Elsevier

Journal of Veterinary Behavior

Volume 10, Issue 4, July–August 2015, Pages 286-294
Journal of Veterinary Behavior

Research
Breed-dependent differences in the onset of fear-related avoidance behavior in puppies

https://doi.org/10.1016/j.jveb.2015.03.002Get rights and content

Abstract

The onset of fear-related avoidance behavior occurs during and, to some extent, defines the sensitive period of development in the domestic dog. The objectives of this study were to identify the onset of fear-related avoidance behavior and examine breed differences in this behavioral development. A total of 98 purebred puppies representing 3 breeds were tested, namely Cavalier King Charles spaniels (n = 33), Yorkshire terriers (n = 32), and German shepherd dogs (n = 33). Data were collected weekly beginning 4-5 weeks after birth until 10 weeks of age. Puppies took part in 4 tests during each visit: a novel item, seesaw, step, and loud noise test. During each test, the presence or absence of fear-related avoidance behavior and crouched posture were noted. Saliva was also collected to measure salivary cortisol concentrations in the puppies before and after testing. A later onset of fear-related avoidance behavior was observed in Cavalier King Charles spaniels compared with German shepherd dog and Yorkshire terrier puppies (F = 11.78, N = 29, P < 0.001). The proportion of treatment puppies that exhibited fear in response to the testing was also different (χ2 = 9.81, N = 56, P = 0.007): Yorkshire terriers (N = 14, 78%), Cavalier King Charles spaniel (N = 10, 53%), and German shepherd dogs (N = 5, 26%). Cortisol concentrations decreased with age. Cavalier King Charles spaniel puppies that demonstrated fear-related avoidance behavior exhibited a greater (t = 2.133, N = 79, P = 0.036) cortisol response than puppies that did not exhibit the behavior. Breed differences in the crouch response to the loud noise test, regardless of age, were observed (F = 18.26, N = 98, P < 0.001). Cavalier King Charles spaniels demonstrated the highest incidence of crouching followed by the Yorkshire Terriers. Breed differences in puppy mobility were observed beginning at 6 weeks of age, with German shepherd dogs demonstrating the most mobility and Cavalier King Charles spaniels the least. The results of this study support the hypothesis that emotional and behavioral development, as well as the onset of fear-related avoidance behavior, varies among breeds of domestic dogs.

Introduction

Fear and anxiety are emotional states induced by the perception of danger and threat to an individual's well-being (Boissy, 1995). Fearfulness is a very important emotional characteristic that predisposes an individual to perceive and react in a similar manner to a wide range of potentially dangerous events. Signs of fear in the domestic dog include physiologic responses, such as increased heart rate, hypersalivation, and elimination; and behavioral responses, such as escape, avoidance, or defensiveness (Sherman and Mills, 2008). Many common canine behavioral problems, including stimulus-specific fears and phobias, fear-related aggression toward humans and other animals, and some urination may be based in fearfulness (Blackwell et al., 2013, Sherman and Mills, 2008). The development of fear-related behavioral patterns in the domestic dog may be influenced by genetics, physiology, sensory perception, environmental exposure, and experience (Overall, 2013).

Developmental changes in a dog's behavior and physiology begin at birth and extend throughout the dog's life with most changes occurring before sexual and social maturity. Several broad time periods, including the “neonatal period,” “transition period,” and “critical period” (sometimes alternatively described as the sensitive period) in domestic canine development have been described (Overall, 2013, Scott and Fuller, 1965). During the “critical period,” which lasts from approximately 3 to 12-14 weeks, pups will approach handlers and, if exposed to humans and other novel social and environmental interactions, will become ‘socialized’ to new experiences (Coppinger and Coppinger, 2001, Freedman et al., 1961, Scott and Fuller, 1965). The first expression of an adult-like fear response motor pattern begins during this time as well. Several factors likely play a role in its onset, including the neurophysiological capability to feel fear sufficiently to prompt an active response by the individual puppy, as well as the neuromuscular coordination to be able to carry out this response.

The specific time when the active avoidance of a fearful stimulus first occurs may vary among breeds. First expression of fear-related avoidance behavior patterns occurred at different ages in a study of German shepherd dog and Labrador retriever pups at Hampshire College.1 At 5 weeks of age, 90% of the German shepherd dogs showed moderate-to-extreme fear, whereas only 4% of Labrador retrievers showed even moderate fear. Furthermore, a delay in the development of fear-related avoidance behaviors appears to be a result of domestication because the onset of these responses is observed in dogs aged around 49 days, compared with wolf pups aged around 19 days (Coppinger and Coppinger, 2001). Domesticated foxes were found to have prolonged sensitive periods for socialization of more than 60-65 days, compared with only 40-45 days in unselected foxes (Belyaev et al., 1985). Differential timing of development of fear response behaviors may influence breed-dependent temperament and behavioral responses in adult dogs.

More than 50 breeds of dogs across all 7 recognized American Kennel Club (AKC) groups have family lines in which “fear/shyness/nervousness/panic/anxiety” are major breeder-reported concerns (Overall et al., 2006). Although fear responses in adult dogs have been widely studied, there is very little published on “normal puppy behavior” and changes over time during puppy development, especially relating to the development of fear and fear-related adult behaviors (Godbout et al., 2007). “Nervous pointer dogs” provide the best example of genetic influence on fear development. This strain of dogs displays an intense and specific fear of humans that has been proposed as a model for human phobias. Beginning around 3 months of age, these dogs show extreme fear, including crouching; slinking away; and, if cornered, freezing in response to human interaction, regardless of environmental influence (Dykman et al., 1979).

Work with foxes selected for varying degrees of tameness showed differing patterns of glucocorticoid concentrations by age. Foxes selected for enhanced aggressiveness had similar plasma cortisol concentrations as those selected for tameness at 30 and 60 days of age, but had significantly greater plasma cortisol on day 45 (Plyusnina et al., 1991). Other studies showed a peak in plasma cortisol at a later age in foxes selected for tameness (Trut et al., 2009). In human infants, different stressors activate the hypothalamic-pituitary-adrenal (HPA) axis, with physical stressors evoking a cortisol response, but with psychological stressors failing to do so (Jansen et al., 2010). Although cortisol has been used in a number of investigations of the fear response in dogs, very little research has been conducted on the HPA axis in young dogs.

The objective of this study was to identify, compare, and contrast the onset of fear-related avoidance behavior and concurrent concentrations of salivary cortisol among 3 specific breeds of purebred puppies aged between 4 and 10 weeks. Additionally, breed differences in development and mobility were identified. By studying canine development and onset of fear-related avoidance behavior, dog owners, breeders, veterinarians, and other professionals gain a more reliable understanding of fear-related development and predictable breed differences. This knowledge could be further applied to improving welfare and standards of rearing, training, socialization, and behavioral modification techniques in domestic dogs of various breeds that are raised as pets and as working dogs. In addition, a broader understanding of the development of the fear response could lead to the prevention of fear-related behavioral problems, by increasing the potential for, and understanding of, appropriately timed exposure and socialization techniques for puppies in the sensitive periods of their development.

Section snippets

Research design

The research was conducted in a randomized complete block design with repeated measures on puppies, which were blocked by litter, within breed. About 98 puppies were tested within 3 purebred dog breeds, namely Cavalier King Charles spaniels (n = 33, 19 treatment and 14 control group puppies), Yorkshire terriers (n = 32, 18 treatment and 14 control group puppies), and German shepherd dogs (n = 33, 19 treatment and 14 control group puppies). Seven litters of Cavalier King Charles spaniels (5

Behavioral tests

There were no effects of sex, litter, or reviewer in any of the analyses. The onset of fear-related avoidance behavior was indicated for any puppy that exhibited immediate, rapid, and pronounced movement away from the object or experience perceived as a hazard in any single test during a testing session. Results from 2 external video reviewers were not significantly different from the results of the original tester's on-site evaluations of the same puppies (F = 0.10, N = 57, P = 0.907).

Discussion

The results of this study support the hypothesis that the onset of fear-related avoidance behavior in domestic dogs varies by breed. Significant breed differences were observed in both the age at onset of fear-related avoidance behavior and the proportion of puppies that demonstrated this behavior. In addition, behavioral responses to the tests and changes in mobility during early puppy development differed among breeds.

These results are in agreement with a previous research by Coppinger2

Conclusion

The results of this study indicate that there are significant differences among the breeds studied in the onset and expression of fear-related avoidance behavior. There were also statistically significant breed differences in development of mobility related to age and incidence of crouching in response to a sudden noise. An expanded and more reliable understanding of breed-specific development has applications in the breeding, rearing, training, socialization, and behavioral modification of

Acknowledgments

The authors extend a special thanks to the cooperating dog breeders who contributed their time and allowed the testing of their litters. They also wish to thank Dr. Raymond Coppinger for his insight into breed differences in development of fear responses in puppies and for his helpful suggestions about the experiment. Salaries and research support for the Ohio State University authors were provided by state and federal funds appropriated to the Ohio Agricultural Research and Development Center,

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