Like most mammals (and many other vertebrates, such as reptiles), canids live in an olfactory world. Olfaction is likely the dog’s primary sense, being about a thousand times more sensitive than humans’. Dogs have more than 220 million olfactory receptors in their nose, while humans have only 5 million. Smelling is an active process, and dogs can inhale air rapidly, at approximately 4-7 Hz (sniffs per second).
The dog’s nose is a physiological compromise between at least six conflicting functions—respiration, vocalization, water balance, temperature regulation, recycling tears, and detection of odorant molecules. It was not explicitly designed to carry out these functions, but is the result of hundreds of millions of years of natural selection and evolutionary change (Bainbridge, 2016).
The sensory parts of the nose developed initially from interactions between more than one cell type. Vertebrates are triploblastic animals whose body plans form from three layers of embryonic cells:
The precursors of the left and right olfactory organs are the paired olfactory placodes, thickenings of the ectoderm on the surface of the snout.
Dogs’ muzzles vary significantly in shape due to centuries of artificial selection to create canine faces that are either well-suited to their intended purpose or considered attractive. Dolichocephalic breeds have extremely long snouts; mesocephalic breeds have more moderately proportioned muzzles, and brachycephalic species have extremely short noses and suffer many problems since their palates are often too long for their heads, causing them to flutter in the respiratory air stream, creating a stertorous noise.
Dogs usually have cold and moist noses. The moisture secreted by mucous glands in the nasal cavity is necessary to help to capture molecules in the air and bring them into contact with the olfactory epithelium inside the nose. The mucous layer absorbs the odor molecules in the olfactory epithelium of the nasal cavity. Then, they are diffused to the cilia of the receptor neurons.
Dogs can widen their nostrils when exercising or savoring an odor by the action of muscles that move the cartilages underlying the planum. The nasal cartilages of the dog are dermocranial in origin and, viewed rostrally, appear to almost entirely encircling the nares. The midline, septal part is the most rostral part of the nasal septum. It provides attachment for the dorsolateral and ventrolateral parts of the cartilages, which may be drawn laterally to flare the nostril. Two layers of muscle act to move the cartilages (Evans 1993).
Olfaction as a whole depends on several aspects: perception—the ability to detect the presence of a volatile compound in the air or water; discrimination—the ability to distinguish different signals in a chemically complex environment; identification—the ability to recognize a signal and compare it with previously memorized information.
The olfactory bulb has been implicated in certain types of olfactory learning and memory (Gheusi et al. 2000), discriminates odor cues in a complex olfactory environment (Doucette et al. 2007), and enhances the sensitivity of odor detection (Jia et al. 2014). The olfactory information is primarily coded at the olfactory bulb level, and it is then transmitted via pyramidal neurons to the olfactory cortex. Different studies in animal models indicate that the right hemisphere responds to novel (unexpected) stimuli, arousal odors, and threatening stimuli. The left hemisphere responds to familiar stimuli and nonaversive smells.
Studies established the importance of olfactory cues in the conspecific and interspecific relational systems of canids and humans (Millot 1994; Miklosi, 2007; de Groot et al. 2014). These olfactory cues are a plausible explanation for my observations of dogs that are insecure with other dogs in an urban environment. I verified an increase in their submissive and displacement activities in areas with many different urine samples, compared to regions with fewer canine odors.
Other studies show how nosework (Duranton & Horowitz, 2018) and environmental enrichment (Hubrecht, 1993) are essential to dogs’ welfare.
Food bowls and their use in dogs’ (and other species’) daily routines are a human culture. Some dogs under human care have food always available, and others have specific schedules. There are controversial and polarizing moral discussions around the idea that “dogs are not in nature” and thus mimicking the natural environment isn’t needed. This position can seem to me a bit selfish and, on some occasions, hypocritical, since we are the ones who have removed dogs from nature, deciding everything for them and using them in activities for our benefit, including scent detection.
The “nothing for free” concept is widely misinterpreted with unnecessary emotional outbursts from humans. That nothing in our lives is for free is a fact. So, using food in versatile stimulation plans (see below) allows the other species to show their natural behaviors and work with several intrinsic mechanisms of the species’ nature. As I said on other occasions, it is not necessary when we remove a species from nature that we remove the species’ nature. Bradshaw (2006) states that “when feeding, domestic cats and domestic dogs both display the legacy of their origins in the Carnivora.”
Jeremy Koster (2021) has an interesting paper about canine studies in “native dogs.” He concludes that “Samples of diverse populations are needed for holistic perspectives on the evolution of domestic dogs. The available evidence suggests that most dogs, both in contemporary and prehistoric settings, differ substantially from NATIVE dogs. Most dogs lack the distinctive genotypes that characterize modern breeds, and their ontogeny has occurred in environments that diverge considerably from the social and ecological settings inhabited by NATIVE dogs. In multiple dimensions, from endocrinology to cognition, the unique phenotypes of domestic dogs have been shaped by this history.”
A provocative paper from Clive Wynne (2021) refers to that as well: “Dogs’ enormous success living in a human-dominated world rests on a set of adaptations to living in close proximity with our species. These include alterations in reproductive and foraging behavior from their ancestor species, wolves, which are readily understood as adaptations to the change from hunting live prey to scavenging on food residues that people offer – whether intentionally or not. The changes in dog social behavior are less obvious and indeed somewhat paradoxical.”
The feeding behaviors of natural-living wolves show many differences from those of domestic dogs; free-ranging dogs do not tend to show cooperative hunting behaviors and instead rely on humans for food (Mangalam and Singh, 2013). When domestic dogs are kept as companions and placed in a confined space, such as a house with essential resources, such as food, opportunities for competition may increase. Resource guarding behavior is still observed in domestic companion dogs (Guy et al., 2001a) in variable degrees and types (Jacobs, 2016) and remains a problematic behavior for pet owners (Pirrone et al., 2015). For dog owners in multi-dog households, resource guarding between dogs is a serious issue given the consistent and frequent interaction between conspecifics (Siracusa, 2016). I can’t entirely agree with Guy et al. and Siracusa’s ambiguous term “resource guarding” since we only find it mainly in the dog literature as a gentle way to describe dominant behavior.
A study by Dr. Abrantes and Anders Hallgren (1986) confirms that the dog’s ancestor, the wolf, Canis lupus lupus, is at work eight to 16 hours within every 24 hours. In nature, the wolf works for its food through tasks like:
The most common reason for behavioral problems we see at the Ethology Institute (since the early 1980s) in dogs (pets) is under-stimulation.
Our experience shows great preventive and active benefits with a versatile stimulation plan (Abrantes, 1984, 2015, 2018) with activities that promote the use of the nose, which can be realistically used as a daily routine for all dog owners to provide various types of stimulation instead of limiting activities by human goals and availability. Instead, this stimulation plan takes into account the natural needs of the dog and its highly developed olfactory sense, using the dogs’ daily food for searching, hiding, and other calm games, together with the stimulation program (communication, nosework, and problem-solving).
Also, I believe that foraging may exploit a conspecific’s spatial knowledge through social learning and imitation of food locations, helping to develop its spatial orientation, memory, and cognition. In a preventive way, it is our experience that a versatile stimulation plan is a preventative and active solution to conflicts since the food is not concentrated in a bowl. Scent detection also shows to be efficient in some Canine Home Alone Problems (CHAP) and helps improve the communication between the owners and the dog.
We split the daily food through three activities: communication skills, searching skills, and problem-solving. In that way, the dog continues with access to its food, and it has a significant part of its natural needs assured. This process helps the owners in a way that doesn’t demand a substantial change in their routines.
I’ll focus only on the tug-of-war games. I’ll not talk about “leave / drop” skills that are not directly related to tug games. At most, they are a complement to tug activities.
Some trainers claim that tug games improve the human-dog bond. The characteristics of Human-Animal Bond (HAB) (Russow, 2002) are based on empirical documents which makes it difficult to determine when we have a reciprocal HAB. Therefore, I didn’t find any academic data to support this statement, only anecdotal statements from trainers. The paper from Cimarelli et.al (2016) evaluated the dog owners’ interaction styles, and it showed how several factors affect the human-dog interaction.
Another common statement is: “Tug-of-war makes dogs more dominant.” Perhaps this is said because canine adults in the wild don’t “play” tug-of-war, and because it involves competition with loads of agonistic behavior. While tug-of-war with domestic dogs is a different situation since there are humans involved, that doesn’t mean that in some situations, tug play is unrelated to competition.
As a side note, I usually consider the balky argument that “dogs are not wolves,” as a myth already debunked with several facts (Abrantes, 2020). It is interesting how some who support standard tug play between humans and dogs on the premise that the dogs naturally do it with other dogs are the first to say about other controversial subjects that humans should not behave like dogs, and may be against using daily food for other activities described above.
The “growling” effect on that play is also a motive for discussion. Faragó et al. (2010) suggest that the results provide the first evidence of context specificity of agonistic vocalizations in the dog.
Rooney et al. (2000) paper suggests that “Winning possession of toys is described as simulating the winning of the battle for the best meat at the end of a pack hunt (…), which can have consequences for the social hierarchy. This idea assumes that play is a contest and the goal is to possess the toy. Although this was the case during dog-dog play, we saw no evidence for it during dog-human play. Since dogs react differently to human and dog play partners, we see no reason to assume that the consequences of dog-human games are the same as dog–dog games.”
In another paper, Rooney et al. (2001) postulated that where appropriate play signals are absent or misinterpreted by the dog, the consequences of play interactions can be associated with dominance aggression.
Another paper from Rooney & Bradshaw (2002) claims that “Characteristics of dog-owner play may be influenced by the current relationship, such that a dominant dog may be more likely to win at tug-of-war, but winning does not cause that dominance. (…) Rooney et al. (2000) showed that dog-human play is less competitive than dog-dog play. There is little evidence that winning during intraspecific play enhances dominance (…) so it is not surprising that winning interspecific games does not. (…) Likewise, dogs in some situations may be unable to distinguish whether an interspecific interaction is playful, and a minority of dogs may never (or rarely) be able to make this distinction. For “true play” to occur, both players must be aware of the playful nature of the interaction, and this is generally achieved via play signals (…). We hypothesize that when play signals are absent or misinterpreted, then the interaction may be perceived as competitive and dominance effects ensue.”
The experiment from Klausz et al. (2014) showed that “the tug-of-war test did not differentiate among the three groups, as we did not observe marked aggressive responses in any of the groups. It cannot be excluded, however, that this could be explained by motivational aspects (i.e., dogs were less motivated to guard the rag than the bone). Anyway, the tug‐of‐war test did not successfully assess possession‐related aggressive behavior in pet dogs.”
Tug-of-war can also have a competitive role, even to a low degree. Bekoff (2018) analyzed a hundred random tug-of-war games between dogs. The preliminary analysis showed that “the evidence we found showed clearly that competition is one, but only one, explanation for what’s happening when dogs play tug-of-war. (…) To me, this tug-of-war study is a great example of how we need to observe dogs closely before assuming we know what their intentions are. Tug-of-war looks like a familiar human game, but dogs don’t play by our rules, and we can get into trouble when we presume that they do.”
A paper from Horváth et al. (2008) examined the effect of human communicative and social behavior on dogs’ inner state (measured in terms of saliva cortisol concentrations) in a play situation. The sample was of operational handlers (border guards and policemen) and their dogs. The paper shows interesting results: “The analysis revealed that the policemen continually disciplined (‘controlled’) their dogs and used sound signals to gain their dogs’ attention during play sessions, while border guards were more empathetic and enthusiastic, and also pet and praised their dogs more often. The positive correlation between the enthusiasm of handler and dogs’ latency of starting to play in the case of policemen, also suggested that the more enthusiasm shown by handlers, the sooner their dogs started to play. Thus we suppose that the differences in behavior, mood, and motivation of the handlers not only influenced their dogs’ motivation and behavior during the play session (…) but also had an effect on the post-play cortisol concentrations, which is in accordance with the findings of previous studies. (…)”
Note: Cortisol saliva samples have also been used in recent studies of training methods. This 10+-year-old paper shows how the activity itself influences cortisol levels. A 2016 paper (Cobb, M.L et al., 2016) did a systematic review and meta-analysis of salivary cortisol measurement in domestic dogs and highlights the “importance of carefully planning and controlling experimental design in addition to recording subject, experimenter, and environmental factors to compare salivary cortisol concentrations within and between individual dogs. Caution should be exercised in comparing different studies using salivary cortisol concentration as a measure, as the results could be a reflection of a plethora of factors.” This is one of the main reasons I’m very reluctant to rely on studies of training methods that seem to only prove the author’s beliefs.
Previous studies from the Ethology Institute, of 10,000+ individual therapy (IT) cases, found correlations between tug-of-war and hyperactivity, object biting, pants pulling, and lead biting. Ball-throwing correlated with hyperactivity, higher stress levels, and difficulties focusing or performing tasks requiring low activity levels. Surprisingly (and inexplicably), both tug-of-war and ball-throwing were more common in canine home alone problems (CHAP) cases than in dogs that could successfully be left home alone.
The results from on-field research I did some years ago showed that from 73 puppies (2-5 months) with a significant tendency to bite the clothes and/or lead, 70 of them were playing tug-of-war or similar rope games with the owners. 64 of them decreased that tendency when the owners switched to activities like nosework. I also studied puppies with the opposite tendency. Of the 97 dogs without clothes or lead-biting tendency, only 20 played tug-of-war or similar with their owners.
These results confirm my hypothesis that owners that play tug-of-war with their puppies as a general standard plan because they read about it or listened to different sources, without having an educated individual plan for their dog, create in the dog an inadvertent generalization with other moving objects and, consequently, an undesirable behavior.
Note: My research above is not a peer-reviewed paper, and as such, it may not have the accuracy I would like it to have. However, since I am my own funding and lab, I have to adapt my research to my fieldwork. In the end, my research provides me with some standards for my work until more accurate research appears. I recommend that all my colleagues do the same, because studies are usually situational. The same research may have different results in other cities, countries, or cultures. This confirms that standardizing a specific play as a need for dogs worldwide may not always be healthy and create many other problems.
Final note: My practical experience also shows that the wild fetch games can have adverse effects. First, it gets harder to have “the dog tired” effect since the dog will be in better shape next time. Second, it may create unwanted accidents with children, adults, or the surrounding environment. Third, excessive repetitive games can generate stereotypical behaviors and increase the dogs’ stress as I often see puppies overuse of (annoying) squeeze toys.
I want to be clear about this article. I’ll summarize my thoughts in four points:
1- I don’t intend to spend time in meaningless “nowhere discussions” on this topic. I have shown my argumentation and references for my position, which I invite you to read first. Then, you can either agree or disagree with it, providing other references for your argument. I can live with your choices in the same way that I wish for you to live with mine.
2- I’m focusing on the context of companion dogs and apparently inexperienced humans who limit themselves through social media advice and dangerous standardization of activities. From there, they create their schedules and rules for the dogs’ activities according to human social life, not individual dog’s needs. I don’t have enough data to expand this article to sports or operational (military/police) fields, but including here my own personal experience in training military police dogs would lead to another discussion about inexperienced handlers that is outside the scope of this article.
3- Many activities can be healthy with the proper education, balance, and adaptability to the individual. The big issue with some activities is the lack of limits or rules from the human side. There is no doubt that some activities directly influence some drives of dogs, and the lack of balance can originate from other behaviors. There are different perceptions of how we define “my dog likes this.” The manipulative way we humans alter the drives and the kinds of play (social, locomotor, and object play) of other species can create different levels of intensity and types of response in individuals.
4- My experience with students worldwide also shows that the advice I give in Denmark is adapted to the reality here and some details cannot be implemented, for instance, in some cities in Portugal. Because of this, with the help of a professional, we should always adjust dogs’ activities with their individual needs in mind.
Edited by Dana Lee
Abrantes, R. (1984). Psykologi fremfor magt. Lupus Forlag.
Abrantes, R. (1986). Hunden, vor ven. Borgen.
Bainbridge (2016). In: Jezierski, T., Ensminger, J., Papet, L.E. Canine Olfaction Science and Law. CRC Press. Taylor & Francis Group.
Bekoff, M. (2018). Canine Confidential. Why Dogs Do What They Do. The University of Chicago Press.
Bradshaw J.W. (2006). The evolutionary basis for the feeding behavior of domestic dogs (Canis familiaris) and cats (Felis catus). J Nutr. 2006 Jul;136(7 Suppl):1927S-1931S. doi: 10.1093/jn/136.7.1927S. PMID: 16772461.
Cimarelli, G., Turcsán, B., Bánlaki, Z., Range, F. and Virányi, Z. (2016). Dog Owners’ Interaction Styles: Their Components and Associations with Reactions of Pet Dogs to a Social Threat. Front. Psychol. 7:1979. doi: 10.3389/fpsyg.2016.01979
Cobb,M.L., Iskandarani, K., Chinchilli, V.M., Dreschel, N.A. (2016). A systematic review and meta-analysis of salivary cortisol measurement in domestic canines. Domestic Animal Endocrinology, Volume 57, Pages 31-42, ISSN 0739-7240. https://doi.org/10.1016/j.domaniend.2016.04.003.
de Groot, J.H., Semin, G.R., and Smeets, M.A. (2014). I Can See, Hear, and Smell Your Fear: Comparing Olfactory and Audiovisual Media in Fear Communication. Journal of Experimental Psychology: General, 143(2), 825–834.
Doucette, W., Milder, J., and Restrepo, D. (2007). Adrenergic Modulation of Olfactory Bulb Circuitry Affects Odor Discrimination. Learning & Memory, 14(8), 539–547.
Duranton, C., Horowitz, A. (2019) Let me sniff! Nosework induces positive judgment bias in pet dogs. Applied Animal Behaviour Science, Volume 211, Pages 61-66, ISSN 0168-1591. https://doi.org/10.1016/j.applanim.2018.12.009.
Evans, H.E. (1993). Anatomy of the Dog. Philadelphia: Saunders.
Faragó, T., Pongrácz, P., Range, F., Virányi, Z., Miklósi, A. (2010). ‘The bone is mine’: affective and referential aspects of dog growls. Animal Behaviour, Volume 79, Issue 4, Pages 917-925, ISSN 0003-3472. https://doi.org/10.1016/j.anbehav.2010.01.005.
Gheusi, G., Cremer, H., McLean, H., Chazal, G., Vincent, J.-D., and Lledo, P.-M. (2000). Importance of Newly Generated Neurons in the Adult Olfactory Bulb for Odor Discrimination. Proceedings of the National Academy of Sciences USA, 97(4), 1823–1828.
Guy, N.C., Luescher, U.A., Dohoo, S.E., Spangler, E., Miller, J.B., Dohoo, I.R., Bate, L.A. (2001a). A case series of biting dogs characteristics of the dogs, their behaviour and their victims. Appl. Anim. Behav. Sci. 74:43-57.
Horváth, Z., Dóka, A., Miklósi, A. (2008). Affiliative and disciplinary behavior of human handlers during play with their dog affects cortisol concentrations in opposite directions. Hormones and Behavior, Volume 54, Issue 1, Pages 107-114. ISSN 0018-506X. https://doi.org/10.1016/j.yhbeh.2008.02.002.
Hubrecht, R.C. (1993) A comparison of social and environmental enrichment methods for laboratory housed dogs. Applied Animal Behaviour Science 37, 345–361.
Jacobs, J.A. (2016). Understanding canine resource guarding behaviour: An epidemiological approach (Doctoral dissertation). Retrieved from: http://hdl.handle.net/10214/964.
Jia, H., Pustovyy, O.M., Waggoner, P., Beyers, R.J., Schumacher, J., Wildey, C., Barrett, J. et al. (2014). Functional MRI of the Olfactory System in Conscious Dogs. PLoS/ONE, 9(1), e86362.
Klausz, B., Kis, A., Persa, E., Miklósi, Á. and Gácsi, M. (2014). A quick assessment tool for human-directed aggression in pet dogs. Aggr. Behav., 40: 178-188. https://doi.org/10.1002/ab.21501
Koster, J. (2021). Most Dogs Are Not NATIVE Dogs. Integrative and Comparative Biology, Volume 61, Issue 1, Pages 110–116. https://doi.org/10.1093/icb/icab016
Mangalam, M., Singh, M. (2013). Differential foraging strategies: motivation, perception and implementation in urban free-ranging dogs. Anim. Behav. 85:763-770.
Miklosi, A. (2007). Dog Behaviour, Evolution and Cognition. Oxford: Oxford University Press.
Millot, J.L. (1994). Olfactory and Visual Cues in the Interaction Systems between Dogs and Children. Behavioural Processes, 33(1–2), 177–188.
Pirrone, F., Pierantoni, L., Mazzola, S.M., Virgo, D., Albertini, M. (2015). Owner and animal factors predict the incidence of, and owner reaction toward, problematic behaviours in companion dogs. J. Vet. Behav. 10:295-301.
Rooney N.J., Bradshaw J.W.S., Robinson I.H. (2000). A comparison of dog-dog and dog-human play behaviour. Applied Animal Behaviour Science, 66 (3) , pp. 235-248. https://doi.org/10.1016/S0168-1591(99)00078-7
Rooney, N.J., Bradshaw, J.W.S., Robinson, I.H. (2001). The importance of play signals during dog–human games. In: Overall, K.L., Mills, D.S., Heath, S.E., Horwitz, D. (Eds.), Proceedings of the Third International Congress on Veterinary Behavioural Medicine, Vancouver, pp. 43–46.
Rooney, N., & Bradshaw, J. (2002). An experimental study of the effects of play upon the dog–human relationship Applied Animal Behaviour Science, 75 (2), 161-176 DOI: 10.1016/S0168-1591(01)00192-7
Russow, L.M. (2002) Ethical implications of the human-animal bond in the laboratory. ILAR Journal 43, 33-7.
Siracusa, C., (2016). Status-related aggression, resource guarding and fear-related aggression in two female mixed breed dogs, J. Vet. Behav. doi: 10.1016/j.jveb.2015.12.001.
Steventon, B., Mayor, R., and Streit, A. (2014). Neural Crest and Placode Interaction during the Development of the Cranial Sensory System. Developmental Biology, 389, 28–38.
Wynne, C.D.L. (2021). The Indispensable Dog. Front. Psychol. 12:656529. doi: 10.3389/fpsyg.2021.656529