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1 Full title: Public attitudes towards free-roaming dogs and dog ownership practices in
2 Bulgaria, Italy, and Ukraine
3 Short title: Public attitudes towards free-roaming dogs and dog ownership practices in three
4 European countries
5 L.M. Smith1*., R.J. Quinnell1., A.M. Munteanu2., S. Hartmann2., P. Dalla Villa3,4, L.M. Collins1*
6
7 1. School of Biology, Faculty of Biological Sciences, University of Leeds, Leeds, UK
8 2. VIER PFOTEN International, Vienna, Austria
9 3. Istituto Zooprofilattico Sperimentale dell’Abruzzo e del Molise “G. Caporale”, Teramo, Italy
10 4. World Organization for Animal Health, OIE Sub-Regional Representation in Brussels,
11 Belgium
12
13 *Corresponding authors:
14 Email: L.Collins@leeds.ac.uk (LMC) and lauren.m.smith026@gmail.com (LMS)
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15 Abstract
16 Overabundant, free-roaming dog populations are associated with risks to public health,
17 livestock losses, wildlife conservation, and dog health and welfare. Dog population
18 management is conducted to mitigate these issues. Assessing dog population management
19 strategies is important to determine their effectiveness, efficiency, and long-term impact. It is
20 essential to also determine how the behaviour and outlook of local communities may influence
21 the efficacy of dog population management. This study aimed to determine public attitudes
22 towards free-roaming dogs and their management and describe dog ownership practices in
23 three European countries using an online questionnaire survey. This study found that most
24 surveyed respondents wanted to see a reduction in free-roaming dog numbers, and felt that
25 this should be achieved through sheltering, catch-neuter-release, and by controlling the
26 breeding of owned dogs. This questionnaire also identified significant associations between
27 public attitudes and dog ownership practices with gender, religious beliefs, age, education
28 level, reason for dog ownership, previous experience with free-roaming dogs, and country of
29 residence. Respondents who identified as: (i) being male, (ii) holding religious beliefs, (iii)
30 owning dogs for practical reasons, (iv) being young, and (v) having no schooling or primary
31 education had a lower probability of neutering and a higher probability of allowing dogs to
32 roam. Respondents who identified as: (i) being female, (ii) feeling threatened by free-roaming
33 dogs, (iii) being older, and (iv) having more education had a higher probability of answering
34 that an increase in free-roaming dog numbers should be prevented. These findings can help
35 to inform future dog population management interventions in these countries and highlight the
36 importance of considering local public attitudes and dog ownership practices in the
37 development of effective dog population management approaches. Including these social
38 factors will ensure that both the community and organisations involved in dog population
39 management work cohesively towards a shared goal.
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40 Introduction
41 Domestic dogs (Canis familiaris) are one of the most abundant species of canids in the world,
42 with total population estimates between 700 million to 1 billion (1,2). Around 75% of this
43 population are classified as “free-roaming”, indicating their ability to roam and reproduce freely
44 (1). Where free-roaming dogs exist in high densities, there are important implications for public
45 health (3–5), livestock losses (6–10) and wildlife conservation (11–13), in addition to issues
46 for the welfare of the dogs themselves (14–17). The management methods applied to control
47 population sizes involve culling, reproductive control, and the use of shelters to house
48 unowned or unwanted dogs (18). Assessing dog population management is important to
49 determine whether these methods are effective and efficient, and to evaluate their long-
50 term impact.
51
52 Human behaviour can shape the success of a population management programme. This
53 includes actions of local communities, the teams involved in dog population management and
54 the governments imposing management strategies. Indeed, the World Organisation for Animal
55 Health (OIE) has identified that understanding public attitudes is important for developing
56 effective dog population control (19). In order for interventions to be successful, there must be
57 public support for both the management method and its aims (e.g. reducing or stabilising the
58 number of free-roaming dogs). Different communities may have different attitudes towards
59 free-roaming dogs and management methods due to culture, religion, and the specific risks to
60 humans, wildlife, livestock, and other companion animals in the area. Organisations involved
61 in dog population management should consider these factors to ensure interventions are
62 effective. For example, free-roaming dog populations can be an important part of a community,
63 providing protection to people and livestock (17). Where management methods aim to reduce
64 free-roaming dog numbers, there may still be demand for dogs in a community. Reduction in
65 numbers could result in increased movement of dogs from neighbouring areas, which has
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66 important implications for disease control (20–22). Prior to implementing management
67 strategies, the level of acceptance of free-roaming dogs in the area should be gauged (i.e.
68 determine whether the public prefer to have fewer free-roaming dogs in the community) so
69 that those involved in dog population management can work towards a goal that benefits the
70 community.
71
72 Dog ownership practices can also influence the success of population management.
73 Encouraging responsible ownership practices is included as an objective in Chapter 7.7 of the
74 OIE Terrestrial Animal Health Code on stray dog population control (19). The OIE defines
75 responsible ownership as: “When a person takes on the ownership of a dog, there should be
76 an immediate acceptance of responsibility for the dog, and for any offspring it may produce,
77 for the duration of its life or until a subsequent owner is found” (19). Unrestricted owned dogs
78 (free-roaming owned) and abandoned dogs are sources of free-roaming dog population
79 increase (19). Dog ownership practices that allow owned dogs to roam and do not prevent
80 reproduction can hinder efforts to control free-roaming dog populations. Those involved in dog
81 population management must determine the extent to which owned dogs contribute to the
82 free-roaming dog population so that management strategies can be tailored appropriately (e.g.
83 by encouraging responsible ownership through legislation and education programmes).
84
85 Questionnaire surveys are frequently used to gain insight into public attitudes, opinions,
86 behaviours, and the demographic and sociological factors associated with these. In terms of
87 dog population management, different attitudes, opinions and behaviours about and towards
88 dogs have been associated with responder gender (23–27), age (23,25,28), education
89 (24,25,29), and previous life experiences (e.g. experience of keeping dogs in childhood) (30).
90 Questionnaires aiming to describe dog ownership, public attitudes, and knowledge have been
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91 conducted in many countries around the world, but few published studies have been carried
92 out in European countries.
93
94 This study assesses how the behaviour and outlook of local communities may influence the
95 efficacy of dog population management, by gauging attitudes towards the presence of free-
96 roaming dogs and of dog ownership practices in three European countries – Bulgaria, Italy,
97 and Ukraine. The objectives of this study are to: (i) determine public attitudes towards the
98 presence of free-roaming dogs; (ii) determine local ownership practices, including whether
99 owned dogs were free-roaming or neutered, the level of dog abandonment, and the reasons
100 for dog abandonment; and (iii) investigate whether demographic and other factors (including
101 age, gender, education level, religious beliefs, and previous experience with dogs) influence
102 ownership practices and attitudes towards free-roaming dogs. This information can inform
103 interventions so that education campaigns can target groups who are at-risk of irresponsible
104 dog ownership behaviours (23,29), as well as provide a baseline for evaluating the impact of
105 interventions on human behaviour and attitudes (29).
106
107 Materials and methods
108 Study design
109 This was a cross-sectional study, with target populations of Bulgaria, Italy, and Ukraine. The
110 study populations were residents who used social media. Subjects were recruited through
111 social media using an online questionnaire (Online Surveys (31)) that was open between the
112 8th of March 2019 and the 21st of December 2019, available in four languages: Bulgarian,
113 Italian, Ukrainian, and Russian. The social media outlets used to distribute the questionnaire
114 included Facebook (32) and Twitter (33). Facebook advertising was used to increase the
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115 visibility of the questionnaire to the study population and increase the number of respondents.
116 Facebook advertising targeted Facebook users who: (i) were recorded in their online profile
117 as living in Bulgaria, Italy, or Ukraine; and (ii) were over the age of 18. The Facebook adverts
118 invited participants to provide their opinion on free-roaming dogs and dog ownership practices
119 (see S1 file for English translation of adverts). Sample sizes were calculated for the three
120 study areas, using Equation 1. A sample size of 385 respondents per study country was
121 necessary to provide estimates with a 5% error margin and 95% confidence interval. Subjects
122 under the age of 18 were filtered in the first page of the online questionnaire.
123
124 Equation 1. Sample size calculation
125
𝑆𝑎𝑚𝑝𝑙𝑒 𝑠𝑖𝑧𝑒
=
𝑧
2
×
𝑝(1
―
𝑝)
𝑒
2
1
+
(
𝑧
2
×
𝑝(1
―
𝑝)
𝑒
2
𝑁
)
126 Where N = population size, e = margin of error, z = z-score, p = population proportion.
127
128 Ethical approval
129 Prior to completing the questionnaire, all participants were asked to consent to their responses
130 being collected, stored, and analysed in an anonymised form for the purpose of reports and
131 publication. No directly identifiable information was collected; all data obtained remains
132 anonymous. Participants were able to withdraw from the questionnaire prior to completion, but
133 as the data was collected anonymously, participants could not withdraw after the questionnaire
134 was submitted. The study was approved by the University of Leeds Ethical Committee
135 (reference BIOSCI 17-003).
136
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137 Questionnaire design
138 The questionnaire was developed in English and translated into Bulgarian, Italian, Ukrainian,
139 and Russian. The questionnaire comprised closed questions regarding the subjects’ attitudes
140 and practices towards dog ownership and free-roaming dog population control. Likert-type
141 scales were used to estimate the level of agreement with specific questions. The questionnaire
142 consisted of three sections: (1) socio-demographic information of the respondent; (2)
143 ownership practices; and (3) attitudes towards the presence of free-roaming dogs and the
144 management of the free-roaming dog population. A copy of the questionnaire in English can
145 be found in S2 File.
146
147 Statistical analyses
148 All predictor and response variables are described in Table 1. Bernoulli logistic regression
149 models were used to test the effect of demographic parameters and respondent experience
150 on the response variables: (i) Neutering status of owned dogs; and (ii) respondents’ answers
151 to the question “Do you think an increase in dogs on the street should be prevented?”. Ordinal
152 probit models (34) were used to test the effect of demographic parameters and respondent
153 experience on: (i) Roaming status of owned dogs; (ii) I do not like the presence of stray dogs
154 around my home or work; and (iii) respondents’ answers to the question “Would you prefer to
155 see: no stray dogs, fewer stray dogs, do not mind stray dogs, more stray dogs”.
156
157 Table 1. Response and predictor variables (self-reported responses to questions)
158 included in the statistical analyses and their levels.
Variables
Levels
Age
* 18-24, 25-34, 35-44, 45-54, 55-64, 65-74 and
75 and above
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Variables
Levels
Children in household
Children in household, no children in
household
Country
Bulgaria, Italy, Ukraine
Dog ownership
Dog owner, non-dog owner
Education status
* No education, primary, secondary, tertiary
Gender
Male, Female, NA (including option Other)
Neutering status of owned dogs
Neutered, not neutered
Owning a dog for practical reasons
Practical, not practical
Religious belief
Religious, non-religious
Feeling physically threatened by dogs
on the street
* Strongly disagree, disagree, neither agree
nor disagree, agree, strongly agree
Been attacked by dogs on the street
Been attacked, not been attacked
Respondent or family members have
been bitten by dogs on the street in last
12 months
Been bitten, not been bitten
Roaming status of owned dogs
Never, Sometimes, Always
I do not like the presence of stray dogs
around my home or work
Strongly disagree, disagree, neither agree nor
disagree, agree, strongly agree
Should an increase in dogs on the
street be prevented?
Yes, No
Would you prefer to see dogs on the
street?
No stray dogs, fewer stray dogs, do not mind
stray dogs, more stray dogs
159 * Ordinal predictor variables analysed as continuous variables in statistical models.
160
161 Effect of parameters on dog ownership practices
162 Model 1 tested the effects of demographic parameters and respondent experience on
163 neutering of owned dogs using a Bayesian Bernoulli logistic regression model. The response
164 variable was neutering status of owned dogs with fixed effects of gender, age, education
165 status, religious belief, owning a dog for practical reasons and country (Table 1). Model 2
166 tested the effects of demographic parameters and respondent experience on the roaming
167 status of owned dogs using a Bayesian ordinal probit model. The response variable was
168 roaming status of owned dogs and fixed effects were the same as for Model 1.
169
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170 Effect of parameters on public attitudes
171 Model 3 tested the effects of demographic parameters and respondent experience on
172 agreement to the statement I do not like the presence of stray dogs around my home or work
173 using a Bayesian ordinal probit model. The response variable was I do not like the presence
174 of stray dogs around my home or work and fixed effects were dog ownership, gender, age,
175 education status, children in household, feeling physically threatened by dogs on the street,
176 been attacked by dogs on street, respondent or family members have been bitten by dogs on
177 the street in last 12 months, and country.
178 Model 4 tested the effects of demographic parameters and respondent experience on the
179 question Do you think an increase in dogs on the street should be prevented? using a
180 Bayesian Bernoulli logistic regression model. The response variable was should an increase
181 in dogs on the street be prevented, with fixed effects the same as in Model 3.
182 Model 5 tested the effects of demographic parameters and respondent experience on
183 response to the question Would you prefer to see: no stray dogs, fewer stray dogs, do not
184 mind stray dogs, more stray dogs using a Bayesian ordinal probit model. The response
185 variable was Would you prefer to see dogs on the street, with fixed effects the same as in
186 Model 3.
187
188 To fit the statistical models using a Bayesian analysis framework, the package “brms” version
189 2.12.0 (35) was used in R version 3.6.1 (36). All models were run with four chains, each with
190 2000 iterations (1000 used for warmup and 1000 for sampling). Thinning was set to one. The
191 total number of post-warmup samples was 4000. Where a response was missing (i.e. a
192 respondent did not answer a question), the response was omitted from the statistical analysis
193 (see S1 Table for number of no responses per variable).
194
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195 Collinearity in the predictor variables was checked using the “vif” function in R package “car”
196 (37) and values lower than three were considered not collinear. Model parameters were
197 summarised by the mean and 95% credible intervals of the posterior distribution (CI; 95%
198 most probable values). A significant effect was determined if the 95% credible intervals of the
199 posterior distribution did not contain zero on the log odds or probit scale. Probabilities were
200 converted from the logit scale to the probability scale by
exp
(𝑥)
1
+
(
exp
(
𝑥
)
)
, and are
201 converted to odds using
exp
(𝑥)
, where x is the posterior value on the logit scale.
202
203 Results
204 Descriptive analyses
205 Demographics
206 The numbers of respondents were 5,434 in Bulgaria, 3,468 in Italy, and 19,323 in Ukraine. All
207 demographic information is provided in S2 Table. Respondents were from multiple regions
208 within Bulgaria, Italy, and Ukraine (see S3 to S5 Tables). A broad range of ages between 18
209 and 64 were represented in all three study countries. Most respondents were female in all
210 three study countries (87.5% in Bulgaria, 83.1% in Italy, and 87.1% Ukraine). In Bulgaria
211 68.9%, 42.0% in Italy, and in Ukraine 67.3% of the respondents considered themselves to be
212 religious. In Bulgaria 36%, Italy 43% and Ukraine 57% of respondents lived in households with
213 children.
214
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215 Ownership practices
216 The main reason for dog ownership in all three study countries was for pleasure and company
217 (Bulgaria 85.5%, Italy 87.7%, Ukraine 70.7%; see Table S6 for detailed responses on
218 ownership practices). In Italy, a higher percentage of respondents acquired their dog from a
219 dog shelter (38.1%), compared to in Bulgaria (9.7%) and Ukraine (9.9%) (Fig 1). In Bulgaria
220 and Ukraine, more respondents found their dog on the street (Bulgaria 35.5% and Ukraine
221 34.6%) or received their dog from friends/family (Bulgaria 32.6% and Ukraine 27.9%). More
222 respondents in Italy answered that they prevent their dog from breeding through neutering
223 (65.4%), compared to 40.4% in Bulgaria and 35.4% in Ukraine. When asked the reason why
224 respondents did not prevent breeding, 37.6% of respondents in Bulgaria, 34.6% in Italy, and
225 13.7% in Ukraine answered: “A dog should reproduce at least once” (Fig 1). When
226 respondents were asked if they allowed their dog to roam outside unsupervised, 59.0% in
227 Bulgaria, 92.1% in Italy and 79.4% in Ukraine responded Never, and 29.5% in Bulgaria, 6.3%
228 in Italy and 16.3% in Ukraine responded Sometimes.
229
230 Fig 1. Ownership practices of respondents in Bulgaria, Italy, and Ukraine. The
231 percentage of respondents who answered each of the answer options regarding (A)
232 acquisition of dog, (B) reasons for not preventing breeding, (C) the outcome of the dog, and
233 (D) reason for relinquishment. * Multi answer question: Percentage of respondents who
234 selected each answer option (i.e. 100% would indicate that all respondents chose this option).
235
236 Most respondents in all study countries responded that they had never given up a dog
237 (Bulgaria 98.5%, Italy 92.4%, and Ukraine 92.2%). Those respondents who had given up a
238 dog mostly answered that this was because of an Animal behavioural problem (Bulgaria
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239 27.3%, Italy 36.5%, and Ukraine 23.8%), or Other reason (Bulgaria 39.4%, Italy 57.5%, and
240 Ukraine 45.3%) (Fig 1).
241
242 Attitudes
243 In Bulgaria and Ukraine, high percentages of respondents had seen a free-roaming dog on
244 the day they filled in the questionnaire (73.3% and 77.3% respectively), compared to only
245 15.4% of respondents in Italy (Fig 2; see S7 Table for detailed results). A higher percentage
246 of respondents in Bulgaria (21.6%) and Ukraine (26.5%) had been attacked by dogs on the
247 street ever in their lifetime, compared to few (4.2%) in Italy. Higher percentages of respondents
248 in Bulgaria answered that they provided care to free-roaming dogs by giving food (90.6%),
249 water (71.0%), and shelter (34.8%), compared to Italy (53.7% food, 44.2% water, 19.0%
250 shelter) and Ukraine (67.5% food, 29.6% water and 9.7% shelter) (S6 Table).
251
252 Fig 2. Attitudes of respondents towards free-roaming dogs in Bulgaria, Italy and
253 Ukraine. The percentage of respondents who answered each of the answer options regarding
254 (A) observation of free-roaming dogs and (B) agreement with statement “I do not like stray
255 dogs being present around my home or work”.
256
257 When respondents were asked their level of agreement with the statement “I do not like stray
258 dogs being present in the streets around my home or work”, responses were varied across
259 the full range of options between strongly disagree and strongly agree in Bulgaria and Ukraine
260 (varying between 14 and 25% for all answer options) (Fig 2). Most respondents in Italy
261 disagreed with this statement (35.8%). In all three study countries, most respondents
262 disagreed (Bulgaria 20.8%, Italy 19.3%, and Ukraine 25.3%) and strongly disagreed (Bulgaria
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263 42.2%, Italy 56.4%, and Ukraine 31.6%) with the statement “I feel physically threatened by
264 stray dogs”.
265
266 Respondents answered most often that the municipality government and volunteer
267 organisations should be responsible for managing the free-roaming dog population (Fig 3; S6
268 Table). Respondents most often answered that they would like to see no (Bulgaria 52.4%,
269 Italy 70.2%, and Ukraine 45.2%) and fewer (Bulgaria 32.8%, Italy 24.3%, and Ukraine 40.6%)
270 free-roaming dogs. Respondents who answered that they would like to see no or fewer free-
271 roaming dogs answered that this should be achieved through sheltering, CNR, and controlling
272 the breeding of owned dogs (Fig 3). Few answered that the free-roaming dog population
273 should be reduced through culling (Bulgaria 1.7%, Italy 1.6%, and Ukraine 6.3%).
274
275 Fig 3. Attitudes of respondents towards dog population management in Bulgaria, Italy,
276 and Ukraine. The percentage of respondents who answered each of the answer options
277 for: (A) who should be responsible for dog population management? and (B) how should free-
278 roaming dogs be reduced?. These were multi answer questions: Percentage of respondents
279 who selected each answer option (i.e. 100% would indicate that all respondents chose this
280 option).
281
282 Statistical analyses
283 All models converged (for all parameters Rhat = 1.00 and effective sample size >1000, see
284 Supplementary information). There was no collinearity in the predictor variables (all values
285 less than three). All raw model results (including the posterior mean values, standard
286 deviations and 95% credible intervals, the 2.5% and 97.5% percentiles of the posterior
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287 distribution) are presented in Tables S8 to S12. Estimates for mean and 95% CIs for
288 probabilities are reported for each model and presented in Table 2. Odds ratios (OR) are
289 reported for predictor variables in the Bernoulli logistic regression models (Models 1 and 4).
290
291 Table 2. Effect of predictor variables on statistical models on the probability scale.
292 Significant results are highlighted in bold. NI = predictor variable not included in the
293 model.
Predictor variable
Model 1
Model 2
Model 3
Model 4
Model 5
Probability
of neutering
(95% CI)
Probability
of answering
Never allow
dog to roam
(95% CI)
Probability
of answering
Strongly
agree (95%
CI)
Probability
of answering
Yes to the
question
“Should an
increase in
stray dogs
be
prevented”
(95% CI)
Probability
of answering
No stray
dogs (95%
CI)
Male
0.38 (0.35-
0.41)
0.74 (0.71-
0.76)
0.17 (0.16-
0.18)
0.97 (0.96-
0.97)
0.53 (0.51-
0.55)
Gender
Female
0.48 (0.47-
0.49)
0.81 (0.80-
0.82)
0.15 (0.14-
0.15)
0.98 (0.98-
0.99)
0.60 (0.59-
0.61)
Religious
0.44 (0.43-
0.45)
0.79 (0.78-
0.80)
NI
NI
NI
Religious
belief
Non-
religious
0.54 (0.52-
0.56)
0.83 (0.82-
0.85)
NI
NI
NI
Practical
0.31 (0.28-
0.33)
0.71 (0.69-
0.74)
NI
NI
NI
Reason for
dog
ownership
Non-
practical
0.48 (0.47-
0.49)
0.81 (0.80-
0.82)
NI
NI
NI
Attacked
NI
NI
0.16 (0.15-
0.17)
0.98 (0.98-
0.99)
0.61 (0.59-
0.62)
Been
attacked
by dogs on
the street
Not
attacked
NI
NI
0.15 (0.14-
0.15)
0.98 (0.98-
0.99)
0.59 (0.58-
0.59)
Bitten
NI
NI
0.19 (0.18-
0.21)
0.98 (0.98-
0.99)
0.65 (0.63-
0.67)
Responde
nt or family
members
have been
bitten by
dogs on
the street
in last 12
months
Not bitten
NI
NI
0.15 (0.14-
0.15)
0.98 (0.98-
0.99)
0.58 (0.57-
0.59)
Yes
NI
NI
0.15 (0.15-
0.16)
0.98 (0.98-
0.99)
0.59 (0.59-
0.60)
Dog
ownership
No
NI
NI
0.15 (0.14-
0.16)
0.98 0.98-
0.99)
0.56 (0.55-
0.57)
Yes
NI
NI
0.15 (0.15-
0.16)
0.98 (0.98-
0.99)
0.585 (0.58-
0.60)
Children in
household
No
NI
NI
0.15 (0.14-
0.15)
0.98 (0.98-
0.99)
0.593 (0.57-
0.59)
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Predictor variable
Model 1
Model 2
Model 3
Model 4
Model 5
18-24
0.40 (0.39-
0.42)
0.78 (0.76-
0.79)
0.14 (0.14-
0.15)
0.980
(0.977-
0.984)
0.57 (0.56-
0.58)
25-34
0.44 (0.43-
0.45)
0.79 (0.78-
0.80)
0.15 (0.14-
0.15)
0.982
(0.980-
0.985)
0.58 (0.57-
0.59)
35-44
0.47 (0.46-
0.48)
0.80 (0.80-
0.81)
0.15 (0.15-
0.16)
0.984
(0.982-
0.986)
0.59 (0.58-
0.60)
45-54
0.51 (0.49-
0.52)
0.82 (0.81-
0.83)
0.16 (0.15-
0.16)
0.985
(0.983-
0.988)
0.60 (0.59-
0.61)
55-64
0.54 (0.52-
0.56)
0.83 (0.82-
0.84)
0.16 (0.15-
0.17)
0.987
(0.984-
0.989)
0.61 (0.60-
0.63)
65-74
0.57 (0.55-
0.59)
0.84 (0.83-
0.86)
0.16 (0.15-
0.17)
0.988
(0.985-
0.991)
0.62 (0.61-
0.64)
Age
75+
0.61 (0.58-
0.63)
0.85 (0.84-
0.87)
0.17 (0.15-
0.18)
0.989
(0.985-
0.993)
0.63 (0.61-
0.65)
None
0.30 (0.24-
0.35)
0.73 (0.67-
0.78)
0.14 (0.12-
0.16)
0.95 (0.92-
0.97)
0.55 (0.51-
0.60)
Primary
0.35 (0.32-
0.39)
0.75 (0.72-
0.79)
0.14 (0.13-
0.16)
0.96 (0.95-
0.98)
0.57 (0.54-
0.60)
Secondar
y
0.41 (0.39-
0.43)
0.78 (0.77-
0.80)
0.15 (0.14-
0.16)
0.98 (0.97-
0.98)
0.58 (0.56-
0.60)
Education
level
Tertiary
0.48 (0.47-
0.49)
0.81 (0.80-
0.82)
0.15 (0.15-
0.16)
0.98 (0.98-
0.99)
0.60 (0.58-
0.60)
Strongly
disagree
NI
NI
0.05 (0.047-
0.054)
0.973
(0.969-
0.977)
0.49 (0.48-
0.50)
Disagree
NI
NI
0.13 (0.12-
0.13)
0.982
(0.980-
0.984)
0.57 (0.56-
0.58)
Neutral
NI
NI
0.26 (0.25 t0
0.27)
0.988
(0.986-
0.990)
0.65 (0.64-
0.66)
Agree
NI
NI
0.44 (0.43-
0.45)
0.992
(0.990-
0.994)
0.73 (0.72-
0.74)
Threatene
d by dogs
on the
street
Strongly
agree
NI
NI
0.64 (0.62-
0.65)
0.995
(0.993-
0.997)
0.79 (0.78-
0.81)
Bulgaria
0.41 (0.39-
0.43)
0.61 (0.59-
0.62)
0.20 (0.18-
0.21)
0.987
(0.983-
0.990)
0.55 (0.53-
0.56)
Italy
0.62 (0.60-
0.64)
0.92 (0.91-
0.93
0.10 (0.10-
0.11)
0.983
(0.979-
0.987)
0.76 (0.74-
0.77)
Country
Ukraine
0.37 (0.36-
0.38)
0.81 (0.81-
0.82)
0.17 (0.16-
0.17)
0.980
(0.978-
0.982)
0.45 0.44-
0.46)
294
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295 Effect of demographic parameters on neutering status of owned
296 dogs
297 Gender, age, education level, owning a dog for practical reasons, religious beliefs and country
298 had significant effects on the neutering status of owned dogs (Table S8). Probabilities of
299 neutering are presented in Table 2. Male respondents had a lower probability of neutering,
300 compared to females (OR 1.47; 95% CI 1.28-1.64). Holding religious beliefs (OR 0.66, 95%
301 CI 0.61 to 0.72) and owning dogs for practical reasons (i.e. guarding or hunting, compared to
302 for pleasure and company; OR 0.49, 95% CI 0.43 to 0.54) were both negatively associated
303 with neutering. Respondent age (OR 1.15; 95% CI 1.12-1.18) and education level (OR 1.29;
304 95% CI 1.17-1.41) were both positively associated with neutering (i.e. the older and more
305 educated a participant, the more likely they were to neuter). Respondents from Italy had a
306 higher probability of neutering compared to Bulgaria (OR 2.32; 95% CI 2.05-2.62) and Ukraine
307 (OR 2.73; 95% CI 2.44-3.01). Respondents from Ukraine had a lower probability of neutering
308 compared to Bulgaria (OR 0.37; 95% CI 0.33-0.40).
309
310 Effect of demographic parameters on roaming
311 Gender, age, education level, owning a dog for practical reasons, religious beliefs, and country
312 had significant effects on the roaming status of owned dogs (Table S9). Probabilities of
313 answering Never allow dog to roam for predictor variables are presented in Table 2. Females
314 had a higher probability of answering that they Never allowed their dog to roam. Respondents
315 who held religious beliefs, and respondents who owned dogs for practical reasons were less
316 likely to answer Never. Age of respondent was positively correlated with answering Never (i.e.
317 older respondents were less likely to allow their dog to roam). Increased education level of the
318 owner was positively associated with answering Never (i.e. respondents with higher levels of
319 education were less likely to allow their dog to roam). Respondents from Italy had the highest
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320 probability of answering Never, respondents in Bulgaria had the lowest probability of
321 answering Never.
322
323 Effect of demographic parameters and respondent experience on
324 answer to “I do not like the presence of stray dogs around home or
325 work”
326 Predictor variables gender, age, owning a dog for practical reasons, feeling threatened by
327 dogs on the street, having been attacked by dogs on the street, respondent or family members
328 have been bitten by dogs on the street in last 12 months, and country had significant effects
329 on agreement with the statement I do not like the presence of stray dogs around my home or
330 work (Table S10). Probabilities for answering Strongly agree for predictor variables are
331 presented in Table 2. Female respondents had a lower probability of agreeing with the
332 statement. Respondents who answered Yes to the question Have you ever been attacked by
333 dogs on the street? had a higher probability of agreeing with the statement. Respondents who
334 answered Yes to the question Have you or your family members been bitten in the last 12
335 months? had a higher probability of agreeing with the statement. Respondent age was
336 positively associated with agreement to the statement (i.e. older respondents were more likely
337 to agree). Agreement with the statement I feel physically threatened by dogs on the street was
338 positively associated with agreement with the statement I do not like the presence of stray
339 dogs around my home or work (i.e. respondents who felt threatened were more likely to agree
340 with the statement that they did not like the presence of dogs around their home or work).
341 Respondents from Italy had the lowest probability of answering Strongly agree, and
342 respondents from Bulgaria had the highest probability of answering Strongly agree.
343
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344 There was no evidence of an effect of: dog ownership, education level, and children in
345 household on agreement with the statement I do not like stray dogs present around my home
346 or work (Table S10).
347
348 Effect of demographic parameters and respondent experience on
349 answering an increase in stray dogs should be prevented.
350 There were significant effects of gender, age, education level, and feeling threatened by dogs
351 on the street on answering Yes to the question Do you think an increase in dogs on the street
352 should be prevented? (Table S11). Female respondents had a higher probability of answering
353 Yes (OR 2.14; 95% CI 1.67-2.65). There was a positive association between answering Yes
354 and respondents’ agreement with the statement “I feel physically threatened by dogs on the
355 street” (OR 1.53; 95% CI 1.37-1.68); their age (OR 1.11; 95% CI 1.03-1.19); and education
356 (OR 1.54; 95% CI 1.24-1.83).
357
358 There was no evidence of an effect of dog ownership, children in household, having been
359 attacked by dogs on the street, respondent or family members have been bitten by dogs on
360 the street in last 12 months or country (Table S11).
361
362 Effects of demographic parameters and respondent experience on
363 the question “Would you prefer to see: no stray dogs, fewer stray
364 dogs, do not mind stray dogs, more stray dogs”
365 Dog ownership, gender, age, feeling threatened by dogs on the street, having been attacked
366 by dogs on the street, respondent or family members have been bitten by dogs on the street
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367 in last 12 months, and country had significant effects on response to this question regarding
368 preference for observing stray dogs (Table S12). Probabilities for answering No stray dogs for
369 predictor variables are presented in Table 2. Male respondents had a lower probability of
370 answering No stray dogs (Table 2). Dog owners had a higher probability of answering No stray
371 dogs. Respondents who answered Yes to the question “Have you ever been attacked by dogs
372 on the street?”, or Yes to the question “Have you or your family members been bitten in the
373 last 12 months” or had children in their household had a higher probability of answering No
374 stray dogs. Agreement with the statement “I feel physically threatened by dogs on the street”
375 was positively correlated with answering No stray dogs (i.e. respondents who feel threatened
376 by dogs on the street are more likely to answer No stray dogs). Respondent age was positively
377 correlated with answering No stray dogs (i.e. older respondents had an higher probability of
378 preferring to see No stray dogs). Respondents in Italy had the highest probability of answering
379 No stray dogs, and respondents in Ukraine had the lowest probability of answering No stray
380 dogs.
381
382 There was no evidence of an effect of children in household and education level on the
383 probability of preference of observing stray dogs (Table S12).
384
385 Discussion
386 This study quantified dog ownership practices and investigated public attitudes towards the
387 management of free-roaming dogs in Bulgaria, Italy, and Ukraine. Risk factors for neutering,
388 roaming and tolerance of free-roaming dog presence have been identified by comparing
389 attitudes and dog ownership practices to demographic factors. This study found evidence for
390 significant effects of gender, religious beliefs, age, education level, reason for dog ownership,
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391 previous experience with free-roaming dogs, and country of residence on ownership practices
392 and attitudes.
393
394 Ownership practices
395 Responsible ownership is an important component of dog population management (19). In
396 order to effectively target dog population management interventions, it is important to
397 understand the level of dog ownership, level of care for owned dogs (e.g. feeding and
398 vaccination) and prevalence of abandonment, neutering and roaming practices. This study
399 quantified the prevalence of ownership practices in Bulgaria, Italy, and Ukraine, allowing us to
400 make comparisons between the countries.
401
402 There were differences in dog-acquiring behaviour between the countries. More respondents
403 in Italy acquired their dogs from a shelter, compared to acquiring from friends or by finding a
404 dog in the street in Bulgaria and Ukraine. The differences in dog acquiring behaviour could be
405 due to a lack of public awareness of local shelters, or perceived differences in shelter quality
406 between the study countries. However, there is currently little research to substantiate these
407 explanations and more work on public awareness is needed. In all study countries, many
408 participants had adopted a dog directly from the street, potentially reflecting the prevalence of
409 free-roaming dogs in the study countries. Fewer participants in Italy paid for their dog. Previous
410 studies have suggested that dogs who are received for little cost are at higher risk of
411 relinquishment (38). However, the number of respondents who answered that they had given
412 up a dog was low across the study countries. These numbers are likely to be an underestimate,
413 given the taboo around relinquishing dogs. A study by Hsu, Severinghaus and Serpell (2003)
414 (30) found similar estimates, where only 5.3% of respondents answered that they had given
415 up a dog, however, far more respondents answered that they knew someone who had given
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416 up a dog (31.9%). This indicates that respondents may underreport relinquishment of owned
417 dogs.
418
419 Responsible dog ownership requires that an owner provides care for a dog until they are
420 transferred to another owner (19). Most respondents who had relinquished a dog in Italy and
421 Ukraine reported they had given their dog to a friend (Fig 1), complying with responsible
422 ownership (19). In Bulgaria, a higher percentage of respondents answered they had “Let free”
423 their dog (Fig 1). Letting a dog free to the street directly increases the free-roaming dog
424 population. Previous studies have found that respondents prefer to let a dog free to the street
425 as it offers the dog an opportunity to live, unrestricted, outside of a shelter and offers the
426 possibility to find another owner through adoption from the street (30). This suggests that some
427 dog owners may perceive letting a dog free to the street as responsible ownership. Further
428 research is required to understand why respondents in Bulgaria chose to let a dog free, instead
429 of giving to a shelter or to another owner.
430
431 Preventing the production of unwanted puppies is an important part of responsible ownership
432 (19). Most respondents answered that they prevented their dogs from reproducing; 50.8%
433 respondents in Bulgaria, 65.3% in Italy, and 35.3% in Ukraine answered that they did so
434 through neutering. These results should be interpreted with caution, as the self-selection
435 process of recruiting for questionnaires can result in biased samples of the populations. It is
436 possible that respondents who were more likely to neuter their dogs (such as those with higher
437 levels of education) were more likely to complete the questionnaire. The true proportion of
438 neutered owned dogs in the study countries may therefore be lower. Neutering of owned dogs
439 can prevent unwanted offspring and, if owned dogs are free-roaming, can help to prevent
440 unowned dogs from reproducing. When respondents were asked why they did not neuter their
441 dog, the most common answer (if one was provided) across all countries was that a dog should
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442 reproduce at least once (Fig 1). Few respondents answered that it was for cost reasons. This
443 contrasts with previous findings in Taiwan (30) and Brazil (39), where respondents cite cost
444 and “too much trouble” as primary reasons for not neutering. As cost, in this study, was not
445 found to be a primary reason that owners did not neuter their dogs, this suggests that in
446 Bulgaria, Italy, and Ukraine, whilst low-cost or free neutering interventions may be important
447 (40), interventions should also address owner attitudes towards reproduction, in order for
448 interventions to have a greater impact.
449
450 This study found evidence for significant associations between country, gender, religious
451 belief, reason for ownership, age, and education level and the probability of neutering (Table
452 S9). These results reflect those reported in other studies (23–27,29). For example, a study by
453 Fielding (2007) in New Providence, The Bahamas (24) also found that respondents with higher
454 levels of education were more likely to have neutered their dog. Similarly, Costa et al., (2015)
455 (29) found that respondents with higher levels of education were more likely to answer that
456 neutering was the best way to control the overabundance of stray animals in Brazil.
457 Respondents with higher levels of education may have a higher level of awareness of
458 responsible ownership and the benefits of neutering, in addition to potentially having a higher
459 income and ability to pay for neutering. Fielding, Samuels & Mather (2002) (23) also found a
460 significant effect of owner age on neutering probability, suggesting that younger owners may
461 have a greater desire to breed from their dog, compared to older owners.
462
463 Owned dogs that are free-roaming contribute to the free-roaming population directly by
464 increasing the population size. Owned free-roaming dogs therefore contribute to the issues,
465 such as the risks to public health (41,42) and wildlife (11,12,43–47). Efforts encouraging
466 responsible ownership may help reduce the number of dogs roaming, and may therefore help
467 to reduce the impacts of the free-roaming dogs on public health and wildlife (19). This study
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468 found evidence for significant effects of gender, religious beliefs, reason for dog ownership,
469 age, education, and country, on the probability of allowing owned dogs to roam (Table S9). It
470 is clear from these results that interventions should be targeted using these demographic risk
471 factors to prevent roaming behaviour, particularly in countries where higher percentages of
472 owned dogs are free-roaming, such as Bulgaria and Ukraine.
473
474 Most respondents (59-92%) across all three countries answered that they never allowed their
475 dogs to roam (Table S5). Again, these results might be biased, for example respondents less
476 likely to allow their dogs to roam may have been more likely to complete the questionnaire.
477 The results are higher than those reported in the Bahamas 57% (48), Bhutan 50% (49),
478 Cameroon 37.7% (50), Guatemala 25.7% (51), urban households in Haiti 54% (52), Kenya
479 19% (53), Mexico 44.9% (54), Ethiopia 15.7% (55), Tanzania 22% (56), and Uganda 21.7%
480 (57), but lower than those reported in semi-urban households in Haiti 62% (52) and Taiwan
481 79% (30). There was a significant effect of study country on roaming probability (Table S9),
482 with respondents in Bulgaria more likely to allow their dogs to roam, compared to Italy and
483 Ukraine. The significant effect of country may reflect differences in dog ownership behaviour
484 and culture.
485
486 Attitudes towards free-roaming dogs
487 In Bulgaria and Ukraine, almost all respondents answered that they had seen free-roaming
488 dogs on the street, whereas in Italy 18.7% of respondents had never seen a free-roaming dog
489 (Fig 2). These results may indicate that the populations of free-roaming dogs are larger in
490 Bulgaria and Ukraine. Within Italy, there are differences in dog population management: some
491 regions permit CNR and the presence of “community dogs” (free-roaming dogs owned by the
492 municipality), whilst other regions only permit dog population management through sheltering.
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493 Respondents living in regions that do not permit community dogs, or in regions with smaller
494 free-roaming dog populations, may be expected to observe fewer free-roaming dogs. Higher
495 percentages of respondents in Bulgaria and Ukraine answered that they felt threatened by
496 free-roaming dogs, and that they or a member of their family had been bitten in the last 12
497 months. These results may also indicate a greater free-roaming dog population size and
498 related problems in Bulgaria and Ukraine.
499
500 A large proportion of respondents across all countries answered that they provided care for
501 free-roaming dogs (Table S6). For example, 90.6% in Bulgaria, 53.7% in Italy, and 67.5% of
502 respondents in Ukraine answered that they provided food for free-roaming dogs. For Bulgaria
503 and Ukraine, these numbers are similar to those reported by Costa et al., (2015) in Brazil,
504 where 61.9% of respondents reported that they or their neighbours fed stray animals, and
505 Massei et al., (2017) (58) in Nepal, where 47% of respondents provided food and care for free-
506 roaming dogs. In a previous study by Slater et al., (2008) (59) in central Italy, only 5% of
507 respondents reported that they provided care for free-roaming dogs. This is much lower than
508 the numbers reported in this study, where 71.5% of Italian respondents answered that they
509 provided care for free-roaming dogs. This may be explained by the potential bias in the
510 recruitment process of this study, respondents who provide care for free-roaming dogs may
511 also have been more motivated to complete the questionnaire. Data was collected by Slater
512 et al., (2008) using an anonymous telephone survey and had a high response rate (74%).
513 Providing care for free-roaming dogs is controversial. Providing food may alleviate welfare
514 issues associated with lack of nutrition in the free-roaming dog population (60–62), but also
515 increases the carrying capacity for the free-roaming dog population.
516
517 Most respondents across all study countries felt that the municipal government and volunteer
518 organisations should be responsible for managing free roaming dog populations, and mostly
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519 by methods such as sheltering, CNR, and by controlling the breeding of owned dogs (Fig 3).
520 These results are similar to those found in previous studies (59,63,64). For example, a study
521 by Ortega-Pacheco et al., (2007) (64) in Yucatan, Mexico found that 52.8% of interviewed
522 households supported the neutering of dogs for dog population management, and felt that the
523 government and society were responsible for dog population management. The results in this
524 study suggest there is support for dog population management through sheltering, CNR, and
525 restricted breeding of owned dogs. Few respondents answered that culling should be used to
526 control the free-roaming dog population (Fig 3). These results are similar to those found by
527 Beckman et al., (2014) (63), but are much lower than results by Costa et al., (2017) (29),
528 where culling was supported by 26.8% of respondents.
529
530 As public attitudes can play an important role in determining the success of dog population
531 management, it is important that organisations involved in dog population management gauge
532 the level of support for reducing free-roaming dogs in the area. Across all three countries,
533 most respondents answered that they would prefer to see fewer or no stray dogs, and that an
534 increase in stray dogs should be prevented. With regards to Italy, these responses correspond
535 with previously reported attitudes in the Teramo province in the Abruzzo region of Italy (59).
536
537 Implications for future interventions
538 The results of this study suggest that the public in the three study countries would prefer a
539 reduction in free-roaming dog numbers, and for this to be achieved through sheltering, CNR
540 and responsible ownership, rather than culling. There is therefore support for the management
541 interventions that are taking place in these study countries. Targeted interventions that can
542 influence the behaviour of those less likely to practice responsible ownership may help to
543 improve responsible ownership and reduce free-roaming dog numbers. For example, as there
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544 was evidence for significant effects of gender and age on roaming and neutering, interventions
545 could be adapted to target men and younger people on responsible ownership practices.
546
547 Questionnaires are important tools for evaluating the impact of interventions on human
548 attitudes and behaviour. This includes monitoring public attitudes and behaviour (such as
549 responsible ownership) to determine whether education campaigns are having a significant
550 effect. There have been numerous studies on public attitudes towards free-roaming dogs and
551 dog ownership practices, but few repeated surveys to assess the effectiveness of dog
552 population control on human attitudes and behaviour (29,65). The results from this present
553 study can be used to target interventions to those who are less likely to practice responsible
554 ownership and the results can also be used as a baseline for monitoring the effect of dog
555 population management interventions on dog ownership behaviours and public attitudes in
556 Bulgaria, Italy, and Ukraine.
557
558 Limitations of questionnaire research methods
559 There are limitations in using questionnaires to determine public attitudes and behaviours.
560 The self-selection process involved in the recruitment for questionnaires can result in a biased
561 sample of the target population, as certain members of the public may be more motivated to
562 complete the survey, for example dog owners, or those with strong views about the subject.
563 In this survey, as with other similarly themed surveys (59), a high percentage of the
564 respondents were female. As responses from male members of the public were lacking, the
565 survey results may not necessarily reflect the views of the wider population. A similarly high
566 percentage of respondents reported to have or be in tertiary education, which is not
567 representative of the wider populations. The questionnaire was also primarily advertised
568 through social media; therefore, members of the public who do not have access to social
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569 media are likely to have been missed. Although this is a limitation, social media provides
570 opportunities to recruit a large and diverse range of participants (see (66,67) for review).
571 Despite the clear biases in questionnaire surveys, given the range of participants in this study
572 (for example, in terms of ages and regions), the results provide an indication of ownership
573 practices and public attitudes, and the statistical models still give us information about the risk
574 factors for behaviours and attitudes.
575
576 Conclusions
577 When planning dog population management interventions, it is important to understand how
578 human behaviour may impact the success of an intervention. This involves understanding how
579 public behaviour, such as dog ownership practices, may influence intervention success, and
580 gauging the level of public support for management interventions. This study found evidence
581 for significant effects of demographic factors on ownership practices and public attitudes.
582 These results can be used to inform future dog population management interventions in these
583 countries. Interventions should consider also carrying out periodic questionnaire surveys to
584 evaluate changes in public attitudes towards responsible ownership and the free-roaming dog
585 population.
586
587 Acknowledgements
588 This research was funded by VIER PFOTEN International. We thank Sarah Ross, Benjamin
589 Cueni, Alesya Lischyshyna, Greta Berteselli, and Matteo Chincarini for providing support with
590 Facebook advertising and translation and all survey participants for contributing to the study.
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28
592 References
593 1. Hughes J, Macdonald DW. A review of the interactions between free-roaming domestic
594 dogs and wildlife. Biol Conserv. 2013 Jan;157:341–51.
595 2. Gompper M. The dog-human-wildlife interface: assessing the scope of the problem.
596 Gompper ME, editor. Oxford: Oxford University Press, UK; 2014. 9–45 p.
597 3. Jimenez S, Perez A, Gil H, Schantz PM, Ramalle E, Juste RA. Progress in control of
598 cystic echinococcosis in La Rioja, Spain: decline in infection prevalences in human and
599 animal hosts and economic costs and benefits. ACTA Trop. 2002 Sep;83(3):213–21.
600 4. Economides P, Christofi G. Experience gained and evaluation of the
601 Echinococcosis/Hydatidosis eradication programmes in Cyprus 1971-1999. In: Craig,
602 P and Pawlowski Z, editor. Cestode Zoonoses: Echinococcosis and cysticercosis: an
603 ermergent and global problem. Amsterdam, The Netherlands: IOS Press; 2002. p. 367–
604 79. (NATO Science Series, Sub-Series I: Life and Behavioural Sciences; vol. 341).
605 5. Morters MK, McKinley TJ, Restif O, Conlan AJK, Cleaveland S, Hampson K, et al. The
606 demography of free-roaming dog populations and applications to disease and
607 population control. J Appl Ecol. 2014 Aug;51(4):1096–106.
608 6. Home C, Pal R, Sharma R, Suryawanshi K, Bhatnagar Y, Vanak A. Commensal in
609 conflict: Livestock depredation patterns by free-ranging domestic dogs in the Upper
610 Spiti Landscape, Himachal Pradesh, India. R Swedish Acad Sci. 2017;46(6):655–66.
611 7. Ciucci P, Luigi B. Wolf and Dog Depredation on Livestock in Central Italy. Wildl Soc
612 Bull. 1998;26(3):504–14.
613 8. Blair B, Townsend T. Dog Predation of Domestic Sheep in Ohio. J Range Manag.
614 1983;36(4):527–8.
615 9. Bergman DL, Breck SW, Bender SC. Dogs gone wild: Feral dog damage in the United
616 States. In: The Thirteenth Wildlife Damage Management Conference 5th April 2009.
.CC-BY 4.0 International licensemade available under a
(which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is
The copyright holder for this preprintthis version posted May 17, 2021. ; https://doi.org/10.1101/2021.05.17.444435doi: bioRxiv preprint
29
617 Saratoga Springs, NY, USA; 2009. p. 177–83.
618 10. Wierzbowska IA, Hedrzak M, Popczyk B, Okarma H, Crooks KR. Predation of wildlife
619 by free-ranging domestic dogs in Polish hunting grounds and potential competition with
620 the grey wolf. Biol Conserv. 2016 Sep;201:1–9.
621 11. Haydon DT, Laurenson MK, Sillero‐Zubiri C. Integrating epidemiology into population
622 viability analysis: managing the risk posed by rabies and canine distemper to the
623 Ethiopian wolf. Conserv Biol. 2002;16(5):1372–85.
624 12. Newsome TM, Stephens D, Ballard G-A, Dickman CR, Fleming PJS. Genetic profile of
625 dingoes (Canis lupus dingo) and free-roaming domestic dogs (C. l. familiaris) in the
626 Tanami Desert, Australia. Wildl Res. 2013;40(3):196–206.
627 13. Doherty TS, Dickman CR, Glen AS, Newsome TM, Nimmo DG, Ritchie EG, et al. The
628 global impacts of domestic dogs on threatened vertebrates. Biol Conserv. 2017
629 Jun;210(1):56–9.
630 14. Fielding W, Mather J. Stray dogs in an island community: A case study from New
631 Providence, The Bahamas. J Appl Anim Welf Sci. 2000;3(4):305–19.
632 15. Rodriguez-Vivas. R.I., Ortega-Pacheco. A., Rosado-Aguilar. J.A. BGME. Factors
633 affecting the prevalence of mange-mite infestations in stray dogs of Yucatán, Mexico.
634 Parasitology. 2003;115:61–5.
635 16. HSI. Case study of an incentive program to encourage the sterilization of dogs (and
636 cats) and greater attention to animal welfare on Abaco Island in the Bahamas.
637 Washington, D.C; 2001.
638 17. Macpherson C, Meslin FX, Wandeler AI. Dog Ecology and Population Biology. In:
639 Macpherson C, Meslin FX, Wandeler AI, editors. Dogs, zoonoses and public health.
640 New York: CABI Publishing; 2002. p. 17–62.
641 18. Dalla Villa P, Kahn S, Stuardo L, Iannetti L, Di Nardo A, Serpell JA. Free-roaming dog
.CC-BY 4.0 International licensemade available under a
(which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is
The copyright holder for this preprintthis version posted May 17, 2021. ; https://doi.org/10.1101/2021.05.17.444435doi: bioRxiv preprint
30
642 control among OIE-member countries. Prev Vet Med. 2010;97(1):58–63.
643 19. World Organisation for Animal Health(OIE). Stray dogs population control. Terrestrial
644 Animal Health Code. 2019.
645 20. Morters MK, Restif O, Hampson K, Cleaveland S, Wood JLN, Conlan AJK.
646 Evidence‐based control of canine rabies: a critical review of population density
647 reduction. J Anim Ecol. 2013;82(1):6–14.
648 21. Ferguson EA, Hampson K, Cleaveland S, Consunji R, Deray R, Friar J, et al.
649 Heterogeneity in the spread and control of infectious disease: consequences for the
650 elimination of canine rabies. Sci Rep. 2015;5:18232.
651 22. Townsend SE, Sumantra IP, Bagus GN, Brum E, Cleaveland S, Crafter S, et al.
652 Designing programs for eliminating canine rabies from islands: Bali, Indonesia as a
653 case study. PLoS Negl Trop Dis. 2013;7(8):1–11.
654 23. Fielding WJ, Samuels D, Mather J. Attitudes and actions of West Indian dog owners
655 towards neutering their animals: A gender issue? Anthrozoos. 2002;15(3):206–26.
656 24. Fielding W. Knowledge of the welfare of nonhuman animals and prevalence of dog care
657 practices in New Providence, The Bahamas. J Appl Anim Welf Sci. 2007;10(2):153–68.
658 25. McKay SA, Farnworth MJ, Waran NK. Current attitudes toward, and incidence of,
659 sterilization of cats and dogs by caregivers (owners) in Auckland, New Zealand. J Appl
660 Anim Welf Sci. 2009;12(4):331–44.
661 26. Blackshaw J, Day C. Attitudes of dog owners to neutering pets: demographic data and
662 effects of owner attitudes. Aust Vet J. 1994 Apr 1;71(4):113–6.
663 27. Wongsaengchan C, McKeegan DEF. The views of the UK public towards routine
664 neutering of dogs and cats. Animals. 2019;9(4):1–16.
665 28. Driscoll K. Attitudes towards animal use. Anthrozoos. 1992;5(1):32–9.
.CC-BY 4.0 International licensemade available under a
(which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is
The copyright holder for this preprintthis version posted May 17, 2021. ; https://doi.org/10.1101/2021.05.17.444435doi: bioRxiv preprint
31
666 29. Costa ED, Martins CM, Cunha GR, Catapan DC, Ferreira F, Oliveira ST, et al. Impact
667 of a 3-year pet management program on pet population and owner’s perception. Prev
668 Vet Med. 2017 Apr;139(A):33–41.
669 30. Hsu Y, Severinghaus LL, Serpell JA. Dog Keeping in Taiwan : Its Contribution to the
670 Problem of Free-Roaming. J Appl Anim Welf Sci. 2003;6(1):1–23.
671 31. Online surveys [Internet]. [cited 2019 Nov 18]. Available from:
672 https://www.onlinesurveys.ac.uk/
673 32. Facebook [Internet]. [cited 2019 Nov 18]. Available from: https://www.facebook.com/
674 33. Twitter [Internet]. [cited 2019 Nov 18]. Available from: https://twitter.com/
675 34. Liddell TM, Kruschke JK. Analyzing ordinal data with metric models: What could
676 possibly go wrong? J Exp Soc Psychol. 2018;79(September):328–48.
677 35. Bürkner PC. brms: An R package for Bayesian multilevel models using Stan. J Stat
678 Softw. 2017;80:1–28.
679 36. R Core Team. R: A language and environment for statistical computing. R Foundation
680 for Statistical Computing, Vienna, Austria. 2013.
681 37. Fox J, Weisberg S. An R Companion to Applied Regression. Third. Thousand Oaks,
682 CA: Sage; 2019.
683 38. New JC, Salman MD, King M, Scarlett JM, Kass PH, Hutchison JM. Characteristics of
684 Shelter-Relinquished Animals and Their Owners Compared With Animals and Their
685 Owners in U.S. Pet-Owning Households. J Appl Anim Welf Sci. 2000;3(3):179–201.
686 39. Santos Baquero O, Marconcin S, Rocha A, Maria Garcia R de C. Companion animal
687 demography and population management in Pinhais, Brazil. Prev Vet Med. 2018
688 Oct;158:169–77.
689 40. Kass PH, Johnson KL, Weng HY. Evaluation of animal control measures on pet
.CC-BY 4.0 International licensemade available under a
(which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is
The copyright holder for this preprintthis version posted May 17, 2021. ; https://doi.org/10.1101/2021.05.17.444435doi: bioRxiv preprint
32
690 demographics in Santa Clara County, California, 1993-2006. PeerJ. 2013;1(18):1–15.
691 41. Tenzin T, Ahmed R, Debnath NC, Ahmed G, Yamage M. Free-Roaming Dog Population
692 Estimation and Status of the Dog Population Management and Rabies Control Program
693 in Dhaka City, Bangladesh. PLoS Negl Trop Dis. 2015 May;9(5):1–14.
694 42. Rinzin K, Tenzin T, Robertson I. Size and demography pattern of the domestic dog
695 population in Bhutan: Implications for dog population management and disease control.
696 Prev Vet Med. 2016 Apr;126:39–47.
697 43. Ritchie E, Dickman C, Letnic M, Vanak AT. Dogs as predators and trophic regulators.
698 In: Gompper ME, editor. Free-ranging dogs and wildlife conservation. Oxford: Oxford
699 University Press; 2014. p. 55–68.
700 44. Vial F, Cleaveland S, Rasmussen G, Haydon DT. Development of vaccination
701 strategies for the management of rabies in African wild dogs. Biol Conserv.
702 2006;131(2):180–92.
703 45. Cleaveland S, Appel MG., Chalmers WS., Chillingworth C, Kaare M, Dye C. Serological
704 and demographic evidence for domestic dogs as a source of canine distemper virus
705 infection for Serengeti wildlife. Vet Microbiol. 2000 Mar 15;72(3–4):217–27.
706 46. Vilà C, Wayne R. Hybridization between wolves and dogs. Conserv Biol.
707 1999;13(1):195–8.
708 47. Sundqvist A-K, Ellegren H, Vila C. Wolf or dog? Genetic identification of predators from
709 saliva collected around bite wounds’ on prey. Conserv Genet. 2008;9(5):1275–9.
710 48. Fielding WJ, Plumridge SJ. Characteristics of owned dogs on the island of New
711 Providence, The Bahamas. J Appl Anim Welf Sci. 2005;8(4):245–60.
712 49. Tenzin T, Namgyal J, Letho S, Infectious SL-B, 2017 U. Community-based survey
713 during rabies outbreaks in Rangjung town, Trashigang, eastern Bhutan, 2016.
714 bmcinfectdis.biomedcentral.com. 2017 Dec 17;17(1):281–6.
.CC-BY 4.0 International licensemade available under a
(which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is
The copyright holder for this preprintthis version posted May 17, 2021. ; https://doi.org/10.1101/2021.05.17.444435doi: bioRxiv preprint
33
715 50. Costa G, Gilbert A, Monroe B, Blanton J, Ngam Ngam S, Recuenco S, et al. The
716 influence of poverty and rabies knowledge on healthcare seeking behaviors and dog
717 ownership, Cameroon. Rupprecht CE, editor. PLoS One. 2018 Jun 21;13(6):1–19.
718 51. Pulczer AS, Jones-Bitton A, Waltner-Toews D, Dewey CE. Owned dog demography in
719 Todos Santos Cuchumatán, Guatemala. Prev Vet Med. 2013;108(2–3):209–17.
720 52. Schildecker S, Millien M, Blanton JD, Boone J, Emery A, Ludder F, et al. Dog Ecology
721 and Barriers to Canine Rabies Control in the Republic of Haiti, 2014-2015. Transbound
722 Emerg Dis. 2016;64(5):1433–42.
723 53. Kitala P, McDermott J, Kyule M, Gathuma J, Perry B, Wandeler A. Dog ecology and
724 demography information to support the planning of rabies control in Machakos District,
725 Kenya. Acta Trop. 2001 Mar;78(3):217–30.
726 54. Kisiel LM, Jones-Bitton A, Sargeant JM, Coe JB, Flockhart DTT, Reynoso Palomar A,
727 et al. Owned dog ecology and demography in Villa de Tezontepec, Hidalgo, Mexico.
728 Prev Vet Med. 2016;135:37–46.
729 55. Tschopp R, Bekele S, Aseffa A. Dog Demography, Animal Bite Management and
730 Rabies Knowledge-Attitude and Practices in the Awash Basin, Eastern Ethiopia. PLoS
731 Negl Trop Dis. 2016;10(2):1–14.
732 56. Sambo M, Lembo T, Cleaveland S, Ferguson HM, Sikana L, Simon C, et al. Knowledge,
733 Attitudes and Practices (KAP) about Rabies Prevention and Control: A Community
734 Survey in Tanzania. PLoS Negl Trop Dis. 2014;8(12):1–10.
735 57. Wallace RML, Mehal J, Nakazawa Y, Recuenco S, Bakamutumaho B, Osinubi M, et al.
736 The impact of poverty on dog ownership and access to canine rabies vaccination:
737 Results from a knowledge, attitudes and practices survey, Uganda 2013. Infect Dis
738 Poverty. 2017;6(97):1–22.
739 58. Massei G, Fooks AR, Horton DL, Callaby R, Sharma K, Dhakal IP, et al. Free-Roaming
.CC-BY 4.0 International licensemade available under a
(which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is
The copyright holder for this preprintthis version posted May 17, 2021. ; https://doi.org/10.1101/2021.05.17.444435doi: bioRxiv preprint
34
740 Dogs in Nepal: Demographics, Health and Public Knowledge, Attitudes and Practices.
741 Zoonoses Public Health. 2017 Feb;64(1):29–40.
742 59. Slater MR, Di Nardo A, Pediconi O, Villa PD, Candeloro L, Alessandrini B, et al. Free-
743 roaming dogs and cats in central Italy: Public perceptions of the problem. Prev Vet Med.
744 2008 Apr;84(1–2):27–47.
745 60. Totton SC, Wandeler AI, Ribble CS, Rosatte RC, McEwen SA. Stray dog population
746 health in Jodhpur, India in the wake of an animal birth control (ABC) program. Prev Vet
747 Med. 2011 Feb;98(2–3):215–20.
748 61. Butler JRA, Brown WY, du Toit JT. Anthropogenic Food Subsidy to a Commensal
749 Carnivore: The Value and Supply of Human Faeces in the Diet of Free-Ranging Dogs.
750 Animals. 2018 May;8(67):1–16.
751 62. Rautenbach GH, Boomker J, De Villiers IL. A descriptive study of the canine population
752 in a rural town in southern africa. J S Afr Vet Assoc. 1991;62(4):158–62.
753 63. Beckman M, Hill KE, Farnworth MJ, Bolwell CF, Bridges J, Acke E. Tourists’
754 perceptions of the free-roaming dog population in Samoa. Animals. 2014;4(4):599–611.
755 64. Ortega-Pacheco A, Rodriguez-Buenfil JC, Bolio-Gonzalez ME, Sauri-Arceo CH,
756 Jiménez-Coello M, Forsberg CL. A survey of dog populations in Urban and rural areas
757 of Yucatan, Mexico. Anthrozoos. 2007;20(3):261–74.
758 65. Boey J. Working with communities to improve the quality of life of British Columbia’s
759 free-roaming dogs and their people. Masters Thesis. University of Victoria; 2017.
760 66. Pedersen ER, Kurz J. Using Facebook for health-related research study recruitment
761 and program delivery. Curr Opin Psychol. 2016;9:38–43.
762 67. Kosinski M, Matz SC, Gosling SD, Popov V, Stillwell D. Facebook as a research tool
763 for the social sciences: Opportunities, challenges, ethical considerations, and practical
764 guidelines. Am Psychol. 2015;70(6):543–56.
.CC-BY 4.0 International licensemade available under a
(which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is
The copyright holder for this preprintthis version posted May 17, 2021. ; https://doi.org/10.1101/2021.05.17.444435doi: bioRxiv preprint
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765
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The copyright holder for this preprintthis version posted May 17, 2021. ; https://doi.org/10.1101/2021.05.17.444435doi: bioRxiv preprint
36
767 Supporting information
768
769 S1 File. Facebook adverts.
770 S2 File. English copy of questionnaire.
771 S3 File. Answer option to question “Are your dog(s) registered and identified” in
772 Bulgarian questionnaire
773 S1 Table. Number of "No responses" to outcome and predictor variables in statistical
774 analysis.
775 S2 Table. Demographic information about respondents in Bulgaria, Italy and Ukraine.
776 S3 Table. Number of respondents in Bulgaria, split by oblasts in Bulgaria.
777 S4 Table. Number of respondents in Italy, split by regions in Italy.
778 S5 Table. Number of respondents in Ukraine, split by oblasts in Ukraine.
779 S6 Table. Respondents answers to questions about ownership practices in Bulgaria,
780 Italy and Ukraine.
781 S7 Table. Respondents answers to questions about attitudes to free-roaming dogs in
782 Bulgaria, Italy and Ukraine.
783 S8 Table. The posterior mean values, error estimates, the 2.5 and 97.5 percentiles of
784 the posterior distribution (CI), Rhat values and bulk and tail effective sample sizes (ESS)
785 for Model 1.
786 S9 Table. The posterior mean values, error estimates, the 2.5 and 97.5 percentiles of
787 the posterior distribution (CI), Rhat values and bulk and tail effective sample sizes (ESS)
788 for Model 2.
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37
789 S10 Table. The posterior mean values, error estimates, the 2.5 and 97.5 percentiles of
790 the posterior distribution (CI), Rhat values and bulk and tail effective sample sizes (ESS)
791 for Model 3.
792 S11 Table. The posterior mean values, error estimates, the 2.5 and 97.5 percentiles of
793 the posterior distribution (CI), Rhat values and bulk and tail effective sample sizes (ESS)
794 for Model 4.
795 S12 Table. The posterior mean values, error estimates, the 2.5 and 97.5 percentiles of
796 the posterior distribution (CI), Rhat values and bulk and tail effective sample sizes (ESS)
797 for Model 5.
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