Abstract
Human-introduced predators, primarily the domestic dog (Canis lupus familiaris), and human-modified landscapes conjointly threaten wildlife across Costa Rica. For arboreal species, including the two-fingered sloth (Choloepus hoffmani), the impact of domestic dogs is amplified in areas of habitat fragmentation. In efforts to navigate discontinuous canopies associated with urban development and human encroachment, C. hoffmani is forced to utilize terrestrial locomotion. This unnatural behavior leaves sloths increasingly vulnerable to predation by domestic dogs, which occupy altered landscapes in high densities. In this report, we detail the ante and postmortem findings associated with C. hoffmani following an extensive attack by three large-breed dogs. The patient sustained severe and fatal polytraumatic injuries targeting the abdominothoracic region. Gross lesions were not readily evident, obscured by unique anatomical characteristics of the species. This report aims to highlight the threat imposed by dogs to sloths and the severity of injuries, with considerations for clinical management in light of C. hoffmani morphology. We review the scope of domestic dog–wildlife conflict in Costa Rica, and propose collaborative mitigation strategies including habitat preservation, domestic dog population control, installation of wildlife corridors, policy initiatives, and dog owner education and public outreach.
1 Introduction
1.1 Domestic dogs as invasive predators in the Anthropocene
Anthropogenic disturbances represent increasingly pervasive threats to native fauna [1,2,3,4,5,6]. One of the most prominent drivers of biodiversity loss and homogenization is the introduction and establishment of invasive species [7,8]. Many domestic animals of non-native taxa serve as human-subsidized predators and cause substantial wildlife mortality annually [9,10,11,12]. Domestic dogs (Canis lupus familiaris) in particular, including owned and feral, threaten a wide variety of species globally [13,14,15,16,17,18,19,20,21,22,23,24,25,26]. These canids have become a notable and ubiquitous conservation challenge, ranking just below cats and rats as the third most-damaging invasive predator [8].
Urbanization is one of the most impactful anthropogenic activities and closely amalgamated with domestic dog–wildlife conflict [27,28,29]. The occurrence and density of dogs around native habitats are heavily influenced by surrounding urban development [30,31]. Human-modified landscapes that transect or edge wildlife zones often present a high abundance of feral and owned dogs [32,33]. In rural or peri-urban (i.e., urban-rural interface) landscapes bordering forests, dogs often roam freely regardless of ownership status [34,35]. Their presence in protected areas and extensive spatiotemporal range has been well documented [32,36,37,38,39]. Domestic dog occupancy is more geographically extensive and influenced to a greater degree by anthropogenic features than other invasive predators, including cats [40]. Human activity thus plays a significant role in the distribution of dogs in wildlife areas and represents a means of intervention when addressing the problem [10,41,42].
1.2 The impact of domestic dogs on wildlife
Domestic dogs threaten native fauna through both direct and indirect routes [11,43]. Indirect threats include disease transmission [44,45,46,47,48,49], competition [18,50,51], and hybridization of [52,53,54] wildlife. Their presence alone may influence the vigilance [55], distribution and land use [56,57,58,59], reproduction [60], and feeding habits [55] of wild species. Although these indirect effects are non-negligible, predation continues to be the predominant threat imposed by dogs, and the prevalence of attacks on wildlife continues to rise [21,25,43,61,62,63]. Domestic dogs have aided 11 vertebrate extinctions and continue to threaten 188 other species, although the true impact is likely underestimated [11,64]. This predation is often recreational as it does not involve consumption of prey [65,66]. Cases of true predation by domestic dogs (i.e., wildlife is consumed) are typically driven by hunger and associated with underfeeding by owners. This scarcity of human-provided resources increases the probability of dog attacks on wildlife species [58].
Information regarding the density and distribution of domestic dogs is often lacking [67,68]. Globally, the population size is estimated to be over 700 million, ranking this species as the most abundant carnivore [11]. In Costa Rica, there were approximately 580,000 dogs in 2011, with an average of 20 dogs per 100 people [69]. A large portion of these dogs are allowed to roam freely, with only 3% living primarily indoors [69,70,71]. Despite the scale of the problem, and excluding the use of dogs for hunting by humans, there is limited literature documenting attacks on wildlife in Costa Rica [72,73,74]. Dog attacks on native Costa Rican species have been documented for Howler monkeys (Alouatta palliata) [75], birds [76], and sea turtles [77,78,79,80] in the country and the nine-banded armadillo [13], lowland tapir [13,81], and coati [21] in other geographic locations.
1.3 Domestic dog attacks on sloths
Domestic dogs present a considerable threat to sloths inhabiting Costa Rica, including the Hoffman’s two-fingered (Choloepus hoffmani) and brown-throated three-fingered (Bradypus variegatus) sloth [82,83]. Numerous wildlife hospitals informally describe dog attacks as a leading cause of sloth intakes [84,85,86,87,88]; yet, literature documenting the phenomenon is sparse. C. hoffmani was reported as a victim to dogs in a 2017 publication, although details on the attack are not provided [83]. Likewise, another study reported local farmers identifying dogs as a predator to the species. This was followed by descriptions of two sloth carcasses that had been preyed upon, although the source of the attack is uncertain [82].
In the case of C. hoffmanni, loss of forest connectivity [89] in conjunction with the presence of domestic dogs has grave consequences [82]. Intact forests are an essential habitat component for this arboreal species, providing a means of locomotion, refuge, and nourishment [90,91,92]. In Costa Rica, anthropogenically changed landscapes have grown to unprecedented levels [93,94]. The negative effects of this tropical deforestation and habitat fragmentation have been documented for multiple sloth species, including C. hoffmani, in terms of altered dispersal, behavior, and survival [82,89,95,96,97,98,99].
As primary folivores, C. hoffmani maintains a niche diet that renders them highly dependent on available and accessible trees [100,101]. To satisfy these dietary requirements, sloths are both capable and willing to travel long distances to locate appropriate foliage [82]. Like other arboreal folivores, this characteristic leaves C. hoffmanni disproportionately susceptible to habitat loss, as they are unable to switch resources when their environment is degraded [102]. In the face of habitat fragmentation, food becomes diminished through loss of tree diversity and less accessible through reduced canopy connectivity [103,104]. As a result, C. hoffmanni is forced to travel further distances, enter unfavorable and novel environments, and modify their means of locomotion by climbing on the ground to navigate between trees [82,98].
In pristine forest, C. hoffmani historically avoids leaving the canopy, only descending to the forest floor once a week for elimination activities (i.e., urination, defecation) [105,106,107]. Descent to the ground, even in undisturbed forest, presents major predation risks to sloths by species including ocelots, jaguars, pumas, tayras, and spectacled owls [107,108]. However, the presence of domestic dogs in fragmented habitats makes the ground an increasingly dangerous place for sloths to navigate. This is due to both the abundance of dogs relative to elusive wildlife predators, and increased travel distance associated with transected habitats for sloths [10,82]. Unfortunately for C. hoffmani, the terrestrial locomotion of this species has been described as laborious and clumsy, rendering them exceptionally vulnerable to predators on the ground [90]. The complex mosaic of human-modified landscapes and human-subsidized predators as they relate to arboreal species must be considered in parallel. As human activity excessively fragments forest, sloths are forced to adapt unnatural ambulation (i.e., sternal crawling on the ground) where they are exposed to and attacked by domestic dogs [96,109].
1.4 Dog attack injuries: clinical considerations
The anatomical makeup of carnivores allows domestic dogs to inflict tremendous bite force through a combination of shearing, tensile, and compressive mechanisms [110,111,112,113,114]. Bites sustained from dogs therefore tend to be severe and often fatal, inciting crush, tear, and avulsion injuries [115,116]. Wounds sustained by companion species (i.e., other dogs and cats) are described as deceptive, with more damage occurring to deeper organs than the skin and subcutis [112,117,118,119]. Despite being common targets of attacks, there is little information available on the presentation of dog bite wounds in wild or exotic species [120,121]. This is significant given that predation by domestic dogs on wildlife is rarely observed [120]. Identifying these injuries in uncommon species may therefore be challenging, leading to an underestimated prevalence of these attacks and improper case management.
When wildlife requires medical care, rapid intake evaluation is vital in minimizing the stress and suffering of patients [122,123,124]. Deciding the fate of undomesticated animals should occur in a timely manner and obtaining a prompt clinical diagnosis is crucial in making said decision [123,125]. Documenting common presentations of wildlife injuries, such as dog attacks, in a taxonomic-specific context is therefore essential for improved recognition and management [120,126,127]. This is particularly important in the evaluation of morphologically unique species, where traditional information may not be extrapolatable [120,128,129].
Moreover, publications on the clinical nature of dog attack injuries in wildlife are limited. Variation in the presentation and topography of wounds across taxa is described in one study [130]. However, the incorporation of morphological information for each species is not described. A single report touches upon the clinical presentation of dog attacks in C. hoffmani specifically. Nonetheless, the information is limited due to the publication maintaining a broader focus on the species [83]. The lack of resources on traumatic dog attacks in sloths is especially unfavorable given the species’ distinct anatomical makeup [131,132] as well as the upward trend in these events across sloths’ ranges [63]. The purpose of this report is to describe the clinical presentation and postmortem lesions observed in C. hoffmani following an attack by dogs, with special consideration to morphology, behavior, and conservation of the species. In addition, this report aims to document the threat that domestic dogs pose to C. hoffmani and other wildlife in Costa Rica.
2 Case report
A subadult Hoffman s two-fingered sloth presented to The Sloth Institute (TSI) in June of 2022 following an attack by domestic dogs. TSI is a nonprofit wildlife rehabilitation and research center located in the Puntarenas Province of Costa Rica. The incident occurred on a nearby residential property, in the area of Manuel Antonio, Costa Rica (9.3923°N, 84.1370°W). A good Samaritan witnessed the attack and reported the involvement of three dogs, including two Doberman Pinschers and one Rottweiler. The dogs were seen mauling the sloth on the ground as it attempted to escape to a nearby tree. The dogs did not consume the sloth and eventually retreated after a prolonged period of attacking. Access to the injured animal was not possible until the following morning when the individual promptly retrieved the patient and contacted center staff. The sloth was found on the ground, in a curled resting position, and presumed dead (Figure 1).
C. hoffmani immediately following attack by domestic dogs, assuming abnormal resting posture at the tree base. Typically, the species will quickly ascend back to the canopy following brief visits to the forest floor. Photograph taken by rescuer.
Upon arrival, the patient was in lateral recumbency and did not resist being handled. Examination revealed that the patient was comatose, hypothermic, and apneic. Auscultation revealed absent lung sounds in all fields bilaterally despite having clear airways. The patient was bradycardic per species-specific parameters (<40 beats per minute) and had weak but synchronous femoral pulses. Dorsal pedal pulses were absent bilaterally. Throughout examination, the degree of bradycardia progressively worsened. The patient showed signs of impaired perfusion, demonstrated by pale mucous membranes, a prolonged capillary refill time, and cold extremities on palpation. Neurologic deficits were also evident. There was no indirect or direct pupillary light reflex, and the patient’s pupils were severely mydriatic. Menace and palpebral reflexes were diminished, and deep pain responses were impaired on all limbs. The patient was mildly dehydrated and had minor bilateral sinking of the eyes. The patient was in adequate body condition at 4.3 kg.
The patient’s hair was wet but intact, with no obvious signs of injury visualized (Figure 2a). Parting of the hair and examination of the skin revealed soft tissue damage, including moderate bruising and superficial abrasions distributed around the cervical region, dorsum, and ventral abdomen (Figure 2b). Small puncture wounds (0.5–3 cm) were located around the left orbital cavity, left cervical spine, left abdomen, and dorsal pelvis. Petechiae were noted on both the left and right pinna. Ecchymoses were present along the ribs, entire dorsum, and proximal left fore and hindlimb. There was a large, irregular-shaped, and circumferential band of bruising on the distal neck, potentially compatible with being bitten in this region and shaken by the dogs during attack. Palpation of skeletal structures was unremarkable, with no obvious fractures or disarticulations noted and normal range of motion. The abdomen was soft on palpation, with no pronounced signs of organomegaly. All remaining structures were unremarkable on physical examination.
Postmortem images of C. hoffmani carcass following attack by domestic dogs. Pictured in (a) sternal recumbency with no discernible signs of traumatic injury and (b) lateral recumbency with hair parted to reveal moderate bruising along the dorsal thorax. Complete removal of the hair revealed (c) numerous lacerations, puncture wounds, and subcutaneous hemorrhage on the dorsum, as well as (d) extensive bruising on the left lateral thorax and proximal forelimb.
Attempts to stabilize the patient (i.e., airway establishment, fluid resuscitation, atropine administration) were underway while the patient was being evaluated initially. However, these efforts were discontinued shortly after the grave condition was recognized. While preparing for humane euthanasia, the patient died without medical assistance just minutes following arrival to the clinic. At that time, a pink frothy liquid was noted in the nares bilaterally.
Immediately following death, a modified abdominal and thoracic point of care ultrasound was performed for teaching purposes. There was a moderate volume of anechoic free peritoneal fluid present bilaterally. However, no fluid could be recovered via abdominocentesis. A mild amount of free intraperitoneal air was also evident. Examination of the thorax revealed a small volume of anechoic pleural effusion. Multiple, adjacent hyperechoic pulmonary B-lines or lung rockets were noted as well.
The patient was preserved via refrigeration until radiographs could be obtained to further assess skeletal injury (Figure 3) and necropsy could be completed. Radiographs revealed no orthopedic injuries in the patient despite the degree of soft tissue injury and reported force of the attack. Open epiphyseal growth plates were noted bilaterally on the distal radius, denoting the sloth as a subadult. All other abnormalities were attributed to radiographic positioning or normal postmortem change.
C. hoffmani radiographs obtained postmortem to assess for orthopedic injury. No skeletal injuries were noted on (a) dorsoventral or (b) left lateral views. All other findings are positional artifacts or attributable to postmortem change.
On necropsy, the carcass was found to be in good postmortem and adequate nutritional condition. Upon removal of hair, extensive traumatic injury was evident (Figure 2c and d). Thirty-five variably sized (0.5–2 cm) surface abrasions, most elongated with opposite angular edges, were noted on the patient and distributed throughout the entire dorsum, ventral thorax, left axilla, left cervical, and left auricular area. Cutaneous ecchymosis was present in the left mammary region, with three linear to oblong-shaped lesions ranging from 3 to 6 cm in length. Linear bruising was present along the neck, extending dorsally to laterally. There were six small (0.5–3 cm), circular to elongated puncture wounds, lacerating both subcutaneous tissue and muscle. These wounds were noted on the left neck, lateral abdomen, and dorsal pelvis. Multiple hemorrhages and hematomas were found, with distribution on the lateral neck, entire thorax and abdomen, proximal left fore and hindlimb, and dorsal pelvis (Figure 4a).
Gross pathological findings associated with C. hoffmani following attack by domestic dogs, including (a) subcutaneous hemorrhage and puncture wounds extending through gluteal muscle, presence of serosanguinous free fluid in the (b) pericardial and (c) pleural space, (d) contusions and puncture wounds on the ventral surface of the stomach, and hemorrhage and emphysema on (e) dorsal and (f) ventral views of the lungs.
Light pink froth was noted in the trachea and bronchi and a moderate volume of serosanguinous fluid was present in the pleural cavity (Figure 4c). The lungs were slightly enlarged, diffusely red, and mottled. Marked, locally extensive, dark red to purple hemorrhage was present on all surfaces and lobes (Figure 4e and f). Focal areas of yellow discoloration were noted on the caudal aspect of the right and left caudal lung lobes. The texture was generally soft, with multifocal spots of firmness felt on the left caudal lobe. There were moderate-sized (2 cm) emphysematous bullae noted focally on the dorsal surface of the right cranial lobe and ventral surface of the right caudal lobe. A moderate amount of hemorrhagic fluid was present in the pericardial sac (Figure 4b). The heart was firm and otherwise unremarkable.
A moderate amount of serosanguinous fluid was noted in the peritoneal cavity as well. The stomach was of normal size for the species and contained appropriate ingesta. There was locally extensive bruising over the ventral aspect of the fundic and cardiac region (Figure 4d). Two small puncture wounds (0.5 cm) were noted on the caudoventral aspect of the fundus with hemorrhagically infiltrated edges. All other gastrointestinal structures were unremarkable. The bladder wall was firm and thickened, with mild petechiae present on the external surface. Bladder mucosa was coated by flocculant exudate and infoldings were noted. A moderate amount of purulent, frothy, white to yellow fluid was likewise noted. Reproductive organs were unremarkable and consistent with the radiographic findings which had confirmed the sloth to be a sexually immature, or subadult, female. No skeletal abnormalities were evident, and no gross lesions were noted in the spinal region. Intracranial examination was not completed. All other findings were unremarkable.
Polytraumatic injury produced by repeated bites and blunt force associated with the attack was determined as the cause of death in this patient. Pleural and pericardial effusions, as demonstrated on necropsy, were presumed to cause the patient’s apnea and impaired cardiopulmonary function. Severe hemorrhage and cavitary effusions suggest that the patient succumbed to hypovolemic shock. Substantial soft tissue injury was present, although penetrating wounds were minimal. The accumulation of blood under the skin and in muscle fascia suggests concurrent rupture of surrounding vasculature; however, the exact site of origin could not be identified. Finally, cystitis, as evident by signs of inflammation and infection in the bladder, was confirmed by necropsy. This may have been an inciting factor for the attack, precipitating the patient’s descent from the tree to urinate despite unsafe conditions and the presence of dogs. Reviewing the timeline provided by the rescuer, it was determined that this sloth was attacked early in the evening and too weak to ascend back up the tree. The sloth likely remained stationary on the ground overnight where it slowly succumbed to its injuries before dying shortly after arrival to the clinic.
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Ethical approval: The research related to animal use has been complied with all the relevant national regulations and institutional policies for the care and use of animals.
3 Discussion
3.1 Clinical management of C. hoffmanni following dog attacks
On initial examination, the extent of injury was not readily evident, given the coarse and thick nature of C. hoffmanni coat. The species maintains extremely dense hair, which has been suggested to serve a variety of roles relevant to an arboreal lifestyle, including camouflage, thermal regulation, nutrient absorption, and redirection of water [133,134,135,136,137]. Likewise, a diverse microbial community of epibionts can be found in the coat, described as a “self-contained system of taxonomic diversity and trophic levels” [138]. Numerous algal, fungal, and bacterial organisms inhabit the hair of sloths and are believed to facilitate symbiosis with the species [136,138,139,140]. This morphology is important to consider clinically. Although this dense coat may mask the external injuries following attack, loss of hair may be detrimental to overall health and long-term survival [137]. This may likewise compromise a patient’s suitability for release following recovery. Full body shaving of C. hoffmanni in this study was only conducted for research purposes and would rarely be appropriate premortem. Nonetheless, failure to recognize or treat dog-inflicted bite wounds without thorough evaluation may lead to infection, sepsis, and death. Although removal of the coat may be warranted at times to facilitate a more-thorough examination, shaving should be minimal in this species when possible.
The lack of external hemorrhage and minimal penetrating injury identified in the patient was unexpected given the length of time, number of dogs, and size of the breeds involved in the attack. Although dog bites are known to be deceptive in terms of skin and subcutaneous damage [119], reports of attacks with similarly sized species (i.e., large canids attacking small breed dogs and cats) often involve extensive deep wounds [141,142,143]. This finding is likely related to the excessively thick integument of C. hoffmani. Skin extends a depth of over 4 mm around the neck and throat, 3 mm on the dorsum, and 1–2 mm in other body regions [132]. To compare, the skin of a domestic canine may be as thin as 0.5 mm in dogs [144] and 0.4 mm in cats, although this is widely variable across breeds [145]. This composition may serve a protective role for C. hoffmani in terms of external trauma to the skin, although additional research is needed to support this hypothesis.
An almost complete absence of adipose tissue leaves the skin closely applied to the thick underlying musculature. Despite minimal subcutaneous and abdominal fat, including that of the omentum, adipose is present around renal structures and the spinal canal [132,135]. Contrastingly, abdominal organs, including a prominent stomach, sit closely against the body wall [83]. These structures may thus be more vulnerable to internal trauma than others, as demonstrated by this patient. Topographically, the sloth was targeted along the axial regions of the body, with appendages largely untouched. Likewise, the kidneys and vertebral regions were intact, with little visible damage on necropsy. This is likely related to both the distribution of adipose tissue and the form of locomotion adapted by C. hoffmani while on the ground (i.e., crawling in a sternal position).
Finally, no orthopedic injuries or long bone fractures were noted in the patient, despite limbs being a commonly reported site of dog attack injuries in other species [112]. The head was generally unscathed, and no skull injuries were evident. This may be related to the defensive mechanisms of C. hoffmani, which involve hissing, biting, and slashing with forelimb claws [146,147]. Unlike Bradypus variegatus, C. hoffmani possesses well-developed facial musculature and large, sharpened canines, allowing them to deliver forceful and damage-inflicting bites when threatened [83,131,148]. Although sloths demonstrate a reduction in muscle mass compared to other mammals, modified distal limb morphology grants them enhanced strength and endurance in their appendages [90,148,149,150,151,152,153,154]. These modifications support their suspensory posture and facilitate powerful flexor musculature [149], fatigue resistance [154], and grip strength exerted with minimal energy expenditure [155]. In addition, limbs lack bony processes, increasing mechanical advantage [151]. Compressive strength in the long bones of C. hoffmani is compromised. However, tensile strength is significantly enhanced to support suspensory function [156]. C. hoffmani may therefore be less susceptible to limb injuries inflicted by dog bites due to the strength and fluid nature of movement in these regions [83]. Predators may likewise avoid these areas during attack, given their potential to inflict damage. However, this is highly dependent on the nature of the bite inflicted [112]. Additional research is needed on the mechanics of C. hoffmani defense mechanisms to better understand the potential outcome.
These findings may be taken into consideration during evaluation of C. hoffmanni following traumatic dog attacks, with priority spots for examination involving the abdominothoracic region and underlying structures. Nevertheless, additional documentation of dog attacks is needed to determine patterns of injury for the species. The lack of marked external trauma, related to integument thickness and coat composition may lead practitioners to underestimate the magnitude of injuries. Additional diagnostic modalities were therefore of immense clinical value for this patient. Ultrasonography, radiology, and necropsy were essential in quantifying the extent of injury in C. hoffmani. Ultrasonography performed on the ventrum does not necessitate hair removal on this species, providing an excellent and truly noninvasive tool. Without these diagnostic aids and postmortem examination, this patient’s clinical presentation would have likely been deceiving. When available, these tools should be utilized for C. hoffmani patients following attack by domestic dogs to ensure timely premortem and accurate postmortem diagnosis.
3.2 Mitigating the impacts of dogs on sloths and other wildlife
Domestic dogs are understated threats to numerous wildlife species, including sloths, and the potential impacts are greater now than historically [157]. In the approaching decades, dog occupancy nearing natural habitats and attacks on wildlife are expected to increase in prevalence [9,11,19,31,43]. The status of Costa Rica as a biodiversity hotspot and rapidly urbanizing country makes this issue particularly critical [158,159]. Wildlife–dog conflict is well-documented as a consequence of anthropogenic origin and the socioecological components of this problem should be considered. It is essential that management strategies are attuned to cultural and regional values [160]. Likewise, a multifaceted approach must be maintained, given the issue’s complexity. We discuss mitigation strategies, including (i) habitat preservation, (ii) domestic dog management and population control, (iii) wildlife corridors facilitating forest connectivity, (iv) owner education, and (v) government policy (Figure 5).
A collaborative approach to mitigate conflict between domestic dogs and sloths or other arboreal wildlife. Anthropogenic land use changes directly contribute to the degradation of wildlife habitats (a). Sloths are forced to enter novel environments in seek of resources and employ terrestrial locomotion in the face of discontinuous canopies (b). These land use changes likewise drive humans and their companion animals to forest edges or interiors (c), where domestic dog and sloths are then obliged to co-exist. The increased spatiotemporal overlap of dogs and sloths results in increased opportunities for predation (d) and resultant upticks of wildlife requiring medical care following these altercations. Addressing this problem requires a multifaceted approach, with target areas for intervention (yellow text and arrows) including habitat preservation, domestic dog management and population control, wildlife corridors facilitating forest connectivity, owner education, and government policy. Asterisks are used to denote interventions in which veterinary and other animal health professionals play a key role.
3.2.1 Habitat preservation
Mitigating wildlife–dog conflict begins with prevention in the context of global change [31,35]. Dynamic alterations in land use to accommodate urban infrastructure and agricultural expansion in Latin America have grown exponentially over the last decade. These changes continue to place pressure on wildlife [121,161,162,163,164]. Despite the success of national policies and programs enacted to preserve natural resources, Costa Rica still maintains the highest percentage of urban populations compared to other countries in Central America [93,165,166,167,168,169,170,171]. Manuel Antonio, the site in which this study occurred, holds the lowest rate of documented deforestation. However, over 90% of deforestation occurs in non-protected areas [170,172]. Numerous studies have demonstrated the value of protected areas and the restriction of dogs in these regions [31,56,172].
Although protected areas facilitate safer habitats for sloths and other wildlife, and reduced accessibility by dogs, this strategy alone is rarely effective [12,31,173]. Protected areas do not account for owner noncompliance, the movement of free-ranging dogs from adjacent lots, or the entry of wildlife onto residential property [28,38]. Likewise, the rate and magnitude of wildlife disturbance far exceeds the speed at which this strategy produces tangible results. Maintaining this strictly preservationist value (i.e., prohibiting human establishment near nature, solely focusing on pristine habitat preservation) is therefore of limited benefit to sloths and other wildlife in the Anthropocene. As urban expansion approaches a tipping point, a paradigm shift is essential [174,175]. Continued global change is inevitable and preserving habitats is crucial, but it must involve additional and complementary approaches [10,31,33,42,43,176,177,178].
3.2.2 Domestic dog management and population control
Traditional means of invasive predator management (i.e., physical removal, lethal control) have been highlighted as controversial, inhumane, and ineffective for domestic dogs, given their abundance and role as companion animals [179,180,181]. Nevertheless, addressing this issue represents a complex conservation challenge, given the interconnectedness of humans and dogs. The role and value of dogs in society, as companion animals and as working breeds, is not to be undermined [182,183]. When appropriately trained and supervised by human caretakers, dogs may have negligible, or even beneficial impacts on wildlife. This is demonstrated by their historical roles as conservation tools and livestock guardians [177,184,185,186,187,188]. Both positive and negative effects of domestic dogs must therefore be considered in an all-encompassing management approach [160].
The capture and transport of unsupervised free-ranging dogs to shelters has also been described as a canine-focused control strategy in some regions [189]. However, elimination of dogs without owners is unlikely to be successful in Costa Rica, given the overburdened and underfunded status of most humane organizations [69]. In addition, this does not target domestic dogs occupying less accessible regions of forest. Sterilization programs, residential fencing to restrict roaming, and barriers to prevent access to protected spaces have been suggested as the most effective canine control strategies [12,35,155]. Improved feeding and care of domestic dogs, through accessible and subsidized assistance, is also a means of mitigation [58,67]. However, even well-fed dogs pose a threat to wildlife. There are numerous reports of attack as a means of recreation for dogs rather than consumption [65,66]. TSI has never observed the consumption of C. hoffmani or B. variegatus following attack. Other strategies for the control of domestic dogs have been suggested, but little research exists on intervention efficacy [9,41,160].
3.2.3 Wildlife corridors
Maintaining or restoring forest connectivity can substantially reduce the threats that domestic dogs pose to sloths and other arboreal species. Intact canopies provide safe routes for arboreal species to transverse and facilitate ease of movement between trees, eliminating unnecessary terrestrial locomotion [190,191,192]. When possible, the establishment or protection of natural canopy bridges should be pursued in areas with known wildlife–dog conflict. If canopy integrity cannot be naturally maintained, installation of artificial wildlife crossings should be completed [35,190,193,194,195]. Corridors in the form of rope bridges are a straightforward, inexpensive, and efficacious intervention [195,196,197,198]. Installation of these structures requires no specialized equipment, depending on tree height [196]. Rope of substantial thickness is typically utilized and securely placed between adjacent but disconnected trees [195,196,197,198].
These structures not only enable dog avoidance by sloths but also protect them from other anthropogenic threats such as electrocution or starvation due to the lack of tree access [35,194,199,200]. Corridors are also used to prevent vehicle collisions in areas where roads and other linear infrastructures transect vegetation [201,202]. The general success of these interventions in reducing wildlife mortality and use of corridors by animals in Costa has been documented for a variety of native species [75,203,204]. Sloths, in particular, are frequent users of rope bridges [205,206]. Camera traps are often set up at artificial crossing sites to monitor animal use and for recreational viewing purposes [201].
As private lands intersect many natural habitats in the country [170], including that of sloths, outreach programs facilitating public willingness to allow these modifications are essential [40]. Contrarily, strategic tree trimming has been used for other species as a means to redirect and prevent access to certain areas [207]. There may be implications for this method in problem spots (i.e., fenced yards with dogs known to target wildlife) to deter use or congregation by sloths and other species. Additional research is needed to determine the efficacy of this strategy.
3.2.4 Owner education and veterinary engagement
The impact of domestic dogs on wildlife is highly dependent on responsible ownership and the key role of dog owners is highlighted in various studies [10,12,58]. Human behavior directly influences the movement and activity of dogs pertaining to wildlife [33,42,173,176]. Management strategies must therefore involve owner compliance [9,67]. Convincing owners to limit or restrict roaming and to provide proper nutrition is suggested as one straightforward management technique [10]. Other low-cost options include the implementation of stringent leash laws, although varying degrees of efficacy have been reported and with little effect on free-roaming populations [36,58,176].
Companion animal veterinarians and other veterinary staff play a key role in this mitigation approach. Client education is a critical and major part of small animal practitioners’ everyday responsibilities [208,209]. This represents an important opportunity for veterinary staff in regard to wildlife. As credible sources of knowledge for their communities and through existing interactions with dog owners, veterinary staff may take the time to engage with clients about their pets’ interactions with wildlife [210,211]. Likewise, they may help guide their clients toward appropriate resources when needed. This communication is important not only for dog–wildlife conflict and the benefit of wildlife but for companion animal health as well [212,213].
Non-veterinary-based education activities and community engagement are also essential in reducing the impact of domestic dogs on wildlife [40,67]. Outreach programs organized by wildlife groups or other relevant bodies should focus on responsible pet ownership and how to facilitate appropriate wildlife interactions [43,177,214,215]. Dog owners living near areas with a high abundance of wildlife should be provided information on the ways they can prevent attacks and who to contact should an attack occurs [9]. Training first responders in non-animal focused fields, such as law enforcement, may also be of value. These stakeholders often receive minimal training in regards to wildlife, yet are frequently contacted by the public in emergent animal situations. Specific training in wildlife handling for relevant organizations may therefore be advantageous in dog-wildlife response efforts. C. hoffmani is particularly difficult and dangerous to handle [83], and this task should be allotted to trained animal health professionals.
3.2.5 Government policy
Finally, policy and intergovernmental changes should be considered [43]. This may include the generation of standard operating procedures and management plans, amongst others. These plans may specify designated wildlife rescue centers, animal control staff, and veterinarians for response activities. Likewise, proper reporting systems should be in place to quantify the problem and identify key areas for invention [43]. Although community and national policy measures are essential in negating the problem of dog–wildlife conflict, various political, economic, and cultural issues prevent many governmental agencies from addressing the issue. Policy development on the topic has been described as highly unlikely at the national level [67]. Additional research and funding are therefore needed on the threat that domestic dogs pose to wildlife to determine the true scope of the problem and properly allocate resources.
4 Conclusions
In summary, our results suggest that domestic dogs in Costa Rica should be recognized as a conservation threat to sloths and other arboreal wildlife. Management of C. hoffmani following attack by domestic dogs involves careful clinical evaluation in the context of their unique anatomical makeup and ecological behavior. Preventing attacks on C. hoffmani and other species involves coordinated management efforts across the scientific disciplines, with emphasis on habitat preservation, domestic dog population control, installation of wildlife corridors, dog owner education, and policy changes. Additional research on domestic dog-wildlife conflict is required to understand the true magnitude of impact, identify novel management approaches, and further evaluate the efficacy of mitigation strategies.
Acknowledgments
The authors thank the TSI team for their clinical and research support as well as the good Samaritans involved in the rescue of this patient.
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Funding information: Funding for this study was provided by The Sloth Institute, a nonprofit organization in Costa Rica: Asociación para el Estudio del Perezoso.
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Conflict of interest: The authors state no conflict of interest.
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Data availability statement: All data generated or analyzed during this study are included in this published article.
References
[1] Dirzo R, Young HS, Galetti M, Ceballos G, Isaac NJB, Collen B. Defaunation in the anthropocene. Science. 2014 Jul 25;345(6195):401–6.10.1126/science.1251817Search in Google Scholar PubMed
[2] Estes JA, Terborgh J, Brashares JS, Power ME, Berger J, Bond WJ, et al. Trophic downgrading of planet Earth. Science. 2011;333(6040):301–6.10.1126/science.1205106Search in Google Scholar PubMed
[3] Eigenbrod F, Hecnar SJ, Fahrig L. Accessible habitat: an improved measure of the effects of habitat loss and roads on wildlife populations. Landsc Ecol. 2008 Feb 1;23(2):159–68.10.1007/s10980-007-9174-7Search in Google Scholar
[4] Gaynor KM, Hojnowski CE, Carter NH, Brashares JS. The influence of human disturbance on wildlife nocturnality. Science. 2018 Jun 15;360(6394):1232–5.10.1126/science.aar7121Search in Google Scholar PubMed
[5] Messmer TA. Human–wildlife conflicts: emerging challenges and opportunities. Hum-Wildl Confl. 2009;3(1):10–7.Search in Google Scholar
[6] Woodroffe R, Thirgood S, Rabinowitz A. People and wildlife, conflict or co-existence?. Vol. 9. New York, USA: Cambridge University Press; 2005.10.1017/CBO9780511614774Search in Google Scholar
[7] Olden JD, LeRoy Poff N, Douglas MR, Douglas ME, Fausch KD. Ecological and evolutionary consequences of biotic homogenization. Trends Ecol Evol. 2004 Jan 1;19(1):18–24.10.1016/j.tree.2003.09.010Search in Google Scholar PubMed
[8] Doherty TS, Glen AS, Nimmo DG, Ritchie EG, Dickman CR. Invasive predators and global biodiversity loss. Proc Natl Acad Sci. 2016 Oct 4;113(40):11261–5.10.1073/pnas.1602480113Search in Google Scholar PubMed PubMed Central
[9] Gompper ME. The dog–human–wildlife interface: assessing the scope of the problem. In: Free-Ranging Dogs and Wildlife Conservation [Internet]. Oxford: Oxford University Press; 2013. [cited 2022 Jul 15] https://oxford.universitypressscholarship.com/10.1093/acprof:osobl/9780199663217.001.0001/acprof-9780199663217-chapter-1.10.1093/acprof:osobl/9780199663217.003.0001Search in Google Scholar
[10] Torres P, Prado P. Domestic dogs in a fragmented landscape in the Brazilian Atlantic Forest: Abundance, habitat use and caring by owners. Braz J Biol Rev Brasleira Biol. 2010 Nov 1;70:987–94.10.1590/S1519-69842010000500010Search in Google Scholar PubMed
[11] Hughes J, Macdonald DW. A review of the interactions between free-roaming domestic dogs and wildlife. Biol Conserv. 2013 Jan 1;157:341–51.10.1016/j.biocon.2012.07.005Search in Google Scholar
[12] Home C, Vanak A, Bhatnagar Y. Canine conundrum: Domestic dogs as an invasive species and their impacts on wildlife in India. Anim Conserv. 2017 Dec 20;21:275–82.10.1111/acv.12389Search in Google Scholar
[13] Horowitz C. Plano de manejo do Parque Nacional de Brasília: avaliação da metodologia de planejamento adotada, execução e resultados alcançados no decênio 79/89. Brasília, Brazil: Brasília Universidade Brasília; 1992.Search in Google Scholar
[14] Henry VG. Predation on dummy nests of ground-nesting birds in the southern appalachians. J Wildl Manag. 1969;33(1):169–72.10.2307/3799666Search in Google Scholar
[15] Hunt GR, Hay R, Veltman CJ. Multiple kagu rhynochetos jubatus deaths caused by dog attacks at a high-altitude study site on pic ningua, New Caledonia. Bird Conserv Int. 1996 Dec;6(4):295–306.10.1017/S0959270900001775Search in Google Scholar
[16] Molina Molina M, Peñaloza J. Dog predation on Páramo white-tailed deer: The case Mucubají, Sierra Nevada National Park. Rev Mem Soc Cienc Nat Salle. 2000 Feb 21;154:139–44.Search in Google Scholar
[17] Butler JRA, du Toit J. Diet of free-ranging domestic dogs (Canis familiaris) in rural Zimbabwe: Implications for wild scavengers on the periphery of wildlife reserves. Anim Conserv. 2002 Feb 1;5:29–37.10.1017/S136794300200104XSearch in Google Scholar
[18] Butler JRA, du Toit JT, Bingham J. Free-ranging domestic dogs (Canis familiaris) as predators and prey in rural Zimbabwe: threats of competition and disease to large wild carnivores. Biol Conserv. 2004 Feb 1;115(3):369–78.10.1016/S0006-3207(03)00152-6Search in Google Scholar
[19] Banks PB, Bryant JV. Four-legged friend or foe? Dog walking displaces native birds from natural areas. Biol Lett. 2007 Dec 22;3(6):611–3.10.1098/rsbl.2007.0374Search in Google Scholar PubMed PubMed Central
[20] Bergman D, Breck S, Bender S. Dogs gone wild: Feral dog damage in the United States. New York: Saratoga Springs; 2009.Search in Google Scholar
[21] Campos CB, Esteves CF, Ferraz KM, Crawshaw PG Jr, Verdade LM. Diet of free-ranging cats and dogs in a suburban and rural environment, south-eastern Brazil. J Zool. 2007 Sep 1;273:14–20.10.1111/j.1469-7998.2007.00291.xSearch in Google Scholar
[22] Oliveira V, Linares A, Corrêa G, Chiarello A. Predation on the black capuchin monkey Cebus nigritus (Primates: Cebidae) by domestic dogs Canis lupus familiaris (Carnivora: Canidae), in the Parque Estadual Serra do Brigadeiro, Minas Gerais, Brazil. Rev Bras Zool. 2008 Jun 1;25:376–8.10.1590/S0101-81752008000200026Search in Google Scholar
[23] Riley Koenig C, Koenig B, Gumert M. Observation of a fatal dog attack on a juvenile long-tailed macaque in a human-modified environment in Singapore. Nat Singapore. 2015 Jan 1;8:57–63.Search in Google Scholar
[24] Barrera R. Análisis de registros de ataques a fauna silvestre chilena por carnívoros domésticos perro (Canis lupus familiaris) y gato (Felis silvestris catus) entre los años 2000 y 2016. Rev Med Vet Investig. 2018;1(1):92–101.Search in Google Scholar
[25] Ridwan ARM, Haris H, Najmuddin MF, Husna HA, Norazlimi N, Zain BMM, et al. Predation of domestic dogs (Canis lupus familiaris) on Schlegel’s banded langur (Presbytis neglectus) and crested hawk-eagle (Nisaetus cirrhatus) on dusky leaf monkey (Trachypithecus obscurus) in Malaysia. J Sustain Sci Manag. 2019, [cited 2022 Jul 15]. http://agris.upm.edu.my:8080/dspace/handle/0/19879.Search in Google Scholar
[26] Nayeri D, Mohammadi A, Qashqaei AT, Vanak AT, Gompper ME. Free-ranging dogs as a potential threat to Iranian mammals. Oryx. 2022 May;56(3):383–9.10.1017/S0030605321000090Search in Google Scholar
[27] Kalnay E, Cai M. Impact of urbanization and land-use change on climate. Nature. 2003 May 29;423(6939):528–31.10.1038/nature01675Search in Google Scholar PubMed
[28] Yen SC, Ju YT, Shaner PJL, Chen HL. Spatial and temporal relationship between native mammals and free-roaming dogs in a protected area surrounded by a metropolis. Sci Rep. 2019 Jun 3;9(1):8161.10.1038/s41598-019-44474-ySearch in Google Scholar PubMed PubMed Central
[29] Elmqvist T, Andersson E, McPhearson T, Bai X, Bettencourt L, Brondizio E, et al. Urbanization in and for the Anthropocene. NPJ Urban Sustain. 2021 Feb 23;1(1):1–6.10.1038/s42949-021-00018-wSearch in Google Scholar
[30] Ordeñana MA, Crooks KR, Boydston EE, Fisher RN, Lyren LM, Siudyla S, et al. Effects of urbanization on carnivore species distribution and richness. J Mammal. 2010 Dec 16;91(6):1322–31.10.1644/09-MAMM-A-312.1Search in Google Scholar
[31] Paschoal AMO, Massara RL, Bailey LL, Doherty PF, Santos PM, Paglia AP, et al. Anthropogenic Disturbances drive domestic dog use of Atlantic forest protected areas. Trop Conserv Sci. 2020 Jan;11(1):1–14. [cited 2022 Jul 16]. http://bioone.org/journals/tropical-conservation-science/volume-11/issue-1/1940082918789833/Anthropogenic-Disturbances-Drive-Domestic-Dog-Use-of-Atlantic-Forest-Protected/10.1177/1940082918789833.full.10.1177/1940082918789833Search in Google Scholar
[32] Paschoal A, Massara R, Santos J, Chiarello A. Is the domestic dog becoming an abundant species in the Atlantic Forest? A study case in southeastern Brazil. Mammalia. 2012 Feb 1;76:67–76.10.1515/mammalia-2012-0501Search in Google Scholar
[33] Soto CA, Palomares F. Human-related factors regulate the presence of domestic dogs in protected areas. Oryx. 2015 Apr;49(2):254–60.10.1017/S0030605313000604Search in Google Scholar
[34] Wandeler AI, Matter HC, Kappeler A, Budde A. The ecology of dogs and canine rabies: A selective review. Rev Sci Tech Int Epizoot. 1993 Mar;12(1):51–71.10.20506/rst.12.1.663Search in Google Scholar PubMed
[35] Chaves ÓM, Júnior JCS, Buss G, Hirano ZMB, Jardim MMA, Amaral ELS, et al. Wildlife is imperiled in peri-urban landscapes: Threats to arboreal mammals. Sci Total Env. 2022 May 15;821:152883.10.1016/j.scitotenv.2021.152883Search in Google Scholar PubMed
[36] Schlacher TA, Weston MA, Lynn D, Schoeman DS, Huijbers CM, Olds AD, et al. Conservation gone to the dogs: When canids rule the beach in small coastal reserves. Biodivers Conserv. 2015 Mar 1;24(3):493–509.10.1007/s10531-014-0830-3Search in Google Scholar
[37] Sepúlveda M, Pelican K, Cross P, Eguren A, Singer R. Fine-scale movements of rural free-ranging dogs in conservation areas in the temperate rainforest of the coastal range of southern Chile. Mamm Biol. 2015 Aug 1;80(4):290–7.10.1016/j.mambio.2015.03.001Search in Google Scholar
[38] de Cassia Bianchi R, Olifiers N, Riski LL, Gouvea JA, Cesário CS, Fornitano L, et al. Dog activity in protected areas: Behavioral effects on mesocarnivores and the impacts of a top predator. Eur J Wildl Res. 2020 Apr 6;66(3):36.10.1007/s10344-020-01376-zSearch in Google Scholar
[39] Schüttler E, Saavedra-Aracena L, Jiménez JE. Spatial and temporal plasticity in free-ranging dogs in sub-Antarctic Chile. Appl Anim Behav Sci. 2022 May 1;250:105610.10.1016/j.applanim.2022.105610Search in Google Scholar
[40] Morin DJ, Lesmeister DB, Nielsen CK, Schauber EM. The truth about cats and dogs: Landscape composition and human occupation mediate the distribution and potential impact of non-native carnivores. Glob Ecol Conserv. 2018 Jul 1;15:e00413.10.1016/j.gecco.2018.e00413Search in Google Scholar
[41] Reed SE, Merenlender AM. Effects of management of domestic dogs and recreation on carnivores in protected areas in Northern California. Conserv Biol. 2011;25(3):504–13.10.1111/j.1523-1739.2010.01641.xSearch in Google Scholar PubMed
[42] dos Santos CLA, Le Pendu Y, Giné GAF, Dickman CR, Newsome TM, Cassano CR. Human behaviors determine the direct and indirect impacts of free-ranging dogs on wildlife. J Mammal. 2018 Oct 10;99(5):1261–9.10.1093/jmammal/gyy077Search in Google Scholar
[43] Young J, Olson K, Reading R, Amgalanbaatar S. Is wildlife going to the dogs? Impacts of feral and free-roaming dogs on wildlife populations. BioScience. 2011 Feb 11;61:125–32.10.1525/bio.2011.61.2.7Search in Google Scholar
[44] Cleaveland S, Appel MG, Chalmers WS, Chillingworth C, Kaare M, Dye C. Serological and demographic evidence for domestic dogs as a source of canine distemper virus infection for Serengeti wildlife. Vet Microbiol. 2000 Mar 15;72(3–4):217–27.10.1016/S0378-1135(99)00207-2Search in Google Scholar
[45] Curi NH, de A, Miranda I, Talamoni SA. Serologic evidence of Leishmania infection in free-ranging wild and domestic canids around a Brazilian National Park. Mem Inst Oswaldo Cruz. 2006 Feb;101(1):99–101.10.1590/S0074-02762006000100019Search in Google Scholar PubMed
[46] Funk S, Fiorello C, Cleaveland S, Gompper ME. The role of disease in carnivore ecology and conservation. J Carniv Conserv. 2001 Jan 1;4:441–66.Search in Google Scholar
[47] Czupryna AM, Brown JS, Bigambo MA, Whelan CJ, Mehta SD, Santymire RM, et al. Ecology and demography of free-roaming domestic dogs in rural villages near serengeti national park in Tanzania. PLoS One. 2016 Nov 28;11(11):e0167092.10.1371/journal.pone.0167092Search in Google Scholar PubMed PubMed Central
[48] Calatayud O, Esperón F, Velarde R, Oleaga Á, Llaneza L, Ribas A, et al. Genetic characterization of Carnivore Parvoviruses in Spanish wildlife reveals domestic dog and cat-related sequences. Transbound Emerg Dis. 2020;67(2):626–34.10.1111/tbed.13378Search in Google Scholar PubMed
[49] da Silva SKSM, Cassano CR, Sousa SD, Campos-Júnior DA, Catenacci LS. The importance of the dog (Canis lupus familiaris) in cocoa farms as carriers of helminths potentially transmissible to humans and wildlife in the Southern Bahia, Brazil. Pesqui Veterinária Bras. 2022 Jul 8;42:1–6. [cited 2022 Jul 16]. http://www.scielo.br/j/pvb/a/w3YS9KC4RCmjgTGhDtphg5P/abstract/?lang=en.10.1590/1678-5150-pvb-6940Search in Google Scholar
[50] Vanak AT, Gompper ME. Interference competition at the landscape level: the effect of free-ranging dogs on a native mesocarnivore. J Appl Ecol. 2010;47(6):1225–32.10.1111/j.1365-2664.2010.01870.xSearch in Google Scholar
[51] Atickem A, Bekele A, Williams SD. Competition between domestic dogs and Ethiopian wolf (Canis simensis) in the Bale Mountains National Park, Ethiopia. Afr J Ecol. 2010;48(2):401–7.10.1111/j.1365-2028.2009.01126.xSearch in Google Scholar
[52] Gottelli D, Sillero-Zubiri C, Applebaum GD, Roy MS, Girman DJ, Garcia-Moreno J, et al. Molecular genetics of the most endangered canid: the Ethiopian wolf Canis simensis. Mol Ecol. 1994 Aug;3(4):301–12.10.1111/j.1365-294X.1994.tb00070.xSearch in Google Scholar PubMed
[53] Leonard JA, Echegaray J, Randi E, Vilà C, Gompper M. Impact of hybridization with domestic dogs on the conservation of wild canids. Free-Ranging Dogs Wildl Conserv. 2013;170:170–85.10.1093/acprof:osobl/9780199663217.003.0007Search in Google Scholar
[54] Torres RT, Ferreira E, Rocha RG, Fonseca C. Hybridization between wolf and domestic dog: First evidence from an endangered population in central Portugal. Mamm Biol. 2017 Sep 1;86(1):70–4.10.1016/j.mambio.2017.05.001Search in Google Scholar
[55] Vanak AT, Thaker M, Gompper ME. Experimental examination of behavioural interactions between free-ranging wild and domestic canids. Behav Ecol Sociobiol. 2009 Dec 1;64(2):279–87.10.1007/s00265-009-0845-zSearch in Google Scholar
[56] Lacerda ACR, Tomas WM, Marinho-Filho J. Domestic dogs as an edge effect in the Brasília National Park, Brazil: interactions with native mammals. Anim Conserv. 2009;12(5):477–87.10.1111/j.1469-1795.2009.00277.xSearch in Google Scholar
[57] Grignolio S, Merli E, Bongi P, Ciuti S, Apollonio M. Effects of hunting with hounds on a non-target species living on the edge of a protected area. Biol Conserv. 2011 Jan 1;144(1):641–9.10.1016/j.biocon.2010.10.022Search in Google Scholar
[58] Silva-Rodríguez EA, Sieving KE. Influence of care of domestic carnivores on their predation on vertebrates. Conserv Biol J Soc Conserv Biol. 2011 Aug;25(4):808–15.10.1111/j.1523-1739.2011.01690.xSearch in Google Scholar PubMed
[59] Zapata-Ríos G, Branch LC. Mammalian carnivore occupancy is inversely related to presence of domestic dogs in the high Andes of Ecuador. PLoS One. 2018;13(2):e0192346.10.1371/journal.pone.0192346Search in Google Scholar PubMed PubMed Central
[60] Sheriff MJ, Krebs CJ, Boonstra R. The sensitive hare: Sublethal effects of predator stress on reproduction in snowshoe hares. J Anim Ecol. 2009;78(6):1249–58.10.1111/j.1365-2656.2009.01552.xSearch in Google Scholar PubMed
[61] Kruuk H, Snell H. Prey selection by feral dogs from a population of marine iguanas (Amblyrhynchus Cristatus). J Appl Ecol. 1981;18(1):197–204.10.2307/2402489Search in Google Scholar
[62] Hughes J, MacDonald D, Boitani L. Roaming free in the rural idyll: Dogs and their connections with wildlife. In: The domestic dog: Its evolution, behavior and interactions with people. Second Edn. Cambridge: Cambridge University Press; 2016. p. 369–84.10.1017/9781139161800.018Search in Google Scholar
[63] Zamora-Nasca LB, di Virgilio A, Lambertucci SA. Online survey suggests that dog attacks on wildlife affect many species and every ecoregion of Argentina. Biol Conserv. 2021 Apr 1;256:109041.10.1016/j.biocon.2021.109041Search in Google Scholar
[64] Doherty T, Dickman C, Glen A, Newsome T, Nimmo D, Ritchie E, et al. The global impacts of domestic dogs on threatened vertebrates. Biol Conserv. 2017 Jun 1;210:56–9.10.1016/j.biocon.2017.04.007Search in Google Scholar
[65] Marks BK, Duncan RS. Use of forest edges by free-ranging cats and dogs in an urban forest fragment. Southeast Nat. 2009;8(3):427–36.10.1656/058.008.0305Search in Google Scholar
[66] Martinez E, Cesário C, Silva IdeO, Boere V. Domestic dogs in rural area of fragmented Atlantic Forest: potential threats to wild animals. Ciênc Rural. 2013 Nov;43:1998–2003.10.1590/S0103-84782013001100013Search in Google Scholar
[67] Zapata-Ríos G. Dogs are more than wet kisses and tail wags: Domestic dogs as invasive species. Anim Conserv. 2018;21(4):287–8.10.1111/acv.12440Search in Google Scholar
[68] Sykes N, Beirne P, Horowitz A, Jones I, Kalof L, Karlsson E, et al. Humanity’s best friend: A dog-centric approach to addressing global challenges. Animals. 2020 Mar;10(3):502.10.3390/ani10030502Search in Google Scholar PubMed PubMed Central
[69] Kartal T, Rowan AN. Stray dog population management. In: Polak K, Kommedal AT, editors. Field manual for small animal medicine. John Wiley & Sons. 2018 [cited 2022 Jul 16]. p 15–29. (Chapter 2). 10.1002/9781119380528.ch2.Search in Google Scholar
[70] Conrad J, Norman J, Rodriguez A, Dennis PM, Arguedas R, Jimenez C, et al. Demographic and pathogens of domestic, free-roaming pets and the implications for wild carnivores and human health in the San Luis region of Costa Rica. Vet Sci. 2021 Apr;8(4):65.10.3390/vetsci8040065Search in Google Scholar PubMed PubMed Central
[71] León B, González SF, Solís LM, Ramírez-Cardoce M, Moreira-Soto A, Cordero-Solórzano JM, et al. Focus: Zoonotic disease: Rabies in Costa Rica – Next steps towards controlling bat-borne rabies after its elimination in dogs. Yale J Biol Med. 2021 Jun;94(2):311.Search in Google Scholar
[72] Hermes MS, Morales A, Bustamante A, Castro M. Wealth and distribution of medium and large mammals in San Lucas; Costa Rica: Universidad Nacional; 2006Search in Google Scholar
[73] Solano Gómez R. Caracterización de los conflictos humano-felinos y otras especies silvestres en el área de amortiguamiento de la Reserva Biológica Alberto Manuel Brenes, 2017-2020. Univ Costa Rica San José Costa Rica; 2020. [cited 2022 Jul 18]. https://www.kerwa.ucr.ac.cr/handle/10669/80912.Search in Google Scholar
[74] García Dobles S. Pasantía en manejo, diagnóstico y terapéutica de especies silvestres en el centro de rescate Toucan Rescue Ranch, San Isidro de Heredia, Costa Rica; 2022Search in Google Scholar
[75] Lindshield SM. Protecting nonhuman primates in peri-urban environments: A case study of neotropical monkeys, corridor ecology, and coastal economy in the caribe sur of costa rica. In: Waller MT, editor. Ethnoprimatology: Primate Conservation in the 21st Century [Internet]. Cham: Springer International Publishing; 2016 [cited 2022 Jul 16]. p. 351–69. (Developments in Primatology: Progress and Prospects) 10.1007/978-3-319-30469-4_19.Search in Google Scholar
[76] Montoya M. Notas históricas sobre la ornitología de la Isla del Coco, Costa Rica. Bresenia; 2007;68:37–57.Search in Google Scholar
[77] Fowler LE. Hatching success and nest predation in the Green Sea Turtle, Chelonia Mydas, at Tortuguero, Costa Rica. Ecology. 1979;60(5):946–55.10.2307/1936863Search in Google Scholar
[78] Sowa SM. Sea turtle patrols of playa preciosa, costa rica and marine mammal and sea turtle boat-based surveys of gulfo dulce, costa rica September to November 2016; 2016.Search in Google Scholar
[79] Cornhill CN. Depredation of olive ridley and loggerhead turtle clutches on beaches with and without predator managemnt; Master thesis. Purdue University Graduate School. 2021.Search in Google Scholar
[80] Guamán Burgos DS. Incidencia de depredadores en el éxito de eclosión de Lepidochelys olivacea en playas de Manabí; 2022 Apr [cited 2022 Jul 18]. http://repositorio.ug.edu.ec/handle/redug/60063Search in Google Scholar
[81] Gatti A, Gatti A, Seibert J, Moreira D, Pós-Graduação P, Biológicas C, et al. A predation event by free–Ranging dogs on the lowland tapir in the Brazilian Atlantic Forest. Anim Biodivers Conserv. 2018 Jan 1;412:311–4.10.32800/abc.2018.41.0311Search in Google Scholar
[82] Vaughan C, Ramírez O, Herrera G, Guries R. Spatial ecology and conservation of two sloth species in a cacao landscape in limón, Costa Rica. Biodivers Conserv. 2007 Jul 1;16(8):2293–310.10.1007/s10531-007-9191-5Search in Google Scholar
[83] Dünner C, Pastor G. Manual de manejo, medicina y rehabilitación de perezosos. Chile Fund Huálamo; 2017.Search in Google Scholar
[84] Helping Sloths By Helping Dogs [Internet]. The Sloth Conservation Foundation. [cited 2022 Aug 16]. https://slothconservation.org/helping-sloths-by-helping-dogs/Search in Google Scholar
[85] “I Want To Hold A Sloth”: Why You Should Never, Ever, Touch Sloths! [Internet]. Toucan Rescue Ranch. [cited 2022 Aug 16]. https://toucanrescueranch.org/i-want-to-hold-a-sloth-why-you-should-never-ever-touch-sloths/.Search in Google Scholar
[86] Oh My Dog! [Internet]. The Sloth Conservation Foundation. [cited 2022 Jul 18]. https://slothconservation.org/oh-my-dog/.Search in Google Scholar
[87] Deforestation Kills Sloths [Internet]. The Sloth Institute. 2021 [cited 2022 Aug 16]. https://www.theslothinstitute.org/2021/07/30/deforestation-kills-sloths/.Search in Google Scholar
[88] Two-toed Sloth [Internet]. Alturas Wildlife Sanctuary. 2022 [cited 2022 Aug 16]. https://www.alturaswildlifesanctuary.org/catalog/two-toed-sloth/.Search in Google Scholar
[89] Garcés-Restrepo MF, Pauli JN, Peery MZ. Natal dispersal of tree sloths in a human-dominated landscape: Implications for tropical biodiversity conservation. J Appl Ecol. 2018;55(5):2253–62.10.1111/1365-2664.13138Search in Google Scholar
[90] Mendel FC. Use of hands and feet of two-toed sloths (Choloepus hoffmanni) during climbing and terrestrial locomotion. J Mammal. 1981;62(2):413–21.10.2307/1380728Search in Google Scholar
[91] Alvarez SJ, Sanchez A, Carmona MM. Density, diet and habitat preference of the two-toed sloth Choloepus hoffmanni in an Andean Forest of Colombia. Final Rep Rufford Small Grant Nat Conserv Bogota Colômbia; 2004. p. 13.Search in Google Scholar
[92] Mendoza JE, Peery MZ, Gutiérrez GA, Herrera G, Pauli JN. Resource use by the two-toed sloth (Choloepus hoffmanni) and the three-toed sloth (Bradypus variegatus) differs in a shade-grown agro-ecosystem. J Trop Ecol. 2015 Jan;31(1):49–55.10.1017/S0266467414000583Search in Google Scholar
[93] Sánchez-Azofeifa GA, Harriss RC, Skole DL. Deforestation in Costa Rica: A quantitative analysis using remote sensing imagery 1. Biotropica. 2001;33(3):378–84.10.1111/j.1744-7429.2001.tb00192.xSearch in Google Scholar
[94] Stan K, Sanchez-Azofeifa A. Deforestation and secondary growth in Costa Rica along the path of development. Reg Env Change. 2019 Feb 1;19(2):587–97.10.1007/s10113-018-1432-5Search in Google Scholar
[95] Chiarello AG. Effects of fragmentation of the Atlantic forest on mammal communities in south-eastern Brazil. Biol Conserv. 1999;89(1):71–82.10.1016/S0006-3207(98)00130-XSearch in Google Scholar
[96] Chiarello AG, Chivers DJ, Bassi C, Maciel MAF, Moreira LS, Bazzalo M. A translocation experiment for the conservation of maned sloths, Bradypus torquatus (Xenarthra, Bradypodidae). Biol Conserv. 2004 Aug 1;118(4):421–30.10.1016/j.biocon.2003.09.019Search in Google Scholar
[97] Moreno S, Plese T. The illegal traffic in sloths and threats to their survival in Colombia. Edentata. 2006 May;2006(7):10–8.10.1896/1413-4411.7.1.10Search in Google Scholar
[98] Chiarello A. Sloth ecology: An overview of field studies.s. In Vizcaino SF, Loughry WJ, editors. The biology of the xenarthra. Gainesville: University Press of Florida; 2008. [cited 2022 Jul 16] p. 269–80.Search in Google Scholar
[99] Cliffe RN, Robinson CV, Whittaker BA, Kennedy SJ, Avey-Arroyo JA, Consuegra S, et al. Genetic divergence and evidence of human-mediated translocation of two-fingered sloths (Choloepus hoffmanni) in Costa Rica. Evol Appl. 2020;13(9):2439–48.10.1111/eva.13036Search in Google Scholar PubMed PubMed Central
[100] McNab BK. Energetics of arboreal folivores: physiological problems and ecological consequences of feeding on an ubiquitous food supply. In: Montgomery, GG, editor. The ecology of arboreal folivores. Washington, DC: Smithsonian Institution Press, 1978. [cited 2022 Jul 16] p. 153–62.Search in Google Scholar
[101] Sánchez-Chavez A, del P. Diet of Hoffmann’s two-toed sloth (Choloepus hoffmanni) in Andean forest. Mammalia. 2021 Nov 1;85(6):515–24.10.1515/mammalia-2021-0016Search in Google Scholar
[102] Garcés-Restrepo MF, Peery MZ, Pauli JN. The demography of a resource specialist in the tropics: Cecropia trees and the fitness of three-toed sloths. Proc R Soc B Biol Sci. 2019 Jan 16;286(1894):20182206.10.1098/rspb.2018.2206Search in Google Scholar PubMed PubMed Central
[103] Benítez-Malvido J, Martínez-Ramos M. Impact of forest fragmentation on understory plant species richness in Amazonia. Conserv Biol. 2003;17(2):389–400.10.1046/j.1523-1739.2003.01120.xSearch in Google Scholar
[104] Tabarelli M, Cardoso da Silva JM, Gascon C. Forest fragmentation, synergisms and the impoverishment of neotropical forests. Biodivers Conserv. 2004 Jun 1;13(7):1419–25.10.1023/B:BIOC.0000019398.36045.1bSearch in Google Scholar
[105] Montgomery GG, Sunquist ME. Impact of sloths on neotropical forest energy flow and nutrient cycling. In: Golley FB, Medina E, editors. Tropical Ecological Systems: Trends in Terrestrial and Aquatic Research [Internet]. Berlin, Heidelberg: Springer; 1975. p. 69–98 (Ecological Studies) [cited 2022 Jul 16] 10.1007/978-3-642-88533-4_7.Search in Google Scholar
[106] Montgomery G, Sunquist M. Habitat selection and use by two-toed and three-toed sloths; 1978.Search in Google Scholar
[107] Voirin B, Kays R, Wikelski M. Why do sloths poop on the ground? In: Lowman M, Devy S, Ganesh T, editors. Treetops at risk: Challenges of global canopy ecology and conservation. New York: Springer; 2013.10.1007/978-1-4614-7161-5_19Search in Google Scholar
[108] Voirin JB, Kays R, Lowman MD, Wikelski M. Evidence for three-toed sloth (Bradypus variegatus) predation by spectacled owl (Pulsatrix perspicillata). Edentata. 2009;2009(10):15–20.10.1896/020.010.0113Search in Google Scholar
[109] Bezerra BM, Barnett AA, Souto A, Jones G. Predation by the tayra on the common marmoset and the pale-throated three-toed sloth. J Ethol. 2008 Apr 22;27(1):91.10.1007/s10164-008-0090-3Search in Google Scholar
[110] Wayne RK. Cranial morphology of domestic and wild canids: The influence of development on morphological change. Evolution. 1986;40(2):243–61.10.2307/2408805Search in Google Scholar
[111] Lindner DL, Marretta SM, Pijanowski GJ, Johnson AL, Smith CW. Measurement of bite force in dogs: A pilot study. J Vet Dent. 1995 Jun 1;12(2):49–52.10.1177/089875649501200202Search in Google Scholar
[112] Holt DE, Griffin G. Bite wounds in dogs and cats. Vet Clin Small Anim Pract. 2000 May 1;30(3):669–79.10.1016/S0195-5616(00)50045-XSearch in Google Scholar
[113] Christiansen P, Adolfssen JS. Bite forces, canine strength and skull allometry in carnivores (Mammalia, Carnivora). J Zool. 2005 Jun;266(2):133–51.10.1017/S0952836905006643Search in Google Scholar
[114] Ellis JL, Thomason J, Kebreab E, Zubair K, France J. Cranial dimensions and forces of biting in the domestic dog. J Anat. 2009;214(3):362–73.10.1111/j.1469-7580.2008.01042.xSearch in Google Scholar PubMed PubMed Central
[115] Neal T, Key J. Principles of treatment of dog bite wounds. J Am Anim Hosp Assoc. 1976;12:657–60.Search in Google Scholar
[116] Pavletic MM, Trout NJ. Bullet, bite, and burn wounds in dogs and cats. Vet Clin Small Anim Pract. 2006 Jul 1;36(4):873–93.10.1016/j.cvsm.2006.02.005Search in Google Scholar PubMed
[117] McKiernan BC, Adams WM, Huse DC. Thoracic bite wounds and associated internal injury in 11 dogs and 1 cat. J Am Vet Med Assoc. 1984 Apr 15;184(8):959–64.Search in Google Scholar
[118] Swaim SF, Henderson RA, Pidgeon RS. Small animal wound management. Small Anim Wound Manag. 1990. [cited 2022 Jul 17]. http://www.cabdirect.org/cabdirect/abstract/19912219620.Search in Google Scholar
[119] Shamir MH, Leisner S, Klement E, Gonen E, Johnston DE. Dog bite wounds in dogs and cats: A retrospective study of 196 cases. J Vet Med Ser A. 2002;49(2):107–12.10.1046/j.1439-0442.2002.jv416.xSearch in Google Scholar PubMed
[120] Dolbeer RA, Holler NR, Hawthorne DW. Identification and assessment of wildlife damage: an overview. Handb Prev Control Wildl Damage. 1994;2:13.Search in Google Scholar
[121] Clarke M, Vandenberg N. Dog attack: the application of canine DNA profiling in forensic casework. Forensic Sci Med Pathol. 2010 Sep 1;6(3):151–7.10.1007/s12024-009-9114-8Search in Google Scholar PubMed
[122] Vogelnest L, Woods R. Medicine of Australian mammals. Victoria, Australia: Csiro Publishing; 2008.10.1071/9780643097971Search in Google Scholar
[123] Mullineaux E. Veterinary treatment and rehabilitation of indigenous wildlife. J Small Anim Pract. 2014;55(6):293–300.10.1111/jsap.12213Search in Google Scholar PubMed
[124] Mullineaux E, Keeble E. BSAVA manual of wildlife casualties. Quedgeley, UK: British Small Animal Veterinary Association; 2016.Search in Google Scholar
[125] Molony S, Baker P, Garland L, Cuthill I, Harris S. Factors that can be used to predict release rates for wildlife casualties. Anim Welf-POTTERS BAR THEN WHEATHAMPSTEAD-. 2007;16(3):361.10.1017/S0962728600027172Search in Google Scholar
[126] Mazet JAK, Hamilton GE, Dierauf LA. Educating veterinarians for careers in free-ranging wildlife medicine and ecosystem health. J Vet Med Educ. 2006 Sep;33(3):352–60.10.3138/jvme.33.3.352Search in Google Scholar PubMed
[127] Ryser-Degiorgis MP. Wildlife health investigations: Needs, challenges and recommendations. BMC Vet Res. 2013 Nov 4;9(1):223.10.1186/1746-6148-9-223Search in Google Scholar PubMed PubMed Central
[128] De Briynea N, Iatridoua D. Challenges seen with treatment of exotic pets in veterinary practice. AWSELVA J. 2016;1–19.Search in Google Scholar
[129] Visser M, Oster SC. The educated guess: Determining drug doses in exotic animals using evidence-based medicine. Vet Clin Exot Anim Pract. 2018 May 1;21(2):183–94.10.1016/j.cvex.2018.01.002Search in Google Scholar PubMed
[130] Gal A, CORA R, Tabaran F, Nagy AL, Catoi C. Canine bite-mark evidence in veterinary necropsy: Case studies featuring the bite-mark examination. Bull Univ Agric Sci Vet Med Cluj-Napoca Vet Med. 2019 Jun 12;76:93.10.15835/buasvmcn-vm:2018.0046Search in Google Scholar
[131] Hayssen V. Choloepus hoffmanni (Pilosa: Megalonychidae). Mamm Species. 2011;43(873):37–55.10.1644/873.1Search in Google Scholar
[132] Wislocki GB. Observations on the gross and microscopic anatomy of the sloths (Bradypus griseus griseus Gray and Choloepus hoffmanni Peters). J Morphol. 1928;46(2):317–97.10.1002/jmor.1050460202Search in Google Scholar
[133] Aiello A. Sloth hair: Unanswered questions. Evol Armadillos Sloths Vermilinguas. Washington: Smithsonian Institution Press; 1985.Search in Google Scholar
[134] Wujek DE, Cocuzza JM. Morphology of hair of two- and three- toed sloths (Edentata: Bradypodidae). Rev Biol Trop. 1986 Nov;34(2):243–6.Search in Google Scholar
[135] Goffart M. Function and Form in the Sloth. Vol. 34, Oxford: Pergamon Press; 1971.Search in Google Scholar
[136] Pauli JN, Mendoza JE, Steffan SA, Carey CC, Weimer PJ, Peery MZ. A syndrome of mutualism reinforces the lifestyle of a sloth. Proc R Soc B Biol Sci. 2014 Mar 7;281(1778):20133006.10.1098/rspb.2013.3006Search in Google Scholar PubMed PubMed Central
[137] Gilmore DP, Da Costa CP, Duarte DPF. Sloth biology: An update on their physiological ecology, behavior and role as vectors of arthropods and arboviruses. Braz J Med Biol Res. 2001 Jan;34:9–25.10.1590/S0100-879X2001000100002Search in Google Scholar
[138] Kaup M, Trull S, Hom EFY. On the move: Sloths and their epibionts as model mobile ecosystems. Biol Rev. 2021;96(6):2638–60.10.1111/brv.12773Search in Google Scholar PubMed PubMed Central
[139] Suutari M, Majaneva M, Fewer DP, Voirin B, Aiello A, Friedl T, et al. Molecular evidence for a diverse green algal community growing in the hair of sloths and a specific association with Trichophilus welckeri(Chlorophyta, Ulvophyceae). BMC Evol Biol. 2010 Mar 30;10(1):86.10.1186/1471-2148-10-86Search in Google Scholar PubMed PubMed Central
[140] Rojas-Gätjens D, Valverde-Madrigal KS, Rojas-Jimenez K, Pereira R, Avey-Arroyo J, Chavarría M. Antibiotic-producing Micrococcales govern the microbiome that inhabits the fur of two- and three-toed sloths. Environ Microbiol. [cited 2022 Jul 18] 2022. http://onlinelibrary.wiley.com/doi/abs/10.1111/1462-2920.16082.10.1111/1462-2920.16082Search in Google Scholar PubMed
[141] Scheepens ETF, Peeters ME, L’Eplattenier HF, Kirpensteijn J. Thoracic bite trauma in dogs: A comparison of clinical and radiological parameters with surgical results. J Small Anim Pract. 2006;47(12):721–6.10.1111/j.1748-5827.2006.00114.xSearch in Google Scholar PubMed
[142] Risselada M, de Rooster H, Taeymans O, van Bree H. Penetrating injuries in dogs and cats. Vet Comp Orthop Traumatol. 2008;21(5):434–9.10.3415/VCOT-07-02-0019Search in Google Scholar
[143] Klainbart S, Shipov A, Madhala O, Oron LD, Weingram T, Segev G, et al. Dog bite wounds in cats: A retrospective study of 72 cases. J Feline Med Surg. 2022 Feb 1;24(2):107–15.10.1177/1098612X211010735Search in Google Scholar PubMed
[144] Miller WH Jr, Griffin CE, Campbell KL. Muller and Kirk’s small animal dermatology. St. Louis, Missouri: Elsevier Health Science. 2012.Search in Google Scholar
[145] Scott DW. Feline dermatology 1900-1978: A monograph. J Am Anim Hosp Assoc. 1980;16(3):128.Search in Google Scholar
[146] Enders RK. Mammalian life histories from Barrow Colorado Island, Panama. Cambridge: Mass the museum; 1935.Search in Google Scholar
[147] Hill N, Tenney SM. Ventilatory responses to CO2 and hypoxia in the two-toes sloth (Choloepus hoffmanni). Respir Physiol. 1974 Dec;22(3):311–23.10.1016/0034-5687(74)90080-2Search in Google Scholar PubMed
[148] Naples VL. The superficial facial musculature in sloths and vermilinguas (anteaters). Evol Ecol Armadillos Sloths Vermilinguas. 1985;4:173–89.Search in Google Scholar
[149] Toole JF, Bullock TH. Neuromuscular responses of sloths. J Comp Neurol. 1973;149(2):259–70.10.1002/cne.901490209Search in Google Scholar PubMed
[150] Grand T. Adaptations of tissue and limb segments to facilitate moving and feeding in arboreal folivores. Ecol Arboreal Folivores. 1978;231:242.Search in Google Scholar
[151] Nyakatura JA, Fischer MS. Functional morphology of the muscular sling at the pectoral girdle in tree sloths: convergent morphological solutions to new functional demands? J Anat. 2011;219(3):360–74.10.1111/j.1469-7580.2011.01394.xSearch in Google Scholar PubMed PubMed Central
[152] Olson RA, Glenn ZD, Cliffe RN, Butcher MT. Architectural Properties of Sloth Forelimb Muscles (Pilosa: Bradypodidae). J Mamm Evol. 2018 Dec 1;25(4):573–88.10.1007/s10914-017-9411-zSearch in Google Scholar
[153] Gorvet MA, Wakeling JM, Morgan DM, Hidalgo Segura D, Avey-Arroyo J, Butcher MT. Keep calm and hang on: EMG activation in the forelimb musculature of three-toed sloths (Bradypus variegatus). J Exp Biol. 2020 Jul 27;223(14):jeb218370.10.1242/jeb.218370Search in Google Scholar PubMed
[154] Spainhower KB, Metz AK, Yusuf ARS, Johnson LE, Avey-Arroyo JA, Butcher MT. Coming to grips with life upside down: How myosin fiber type and metabolic properties of sloth hindlimb muscles contribute to suspensory function. J Comp Physiol B. 2021 Jan 1;191(1):207–24.10.1007/s00360-020-01325-xSearch in Google Scholar PubMed
[155] Mossor AM, Austin BL, Avey-Arroyo JA, Butcher MT. A horse of a different color?: Tensile strength and elasticity of sloth flexor tendons. Integr Org Biol. 2020 Jan 1;2(1):obaa032.10.1093/iob/obaa032Search in Google Scholar PubMed PubMed Central
[156] Mossor A, Young J, Butcher M. Does a suspensory lifestyle result in increased tensile strength?: Organ level material properties of sloth limb bones. J Exp Biol. 2022 Feb 10;225:1–12.10.1242/jeb.242866Search in Google Scholar PubMed
[157] Weston MA, Stankowich T. Dogs as agents of disturbance. In: Gompper ME, editor. Free-ranging dogs wildl conserv. Oxford: Oxford Academic; 2013. p. 94–113.10.1093/acprof:osobl/9780199663217.003.0004Search in Google Scholar
[158] Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J. Biodiversity hotspots for conservation priorities. Nature. 2000 Feb;403(6772):853–8.10.1038/35002501Search in Google Scholar PubMed
[159] Mittermeier RA, Turner WR, Larsen FW, Brooks TM, Gascon C. Global Biodiversity Conservation: The Critical Role of Hotspots. In: Zachos FE, Habel JC, editors. Biodiversity Hotspots: Distribution and Protection of Conservation Priority Areas [Internet]. Berlin, Heidelberg: Springer; 2011. p. 3–22. [cited 2022 Jul 18]. 10.1007/978-3-642-20992-5_1.Search in Google Scholar
[160] Gompper ME. Adding nuance to our understanding of dog–wildlife interactions and the need for management. Integr Comp Biol. 2021 Jul 1;61(1):93–102.10.1093/icb/icab049Search in Google Scholar PubMed
[161] Wittemyer G, Elsen P, Bean WT, Burton ACO, Brashares JS. Accelerated human population growth at protected area edges. Science. 2008 Jul 4;321(5885):123–6.10.1126/science.1158900Search in Google Scholar PubMed
[162] Chazdon RL, Holl KD, Milder J, Finegan B, Martinez Salinas A, Imbach PA, et al. Biodiversity conservation in human-modified landscapes of Mesoamerica: past, present and future. Programa Cambio Climático Cuencas PCCC; 2010.Search in Google Scholar
[163] Kim D, Sexton JO, Townshend JR. Accelerated deforestation in the humid tropics from the 1990s to the 2000s. Geophys Res Lett. 2015;42(9):3495–501.10.1002/2014GL062777Search in Google Scholar PubMed PubMed Central
[164] Muñoz P, García-Rodríguez A, Sandoval L, Muñoz P, García-Rodríguez A, Sandoval L. Urbanization, habitat extension and spatial pattern, threaten a Costa Rican endemic bird. Rev Biol Trop. 2021 Mar;69(1):170–80.10.15517/rbt.v69i1.41742Search in Google Scholar
[165] Sánchez-Azofeifa GA, Pfaff A, Robalino JA, Boomhower JP. Costa Rica’s payment for environmental services program: Intention, implementation, and impact. Conserv Biol. 2007;21(5):1165–73.10.1111/j.1523-1739.2007.00751.xSearch in Google Scholar PubMed
[166] Morse WC, Schedlbauer JL, Sesnie SE, Finegan B, Harvey CA, Hollenhorst SJ, et al. Consequences of environmental service payments for forest retention and recruitment in a Costa Rican biological corridor. Ecol Soc. 2009;14(1):1–20.10.5751/ES-02688-140123Search in Google Scholar
[167] Gonzalez-Maya JF, Víquez-R LR, Belant JL, Ceballos G. Effectiveness of protected areas for representing species and populations of terrestrial mammals in Costa Rica. PLoS One. 2015;10(5):e0124480.10.1371/journal.pone.0124480Search in Google Scholar PubMed PubMed Central
[168] Maria A, Acero JL, Aguilera AI, Lozano MG. Central America urbanization review: making cities work for Central America. Washington, DC: World Bank Publications; 2017.10.1596/978-1-4648-0985-9Search in Google Scholar
[169] Sanchez RV. Conservation strategies, protected areas, and ecotourism in Costa Rica. J Park Recreat Adm. 2018;36(3):115–28.Search in Google Scholar
[170] Tafoya KA, Brondizio ES, Johnson CE, Beck P, Wallace M, Quirós R, et al. Effectiveness of Costa Rica’s conservation portfolio to lower deforestation, protect primates, and increase community participation. Front Env Sci. 2020;8:212. [cited 2022 Jul 19]. https://www.frontiersin.org/articles/10.3389/fenvs.2020.580724.10.3389/fenvs.2020.580724Search in Google Scholar
[171] Ortiz DI, Piche-Ovares M, Romero-Vega LM, Wagman J, Troyo A. The impact of deforestation, urbanization, and changing land use patterns on the ecology of mosquito and tick-borne diseases in Central America. Insects. 2022 Jan;13(1):20.10.3390/insects13010020Search in Google Scholar PubMed PubMed Central
[172] Broadbent EN, Zambrano AMA, Dirzo R, Durham WH, Driscoll L, Gallagher P, et al. The effect of land use change and ecotourism on biodiversity: A case study of Manuel Antonio, Costa Rica, from 1985 to 2008. Landsc Ecol. 2012 May 1;27(5):731–44.10.1007/s10980-012-9722-7Search in Google Scholar
[173] Parsons AW, Bland C, Forrester T, Baker-Whatton MC, Schuttler SG, McShea WJ, et al. The ecological impact of humans and dogs on wildlife in protected areas in eastern North America. Biol Conserv. 2016 Nov 1;203:75–88.10.1016/j.biocon.2016.09.001Search in Google Scholar
[174] Heller NE, Zavaleta ES. Biodiversity management in the face of climate change: A review of 22 years of recommendations. Biol Conserv. 2009 Jan 1;142(1):14–32.10.1016/j.biocon.2008.10.006Search in Google Scholar
[175] Robbins K. The biodiversity paradigm shift: Adapting the endangered species act to climate change. Fordham Envtl L Rev. 2015;27:57.Search in Google Scholar
[176] Schneider TJ, Maguire GS, Whisson DA, Weston MA. Regulations fail to constrain dog space use in threatened species beach habitats. J Env Plan Manag. 2020 May 11;63(6):1022–36.10.1080/09640568.2019.1628012Search in Google Scholar
[177] Sepúlveda MA, Singer RS, Silva-Rodríguez E, Stowhas P, Pelican K. Domestic dogs in rural communities around protected areas: Conservation problem or conflict solution? PLoS One. 2014 Jan 20;9(1):e86152.10.1371/journal.pone.0086152Search in Google Scholar PubMed PubMed Central
[178] Carter SB. Establishing a framework to understand the regulation and control of dogs in urban environments: A case study of Melbourne, Australia. SpringerPlus. 2016 Jul 27;5(1):1190.10.1186/s40064-016-2843-8Search in Google Scholar PubMed PubMed Central
[179] Dalla Villa P, Kahn S, Stuardo L, Iannetti L, Di Nardo A, Serpell JA. Free-roaming dog control among OIE-member countries. Prev Vet Med. 2010 Oct 1;97(1):58–63.10.1016/j.prevetmed.2010.07.001Search in Google Scholar PubMed
[180] Smith LM, Hartmann S, Munteanu AM, Dalla Villa P, Quinnell RJ, Collins LM. The effectiveness of dog population management: A systematic review. Animals. 2019 Dec;9(12):1020.10.3390/ani9121020Search in Google Scholar PubMed PubMed Central
[181] Villatoro FJ, Naughton-Treves L, Sepúlveda MA, Stowhas P, Mardones FO, Silva-Rodríguez EA. When free-ranging dogs threaten wildlife: Public attitudes toward management strategies in Southern Chile. J Env Manage. 2019 Jan 1;229:67–75.10.1016/j.jenvman.2018.06.035Search in Google Scholar PubMed
[182] Beck AM. The biology of the human–animal bond. Anim Front. 2014;4(3):32–6.10.2527/af.2014-0019Search in Google Scholar
[183] Cunningham-Smith P, Emery K. Dogs and people: Exploring the human-dog connection. J Ethnobiol. 2020 Dec;40(4):409–13.10.2993/0278-0771-40.4.409Search in Google Scholar
[184] Hurt A, Smith DA. Conservation dogs. Canine Ergon Sci Work Dogs. Boca Raton: CRC Press; 2009. p. 175–94.10.1201/9781420079920.ch9Search in Google Scholar
[185] Hurt A, Guscio D, Tirmenstein DA, Richards N, Burch A, Marler M. Using search dogs for biological eradication programs—A tale about Dyer’s Woad (Isatis tinctoria L.); 2014.Search in Google Scholar
[186] Bennett EM, Hauser CE, Moore JL. Evaluating conservation dogs in the search for rare species. Conserv Biol. 2020;34(2):314–25.10.1111/cobi.13431Search in Google Scholar PubMed
[187] Musyoki C. Crop defense and coping strategies: Wildlife raids in Mahiga’B’village in Nyeri District, Kenya. Afr Study Monogr. 2014;35(1):19–40.Search in Google Scholar
[188] Woodroffe R, Frank LG, Lindsey PA, ole Ranah SMK, Romañach S. Livestock husbandry as a tool for carnivore conservation in Africa’s community rangelands: A case–control study. Vertebr Conserv Biodivers. 2007 Oct 27;5:419–34.10.1007/978-1-4020-6320-6_28Search in Google Scholar
[189] Wierzbowska IA, Hędrzak M, Popczyk B, Okarma H, Crooks KR. Predation of wildlife by free-ranging domestic dogs in Polish hunting grounds and potential competition with the grey wolf. Biol Conserv. 2016 Sep 1;201:1–9.10.1016/j.biocon.2016.06.016Search in Google Scholar
[190] Lindenmayer DB, Laurance WF. The ecology, distribution, conservation and management of large old trees. Biol Rev Camb Philos Soc. 2017 Aug;92(3):1434–58.10.1111/brv.12290Search in Google Scholar PubMed
[191] Pinho BX, Peres CA, Leal IR, Tabarelli M. Chapter Seven - Critical role and collapse of tropical mega-trees: A key global resource. In: Dumbrell AJ, Turner EC, Fayle TM, editors. Advances in Ecological Research. Academic Press; 2020 [cited 2022 Dec 10]. (Tropical Ecosystems in the 21st Century; vol. 62). p. 253–94. https://www.sciencedirect.com/science/article/pii/S006525042030009X.10.1016/bs.aecr.2020.01.009Search in Google Scholar
[192] Wilson R, Marsh H, Winter J. Importance of canopy connectivity for home range and movements of the rainforest arboreal ringtail possum (Hemibelideus lemuroides). Wildl Res. 2007 Jun 27;34:177–84.10.1071/WR06114Search in Google Scholar
[193] Trzyna T. Urban protected areas: Profiles and best practice guidelines (Best Practice Protected Area Guidelines Series No. 22). Gland Switz IUCN Recuperado Httpscmsdata Iucn.Search in Google Scholar
[194] Paschoal AMO, Massara RL, Bailey LL, Doherty PF, Santos PM, Paglia AP, et al. Anthropogenic disturbances drive domestic dog use of Atlantic forest protected areas. Trop Conserv Sci. 2020 Jan [cited 2022 Dec 10];11(1). http://bioone.org/journals/tropical-conservation-science/volume-11/issue-1/1940082918789833/Anthropogenic-Disturbances-Drive-Domestic-Dog-Use-of-Atlantic-Forest-Protected/10.1177/1940082918789833.full.10.1177/1940082918789833Search in Google Scholar
[195] Balbuena D, Alonso A, Panta M, Garcia A, Gregory T. Mitigating tropical forest fragmentation with natural and semi-artificial canopy bridges. Diversity. 2019 Apr;11(4):66.10.3390/d11040066Search in Google Scholar
[196] Cunneyworth PMK, Donaldson A, Onyancha F. Canopy bridges are an economical mitigation reducing the road barrier effect for three of four species of monkeys in Diani, Kenya. Folia Primatologica. 2022 Jun 28;93(3–6):217–34.10.1163/14219980-bja10002Search in Google Scholar
[197] Ow S, Chan S, Toh YH, Chan SH, Lakshminarayanan J, Jabbar S, et al. Bridging the gap: assessing the effectiveness of rope bridges for wildlife in Singapore. Folia Primatologica. 2022 Apr 21;1(aop):1–12.10.1163/14219980-20211110Search in Google Scholar
[198] Weston N, Goosem M, Marsh H, Cohen M, Wilson R. Using canopy bridges to link habitat for arboreal mammals: Successful trials in the Wet Tropics of Queensland. Aust Mammal. 2011 Jan 1;33:93–105.10.1071/AM11003Search in Google Scholar
[199] Birot H, Campera M, Imron MA, Nekaris K. Artificial canopy bridges improve connectivity in fragmented landscapes: The case of Javan slow lorises in an agroforest environment. Am J Primatology. 2020;82(4):e23076.10.1002/ajp.23076Search in Google Scholar PubMed
[200] Gregory T, Carrasco-Rueda F, Alonso A, Kolowski J, Deichmann JL. Natural canopy bridges effectively mitigate tropical forest fragmentation for arboreal mammals. Sci Rep. 2017 Jun 20;7:3892.10.1038/s41598-017-04112-xSearch in Google Scholar PubMed PubMed Central
[201] Chan BPL, Lo YFP, Hong XJ, Mak CF, Ma Z. First use of artificial canopy bridge by the world’s most critically endangered primate the Hainan gibbon Nomascus hainanus. Sci Rep. 2020 Oct 15;10(1):15176.10.1038/s41598-020-72641-zSearch in Google Scholar PubMed PubMed Central
[202] Teixeira FZ, Printes RC, Fagundes JCG, Alonso AC, Kindel A. Canopy bridges as road overpasses for wildlife in urban fragmented landscapes. Biota Neotropica. 2013;13(1):117.10.1590/S1676-06032013000100013Search in Google Scholar
[203] Flatt E, Basto A, Pinto C, Ortiz J, Navarro K, Reed N, et al. Arboreal wildlife bridges in the tropical rainforest of Costa Rica’s Osa Peninsula. Folia Primatol (Basel). 2022 Apr 21;93(3–6):419–35.10.1163/14219980-20211109Search in Google Scholar
[204] Narváez-Rivera GM, Lindshield SM. Assessing the importance of artificial canopy bridge design for Costa Rican monkeys in an experimental setting. Folia Primatol (Basel). 2022 Sep 6;93(3–6):397–417.10.1163/14219980-20211104Search in Google Scholar
[205] Laidlaw K, Broadbent E, Eby S, Laidlaw K, Broadbent E, Eby S. Effectiveness of aerial wildlife crossings: Do wildlife use rope bridges more than hazardous structures to cross roads? Rev Biol Trop. 2021 Sep;69(3):1138–48.10.15517/rbt.v69i3.47098Search in Google Scholar
[206] Villalobos-Hoffman R, Ewing JE, Mooring MS. Do Wildlife Crossings Mitigate the Roadkill Mortality of Tropical Mammals? A Case Study from Costa Rica. Diversity. 2022 Aug;14(8):665.10.3390/d14080665Search in Google Scholar
[207] Rosatte R Management of raccoons (Procyon lotor) in Ontario, Canada: do human intervention and disease have significant impact on raccoon populations? 2000.10.1515/mamm.2000.64.4.369Search in Google Scholar
[208] Janke N, Coe JB, Bernardo TM, Dewey CE, Stone EA. Pet owners’ and veterinarians’ perceptions of information exchange and clinical decision-making in companion animal practice. PLoS One. 2021 Feb 1;16(2):e0245632.10.1371/journal.pone.0245632Search in Google Scholar PubMed PubMed Central
[209] Latham CE, Morris A. Effects of formal training in communication skills on the ability of veterinary students to communicate with clients. Vet Rec. 2007 Feb 10;160(6):181–6.10.1136/vr.160.6.181Search in Google Scholar PubMed
[210] Deem S. The veterinarian’s role in conservation. J Am Vet Med Assoc. 2004 Nov 1;225:1033–4.10.2460/javma.2004.225.1033Search in Google Scholar PubMed
[211] Herten J, Meijboom F. Veterinary responsibilities within the one health framework. Food Ethics. 2019 Aug 1;3:109–23.10.3920/978-90-8686-869-8_43Search in Google Scholar
[212] Day MJ. One health: the importance of companion animal vector-borne diseases. Parasites Vectors. 2011 Dec;4(1):1–6.10.1186/1756-3305-4-49Search in Google Scholar PubMed PubMed Central
[213] Gibbs SEJ, Gibbs EPJ. The historical, present, and future role of veterinarians in One Health. Curr Top Microbiol Immunol. 2013;365:31–47.Search in Google Scholar
[214] David P, Rundle-Thiele S, Pang B, Knox K, Parkinson J, Hussenoeder F. Engaging the dog owner community in the design of an effective koala aversion program. Soc Mark Q. 2019 Mar 1;25(1):55–68.10.1177/1524500418821583Search in Google Scholar
[215] Rundle-Thiele S, Pang B, Knox K, David P, Parkinson J, Hussenoeder F. Generating new directions for reducing dog and koala interactions: A social marketing formative research study. Australas J Env Manag. 2019 Apr 3;26(2):173–87.10.1080/14486563.2019.1599740Search in Google Scholar
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