Long-term Effects of Early Environments on

the Behavior and Welfare of Dogs

James A. Serpell, PhD

Center for the Interaction
of Animals and Society

School of Veterinary Medicine

University of Pennsylvania
<[email protected]>

Purdue University is an equal access/equal opportunity/affirmative action university.

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Why Study Canine Behavioral Development?
• Animal Welfare: Behavior problems disrupt the
human-animal bond. Primary reason why dogs
are abused, abandoned, or disowned;
contributory factor in 40-50% of all shelter
relinquishments. Making them the #1 cause of
premature death in American dogs
• Public Health: 4.5 million Americans are bitten by
dogs every year and ± 800,000 require medical
treatment. Dog attacks cause 20-30 human
deaths /year in the USA.
• Public Service: Behavior problems are the primary
reason why working dogs (guide dogs, search &
rescue dogs, detector dogs, etc.) are released
from breeding and training programs.
• Little known: Current guidelines on puppy care
and husbandry based on a few studies conducted
in the 1950s & 60s.
 Scott & Fuller (1965)
Genetics and Social Behavior of the Dog.

“The young dog should be

introduced, at least in a preliminary
way, to the circumstances in which
it will live as an adult, preferably by
8 weeks, and certainly no later
than 12 weeks of age.”

“The ideal time to produce a close

social relationship between a
puppy and his master occurs
between 6 and 8 weeks of age. This
is the optimal time to remove a
puppy from the litter and make it
into a house pet.”
The Classic Model of Puppy Socialization (Scott & Fuller, 1965)

Primary Socialization Period

Eyes open

Auditory startle reflex

Birth
Optimum Period for
Socialization

Approaching a Passive Stranger

Avoiding an Active Stranger
Wolf Avoidance

1 2 3 4 5 6 7 8 9 10

Age in Weeks
Canine Development
Research at Penn Vet
 Canine Behavioral Assessment
& Research Questionnaire

Dog owners/puppy-raisers/handlers asked to rate their

dogs’ behavioral responses to a 100 different everyday
situations or stimuli.
Principal Components Factor Analysis used to extract 14
distinct behavioral subscales, and 22 miscellaneous behaviors.

Validity and reliability of most of these subscales and

items have now been confirmed.

6
 Factor Analysis

Q13 Q11
Q5 Q7
Q6 Q10 Q9
Q4
Q2 Q3 Q8

Q1 Q14 Q12

Factor analysis is a statistical technique for condensing

information by grouping related items into separate
factors or subscales.
14 C-BARQ Subscales Extracted by
Factor Analysis
Stranger-directed aggression (10 items)
Owner-directed aggression (8 items)
Dog-directed aggression (4 items)
Excitability (6 items)
Familiar dog aggression (4 items)
Energy (2 items)
Stranger-directed fear (4 items) Chasing (4 items)
Dog-directed fear (4 items) Trainability (8 items)
Nonsocial fear (4 items)
Attachment/attention-seeking (6 items)
Separation-related behavior (8 items)
Touch sensitivity (4 items)
Hsu, Y. & Serpell, J.A. Journal of the American
Veterinary Medical Association, 223(9): 1293-
1300, 2003.
 22 Miscellaneous C-BARQ Items
Escaping/roaming
Rolling in scent Pulling on leash
Coprophagia Marking with urine
Chewing objects Submissive/emotional urination
Mounting Separation urination
Food begging Separation defecation
Food stealing Hyperactivity Staring (compulsive)
Fear of stairs
Snapping at flies (compulsive)
Tail-chasing/spinning
Shadow/light-chasing (compulsive)
Persistent barking
Autogrooming (self)
Allogrooming (others)
Other abnormal /stereotypic
 0 1 2 3 4 -

http://www.cbarq.org
C-BARQ Background Questions
1. Dog’s age (in years/months)
2. Breed
3. Sex
4. Weight (approximately)
5. Whether spayed/neutered
6. Age spayed/neutered (weeks/months)
7. Primary reason for spaying/neutering
9. Where dog was acquired (source)
10. Its age when acquired (weeks/months)
11. Whether dog involved in work/sports/recreational
activities, and what kinds?
12. First dog owned?
13. If not, number owned previously?
14. Did owner grow up with dogs as a child?
15. Number of other dogs in household
16. Relative ages of other dogs in household.
C-BARQ website went live in 2005
• Database now contains behavioral profiles on
approximately 40,000 pet dogs, and 30,000
working guide /service dogs.
• Allows us to generate highly reliable normative
behavioral data on these dog populations, both as
a whole and according to breed.
What Can the C-BARQ Tell Us
About Puppy Development?
How Does a Puppy’s Early Experience Influence
It’s Behavioral Development?
Common belief among veterinarians, behaviorists and trainers
that puppies obtained from pet stores are more susceptible to
developing health and behavioral problems.

CBE
Effects of Early Environment:
Pet Stores vs. Noncommercial Breeders

 We compared the C-BARQ

scores of adult dogs whose
owners acquired them as
puppies from either pet
stores (N=413) or
noncommercial breeders
(N=5657).
 Dogs from these two
sources are comparable
because they are usually
purebred and acquired at
similar ages.
 Results (Logistic Mixed Model)
Acquisition from a pet store predicted greater prevalence of:
Outcome Direction Odds Ratio P-value 95% CI
Separation-related Increase in pet store 1.58 0.002 (1.19, 2.11)
behavior dogs
Owner-directed Increase in pet store 3.13 <0.001 (1.87, 5.23)
aggression dogs - intact
Increase in pet store 1.44 0.006 (1.11, 1.87)
dogs- neutered
Stranger-directed Increase in pet store 1.59 0.003 (1.18, 2.16)
aggression dogs
Non-social fear Increase in pet store 1.44 0.047 (1.01, 2.07)
dogs
Familiar dog Increase in pet store 1.35 0.021 (1.05, 1.74)
aggression dogs
Dog-directed fear Increase in pet store 1.33 0.030 (1.03, 1.71)
dogs
Dog-directed Increase in pet store 1.96 <0.001 (1.44, 2.67)
aggression dogs
McMillan, F.D., Serpell, J.A., Duffy, D.L., Masaoud, E. & Dohoo, I.R. Differences in
Touch sensitivityMcMillan,
Increase
F.D., in pet store
Serpell, Duffy, D.L.,1.58
J.A.,characteristics
Masaoud, 0.002I.R. Differences
(1.18,
in 2.11)
behavioral and psychological betweenE.dogs
& Dohoo,
obtained as puppies from
dogs
petbehavioral
stores andand psychological
those obtained fromcharacteristics between
noncommercial dogs obtained
breeders. as puppies from
JAVMA, 2013.
pet stores and those obtained from noncommercial breeders. JAVMA, 2013.
* Possible effects of breed, sex, age, body weight, whether neutered, presence19
of other dogs in household, and training all taken into account in the analyses.
C-BARQ Data: Persistent barking
C-BARQ Data: House soiling (urination)
 Possible sources of observed differences
Pet store Noncommercial breeder
No information Genetics: Little or no selection for Genetics: Positive selection for
temperament. temperament.
Early socialization: Commercial Early socialization: Most NCBs devote
No information breeding operations give little attention some effort toward socializing puppies
to appropriate socialization. prior to sale.
Epigenetics: Parents more likely to be Epigenetics: Parents less likely to be
* stressed prior to breeding / during
gestation.
stressed prior to breeding / during
gestation.
Early life adversity (ELA): Stressful early ELA: Less stressful early environment:
* environment: Early weaning and
separation from mother/littermates;
Appropriate age of weaning and
separation from mother/littermates;
multiple episodes of transport to the only single episode of transport from
“broker”, the pet stores, and final breeder to final home.
homes; mixing with unfamiliar puppies;
handling by strangers, etc.
Owner differences: Pet store Owner differences: Breeder
acquisitions more likely to be acquisitions tend to be made by people
* spontaneous ‘spur of the moment’,
rather than carefully considered.
who have given relatively careful
thought to owning a puppy. Owners
Owners of this type may be less likely to be more experienced and
experienced and / or less committed. committed.
22
Epigenetics: Do the Breeding Dogs from CBEs Exhibit Higher
than Normal Rates of Stress / Anxiety?
Methods
1. Solicitation of adopters of ex-
breeder Commercial Breeding
Establishment (CBE) dogs

2. Participants completed C-BARQs on

332 former CBE dogs

3. Results from CBE dog adopters

were compared to results from a
convenience sample of C-BARQ
evaluations of 332 pet dogs from
the C-BARQ database matched for
breed, sex, age and neuter status.
Results (Generalized Linear Models)
CBE ex-breeder dogs displayed unusually high levels
of fear/anxiety and house-soiling
Outcome Direction Odds Ratio P-value 95% CI
Stranger-directed Increase in CBE 8.12 < 0.0001 (1.73, 2.48)
fear ex-breeders
Non-social fear Increase in CBE 6.62 < 0.0001 (1.51, 2.27)
ex-breeders
Fearful on stairs Increase in CBE 5.98 < 0.0001 (1.35, 2.23)
ex-breeders
Touch sensitivity Increase in CBE 3.19 < 0.0001 (0.8, 1.52)
ex-breeders
House soiling Increase in CBE 2.81 < 0.0001 (0.65, 1.42)
(urination) ex-breeders
House soiling Increase in CBE 2.07 0.0003 (0.33, 1.12)
(defecation) ex-breeders
Urine marking (in Increase in CBE 2.06 0.001 (0.29, 1.16)
home) ex-breeders

* CBE ex-breeders and convenience sample of pet dogs matched for

breed, sex, age, and neuter status.
25
Stranger-directed Fear

3.5
3
2.5
2 +812%
1.5
1
0.5
0
 Non-social fear
Fear of novel objects, sounds, movements, etc.

3.5
3
2.5
+662%
2
1.5
1
0.5
0
 FEAR-RELATED TERMS PEOPLE
USED IN DESCRIBING THEIR DOGS
 “skittish” (44)

 “startles easily” (10)

 “always on alert, on edge, on guard, and hyper-alert” (5)

 “overly reactive, jumpy, or easily unnerved, frightened,

scared, spooked, or panicked” (27)

 “frightened by sudden or quick movements or sounds” (33)

 “frightened of everything or almost everything” (24)

 “frightened all the time under any circumstances” (12)

ELA: Do Adverse Early Experiences Affect the
Development of Behavior in Dogs
(the Influence of Re-homing)?

Methods: Used the C-BARQ database to analyze the

association between ‘age acquired’ and the
severity/prevalence of of behavior problems in dogs.
 Effects of Early Adversity:
Age When Acquired
N = 17,339 Kruskall-Wallis ANOVA, P < 0.0001)
1.2

0.8 4-6 weeks

7-9 weeks
0.6 10-12 weeks
13-15 weeks
0.4
16-18 weeks
> 18 weeks
0.2

0
Stranger Owner Dog Nonsocial Separation
aggression aggression aggression fear problems
Effects of Early Adversity:
Age When Acquired
N = 17,339 Kruskall-Wallis ANOVA, P < 0.0001)
2.5

4-6 weeks
1.5
7-9 weeks
10-12 weeks
1 13-15 weeks
16-18 weeks
0.5 > 18 weeks

0
Attention Excitability Persistent House soiling
seeking barking

31
 Scott & Fuller (1965)
Genetics and Social Behavior of the Dog.

“The young dog should be

introduced, at least in a preliminary
way, to the circumstances in which
it will live as an adult, preferably by
8 weeks, and certainly no later than
12 weeks of age.”

“The ideal time to produce a close

social relationship between a
puppy and his master occurs
between 67 and 89 weeks of age. This
is the optimal time to remove a
puppy from the litter and make it
into a house pet.”

Effect of Early Weaning?

Owner Differences: Lessons from Guide
Dogs
• All guide dog puppies are reared in the
same kennel environment and receive
the same level of early socialization.
• All puppies are re-homed with puppy-
raisers at 7-9 weeks, and C-BARQed at
12 months of age.
• Additional information collected from
puppy raisers regarding characteristics
of puppies’ rearing environment.
• Analyzed associations between these
environmental variables and C-BARQ
scores at 12 months of age.

Serpell, J.A. & Duffy, D.L. 2016. Frontiers in Vet. Sci., doi: 10.3389/fvets.2016.00049
 Field Service
(18-24 months old)
Return to Center
For Training
Placement with (15-18 months old)
Volunteer Puppy Raiser
(7-9 weeks old)
Birth

C-BARQ
6 mos 12 mos Released
& Adopted
Dogs Reared By More Experienced Puppy-Raisers
Tend to Have Fewer Problems with Fear & Anxiety
Puppies raised with other dogs in the household
display lower levels of owner-directed aggression

Serpell, J.A. & Duffy, D.L. 2016. Frontiers in Vet. Sci., doi: 10.3389/fvets.2016.00049
Less Experienced Owners Are More Likely to
Acquire Puppies from Pet Stores
6

% Acquisition from Pet Store

4

0
Previous First dog
owners owned
Conclusions
• Aspects of early environment exert profound, long-
term effects on the behavior of dogs.
• Acquisition of puppies from pet stores is associated
with higher prevalence of almost all major behavior
problems.
• Causal mechanism(s) for this association remain
unclear, but epigenetic influence of maternal stress,
adverse effects of early weaning, and inexperienced
owners may all be contributory factors.
• Additional studies needed to identify main causal
factors.
• The current recommended re-homing age for
puppies should be amended to 7-9 weeks pending
further study of the effects of early weaning / re-
homing.
• The sensitive period for socialization doesn’t end at
12 weeks. It continues for at least the first year of
life.
Thank You!