Canine feeding behavior

Introduction

Two trends appear to have become fashionable amongst dog owners in recent years:

• Natural feeding: Feeding of diets that are based on the composition of wild wolf diets, often including raw ingredients.

• Dominance-based training methods: The use of gestures of dominance, such as feeding order or restriction of privileges, to establish control based on increased owner status as a pack leader rather than through reinforcement of desirable behaviors using food rewards.

Both trends are rooted in a popular return to a naturalistic view of dogs, but share the common weakness that they do not take into account the impact that the presence of humans has had on domestic dogs and wolves. This article will provide an overview of the feeding behavior and preferences of wolves and dogs, and provide an indication of how a better understanding of this subject can lead to fewer health and behavioral problems in domestic dogs.

The relationship between people and dogs

The history of the relationship between people and dogs is a long one. Homo sapiens is thought to have emerged in Africa approximately 250,000 years ago, after a period of increasing skull expansion in early hominid species which began 150,000 years earlier. Although there is evidence of gradual development of tool use and cultural advancement in our species throughout its history, there appears to have been a surge in cultural development which culminated in “behavioral modernity” approximately 50,000 years ago; namely the presence of symbolic culture, language and specialized technology, which contain all of the elements recognizable in subsequent civilizations, including the keeping of animals (Figure 1).

The ancestor of the domestic dog is Canis lupus (the grey wolf), which became a species separate from the coyote approximately 1-2 million years ago. The geographic origin of the domestic dog remains controversial. Genetic studies have pointed to an origin in South-East Asia, the Middle East or South-East China 1 2 3, with a possibility of genetic divergence from the wolf beginning up to 100,000 years ago. However, the most recently published analysis of the mitochondrial DNA of prehistoric canids and modern dogs suggests that domestication began 18,800-32,100 years ago 4. The earliest accepted archaeological evidence of canine domestication is the 33,000-year-old remains of a dog found in Siberia in 2010 5, which was subsequently found to be more closely related genetically to the modern domestic dog than the wolf 6.

In general, the genetic and archaeological evidence indicates that while there may have been some association between our species early in the history of Homo sapiens, dogs only began to undergo the process of domestication in the era of human behavioral modernity (Figure 2). This is significant, because it means that the dog would have been present prior to, and throughout, the development of agriculture. It would therefore have been part of human communities during the development of the most fundamental aspects of human culture relating to the preparation and consumption of food. From the very beginning of its association with humans, the domestic dog’s diet and feeding habits would have been heavily influenced by the practices and expectations of people.

The wolf (Canis lupus)

Diet

The behavior of modern wolves is often referred to as the basis for understanding the behavior of domestic dogs. While there is a lot to be gained from this, the modern wolf is in fact as much the product of the influence of humans as the domestic dog is, and this may be particularly true with respect to diet. The wolf was once one of the most widely distributed mammals, living throughout the northern hemisphere. In the areas where it continues to survive, its dietary range includes other mammals (ranging in size from small mammals to large ungulates), snakes, reptiles, birds and their eggs, fish, primates, carrion, berries, vegetables and fruit.

Having such a wide range of potential food sources, wolves have a number of food-competitors, including coyotes, jackals, foxes and bears. Being bigger and better organized group hunters than many of their competitors, wolves are more successful predators of large ungulates, and hence we see a predomination of moose, deer, bison and caribou in the diet of modern wolves. This has given rise to a perception that this is the natural diet of wolves, and that they and domestic dogs are almost pure carnivores.

With the development of agriculture, humans began to enclose and cultivate land, keep animals and drive away predators and pests. The expansion of agriculture, human settlements and trading routes would have had a progressively limiting effect on the range of habitats available to wolves, thereby also restricting their diet 7. This change was relatively rapid, within less than 2% of the history of the species (Figure 3). Now confined to a range that is less than half the size it once was, and to areas are generally less supportive of human habitation, the modern wolf is presented with a very different range of foraging opportunities which may not be representative of its past. So although modern wolves predominantly hunt large ungulates, this may be the result of choice restriction and competition with other species. This idea is supported by aspects of the wolf’s anatomy; for example, its dentition is similar to that of that jackal, which is omnivorous 7 8.

The current dietary range and dentition of wolves suggest that they may be best classified as facultative carnivores; the bulk of their preferred diet is animal flesh, supplemented with plant material, but they can subsist on an entirely non-animal diet. However, prior to human persecution, their dietary habits may have been more varied and omnivorous. The intrinsic flexibility of this omnivorous nature would have been an advantage during and after domestication, when the dog’s diet would have contained little protein, ultimately leading to the permanent adaptation to a carbohydrate-rich diet which has been observed in genomic studies of the domestic dog 9.

Hunting and feeding

When hunting large ungulates, wolves operate as a cooperative group with only two or three wolves actually participating in the killing 10. The rest will be involved in a variety of roles including breaking a selected individual away from its herd, running it down, or keeping other members of the herd away whilst it is being hunted. In areas where wolves currently depend on elk as a food source, each wolf typically catches one or two elk per month, depending on season, but they have been observed to survive on scavenged food alone for periods of up to 10 weeks 10. Wolves are therefore adapted to a “feast or famine” foraging pattern, in which there may be long periods without a successful hunt.

If a hunt is successful, all members of the group seek to gain a share of the carcass. It is important that the sharing of the carcass does not result in injury to group members, for two reasons. Firstly, the ability of the group to continue hunting depends on the fitness of all of its members. Secondly, the members of wolf groups are often related, so there is a genetic basis for altruism; sharing food with close relatives increases the probability of a proportion of an individual’s own genes being passed to future generations. Feeding order is not only affected by the relative status and role of individuals in the group, but also an individual’s need for food. Juvenile animals are not involved in the process for competing on a hierarchical basis for food.

Wolves have therefore evolved systems of communication and competitor evaluation that enable them to deal with very difficult situations of competition between group members that prevent serious injury.

Foraging in itself is a highly motivated behavior, independent of the need to obtain food. This has been confirmed by the phenomenon of “contrafreeloading” which has been observed in a wide range of wild and laboratory animal species, including wild canids 11 12. “Contrafreeloading” occurs when an individual chooses to work to gain access to food that is also available for free –it appears that in most species it is preferable to perform an operant response in order to gain food reinforcement, rather than simply to consume the food (Figure 4).

Domestication

The ability of wolves to subsist on scavenged food and a non-animal diet may have been crucial to their suitability for domestication. It is not clear how this started, but two of the main theories for canine domestication are that either wolf cubs were trapped and reared, or that wolves were partially “self-domesticated” when they were attracted into human settlements by the opportunity to scavenge food. Voluntary phases of domestication may have occurred during periods of reduced prey availability, with a subsequent selective pressure in favor of animals that were bold, sociable and attracted to a diet that was composed of non-animal food. It is suggested that the main trait passed on by successful animals to their offspring was a reduction in flight threshold (the distance at which an avoidance-escape response is triggered), so that successive generations became increasingly tolerant of human proximity.

The urge to contrafreeload may have provided the basis for initial interactions with people and the earliest responses to training (Figure 5); the motivation to perform an operant response for reinforcement is at the heart of dog training. Evidence from studies comparing the effectiveness of training methods based on dominance, punishment and positive reinforcement strongly suggest that positive reinforcement with food produces superior outcomes and is less stressful for the dog 13 14. It is likely that food-based training formed the basis for early human-dog interactions, because even rudimentary knowledge of wolf social behavior would have been unavailable to our early ancestors.

Even with improving agricultural methods, meat or fish-based dietary protein would have been of high value to people. Trapped wolf cubs, and early domestic dogs, would have been maintained on a diet that contained only a small quantity of lower quality protein, together with scraps of human food that was mostly fat and carbohydrate. However, they would have received food on a more regular basis than wild wolves, reducing the need for competition and establishing a relationship with people based on feeding.

The conflict-limiting behavior of wolves is also important for their ability to fit into human communities; domestic dogs would be intolerable as companions or working animals if they were always violently competitive over food.

As domestication proceeded, and dogs started to become a part of human communities, new selection pressures would have become important. Sociability, tolerance of handling and an ability to respond to human communication would all have become increasingly important, with those animals which did not show early promise being removed from the breeding population. This selection process favored the retention of juvenile physical and behavioral characteristics into adulthood (neotenisation); for example, floppy ears, heavy loose jowls, increased playfulness, behavioral plasticity, and reduced competitiveness and aggressiveness.

In a series of experiments lasting more than 50 years, it has been shown that selective breeding for friendliness in silver foxes leads to heritable changes in sociability and dependence on people, together with changes in coat color and markings that are similar to those thought to have occurred during the domestication of the dog 15 16. Selective breeding for traits that made dogs sociable and workable has had far reaching effects on their ability to relate to humans. For example, domestic dogs and human children exhibit comparable abilities to attend to and process information from human facial expressions 17. This ability is not observed in wolves when they are reared in the same manner as domestic pets.

Further artificial selection has seen the enhancement of breed-specific behavior, with dogs being more specialized in certain parts of the hunting behavioral sequence, e.g., dogs that favor pointing or herding behavior. Some of these behaviors have become so enhanced that they would have a negative impact on survival and fitness if present in a wild animal. Evidence for this distortion in hunting behavior comes from studies of feral dogs, which appear incapable of co-operative hunting in the manner of wolves, and instead depend on scavenging 18. Therefore, in terms of diet and feeding behavior, the end result of a host of natural and artificial selection pressures was that domestic dogs were able to thrive on a diet that was less meat-based, be less fussy about the kind of food they would eat, accept a shift from “feast and famine” to regularly fed meals, and be less competitive over food. They traded the ability to hunt effectively as a group for being able to read and respond to emotional and communicative signals in people, and thereby develop a relationship with people that was based on feeding and reinforcement.

Satiety and food preference

In herbivorous and omnivorous species diet selection has been linked to mechanisms for establishing an optimal macronutrient balance. It was thought that these mechanisms were unnecessary in carnivores, as their diet was assumed to be innately balanced and invariant 19. However, the diversity of the wolf diet implies that some mechanisms for food selection do exist in this species. A recent study has shown that domestic dogs select a diet that favors an overall balance of 30% protein, 63% fat and 7% carbohydrate (with respect to metabolizable energy) 19. This is very different from the diet selected by domestic cats, which is more heavily biased toward protein (52% protein, 36% fat, 12% carbohydrate) 20, which relates to the obligate carnivorous nature of the domestic cat and the relatively higher protein:fat ratio in the small mammals (e.g., mice) that form the basis of its natural diet.

In a number of studies, dogs have shown a tendency to consume food in excess of their energy requirements. When fed ad libitum and given a choice of dietary components, dogs did regulate their protein and overall energy intake, but the regulated energy level was around twice the mean daily requirement 19. This implies that dogs have inherited satiety mechanisms that are the result of adaptation to a “feast or famine” food availability in wolves.

Wolves have been observed to consume as much as 10 kg of meat during the initial feeding bout after killing a large ungulate 10. It is also suggested that rapid eating may have been favored during domestication, when competition for food would have been high 7 but intraspecific and interspecific violence would not have been tolerated by humans. This has implications for weight control in dogs. Satiety is the result of a combination of hormonal and physical signals from the gastrointestinal tract that indicate that sufficient food has been consumed. In many mammals, including man, a range of hormones including ghrelin, cholecystokinin, peptide YY (PYY), oxyntomodulin, and adipokines play a role in satiation. Evidence from trials of the weight-controlling drug dirlotapide, which is thought to act through PYY, indicates that manipulation of the satiety mechanism in the dog can be effective in the treatment of obesity 21.

However, it is clear that in many situations wolves continue to feed until gastric distension limits further intake. It appears that the same is true, at least in part, with dogs. High fiber levels in the diet, which lead to increased stomach distension, have been shown to increase satiety and decrease voluntary intake in the short and medium term after a meal, with an even greater effect when the diet was both high in protein and fiber 22. Such a diet has been shown to have a beneficial role in weight loss in dogs 23.

Implications for domestic dogs as pets

Problem prevention

Proper socialization and habituation during the sensitive period (3-12 weeks of age) are generally regarded as the key to healthy behavioral development. However, knowledge of the “contrafreeloading” nature of dogs and the retention of juvenile behavior in the domestic dog indicates that the use of food rewards, and feeding in general, to train and develop a bond with puppies is the method most likely to be effective. From the known ethology of wolves and dogs, dominance-based methods will be meaningless, or even intimidating, to puppies.

This is supported by evidence for a reduced rate of aggression in dogs trained using positive reinforcement with food, and an increased attentiveness toward owners who employed positive reinforcement 24

. Training has also been shown to have generally beneficial effects such as an increase in problem-solving ability in dogs 25

; an ability to solve problems reduces frustration and an individual’s need to act instinctively when faced with challenge or conflict.

The commonest owner-directed aggression problems in dogs involve resource guarding, and many owners will be shocked when they first encounter food guarding in their young dogs. Knowledge of the competitive behavior of wolves around food, and their use of signaling to avoid fights, shows us that to some degree food guarding is normal in this species. As a result dogs should generally not be challenged over food but should be left to eat in peace. This goes against the traditional view that an owner should repeatedly challenge a dog over its food until it is willing to relinquish the food bowl. The reason is that the traditional method teaches the dog that the owner is a potential competitor, in the manner of another member of a wolf pack. It may learn to relinquish food that is of modest palatability and which is freely available, but the fact that the owner is now regarded as a competitor means that the dog may guard far more ferociously scavenged or stolen food that has not been gifted by the owner, and which is high in fat or protein. This food is not only more palatable but also important for the dog’s diet selection in favor of fat and protein. It is better to establish an association between the presence of the owner and the availability of high value food; for example, by adding small amounts of highly palatable items to the bowl while a puppy is feeding (the food offered should not exceed 10% of the daily calorie requirements).

Problems with eating

Such problems can include gluttony, scavenging, begging and pickiness. We should expect dogs to be gluttonous, and we can also use an understanding of their normal feeding behavior to explain problems such as pickiness. Feeding behavior often involves the rapid consumption of large amounts of food at one meal, with the main limitation being gastric distension. Scavenging is driven by a need to find supplementary sources of food in anticipation of famine periods, and begging and stealing are an extension of “contrafreeloading”. Once a dog has learned that by climbing onto a kitchen worktop it can steal and eat an entire roast dinner, it is very unlikely that this behavior can be extinguished. This general tendency toward food overconsumption by most dogs means that owners are forced to control their dog’s food intake, and to accept and take responsibility for preventing food stealing and begging.

Picky eating is influenced by the same underlying mechanisms. Often, when the diet of picky eating puppies is analyzed, the animals are in fact getting more than sufficient calories, but mostly through begging for human food that is often high in fat. They refuse to eat from a bowl. This problem can therefore be viewed in terms of normal diet selection in dogs, and the effect of “contrafreeloading”; these dogs may be motivated to perform operant behaviors such as begging in order to get food. For picky eaters, scavengers and food thieves, a very successful solution is therefore to provide all food through puzzle or activity feeders and training, which enhances the “contrafreeloading” and foraging aspects of feeding behavior (Figure 6). Having a range of different feeders increases the complexity and diversity of problem solving and foraging behavior available to dogs, which is more important to them than the palatability and range of food flavors.

Conclusions

The trend toward “natural feeding” has focused on the composition of the diet, and has increased owner awareness regarding the quality of the ingredients in their pet’s food. However, the composition of the recommended diets is often based on dietary patterns observed in modern day wolves. For all the reasons discussed previously, these diets may not be representative of what the wolf ancestors of domestic dogs ate before humans restricted their range, and they do not take into account changes that have occurred in food selection and nutritional requirements during domestication of dogs.

This approach to natural feeding also overlooks aspects of feeding that may be much more important to the dog’s psychological wellbeing and the way in which they relate to us. Despite the fact that we see the same foraging behaviors in dogs as we do in wolves, most dogs are expected to take all their food from a bowl and are generally unable to forage. Many are trained using methods that exclude the use of food treats, which not only frustrates a dog’s natural drive to obtain food reinforcement through operant behaviors, but also removes one of the key aspects of the development of a trusting and non-competitive relationship between dog and owner. The subsequent obedience and behavioral problems that owners experience often lead them to use dominance and punishment-based methods that further conflict with the motivations of dogs. It is therefore important that we, as veterinarians, begin to overturn common misunderstandings of the central role that feeding had during the process of domestication, and continues to have in the forging of a relationship between a dog and its owner.