Evaluation of Dynamics, Demography and Estimation of Free-Roaming Dog Population in Herat City, Afghanistan

Simple Summary Understanding the demography, population size, and dynamics of free-roaming dogs (FRD) is essential for developing an effective dog-population-management and rabies-control programme. The existence of an uncontrolled FRD population in Herat, Afghanistan, is causing threats to public health and has raised concerns for their welfare. The aim of this study was to evaluate the demographic structures and estimate the FRD population size in Herat city, Afghanistan. The photographic sight–resight method utilized and human-to-FRD ratio in this study yielded a density of 10 dogs/km2 and an estimated ratio of 315:1. Dogs were predominantly adult males with a good health status and ideal body-condition score. The knowledge of FRD demography and population size provided by this study could be used by the local government for much more effective planning, implementation and monitoring of dog-population-control programmes. Abstract FRDs pose a serious challenge in countries where dog-bite-related rabies is endemic. Understanding the size and core demographic characteristics of FRD populations is essential for the planning and implementation of effective dog-population and canine-rabies-control programmes. The photographic sight–resight method was used to estimate the FRD population and evaluate its demographic characteristics in Herat city. A total of 928 free-roaming dogs (FRD) were identified through 3172 sightings, and the total free-roaming population was estimated to amount to 1821 (95% CI: 1565–2077), which led to the estimation of 10 dogs/km2 and the human-to-FRD ratio of 315:1. The male-to-female ratio was 2.85:1. The majority of them were healthy, with an ideal body score. Although the FRD density is considered low, it is still a concern and significant, since the majority of the people are unaware of the importance of canine populations in the transmission of zoonotic diseases such as rabies, and there were no specific measures for managing and controlling FRD populations. The information gained can be useful in animal health planning to design effective dog-population-control programmes, and for the planning of national rabies-prevention programmes.


Introduction
The familiar, widely distributed and phenotypically diversified domestic dog (Canis lupus familiaris) is one of our closest animal companions [1][2][3][4]. It is the most popular owned pet species in the world [5,6]. Dogs are considered part of the family, particularly in developed countries [7]. Although pet dogs are usually restricted in their behaviour, a significant proportion of global dog population are free-roaming on the streets (and are commonly known as free-roaming dogs/FRDs) [8]. Some reports have estimated that 75% of the 700 million world dogs population are stray FRDs [9][10][11][12]. Other reports estimated that there were 800 million dogs in the world and that 300 million were FRDs [13], explaining why they are a common sight in many countries [14]. The management of FRDs

Study Design and Sampling
The study was designed as a cross-sectional study and was conducted between September 2020 and April 2021 in all 15 districts of Herat city using photographic sight-resight methods to estimate and evaluate the FRD population. In this study, FRDs were defined as dogs that were not under the direct control of any person or were possibly owned but roaming during the survey period. The FRD survey was enhanced by dividing Herat city into 31 blocks, and each block (demarcated by large roads) covered an area of ~5 km 2 . Each block was visited twice daily, in the early morning and evening. During the field survey, representatives from each predetermined area were informed the day before a survey of the area was conducted.

Study Design and Sampling
The study was designed as a cross-sectional study and was conducted between September 2020 and April 2021 in all 15 districts of Herat city using photographic sight-resight methods to estimate and evaluate the FRD population. In this study, FRDs were defined as dogs that were not under the direct control of any person or were possibly owned but roaming during the survey period. The FRD survey was enhanced by dividing Herat city into 31 blocks, and each block (demarcated by large roads) covered an area of~5 km 2 . Each block was visited twice daily, in the early morning and evening. During the field survey, representatives from each predetermined area were informed the day before a survey of the area was conducted.

Survey Methods
The survey was conducted using the photographic sight-resight (PSR) method. A preliminary PSR survey revealed that the most active times for FRDs were the early morning (4:30-6:30 a.m.) and evening (6:30-8:30 p.m.). Streets and alleys were traversed by a car at a maximum speed of 20 km/h. Once a dog or group of dogs were observed, photographs were taken by using a Nikon COOLPIX P510 digital camera (Nikon company, Tokyo, Japan) at appropriate angles from a convenient distance. All observable characteristics of each dog were recorded including its sex (male; female; not verified), age (puppy (<6 months); young (6 months to 1 year); adult (>1 year)), reproductive status (pregnant; Animals 2023, 13, 1126 4 of 17 lactating; female in oestrus; not verified), body-condition scoring, observable health status (lameness; emaciation; skin lesions or dermatitis (abnormal changes in any area of the skin); mad dog signs), details of coat colour (composition; primary or secondary colour), coat condition (wounded; healthy; clean; dirty) and coat hair condition (long; medium; short), along with its GPS location (using a Garmin 60CS device). In addition, the activity of the FRD at the time of the survey (active; inactive; feeding or foraging), its social behaviour (alone; in a group), its reaction during the surveyor (friendly approaches; low-posture approaches; growls or barks; attacks the surveyor; ignores the surveyors; runs away), its location (road; sidewalk; playground; field; parking lot; underneath a car; bushes; dump sites; slaughterhouse; biological-waste-disposal sites; other places) and its proximity (presence ≤ 20 m) to garbage-disposal sites, such as garbage dumps/points or temporary accumulated litter along the streets and alley, were recorded.

Data Collection
All of the above parameters were provided in a predefined format to facilitate the data-collection process during the survey. Then, the photographs were reviewed to identify each dog by using distinguishable natural marks (on their flanks, ears, head and tail), body condition, details of coat colour, coat hair condition, age, sex, reproductive status and ears/tail amputation. The first time an individual dog was observed, this was defined as the initial sighting (capture) event. The subsequent encounters with the same dog were considered resighting (i.e., recapture). The identification of dogs relied on direct observation and photographs and, thus, none of the dogs were physically captured in this study. Following completion of the identification, each dog was given a unique identification code. The GPS location of each dog was loaded into GIS software (ArcMap version 10.4) and displayed on the map. Data through field survey using the PSR method were collected, then processed and analysed ( Figure 2). Flowchart of the data collection through field survey using PSR method. 391 photos were excluded due to poor quality and duplication.

Data Management and Analysis
Collected data were computed using Microsoft Excel (version: 16.0.4266.1001). Descriptive statistics were produced and 95% confidence intervals were calculated by using GraphPad Prism version 8.0.2 for Windows (GraphPad software, Lajolla, CA, USA). The chi-square test was utilized to examine variation in different categories (sex, age group, Figure 2. Flowchart of the data collection through field survey using PSR method. 391 photos were excluded due to poor quality and duplication.

Data Management and Analysis
Collected data were computed using Microsoft Excel (version: 16.0.4266.1001). Descriptive statistics were produced and 95% confidence intervals were calculated by using GraphPad Prism version 8.0.2 for Windows (GraphPad software, Lajolla, CA, USA). The chi-square test was utilized to examine variation in different categories (sex, age group, bodycondition score, reproductive status) between groups using GraphPad Prism. GPS points of FRDs were loaded into ArcGIS 10.4 to be displayed on the map. The estimation of the FRD populations was made using the Lincoln-Petersen formula with Chapman's correction.
The variance of N was estimated using Seber's formula [48]: An approximate 95% confidence interval for N was estimated as: where N is the total population size, n1 is the number of dogs sighted/photographed on the first occasion, n2 is the number of dogs sighted/photographed on the second occasion, and m2 is the number of dogs resighted.

Number of FRDs
A total of 928 unique FRDs (predominantly male) were identified through 3172 reliable sightings in fifteen districts of Herat city during the survey period ( Figure 3).  Photos were available for 99.1% of these dogs (due to restrictions on photography on the roads around security areas, political representations of foreign countries and poor quality of photographs). The total FRD population was estimated to be 1821 (95% CI: 1565-2077), leading to an estimate of 10 dogs/km2, with a human-to-dog ratio of 315:1 (3.17 dogs per 1000 people). Most dogs were identified during the morning shift (probably due to ample amount of uncollected garbage, and less human interference). The number of dogs identified in each district ranged from 27 to 123, bearing a linear relationship of R² = 0.0627, y = 1.8643x + 46.952. Most dogs were recorded in districts 5, 9 and 15, while the lowest FRD population density was recorded in districts 2, 10, 1 and 7. Photos were available for 99.1% of these dogs (due to restrictions on photography on the roads around security areas, political representations of foreign countries and poor quality of photographs). The total FRD population was estimated to be 1821 (95% CI: 1565-2077), leading to an estimate of 10 dogs/km 2 , with a human-to-dog ratio of 315:1 (3.17 dogs per 1000 people). Most dogs were identified during the morning shift (probably due to ample amount of uncollected garbage, and less human interference). The number of dogs identified in each district ranged from 27 to 123, bearing a linear relationship of R 2 = 0.0627, y = 1.8643x + 46.952. Most dogs were recorded in districts 5, 9 and 15, while the lowest FRD population density was recorded in districts 2, 10, 1 and 7.
Out of 928 FRDs, 441 (48%; 95% CI = 51.5-45%) were seen ≤20 m from the garbage sites (including places which accumulations of garbage are left temporarily, in small amounts such as the roadsides and sidewalks and official dump sites) (Table 4 and Figure 7). Although no significant variation was observed in the activities of FRDs during the survey time (χ2 = 38.70, df = 28, p < 0.08), a significant difference was found in the number of dogs sighted within 20 m of garbage dumps/accumulated litter (χ2 = 127.9, df = 14, p < 0.0001) across the districts.   Figure  7). Although no significant variation was observed in the activities of FRDs during the survey time (X 2 = 38.70, df = 28, p < 0.08), a significant difference was found in the number of dogs sighted within 20 m of garbage dumps/accumulated litter (X 2 = 127.9, df = 14, p < 0.0001) across the districts.  Out of the 629 (68%) dogs that were seen in packs, 60.2% were male dogs, 21.5% were female dogs and 18.3% were dogs with unverified gender. Out of the total male dogs, female dogs and dogs with unverified gender, 67% (379/562), 68.5% (135/197) and 68% (115/169) were seen in packs during the survey period, respectively. The most common composition of social structure was observed as MM/0, MM/UF, MM/MF and UM/UF (Figure 8). The social behaviour was varied in each district (Figure 9).
Out of the 629 (68%) dogs that were seen in packs, 60.2% were male dogs, 21.5% were female dogs and 18.3% were dogs with unverified gender. Out of the total male dogs, female dogs and dogs with unverified gender, 67% (379/562), 68.5% (135/197) and 68% (115/169) were seen in packs during the survey period, respectively. The most common composition of social structure was observed as MM/0, MM/UF, MM/MF and UM/UF (Figure 8). The social behaviour was varied in each district (Figure 9).

Single
In groups  Out of the 629 (68%) dogs that were seen in packs, 60.2% were male dogs, 21.5% were female dogs and 18.3% were dogs with unverified gender. Out of the total male dogs, female dogs and dogs with unverified gender, 67% (379/562), 68.5% (135/197) and 68% (115/169) were seen in packs during the survey period, respectively. The most common composition of social structure was observed as MM/0, MM/UF, MM/MF and UM/UF (Figure 8). The social behaviour was varied in each district (Figure 9). In groups
As in many previous studies around the world [7,21,40,46,50,[55][56][57], the photographic sight-resight method was utilized in this study to evaluate demographic characteristics and estimate the FRD population size in Herat city. This method has several advantages, such as reducing the cost of the survey, reducing the risk of researchers' exposure to dog bites or rabies and reducing the scaring of targeted FRDs in the study population, which would result in them fleeing away (because individual dogs are not physically captured in this method and only photographed from a distance without disturbing their natural behaviour). In addition, the use of digital photography is useful during field surveys to reduce misidentification of the individual dogs, which can lead to inaccurate evaluation and estimation. Like many previous studies conducted elsewhere [47,48,58,59], the Lincoln-Petersen formula with Chapman's correction was applied to estimate the FRD population. This method has an advantage over other methods as it requires only two sighting sessions [60].
The FRD per km 2 was estimated at 10 dogs/km 2 , in this study which is lower compared to findings from some other parts of the world, such as 1081 dogs/km 2 in San Francisco de Campeche, a city in Mexico [50], 242 dogs/km 2 in Tiswadi taluka, in the state of Goa in southwest India [61], 52 dogs/km 2 in Dhaka city, Bangladesh [48], 57 dogs/km 2 in Aarey Milk Colony, a suburb of Mumbai, India [46], 119 dogs/km 2 in the Coquimbo region of Chile [1], 334 dogs/km 2 in Iringa, Tanzania [62], and 225 dogs/km 2 in Shimotsui, Kurashiki city, Japan [63], but rather high compared to the 1.3 dogs/km 2 reported by Rinzin [59] in Bhutan. However, our finding was nearly consistent and comparable with the 14 dogs/km 2 and 12.25 dogs/km 2 reported by Hossain et al. [40] in Raipura Upazila, Bangladesh and Bouaddi et al. [38] in EL Jadida, Morocco, respectively. Nevertheless, the dog density was reported to completely vary, from as low as 1 dog/km 2 [1] and 1.3 dogs/km 2 [59] to as high as 1380 dogs/km 2 [1] and 2930 dogs/km 2 [54]. Therefore, this result generally reflects the lower abundance of free-roaming dogs than that reported elsewhere, probably due to the low percentage of owned dogs and high number of confined owned dogs, or possibly due to the recent fencing of public places, such as parks, which has restricted the shelter of stray dogs and interference of humans in garbage sites, which has restricted accessibility of free-roaming dogs to foods, consequently causing them to move to semi-urban and rural areas.
The highest number of FRDs was recorded in districts 5, 9 and 15 of Herat city. The possible factors associated with the highest abundance of FRDs in district 5 were the high density of the human population, unrestricted properties for the roaming of dogs (parks, parking lots), many commercial storerooms, large food and construction markets and the existence of many restaurants and dump sites that directly or indirectly provided food and shelter for FRD populations. Additionally to the factors mentioned above, a part of district 9 is the transportation point and vehicle station of several villages, and when travellers leave the area, they usually leave behind edible garbage along the roads and sidewalks, which attracts more FRDs in the area during times of lower human interference (early morning/evening/night). The density of the FRD population in district 15 was probably due to the high density of people, the size of the area, the presence of more owned dogs, the relative poverty of the residents, the lack of municipal services such as regular garbage collection and the bringing and releasing of unwanted dogs to this area from other regions by their owners (according to several residents).
The sex ratio of FRDs in this study skewed towards males (61%), which is consistent with the findings from other parts of the world [7,21,40,41,44,48,50,51], but is in contrast to (55.3% females) reports in Bali and Indonesia by Hiby et al. [33]. However, many studies have reported male dogs outnumbering females in FRD populations, and this disparity could be attributed to the preference of communities for male dogs or a high female dog mortality rate [21]. Based on our visual observation, 7.61% of dogs were identified as pregnant in this study, which is close to the percentage reported by Rinzin et al. [59] of 6.2%.
The age distribution was highly skewed toward adults, which is similar to the findings reported by others [7,21,40,50,59]. Possibly, the low density of puppies and young FRDs is due to the death of FRD puppies by accidents and deliberate poisoning or the absence of any communal or group care of pups by other females, which would agree with the report by Tiwari et al. [21]. Furthermore, it may be due to their susceptibility to diseases, such as distemper and canine parvovirus, which has resulted in high mortality and a consequently lower percentage of young dogs.
A high proportion of dogs (60.13%) were found to have a good body-condition score (BCS3), which indicates higher survivability and better capabilities to reproduce. Our finding is quite similar to what was recorded by other researchers, but is slightly lower than the finding by Cortez-Aguirre et al. [50]. However, most of the identified FRDs in Herat city had an ideal body-condition score, which is probably related to the availability of food (edible garbage), feeding of FRDs by the community or the lower density of dogs, which causes less competition, or, perhaps, a proportion of these dogs were actually free-roaming owned dogs, freely allowed to roam the neighbourhood.
Generally, the health status of FRDs was good, considering their stray status. The percentage of FRDs with skin lesions or dermatitis which was recorded (mostly in the males) in this study was low compared to the findings reported by Tenzin et al. [48], Cortez-Aguirre et al. [50] and Hiby et al. [33] in Dhaka city in Bangladesh, Campeche city in Mexico and Sanur in Bali, respectively Moreover, the fact that skin lesions were recorded mostly in male dogs is consistent with the finding by Cortez-Aguirre et al. [50], but different from the finding by Tenzin et al. [48]. Emaciation was recorded only in 2.6% of the dogs in this study, which is inconsistent with the findings of 23.2% by Hiby et al. [33], 12% by Tiwari et al. [21] and 8.9-10.6% by Hiby and Hiby [14]. In this study, most dogs had no visible injuries, and only 10.02% of the FRD exhibited visible injuries or wounds, in which our finding concurs with the finding reported by Hiby et al. [33].
A high proportion of FRDs were seen on the roads and sidewalks, which is possibly correlated with the abundance of edible litter since garbage is not collected regularly, and this finding concurs with those reported by Kato [54], Tenzin et al. [48] and Cortez-Aguirre et al. [50]. It is believed that the distribution of roaming dogs is associated with the management of garbage-collection points [48]. In this study, around 48% of the FRDs were found around a 20 m radius of garbage sites, which is quite similar to the finding of Tiwari et al. [21]. Similarly, a high percentage of dogs (68%) were active, which is comparable to that observed and reported by Tiwari et al. [21], with 43%.
In this study, around 68% of dogs were observed in groups, which was comparable with the 59.2% reported in Antananarivo, Madagascar [36]. The most common composition of social structure was male groups and male-female groups. This is probably due to the outnumbering of males compared to females, where the male groups incorporate females depending on their availability. However, there are significant dangers in forming groups, as groups of roaming dogs are not normally tolerated by the public.

Conclusions
In conclusion, having knowledge of the FRD population is crucial for the effective control of dog populations and the implementation of rabies-control programmes. This study provided the size of the population, demographic data, health status and dynamics of FRDs in Herat city, Afghanistan, by using the photographic sight-resight method. The human-to-FRD ratio was estimated at 315:1, with a density of 10 dogs/km 2 . A higher proportion of dogs were male and they were predominately adults. Generally, the health status of FRDs was good, with the majority of the FRD population found to have an ideal body-condition score. Skin lesions/dermatitis, lameness and emaciation were recorded only in 18% of FRDs. Most dogs were seen on the roads and sidewalks and a high proportion were active, and almost half of them were seen near garbage sites. Nearly half of them did not tolerate human presence and fled whenever approached. The abundance of FRDs and lack of prophylactic programmes targeting FRDs have generated public health problems in Herat city. The baseline information gained by this study could be used by the local government for the planning, implementation and monitoring of effective dog-populationcontrol interventions, as well as for animal health planning, such as in canine-rabies control. Therefore, we feel there is a value in further studies at different times of the year. Additionally, similar studies are recommended in rural areas of the Herat province to obtain comprehensive FRD ecological data for the effective control of the dog population and rabies.