our understanding of ancestral canine behaviour comes from observations of closely related wolf species and modern day feral dog groups. Pair bonds have been reported and are especially important when considering relationships such as the bitch-pup bond. However, free-living dogs typically associate into larger groups, which consist of a number of individuals.
Although members within a group are socially bonded, territories are such that individuals are not constantly in each others presence. It is therefore essential that group members are able to effectively recognize each other as part of their social group upon meeting. It is also important that they are able to communicate with each other remotely. Individuals that do not belong to the group need to be identified, and where necessary excluded, as they may compete for vital resources or mates. Scents play a major role in achieving these objectives.
Scientific understanding of scent marking behaviour is largely drawn from studies of rodents, in particular mice, which are easier to study than large groups of dogs. From a combination of body scents and the distribution and properties of scent marks it appears that mice can determine an individual’s identity, sex, relatedness, challenge potential, health status and how long it has been since a scent mark depositor was there! They can then use this information to determine how to respond to particular individuals if and when they meet and whether or not it is safe to stay in the area.
It is likely that dogs may also gain social, temporal and maybe even health information from scent marks which, with visual, tactile and auditory support, may determine their behaviour in both domestic and feral situations. Our understanding of the social relevance and behavioural effect of dog scents, though currently not as detailed as it is in mice, is growing. Recent advances, including behavioural and molecular studies of a pheromone secreted by bitches that calms her pups, has given us a more detailed understanding. By creating synthetic versions of these pheromones, such as dog appeasement pheromone, (DAP) we also gain potential tools which, with care and appropriate guidance, may be used to modify behaviour in a beneficial manner in a domestic environment. In the following section we review what we do know about how dogs use scents to communicate and how we can use it to gain a better understanding of our domestic companion and their ‘problems’.
Upon meeting dogs use a combination of postures, sounds and body scents to gain information about each other (Who is this? Is he a threat?).
The big advantage of scents over visual and auditory signals is that they can be deposited in the environment as marks which gradually release volatiles to convey social information about the depositor in his or her absence, much as we leave messages with a pencil and paper. Unlike the perception of sound and vision scents are less disturbed by the environment and have a relatively long life.
Odours that provide socially important information in mammalian species are known to be released from many locations on the body including the mouth (saliva), urogenital tract (urine, vaginal fluid) or released from specialised secretory glands near the skin surface (oily or watery cellular secretions). Dogs may use all of these substances to convey social communication, though to human observers the deposition of urine marks is the most apparent marking behaviour and has thus drawn the most attention.
Urination by dogs serves two functions, the removal of potentially harmful liquid waste from the body (elimination) and to convey socially significant, individual specific, information to other dogs (marking), typically in the absence of the marking animal.
Males mark in a very characteristic manner by depositing their urine in brief directed bursts by raising one of their hind legs; high if the urine is directed at a vertical target and lower if at a horizontal target. Urine may not be eliminated on up to a third of these occasions (often also observed in pet dogs), though figures vary widely between studies. Occasionally males may squat to urinate, particularly if castrated, which is the typical marking posture of females. Occasionally females may raise the leg into a more male-like posture.
In feral dog colonies, and indeed our pet dog population, adult male dogs urinate about three times as often as females. Most of the time males will expel their urine as marks but females mainly urinate to relieve themselves but may mark to advertise their reproductive status.
The positioning of scent marks can be particularly revealing when it comes to determining their purpose. Detailed studies have shown that marks are deposited mostly at courting sites. The sexual basis of urine marks is supported by studies, which have shown that males are more attracted to urine odours of females than vaginal or anal sac scents, particularly when females are in heat. In the presence of females males will keenly and possessively overmark female urinations probably to convey ownership (though mating in feral groups is typically not exclusively between known breeding animals). However, overmarking (and queuing to do so) is also seen within sexes and is often seen in domestic dogs and wolves. It is not clear whether this serves as an indicator of challenge potential (what the researchers interpreted as status) by the over-marker, or to make a ‘family’ mark at significant points in the territory.
Marks are also frequently deposited at feeding sites and territory boundaries with nest sites being rarely marked. This suggests that the function of scent marking is twofold. The first is to attract mating partners (both sexes) and claim them (males). The second is to claim and defend territorial borders (which in dogs will often partially overlap with other groups) and feeding sites. Nesting sites are probably not marked with urine as to do this would draw attention to youngsters.
Though all individuals do appear to mark, there is variation in the number of times different individuals of the same sex mark. This is likely to be related to the researchers assessment of their position in the social hierarchy (the subject of what constitutes canine hierarchy is discussed elsewhere in this book) being higher for high status individuals (who have priority to mate), in particular the males. Studies have shown that individuals who attain a high-status in the group (particularly males) generally mark at a higher rate, and further increase their marking frequency when they are challenged. It is quite possible that such changes in social behaviour are related to changes in the animal’s emotional state. From a functional perspective in natural environments depositing marks at territory borders takes time and energy and exposes individuals to greater levels of stress and danger. Therefore the ability to constantly do this is thought to reveal the individuals superior qualities and thus i) be attractive to the opposite sex and ii) deter or combat challenges (and thus the chance of injuries) from other males. In mice individuals of a lower status will typically inhibit their marking response, depositing their urine less often and in larger amounts which appear to act as a message to higher status individuals that they do not pose a challenge to them. Whilst it is unclear whether this happens in dogs the release of large volumes of urine (and also faeces) is widely interpreted as being an indicator of anxiety in many species which is likely to correlate to an individual’s social status.
When a dog defecates a small amount of fluid may also be secreted from the anal glands. Rarely, anal glands may also be voluntarily discharged without defecation, but such behaviour is much more common in the more distantly related cousins of the dog such as hyena. In wolves, deposition of faeces along territory borders and trails suggests that they may play a role in designating ownership of an area.
Both faeces and anal gland secretions have been considered as sources of socially significant scents in dogs relating to sexual attraction, territory marking or signalling of danger. But what is the evidence?
Anal sac secretions contain a solution of lipids, particulate material and bacteria which help to produce an odour. It is thought that the number of volatiles identified in anal sac secretions and the between sample variation is sufficient for unique combinations to occur in different dogs and could therefore be used as a label to convey ownership of territories. Although deposition patterns in wolves suggest this is a possibility in that species there is virtually no evidence for this in feral or domestic dogs. There appears to be little attraction of potential mates to anal gland secretions, at least relative to urine marks. Anecdotal evidence suggests that discharge of anal sacs occurs with fear or anxiety inducing situations. This has not however been supported by examining the responses of dogs to these odours.
The sources of scents discussed above, and their relevance to dog communication, have drawn most attention from scientists interested in theories of animal behaviour. Other pheromones, such as that secreted by bitches which acts to pacify their puppies, have raised interest not only because of what they reveal about canine behaviour per se, but also because of their potential use in an applied context in the domestic environment. However dogs secrete many other substances which could also be important to them, some of which are described below, which have yet to be studied in detail.
Upon meeting dogs are typically drawn to investigate the ano-genital region where they may be particularly concerned with information conveyed in urinary odours. They are also drawn to investigate the facial region though clearly this involves an element of danger! Licking may also occur, which in wolves is usually directed by the more inhibited individual of any pair. Domestic dogs are also often seen by their owners to lick other areas of each others bodies (notably mouths and ears) and dogs will often also lick their owners which may be rewarded or discouraged by owners. Dog saliva is known to have some anti-bacterial properties and thus licking may have some health benefits and mutual grooming of each others hard-to-reach areas may play a role in social bonding. However saliva, distributed by licking, may also have a communication role. Proteins found in the saliva of dogs have a notable degree of similarity to those that mice, and other species, use to communicate their identity. It is therefore plausible that saliva may be used to convey identity, ownership or group membership.
Given the sensory differences that exist between dogs and humans, it is remarkable that by and large we co-exist so amenably. Through the gradual process of association for mutual benefit that lead to the domestication of dogs we have managed to learn to understand each other to some extent, but not entirely.
During the process of domestication of dogs we have altered many factors that influence how dogs behave. Dogs rarely live with groups of other individuals of their species, typically living as the only canine or one of a pair in a household. By not allowing dogs to breed freely we have influenced how dogs behave by generally not selecting those with unfavourable characteristics to breed from and tending to select for juvenile and/or highly specific characteristics. By using procedures such as neutering we have influenced the hormonal profile of our companion dogs which has many profound effects on behaviour, such as reducing sexual behaviour. Management of dogs as part of our households also removes the requirement for dogs to perform natural behaviours (though not necessarily the motivation) and training serves to shape the behaviour of animals through reinforcement. Evidence also suggests that when living with humans dogs often override olfactory cues with information gained visually which indicates a sensory shift on their part to communicate more effectively with their primarily visually orientated owners!
Given all of these influences on the domestic dog, how important is their sense of smell and scent communication to them. How, when and why does it impinge on our generally positive relationships with our companion dogs?
We have discussed how it is part of a dogs natural behaviour to mark the territory in which their group resides. However, in a domestic situation there is a fundamental difference – the humans that form part of the ‘group’ do not urinate to mark the territory borders or to show their challenge potential. Furthermore they do NOT appreciate the canine members of the group performing these tasks at important sites (from the dog’s perspective) in the territory, restricting them to specific sites such as the garden! How is this interpreted by the dog? This may depend on the initial human-driven toilet-training process and the relative challenge potential of the dog in the household group. A puppy, who doesn’t yet know better or is unable to help him or herself, can perhaps be forgiven for urinating in the house. But when an adult dog, who the owner believes should know better, releases urine in the house conflict occurs between animal and owner.
When an owner asks for advice on inappropriate elimination they are normally referring to a breakdown in toilet training. Their dog has begun to urinate and/or defaecate in areas the owner finds unacceptable. This doesn’t mean that it is necessarily showing abnormal behaviour just that the dog is going to the toilet in the wrong place. There are a plethora of differential diagnoses for inappropriate elimination. These include certain medical conditions, age related problems, environmental change, incomplete house training and faulty learning, breed type, inadequate management, substrate preference, over-excitement, fear-related urination, attention seeking behaviour, challenge potential related and anxiety problems. The diagnoses related to scent-marking are challenge potential marking, attention-seeking behaviour and some anxiety problems.
Since inappropriate elimination can be a complicated area to diagnose successfully it is important that the owner seeks professional help in dealing with this problem. The dog should first be examined by a veterinary surgeon to rule out any medical problems. There are many common medical disorders related to urinary problems such as, urinary tract disease, congenital or anatomical malformation, endocrine disorders and neurological abnormalities. Problems relating to inappropriate defaecation include bacterial and viral conditions, obstructions, food allergies, age related problems, activity levels and changes in gastrointestinal motility. If there are no obvious medical reasons the owners can then be referred to a qualified behaviourist.
Both adult males and females may display this behaviour. To differentiate between scent marking and other diagnoses it is important to look at the amount, frequency, directionality and locality of the urine deposited. When urine and associated scent secretions are used for communication only small amounts are usually deposited frequently and directed at prominent places, though animals may release more in environmentally and socially stressful situations. Often the dog will mark after investigating and sniffing several spots. Commonly reported places are the sides of furniture and walls, standard lamps, upright vacuum cleaners, shopping bags and visitors trouser legs. It is also common for dogs to jump up onto a bed and urinate or defaecate on the duvet. There are different motivating factors reported for inappropriate scent marking behaviour. Confident dogs will often mark for territory maintenance. Others may have learned that if they perform these behaviours they get attention and some dogs may mark as a consequence of feeling anxious. It is therefore, important that the underlying factors are clearly understood before employing a behavioural modification programme.
Both urination and defecation may be used to scent mark, which is normal canine behaviour, but inappropriate to owners when it occurs within the home. Among females scent marking is affected by their hormonal state and they will pass small amounts of urine more frequently when in pro-oestrus, oestrus and post parturition. Marking behaviour can be reduced by neutering and ‘problem’ marking can be prevented or at least decreased in over 50% of male dogs by castration. However scent marking is not controlled exclusively by current levels of reproductive hormones circulating in an animal’s bloodstream; hormones produced in other parts of the body play a role and social responses and emotional state may also influence physiological processes leading to the exhibition of such behaviour patterns. In multi-dog households and free-ranging groups over-marking is common and more confident females will urinate over urine marks made by males or other females to reaffirm their challenge potential. The dogs that tend to show this confident marking behaviour also tend to show other challenging postures towards other dogs such as direct staring, assertive body language and vocalising. If scent-marking behaviour occurs within a multi-dog household it is important to address this problem by reassessing the relationship between the dogs and treating them accordingly. However, challenge potential marking may also occur in a home where only one dog resides if there is social stress. Commonly a dog will mark on walls or furniture and even a trouser leg in front of their owners. The leg raising posture on its own may also as act as a visual threat display. The dog may also show other responses to social stress such as aggressive behaviour or persistent attention-seeking.
Since the smell of urine in a particular place may encourage the dog to over-mark, it is advisable to clean the areas used thoroughly. Biological washing powder is often used and the area wiped with surgical spirit. There are also several commercial furniture deodoriser sprays which clients have recommend.
A relevant case study involved a Jack Russell dog called Bob who lived with a recently married couple who, on demand, gave him every thing he asked. They constantly played throw the squeaky toy for him, gave into his food begging, allowed him to persistently climb all over them and at night he would artfully push the husband out of the bed. As soon as either of them stopped interacting with him he would run into the hallway and defaecate on the mat. This made both owners react and although Bob was told off he still gained a reaction from them albeit a negative one which maintained this behaviour. He would also walk boldly over towards any visitors, cock his leg up and urinate all over their trousers. It was this particular behaviour that the owners initially asked advice about.
The owners were tactfully asked to ignore attention-seeking behaviour and, if necessary, gently push Bob away without looking or talking to him when he tried to initiate any form of unwanted contact. They were then asked to solicit all interactions with Bob by first asking him to come to them, to sit down and to wait. He was not allowed to have a fuss, a treat, his dinner, lead on or a toy until told. Bob soon learned that to get nice things he had to sit down calmly and wait first. When visitors arrived they were asked to ignore him and for a few weeks he was kept on a lead in this context. All marks were cleaned using biological washing powders and a deodorising spay and he has not marked since.
Some dogs, typically of low confidence and/or a nervous disposition, may mark as a consequence of feeling anxious or unsure of a new environment. There are many reported cases of dogs that urinate or defaecate when they first enter new surroundings. Once they have performed the deed they rarely repeat it. To discourage this behaviour a deposit of their smell can be laid prior to the dog entering by wiping an old towel/blanket that the dog has been sleeping on around the walls and furniture. It would also be advisable to have the dog with you and supervised until it has gained in confidence.
Some dogs find it hard to cope when left and may show anxiety problems such as increased vocalisation, destructive behaviour and elimination problems. Usually these involve full bladder elimination of urine and not scent marking as such. However, it has been suggested that some dogs scent mark to increase their feeling of security. Therefore, the separation-anxiety problem needs to be addressed before the marking will decrease. Not all problems are mutually exclusive and can figure a multitude of underlying causes and it is important that each dog should have a medical check up before referred to a qualified behaviourist. In some cases appropriate drug therapy may be recommended by the veterinary surgeon. In these cases and concurrent to the behavioural modification programme the dog appeasement pheromone (DAP) may be of some use.
Rolling is a normal canine scavenging and hunting and possibly confidence related behaviour, which is generally ignored unless the odour is unpleasant to humans – such as rotting fish! It is fair to say that a dog’s motivation to pursue such odours is usually very high so if the owner does not wish their dog to smell like a rotting fish they should anticipate rolling behaviour and work further on reinforcing effective leave and recall behaviours. After a bath rolling is likely to aid manipulation of the dog’s scent glands and spread their scent over their body once more. To stop them rolling in the mud directly after a bath it is advisable to keep them indoors and give an alternative low-odour substrate to roll in, such as their bedding.
Intact male dogs roam more frequently than castrated ones and will sniff out sexually receptive females over long distances. The obvious dangers include being injured or killed on the roads and causing third party injuries or fatalities. Unsupervised dogs also pose a health hazard and fighting can also break out with other roaming males. It is therefore, important that this problem is addressed. Since roaming behaviour is usually hormonally modulated castration will help to decrease this behaviour by about 90%. However, this behaviour also has a learned component, and the longer the dog has been showing this behaviour the less likely castration will help in reducing it.
If after neutering the dog is still an ingenious escapologist the owner should make sure it is sufficiently exercised and its attention needs are met and that it wants to stay with the owners rather than being made to. Eight feet high fencing sunk into concrete and surrounded by razor wire may physically stop the dog from running away but it will not stop the dog wanting to. A qualified behaviourist will be able to help with this problem.
Many dogs pinch scent impregnated items, such as tissues. This can include the owner’s underwear which the dog may refuse to give back. Why a dog would choose these items over and above others we can only surmise. However, these items of clothing do carry a relatively large amount of the owner’s scent. They are also a handy size to fit comfortably into a dog’s mouth. These items when taken, procure an explosive reaction from the embarrassed owner. Therefore, the dog quickly learns to make the association between the item and the reaction of their owner, which may be interpreted as play, such as tug-of-war. The initial motivation to take these items thus changes from a natural interest in group odours to a learned association, which gains the reward of attention. One solution to overcome such an attention seeking motivation is to dissociate the item with the reward. Instead of becoming all flustered and chasing the dog around the house simply ignore the dog and fetch something ‘better’ (determined by your excitement and interest) such as the dog’s favourite toy or treat. Become very interested in this ‘first prize’ and the dog will quickly lose interest in it’s now ‘second prize’ and will come trotting over. Do not try and force the item away from the dog, simply ignore and wait until the item is dropped. Carefully pick up the soggy underwear and sometimes ask the dog to sit, wait and take what you have. The dog will learn that to receive nice things it has to sit and wait first and that pinching items of underwear does not achieve the desired result of attention. Some dogs will take items impregnated with the owners scent to lie on, or lie on those that are already available at times of stress, such as during separation anxiety. This acts as a maintenance stimulus that increases their capacity to cope.
Scents are important to dogs, much more so than to us. They convey messages relevant to their (ancestral) survival and social behaviour. Such messages are not obvious to us humans, as we do not have the same ability or motivation to respond to them. Unfortunately this can and does sometimes lead to a breakdown in dog-human communication. Scientific studies of the behaviour and physiology of dogs and the experience of behavioural counsellors in deciphering how to deal with dog-human misunderstandings has helped to unravel some of the secrets of the canine world of scents. However there is still much to learn which requires us to keep our eyes, ears and most pertinently our noses open to what our dogs are telling us.