Dog and cat-related attacks on wildlife in the Metropolitan District of Quito, Ecuador: an integrative approach to reduce the impact

ABSTRACT Surveillance and control of dogs and cats (D&C) have become increasingly important for the conservation of biodiversity in protected areas. However, despite the increase in densities of free-roaming D&C in urban areas, especially in developing countries, the impact on wildlife is poorly documented. The Metropolitan District of Quito (MDQ) in Ecuador, contains a high biodiversity of native fauna, but free-roaming dog populations have tripled in recent years, with no published information about possible consequences on wildlife. We conducted a retrospective analysis of patients admitted to a Veterinary Hospital in Quito between July 2017 and June 2022 to determine the incidence of D&C attacks on wildlife from the MDQ. A total of 429 wild specimens (79.5% birds, 17.2% mammals and 3.3% reptiles), including 59 species (4 vulnerable, 1 endangered and 1 critically endangered), were treated for injuries inflicted by D&C. Attacks increased every year on record, and 79% of specimens did not survive. Given that current governmental regulations for the control of domestic animals have not been effective, we propose to address the global issue from a multidisciplinary perspective, considering predation by D&C, biodiversity conservation, animal welfare, human health, and public policies as intertwined phenomena. The goal of this approach is to achieve greater awareness and increase the effectiveness of management programs, while improving the health of animals, humans, and the environment in which they live. Additionally, we recommend government support to replicate this research in other wildlife rehabilitation and rescue centers to understand the scope of the issue nationally.


Introduction
The introduction of invasive species is one of the most significant threats inflicted by humans on biodiversity worldwide (Mollot et al. 2017).Mammalian predators are among the most damaging invaders, having caused considerable decline and extinction of native species.Specifically, domestic dogs have contributed to the extinction of at least 11 vertebrates and are a known risk to 188 threatened species (Doherty et al. 2017).Likewise, domestic cats have been implicated in the extinction of at least 63 species and threaten another 367 species (Doherty et al. 2016).Furthermore, the decline and extinction of native species can have cascading effects on entire ecosystems (Doherty et al. 2015).Dogs and cats (D&C) range from completely dependent on humans to feral, but all can have direct and indirect impacts on natural communities through predation, disturbance, pathogen transmission, competition, and hybridization (Hughes and Macdonald 2013;Loss and Marra 2017).How domestic predators interact with wildlife depends largely on their population density, and the extent to which humans restrain and care for them.In fact, D&C can be considered subsidized predators whose densities are above what would normally be expected if human resources were not available, accelerating the effects of predation (Gompper 2013;Maeda et al. 2019).Nevertheless, both the control of free-roaming movements (Sepúlveda et al. 2015;Cecchetti et al. 2022) and adequate feeding (Silva-Rodríguez and Sieving 2011) reduce wandering and hunting behaviors.In this sense, differences in human perceptions and attitudes may play a significant role in how domestic carnivores interact with wild animals.For example, several studies show that in places where dogs are not perceived as a threat, they were left to roam freely and regularly preyed on wildlife (Schüttler et al. 2018).Conversely, in natural areas where dogs were not allowed, there was no alteration in wildlife activity patterns compared to areas that allowed them (Lenth et al. 2008).Regarding cats, owners are less aware of CONTACT Eduardo A. Díaz eadiaz@usfq.edu.ecSupplemental data for this article can be accessed online at https://doi.org/10.1080/26395916.2023.2191735.the threat that free-roaming cats pose to wildlife and perceive confinement as restrictions on cats´ natural behaviors (Crowley et al. 2020;Cecchetti et al. 2022).However, the engagement of owners and caretakers to free-roaming cat management programs has the potential to improve approval and participation rates, thereby improving the outcomes of future management programs (McDonald et al. 2018;McLeod et al. 2019).
Although hundreds of studies have shown that domestic predators constitute an increasingly important conservation threat worldwide, there is a paucity of data in urban areas, particularly regarding wildlife predation, and published studies are limited mainly to developed countries (Weston et al. 2014;Kikillus et al. 2016;Pavisse et al. 2019).This is a significant information gap in the global impact of domestic predators, as human populations are expected to continue to expand in the coming decades with a correlated increase in domestic animals (Schenk and Souza 2014;Doherty et al. 2017).Indeed, D&C can reach higher densities in human populated areas (Tiwari et al. 2019;McDonald and Skillings 2021).Interestingly, although urbanization generally results in reduced biodiversity, certain taxa can reach high densities in these habitats, increasing the importance of urban spaces for global conservation (Goddard et al. 2010).Therefore, as urbanization continues to expand, urban-wildlife research is fundamental for urban planners and conservation professionals to create livable cities for both humans and wildlife.Studies in South America, one of the continents with the highest urbanization rates in recent years, are scarce (Collins et al. 2021).In Ecuador, the interaction between D&C and wildlife has been studied in the Galapagos Islands (Phillips et al. 2012;Padilla et al. 2018), and in continental protected areas of the high Andes (Zapata-Ríos and Branch 2016;Zapata-Ríos et al. 2018).Additionally, two clinical cases of threatened wild species attacked by dogs have recently been published (Díaz et al. 2020(Díaz et al. , 2021)), but scientific research in urban areas is lacking.
The human population of the Metropolitan District of Quito (MDQ) has increased by sevenfold since 1950, reaching 2,239,191 inhabitants in 2010 (last official census), and accounting for 15.5% of the Ecuadorian population (INEC 2022a).Likewise, the abundance of free-roaming dogs tripled between 2013 and 2019, reaching 8.33 dog/km in urban areas of the MDQ (Cárdenas et al. 2021).Promoting ecological sustainability within the MDQ requires citizen awareness of the importance of conserving biodiversity (Morales-Espín et al. 2021).National and regional legislation suggests regulations for the control of domestic animals and the protection of wildlife, but one of the greatest complexities that its application has presented has been the lack of awareness about the established measures (CDMQ 2021).The management of domestic animals is controversial because they are intimately linked to humans, and to be successful, requires the involvement of local communities and animal welfare organizations (Hughes and Macdonald 2013).However, relying solely on public opinion, without considering scientific evidence, could lead to management outcomes that continue to endanger biodiversity (Loss and Marra 2017).Therefore, it is necessary to implement technical and legal measures to increase control of freeroaming D&C populations and promote their confinement, as well as stimulate social change through education campaigns that draw attention to the consequences on wildlife conservation (Schüttler et al. 2018).Documenting the impact on patients admitted to wildlife rehabilitation and rescue centers (WRRC) is the first step in education aimed at changing human behavior and conservation-related public policy (Mcruer et al. 2017).However, the global impacts can be better understood and managed examining other possible negative effects of increased lack of control of D&C, such as animal welfare and public health (Doherty et al. 2017).
In order to obtain information about D&C attacks on wildlife in the MDQ, we retrospectively analyzed a database of medical records from the Wildlife Veterinary Hospital of the Universidad San Francisco de Quito (USFQ-WVH).This is the first study on the subject in Ecuador, and the knowledge obtained may be helpful to better understand the interaction between D&C and wildlife in the MDQ.We also describe other potential threats from a multidisciplinary perspective, hoping to increase public awareness of free-roaming D&C issues and provide local authorities with objective data on threats to urban wildlife, animal welfare and public health.

Study area
The MDQ is the administrative area that encompasses the city of Quito, the capital of Ecuador.It is divided into 32 urban parishes and 33 rural parishes.A parish is the smallest administrative and political unit with powers to apply public policy (Cabrera-Barona et al. 2019).The latest Ecuadorian census reported a population of 2.2 million inhabitants in 2010, of which 72% (1.6 million people) live in the urban area, and 28% (0.6 million people) in the rural area (INEC 2022a).For 2020, the projected MDQ population was 2.8 million (INEC 2022b).The District has a total area of 423,074 ha in the northern Andes of South America, between the eastern and western branches of the Andes.The area contains high biodiversity levels, as a result of landscape and climate heterogeneity, including 111 mammal, 542 bird, 53 reptile, 92 amphibian, and 21 fish species, some endemic, in as many as seven different identified ecosystems (MECN 2010).In 2013, the estimated abundance of free-roaming dogs in the MDQ was 2.89 dogs/km in urban parishes and 2.25 dogs/km in rural parishes.In 2019, the estimated abundance increased to 8.33 dogs/km and 6.51 dogs/km respectively (Cárdenas et al. 2021).To the authors' knowledge, there are no records on the abundance of freeroaming cats in the MDQ.

Data collection and analyses
This study was carried out using data obtained from the medical records of the USFQ-WVH.The information of each wild animal admitted from July 2017 to June 2022 was sorted and classified in a database, including: (i) date of admission, (ii) origin of the patient, (iii) cause of admission, (iv) sex and age group, (v) common and scientific names, (vi) national and international conservation status, (vii) global population trend, and (viii) outcomes in three categories: released, dead (died in care OR euthanized due to injuries) and transferred (to other WRRC).Individuals not identified to the species level and non-native species were removed from the database.Patients that did not come from the MDQ, and those that were not related to D&C attacks, were also excluded from this study.We identified dog or cat attacks based on the wound patterns.Dogs typically have wider and blunter teeth and powerful jaws that can cause significant damage from lacerations and crush injuries that often remain open.In contrast, cats have thinner, sharper teeth, and weaker bite force which generally results in less destructive small puncture wounds that tend to close almost immediately (Smith et al. 2000).We used percentages to summarize the data and evaluated the significance of temporal variation calculating a trend line using linear regression (Ott and Longnecker 2010).

Discussion
Our results provide important baseline information about the number, taxa, threat category, and mortality of wild animals attacked by D&C in the MDQ.These data describe a direct impact on native wildlife that had not previously been quantified in Ecuador.According to the clinical record database, D&C-related attacks are a leading cause of morbidity (11.5% of all admissions) and mortality (79% attacked patients did not survive) for wildlife species admitted to the USFQ-WVH.We recorded six species listed under some degree of threat at the national level (Black-breasted Puffleg, Elegant Snail-eaters, Golden-bellied Snake, Kichwa Porcupine, Little Red Brocket, and Tayra), six species that have not been evaluated in Ecuador (Andean Tapeti, Common Pigeon, Little Black Serotine, Mallard, Ovenbird, and White-lipped Mud Turtle), and eight species without data on global population trends (Andean Tapeti, Brown Wood Turtle, Cope's Tropical Racer, Golden-bellied Snake, Little Black Serotine, Montane Myotis, Sparkling Violet-ear, Striped Hog-nosed Skunk).It is also likely that a large number of animals attacked by D&C were consumed by the predator or scavengers, found dead and not reported, or the attack went unnoticed (Loyd et al. 2017;Mcruer et al. 2017).As such, our results represent gross underestimations, both in terms of threat and the total number of individuals and species affected.These results are consistent with those obtained by other authors who also reported D&C  All of these data highlight the need to control the amount of free-roaming D&C to reduce their interactions with, and negative impact on, wildlife.Control of D&C populations poses particular challenges, as they are closely tied to people, but also pose a significant hazard to conservation when they interact with wildlife, requiring an interdisciplinary approach to assess successful results (Hughes and Macdonald 2013;Loss and Marra 2017;Belsare and Vanak 2020;Gunther et al. 2022).Engagement of local people and community support are often key to the success of management programs, and greater acceptance is achieved by integrating animal welfare and human health objectives, rather than focusing solely on conservation goals (Kikillus et al. 2016;Doherty et al. 2017).Indeed, even though since 2017, the Ecuadorian Organic Code of the Environment establishes the obligation of Metropolitan Governments to conserve and restore biodiversity by controlling the overpopulation of domestic animals (COA 2017), the abundance of free-roaming dogs tripled in the MDQ between 2013 and 2019 (Cárdenas et al. 2021).In addition, although there are no published data on freeroaming cats in the area, our analysis shows an increase in the number of individuals attacked by both dogs and cats.Increases in cat predation on wildlife has been previously associated with parallel increases in cat densities (Pavisse et al. 2019), so we could assume that the abundance of cats is also increasing in the MDQ.These findings have management implications for the responsible municipalities, and the authorities should take additional measures to prevent interactions between domestic animals and wildlife, since one of the greatest complexities that the application of prevention and control programs has presented has been the lack of people's awareness (CDMQ 2021).If programs to reduce D&C-wildlife interaction are to be successful, it will be necessary to be creative and to engage all stakeholders (Plaza et al. 2019).We propose to extend the scope of the problem, considering D&C predation, biodiversity conservation, animal welfare, human health, and public policies as entangled phenomena, since the uncontrolled D&C populations impact wildlife conservation, compromise animal welfare, contribute to the spread of diseases, and are largely due to a lack of effective education and control policies.The purpose of this approach is to create a greater scientific, social, and political commitment to effectively address the problems of uncontrolled and free-ranging D&C populations in the MDQ.
Documenting the impact of domestic predators on wildlife admitted to WRRC is the first step in changing human behavior that will eventually contribute to solving the problem (Mcruer et al. 2017).It is important to engage owners in the management of their pets to prevent free roaming and to reduce the number of wild animals attacked by D&C that present in WRRC (Schenk and Souza 2014;Linklater et al. 2019).In fact, most attacks occur when D&Cs are not with people (Home et al. 2018), when free-roaming D&C are more exposed to health and welfare hazards.As such, approaches to reduce their roaming would not only benefit wildlife by reducing interactions but also benefit pets that return home to humans (Cecchetti et al. 2022).Additionally, pet owners are often animal welfare advocates, thus raising awareness of wildlife welfare can also contribute to behavioral changes (Loyd et al. 2017).Therefore, it is essential to take a humane approach, since both domestic and wild animals are sentient beings with the capacity to suffer, to empathize with the community and achieve maximum cooperation, rather than simply providing information in the hope that people act accordingly (Holderness-Roddam and McQuillan 2014).
Human health is also a major concern worldwide due to the close contact of people with D&C, and their capacity to harbor both zoonotic and epizootic pathogens (Gerhold and Jessup 2013;Macpherson et al. 2013).In Ecuador, D&C have been identified as reservoirs of viruses, bacteria, and parasites of importance for public health (Calvopiña et al. 2015;Ortiz-Prado et al. 2016;DiGangi et al. 2019;Orlando et al. 2020;Rivadeneira-Barreiro et al. 2021).Specifically, in the 1990s Ecuador suffered one of the highest rates of rabies per capita in the Americas due to the lack of effective control policies.In response, the Ministry of Health carried out massive canine vaccination campaigns, and the incidence of urban rabies clearly decreased; in 2004 and 2009 the last cases of canine and human urban rabies were reported in the country, respectively (Ortiz-Prado et al. 2016).Nevertheless, vaccinated D&C can still transmit pathogens for which they have not been immunized and suffer from other diseases that compromise their health and welfare.The World Organization for Animal Health recognize that access to veterinary services is critical to improve the health and welfare of animals while addressing the risks of zoonotic diseases (OIE 2021).Comprehensive veterinary programs, including preventive veterinary care, spay/neuter, and education campaigns, have been shown to improve the health and welfare, while reducing the number of free-roaming D&C (Yoak et al. 2014;Schurer et al. 2015;Hiby et al. 2017;Baker et al. 2020).However, given the high cost in terms of human and financial resources, there is a need to establish subsidized services, especially in developing countries, which depend on well-functioning animal and public health system (Baker et al. 2018).
Ecuador is making slow progress on biodiversity conservation despite the existence of a solid policy framework, possibly due to financial challenges and knowledge gaps.Collaboration with national and international organizations will be necessary to improve these issues (Mestanza-Ramón et al. 2020).The present study has been carried out with this aim using data obtained from the clinical records of the USFQ-WVH.However, despite that the Organic Code of the Environment establishes the creation of WRRC at national level (COA 2017), there is not a centralized database that records the interactions between domestic animals and wildlife to assess threats on a larger spatial scale.Ecuadorian authorities are required, under regional (CDMQ 2021), national (CRE 2008), and international (CBD 1992) legal obligations, to implement policies aimed at preventing the negative impacts of invasive species, but scientific uncertainty about the real impact of domestic pets on wildlife and public perceptions fuels disagreement and makes it difficult to implement regulations (Trouwborst et al. 2020).In this sense, although it is undeniable that our results corroborate that D&C prey on native wildlife, the evidence that this is a threat to the viability of populations is controversial.As such, we suggest applying the precautionary principle.This principle calls for action to protect biodiversity when there is a scientifically plausible but unproven risk, providing a justification for immediate intervention while definitive studies are conducted.It is essential to include consultation with all stakeholders (conservationists, animal welfare advocates, veterinarians, physicians, and policy makers) to implement precautionary measures that have widely support and applicable to local circumstances.Some of the recommended measures include pet registration, restrictions on the maximum number of animals allowed per household, mandatory sterilization and vaccination, and confinement of free-roaming specimens (Grayson and Calver 2004;Lilith et al. 2006;Calver et al. 2011).
In conclusion, the role of WRRC is controversial because the resources and effort invested in saving individual animals may not translate into positive effects on the conservation of wildlife populations.However, WRRC may contribute to a wide variety of important activities not only for the reintegration of wild specimens, but also for assessing environmental health through wildlife monitoring, as well as raising awareness through public education (Sleeman and Clark 2003;Sleeman 2008).Therefore, WRRC are in a unique position to advance the knowledge and conservation of biodiversity, but the lack of infrastructure, technology, and financial resources are some of the greatest challenges Ecuador must face in the coming years if we hope to achieve a standardizing system of records that will optimize effectiveness of WRRC (Mestanza-Ramón et al. 2020;Orlando et al. 2020).An increase in governmental support would prevent the loss of valuable information and facilitate long-term trend studies based on a cohesive national database (Romero et al. 2019;Long et al. 2020).There are some limitations of the study that must be considered when interpreting the results.The fact that not all the attacked animals were found and taken to the USFQ-WVH implies a bias in the database.In addition, specimens whose wounds did not clearly correspond to attack patterns were excluded, which could also underestimate the true prevalence of interactions with D&C.Another limitation is that the study only includes wildlife from the MDQ, which geographically biases results.However, although the results are probably conservative and not appropriate to assess the real impact of D&C on native wildlife at the population level, our findings provide valuable background information, as it is the first analysis about this topic in Ecuador.In the future, this type of research should be extended to WRRC in other regions of the country, in order to obtain standardized information that will helps in the development of a comprehensive D&C management plan at the national level.

Figure 2 .
Figure 2. Outcome of patients admitted to USFQ-WVH (2017-2022) according to attacks by dog or cat, and the taxonomic group.