Synergistic Threats to Wild Fauna in Ecuador: Using a Novel Data Source to Estimate the Impacts of Trafficking and Human–Wildlife Conflict

Abstract

Wildlife trafficking and human–wildlife conflict are major causes of species decline. The illegal nature of wildlife trafficking makes it hard, and sometimes dangerous, to study. ‘Mansión Mascota’ is a veterinary clinic in Guayaquil, Ecuador, which, through agreement with the Ecuadorian Ministry of the Environment, receives confiscated wildlife for treatment. Mansión Mascota also receives injured and abandoned wildlife brought in by the authorities and the public. Between January 2018 and September 2022, the clinic received 3212 wild animals from ≥171 taxa, including mammals, birds, reptiles, and amphibians. Through the classification of records based on reported use, native distribution, and evidence of capture/pet keeping, we were able to classify 1127 animals of 68 species as subject to wildlife trafficking. Turtles were the most abundant group (69%). The majority of turtles (91%) and primates (80%) were of Amazonian origin, whereas 90% of psittacines and 97% of carnivores had potential coastal origins. Threatened and conservation-dependent species were common in the traffic. Furthermore, ≥955 animals of 106 species were brought to the clinic due to anthropogenic wildlife conflict. Trafficking, combined with the high number of injured animals, highlights the synergistic threats facing wildlife in Ecuador.

1. Introduction

Growing human populations are putting unsustainable demands on natural habitats worldwide, destroying ecosystems and driving many species towards extinction through unsustainable use [1,2,3]. The expansion of human populations also brings wildlife into direct contact with infrastructure and domestic animals, fragments habitats, increases incidence of crop raiding and perceived attacks on humans and domestic animals, and increases the opportunity for and incidence of hunting and wildlife trafficking [4,5,6,7,8]. This is most acutely seen in the tropics, where these synergistic threats are leading to the extirpation and extirpation of populations and species [9,10,11,12,13].

Hunting for subsistence and trade, both legal and illegal, is increasing [13,14,15,16]. Consequently, unsustainable harvest for trade and traffic represents a major driver of extinction for many species [17,18,19,20,21,22]. The negative effects of hunting on wildlife populations increase with proximity to human settlements, in rural areas where people rely on forest resources, and from where animals can be transported to city markets [12,13]. The value of the illegal wildlife trade has been estimated at between USD 7 and USD 23 billion per year, making wildlife crime one of the most lucrative illegal trades, often run through sophisticated, international and well-organized criminal networks seeking to exploit the high rewards and low risks of the trade [23,24,25]. Furthermore, depending on the measures used, wildlife trafficking could be seen as the most serious illegal trade in terms of its effect on society though disease transmission and socioeconomic impacts, particularly after the COVID-19 pandemic [26].

Precise data on the true scale of threats from the illegal wildlife trade and human–wildlife conflicts are scarce, although some databases do exist, such as that of the Convention on Internation Trade in Endangered Species (CITES); this focuses on cross-border/International trade, not that at the sub-national level. The necessarily clandestine and risk-filled nature of wildlife trafficking, and the local nature of many conflicts, makes gathering data difficult, and sometimes dangerous [27,28,29]. This lack of data hinders targeted actions to mitigate threats through action plans and national conservation strategies [30]. The lack of reliable record keeping by wildlife authorities has been documented in several countries [29,31,32,33]. Issues arise from the misidentification of species, incomplete data on the origin, number, state of, and final deposition of wildlife, as well as the lack of records of many incidences of mortality due to conflict and trafficking [32,34]. Furthermore, the synergistic effects of human–wildlife conflicts affecting species that are susceptible to wildlife trafficking is rarely documented. Primates, parrots, parakeets, turtles and carnivores such as felids have all been highlighted in studies on the illegal trade in Latin America [35,36].

Ecuador covers less than 0.1% of the earth’s surface, but harbours a significant portion of global species diversity, including approximately 15% of bird species [37], 6% of mammals [38], 8% of amphibians [39] and 4% of reptiles [40]. Ecuador also has the second highest proportion of threatened species in each terrestrial vertebrate group by country [41]. Notwithstanding the legal prohibition on the trade, hunting, transportation, and keeping of wild-caught wildlife as pets in Ecuador (Decreto No 1.529, and No 3.399—Ley Forestal Y De Conservacion De Areas Naturales Y Vida Silvestre and artículo 247—Código Orgánico Integral Penal), Scheffers, Oliveira, Lamb and Edwards [20] highlighted continental Ecuador as a global hotspot for wildlife trade and trafficking. A recent study included a list of 117 species that are subject to trafficking for bushmeat or the pet trade in Ecuador [42], but the true number is expected to be greater. Demand for wildlife leads to the transportation of animals to areas outside of their natural ranges, often to large urban centres and port cities, facilitating access to more lucrative national and international markets [12,13,17,31,43,44]. The coastal city of Guayaquil, on the country’s southern Pacific coast, is the most populous city in Ecuador and has grown considerably over the last 30 years, which, among other things, has led to increasing threats to wildlife and habitats through an increased incidence of human–wildlife conflict [45]. Given this rapid expansion of anthropogenic stressors, the impact of even low levels of hunting and traffic from coastal areas could have drastic impacts on species.

Finding new sources of data on wildlife trafficking, and the effect of human–wildlife conflicts (defined as any anthropogenic activity or infrastructure which negatively effects wildlife, either intentionally or passively) in general, is paramount if we are to fully understand their impact. Studies based on market surveys and seizure data (wildlife trafficking), road censuses (roadkill), and the publication of incidental reports (electrocution, poisoning) are available for some countries and/or taxa, but only provide partial data [6,31,46,47]. Records from veterinary practices providing wildlife healthcare represent underexploited resources for data that could provide valuable information about the anthropogenic pressures faced by wildlife, and their direct impact on health and welfare [48,49,50,51]. These practices often admit wildlife seized by government authorities, as well as injured wildlife found and handed in by the general public, providing a snapshot of the threats to wildlife in a given area, the diversity of species affected, and the numbers of animals involved.

We used data from a veterinary clinic, ‘Mansión Mascota’, in Guayaquil to gain insight on the combined effects of wildlife trafficking/pet keeping and human–wildlife conflict in coastal Ecuador and nationally. Mansión Mascota is a private practice supported by Proyecto Sacha (www.proyectosacha.org), which, through agreement with the Ecuadorian Ministry of the Environment, receives wildlife for medical assessment, treatment, relocation, and possible release [52]. Here, we analyze data on wildlife brought to this practice over an almost 5-year period to determine trends in diversity, conservation status, threats, and the approximate geographic area of origin of affected animals. This was performed to aid conservation planning and actions through the provision of data on wildlife trafficking and human–wildlife conflict in Ecuador and regionally, and to highlight the extent of these threats, as well as to demonstrate the usefulness of novel data sources.

2. Materials and Methods

2.1. Data Collection

We used data on wildlife brought to the Mansión Mascota veterinary practice in Guayaquil, Guayas province, Ecuador. As well as receiving animals from the authorities, the practice also receives pets and injured wildlife brought in by the public. Data were provided by the clinic covering the period from January 2018 to September 2022, and a database built using information taken directly from each animal’s admission form. The data collected included the following: the animals’ taxonomic identification, geographic origin, declared reason of admission, referral institution, clinical cause of admission, and final disposition (

Table 1. Categorization and completeness of data obtained from Mansión Mascota’s wildlife admission forms.

Variable	Categories	Description	Missing Data
Case identification	Arrival date		0%
	File number
Taxonomic identification	Class	Taxonomic identification (Latin name) to the most precise level possible, cross-referenced with common name in Spanish [38,51,52,53].	2% (N = 64) data
	Order
	Family
	Genus
	Species
Geographic origin	Province	Location where the animal was originally received by the authorities or found by civilians.	0%
	City
	Locality
Declared reason of admission	Confiscated	Animals seized by authorities and pets retained due to illegal possession.	26% (N = 841)
	Found	Animals declared as abandoned or found.
	Surrendered	Animal declared rescued or voluntarily surrendered.
	Injured	Animal hit on a road, electrocuted, shot, or otherwise injured.
	Transferred	Animal examined by request of government authorities during their transfer or release.
Referral institution	Civilian	Animal was brought by a person not affiliated to any institution.	0%
	Environmental police
	Guayaquil municipality
	Ministry of Environment, Water, and Ecology
	Other	Includes: firefighters, Police, Army, Ministry of Interior, Ministry of Fisheries, and Guayaquil Park officers.
Clinical cause of admission	Various	Examples: “Debilitated, emaciated, eating only bananas since it was bought”. “Multiple wounds caused by stones thrown by children”. “Stunned, found on the floor next to a window”. “Broken bone”. “Dead mother, in need of critical paediatric care”.	34% (N = 1088)
Final disposition	Death	Includes: received dead, died under medical care, and euthanized.	0%
	Release	Animal released from Mansión Mascota to natural habitat.
	Transfer	Animal released from Mansión Mascota to a captive facility for custody, rehabilitation, or permanent captivity.

). There is no national standardization of registration forms or categories for clinical records in Ecuador. As such, the clinical data were adapted to the international standards put forward by the US National Wildlife Rehabilitation Association (NWRA) and the International Wildlife Rehabilitation Council (IWRC) [53,54].

Efforts to correctly identify species were made in situ by RV during visits to the clinic. In some cases, we could identify animals to the sub-specific level, but as this was not possible in all cases, we analyzed data to the species level only, except where sub-species are specifically mentioned. Using our corrected taxonomic identity for each animal, we assigned ‘global conservation status’ according to the IUCN Red List [41] and national conservation status for Ecuador following Tirira, et al. [38], Freile, et al. [55], and Carrillo, et al. [56]. Through an extensive search of online databases (bioweb, iNaturalist, eBird, the Reptile Database, and the IUCN Red List) and scientific papers, and by consultation with local specialists, we determined each species’ native distribution and categorized it as non-native and native to the country. For geographic analyses, the species’ distributions in Ecuador were broadly sub-divided between Coastal, Andean, and Amazonian distributions according to published distribution maps for each species. In the case of species with distributions that cover more than one region, we chose to be conservative and considered these as coastal in the analyses. Due to the peripheral Andean distribution of some testudines and primates, species in these groups with less than 10% of their natural distribution in the Andes were considered as either Amazonian or Coastal.

2.2. Data Analysis

From our database, we calculated the number of individuals per species and the species diversity and evaluated two main threats to wildlife: (1) wildlife trafficking and illegal pet keeping, and (2) human–wildlife conflict. We further explored the welfare and survival of animals received at the clinic and final disposition. We estimated the frequency of admissions in the overall dataset, according to the declared reason for admission, and by referral institution. We evaluated the completeness of the sample and estimated the number of species received at the clinic due to anthropogenic causes through a species accumulation curve using the abundance-based Chao estimator after 100 random permutations in the R package ‘vegan’ version 2 [57]. All data categorization, analysis, and visualization was conducted in R version 4.3.1 [58].

We compiled a list of previously known ‘Wildlife Species Subject to Traffic’ (WSST, from the Spanish ‘Especies Silvestres Sujetas a Tráfico de Fauna’) based on published data from the Ecuadorian Ministry of Environment, which identifies 117 species as known to be trafficked in the country [42]. We added nine primate species reported to be trafficked by Tirira [59] and seven bird species reported to be trafficked by Crespo-Gascón, et al. [60] but not included in government data to this WSST list [42]. As not all traffic events in our dataset were explicitly declared or recognized on admission forms, we examined the database, creating an expanded list (hereinafter WSST+), inferring the incidence of wildlife trafficking in the following cases: (1) native species whose admission forms explicitly gave evidence that they were victims of trafficking in some form (e.g., kept as pet, offered for sale, seized), (2) cases not explicitly recorded as traffic, but involving species whose native distributions do not include the Guayas province or the province where they were received by the authorities, suggesting that they had to have been trafficked at some point to have been found outside of their natural distribution range (for example, species non-native to Ecuador, or native Ecuadorian species naturally restricted to the Amazon or the Andes that could not have reached the geographic area from which they arrived to the clinic without being transported by people, with trafficking implicit in this case as wildlife transport is illegal in the country), and (3) animals found in circumstances that suggest they were hunted to be kept in captivity (for example, baby monkeys which could not have survived on their own in the wild or carnivores being fed, or animals with evidence of being tied, chained, collared or otherwise held captive by people). We generally employed a conservative estimate of geographic origin, meaning that species with native distributions that included the Ecuadorian coast as well as Andean or Amazonian distributions were not considered trafficked by distribution, even though this was a possibility; hence, our results for some taxa represent a minimum estimate of trafficking.

To evaluate the impact of human–wildlife conflict on wildlife, we reviewed the records of animals needing medical attention due to negative interactions with people, infrastructure, or domestic animals. Based on reports in the dataset, we defined six types of negative interaction: (1) human interference with nesting and nursing, (2) wildlife impacted by buildings/infrastructure, (3) vehicle impact, (4) human and/or domestic animal attack, (5) electrocution, and (6) fire. For each type of interaction, we identified the main impacts on animal health and welfare, and estimated the mortality rates. Our estimates of mortality rates represent a minimum of the true number, as animals found dead are rarely brought to the clinic. We further assessed the impact of these interactions against our expanded list of WSST+ species as synergistic threats.

To determine areas with high incidences of trafficking and human–wildlife conflict, we mapped source localities when data were available in the admissions records. Mapping was carried out in ArcGIS 10.8 [61]. We calculated the number of individuals received from each locality and determined the source localities for WSST+ species. We repeated this process separately for the orders carnivora, primate, testudines and psittaciformes. The Andean cordillera represents a physical and ecological barrier that separates the coast from the Amazon; therefore, we characterized primates and testudines as coastal or Amazonian according to their native geographic distribution (over 90% of coverage in one region) to further assess if these species are locally sourced or most likely transported across the Andes. A similar geographic analysis was not possible for other taxonomic groups.

3. Results

3.1. Overall Results

A total of 3212 individuals of at least 171 different species were admitted to the clinic in the 57 months between January 2018 and September 2022. Wildlife was brought to the clinic approximately every other day, with a median of two animals per day and 46 animals per month in an almost constant trend (Figure S1). July 2021 was an outlier in that 467 animals were received, which included 410 river turtles (Podocnemis expansa, Podocnemis unifilis, Kinosternon scorpioides, Chelydra acutirostris) brought to the clinic by wildlife authorities for evaluation prior to planned translocation and release. The species accumulation curve showed that there were probably more species impacted by human–wildlife conflict and trafficking than those recorded in our data set (Figure S2). The abundance-based Chao estimate indicated that ~232 species (SE = 21) may be affected within the area of influence of the clinic.

The majority of animals were brought to the clinic by government officers (environmental police 41%, Guayaquil municipality 19%, Ministry of Environment 14%, others 1%), and at least 25% were surrendered or brought for medical attention by civilians. Reasons for admittance to the clinic were recorded in 74% of the cases (Table 1). The most common reason that wildlife was brought to the clinic was reported as found/abandoned (21%, n = 675, 60 species), followed by surrendered by the owner (16%, n = 525, 103 species), needed attention for injuries (13%, n = 421, 87 species), and required medical examination during a pre-release transfer (18%, n = 584, 14 species); only 5% (n = 166, 45 species) were recorded as confiscated from traffic (Figure 1).

3.2. Trafficking and Illegal Pet Keeping

The clinical records of 246 animals (7.6% of all animalsin admissions records) from at least 51 species (29.8% of total diversity) included specific statements of wildlife trafficking and illegal pet keeping. Considering each species’ native distribution and details of the animals’ state upon reception, the estimated number of trafficked animals rose to 1127 (35.1% of all animals) from 68 species (39.8% of total diversity). This led to the identification of a further 26 species being trafficked that were not previously reported as trafficked in Ecuador [42,59,60]. We considered this expanded list as WSST+ in subsequent analyses. The species most commonly recorded as trafficked were the Pacific parrotlet (Forpus coelestis n = 42), the red-masked parakeet (Psittacara erythrogenys n = 19), and the blue-headed parrot (Pionus menstruus n = 17). Including all cases in our WSST+ list, Amazon river turtles (Podocnemis expansa n = 449, and Podocnemis unifilis n = 90) and mud turtles (Kinosternon leucostomum n = 122, Kinosternon scorpioides n = 115) were by far the most common (Table S1, Figure 2). Excluding turtle species involved in the mass transfer of trafficked animals by authorities prior to release, the most common species in our WSST+ list were the red-masked parakeet (Forpus coelestis n = 42), the South American Snapping turtle (Chelydra acutirostris n = 27), Humboldt’s squirrel monkey (Saimiri cassiquiarensis = 26) and the non-native Pond slider (Trachemys scripta n = 23).

The trafficked species in our records included many considered as threatened by the IUCN and under Ecuadorian Law. Among the animals recorded as victims of trafficking or illegal pet keeping, there were 41 animals from 9 species considered threatened on the IUCN Redlist, and 75 animals from 20 species protected under Ecuadorian Law. Including all species in our WSST+ list, the number of animals of threatened species on the IUCN Redlist and under Ecuadorian law was 125 animals from 15 species, and 691 animals from 21 species, respectively (Table S1). The South American river turtle (Podocnemis expansa) is considered Conservation Dependent (CD) by the IUCN and Critically Endangered (CR) under Ecuadorian law, and was the most commonly trafficked species. Three of the trafficked primate species are classified as Critically Endangered (CR) by the IUCN: the Ecuadorian mantled howler monkey (Alouatta palliata ssp. aequatorialis), the Ecuadorian white-fronted capuchin (Cebus aequatorialis), and the non-native cotton-top tamarin (Saguinus oedipus). In addition, the American crocodile (Crocodylus acutus) is considered CR under Ecuadorian law, and reported as trafficked. Another seven taxa, including the native Ecuadorian sub-species’ Amazona autumnalis, Bassaricyon medius, Kinosternon leucostomum, Lagothrix lagothricha ssp. lagothricha, Lagothrix lagothricha ssp. poeppigii, Odocoileus virginianus ssp. peruvianus, Rhinoclemmys melanosterna, and Tamandua mexicana are considered Endangered (EN) under Ecuadorian law and were trafficked (Table S1).

There were also ≥80 animals brought to the clinic and registered as “rescued” without precise details to determine if this meant rescued from trafficking or from a dangerous conflict situation. Records of 97 animals declared as “found on the ground” and “found immobile” lacked detail to ascertain if they corresponded to unadmitted illegal pet keeping, incidental findings of escaped pets, or animals affected by conflict.

3.3. Threats from Human—Wildlife Conflict

At least 955 wild animals of 106 species were brought to the clinic requiring medical attention as a result of negative interactions with humans, infrastructure, or domestic animals (Table S2). These included orphaned animals in need of nursing (n = 343) and animals with physical injuries (n = 329). The mortality rate for these animals was 47%. The species most frequently affected were the common opossum (Didelphis marsupialis n = 261), the fulvous whistling duck (Dendrocygna bicolor n = 90), the Peruvian pygmy owl (Glaucidum peruanum n = 45), the common barn owl (Tyto alba n = 16), the common green iguana (Iguana Iguana n = 14), all of IUCN Least Concern, and the Central American boa (Boa imperator n = 30), considered vulnerable. Another 86 individuals arrived severely injured (deep wounds, broken bones, member amputation, and necrosis), but the causes of their injuries were not recorded (Table S2).

3.4. Synergistic Threats to Trafficked Species

Fifty-eight species, representing 43% of the 136 native species previously reported as WSST [42,59,60], were received at Mansión Mascota between 2018 and 2022. Considering all species on our WSST+ list, 66% (n = 2121) of animals received at the clinic belong to species affected by trafficking. Of these, we found that 33 species previously reported as WSST and 10 species identified as WSST+ were impacted by other negative interactions with humans, infrastructure or domestic animals, resulting in synergistic threats of human origin. This synergy most heavily affected ducks (order Anseriformes, n = 90), boas and iguanas (order Squamata n = 71), carnivores (order Carnivora, n = 55), and raptors (orders Strigiformes, n = 45; Accipitriformes, n = 20; and Falconiformes, n = 2). Other WSST+ species that were frequently admitted were sloths and anteaters (order Pilosa, n = 65), rodents (order Rodentia, n = 53), doves and pigeons (order Columbiformes, n = 47), passerines (order Passeriformes, n = 23), and caimans (order Crocodilia, n = 16), but their admission forms lacked enough detail to infer the specific reasons for admittance (Figure 3).

Many globally threatened species on our WSST+ list were also affected by other human–wildlife conflicts; these included C. aequatorialis (Critically Endangered, CR), A. p. ssp. aequatorialis (CR), and the nationally threatened species Podocnemis expansa (CR), Bassaricyon medius (Endangered, EN), Kinosternon leucostomum (EN), Crocodylus acutus (CR), and Tamandua mexicana (EN). Other species listed as threatened under Ecuadorian Law, namely Amazona lilacina (CR), Falco peregrinus (EN) and Lampropeltis micropholis (EN), were similarly affected by human–wildlife conflict, but not included in the trafficking cases documented in this study.

Some individual animals in our dataset were simultaneously affected by traffic and human–wildlife conflict; for example, one presumedly escaped pet, an Ecuadorian white-fronted capuchin (C. aequatorialis), needed to be removed from the interior of a commercial building in Guayaquil; in addition, an escaped or illegally kept indigo bunting (Passerina cyanea) was attacked by domestic pets, and there were cases of escaped or abandoned Amazonian turtles (P. expansa, P. unifilis, and C. denticulata) found on roads in Guayaquil.

3.5. Geographic Analysis of WSST+ Species Origin

Two percent of animals received at the clinic could not be identified to the species level and as such their natural distributions could not be determined. Non-native species represented ≥1.2% of the animals received at the clinic. Regarding the native species received at the clinic, wildlife was brought from 12 of Ecuador’s 24 provinces, with Guayas province and the city of Guayaquil, within Guayas, by far the most common source (66%) (Figure 4). Wildlife was received from ≥60 specific localities (Figure 4A). At least 76% percent of the native fauna admitted to the clinic have natural distributions that include the coastal region, 24% have predominantly Amazonaian distributions (including some species with partial, <10%, Andean distributions), <1% are restricted to the Andes, and <1% are restricted to the Galapagos islands.

Among the WSST+, 73.9% of testudines and 63.6% of primates were of Amazonian origin, whereas 92.3% of the psittacines (parakeets, parrots, and macaws) and 99.2% of the carnivores could have originated from the Coastal region (Figure 4B,E). The source localities of the coastal primates (n = 28; Alouatta paliatta ssp. aequatorialis and Cebus aequatorialis) were diverse (15 localities, 4 provinces), but with 82.1% of them coming from Guayas province and 42.8% from Guayaquil itself; meanwhile, Amazonian primates were less disperse (n = 49; 9 localities, 3 provinces), with 91.8% from Guayas province and 71.4% from Guayaquil (Figure 4B). The species richness of the coastal and Amazonian testudines was similar, but coastal turtles were received from a more restricted area (10 localities, 5 provinces) than Amazonian turtles (15 localities, 3 provinces) (Figure 4C). It is important to note that about two thirds of the coastal primates and testudines received at the practice were not documented as being trafficked. Carnivores were the only group whose localities were evenly distributed and did not cluster in Guayaquil (34 localities, 7 provinces) (Figure 4D).

3.6. Final Disposition of Wildlife Received at the Clinic

At least 29% of the animals received at the clinic did not survive; 848 died due to sickness or injuries sustained prior to arrival, of which 100 had to be euthanized. A further 15% (n = 468) were placed in captive facilities, either for rehabilitation or permanent captivity, and 56% (n = 1796) were released back to their natural habitat.

Some animals were euthanized in cases of severe trauma, including mostly open fractures and severe tissue damage. Of the animals that were dead upon arrival or died while receiving medical attention, 24% (n = 204) arrived wounded or with severe trauma, 19% (n = 164) were orphaned animals in need of nursing, and 3% (n = 23) presented infections, myasis, or severe dehydration. Some of these clinical conditions were overlapping (e.g., orphaned animals with trauma or infected wounds).

Released animals included those brought for medical checks during their transfer (30%, n = 538), animals that successfully recovered from their injuries (10%, n = 187), and orphaned animals that received pediatric care (9%, n = 157). Other released animals were those native species found, surrendered, or confiscated in good condition and those that were not injured or sick.

4. Discussion

The use of novel data sources can provide important information when other sources are unreliable or scarce. Precise data on the true scale of threats from the illegal wildlife trade and human–wildlife conflicts are limited [22]. Comprehensive databases rarely exist for wildlife trafficking, and many animals recovered from traffic streams are often recorded as ‘found’ or ‘source unknown’ in existing databases for reasons ranging from the lack of importance given to small-scale trafficking and pet keeping, reticence on the part of authorities to employ legal punishments in cases of impoverished offenders, to the want to reduce workload or simple corruption [32]. In addition, trafficking studies based on traditional data sources (e.g., CITES; government records) often lack detail on the health and welfare impacts on trafficked animals, and/or their final placement. This scarcity and unreliability of official records makes systematically tackling these issues difficult [27,28,31,32,33]. We show that the use of veterinary practice records can provide important information about synergistic threats to wildlife and data on the diversity and number of wildlife in the illegal trade [46,49,62]. We found that a large number of the individual records in our data set were incomplete, missing detailed taxonomic identification and/or the reason for admission. Even so, we were able to clean and interpret the raw data provided to show more clearly the diversity and sources of animals received at Mansión Mascota. The numbers here should be treated as minimum estimates due to uncertainties in the reasons for admission. Species accumulation curves based on our conservative estimates predicted greater species diversity, and therefore a greater number of individual animals and species being affected. Many animals confiscated by the authorities, i.e., those in good health, or those found dead, i.e., roadkill, will in many cases not arrive at the clinic, thus further leading to an underestimation of the true number of animals affected. Furthermore, animals hunted for bushmeat consumption, such as red brocket deer (Mazama americana) or Hoffmann’s two-toed sloth (Choloepus hoffmanni), and those killed for other reasons, such as perceived pest control and crop-raiding, would fall out of the scope of the clinical records we evaluated [63,64].

The large number of wildlife admitted to the center may be atypical of veterinary practices in general, with the agreement between ‘Masion Mascota’ and the government authorities accounting for 75% of animals admitted. However, a quarter of animals were surrendered or brought in by the general public. The official government reports for Ecuador for 9 years between 2003 and 2014 (data for 2005, 2010 and 2012 not available) reported a total of 5135 live animals, across birds, mammals and reptiles, being seized nationally during this period, averaging 571/year [65,66,67], about double that which we found using our expanded estimate in this single clinic in Guayaquil [52]. The high diversity in origin and species, and the number of individual animals, indicates that Guayas province is a hotspot for illegal wildlife trafficking and human–wildlife conflict. Guayaquil is Ecuador’s largest city and nearly half of the country’s population live in the coastal region, increasing the market size for wildlife in this region. Additionally, Guayaquil being the country’s most important port (Handling ~90% of commercial flow adding to the national economy) makes it a node for international trafficking [68]. This is contrasted by official government reports that in 2014, the only year with available data, show a total of just 49 animals across birds, mammals and reptiles being seized live in Guayas [65].

When comparing records explicitly documented as traffic events with those for which traffic was inferred, our expanded estimate on trafficked wildlife received at the clinic is over 5 times as high in terms of individuals received and almost one and half times as high in terms of species diversity than that specifically reported in the clinical record sheets. This further suggests that a large amount of illegal pet keeping/trafficking is not being recorded as such. Studies from Peru have identified a similar trend, where there was an almost 50% dissimilarity between the species diversity identified in wildlife being sold in markets and those in confiscation records [31]. Similarly, the clinical records included specific statements of trafficking or pet keeping for many animals, but only those which were not recorded as confiscated. The most commonly trafficked species included turtles and tortoises, parrots, primates, and carnivores. Almost half of the species diversity previously listed as WSST in Ecuador [42,59,60] were received by the clinic (Table S1), and almost all of these were trafficked. Through our revision of clinical records and improved species identification and analysis of native distributions, we were able to identify an additional 26 species that have not previously been listed as subject to trafficking in Ecuador, again suggesting that official data underestimate the scale and severity of wildlife trafficking. Record keeping by wildlife authorities has been shown to be lax in previous studies in Peru and Latin America [32,33], which can lead to underestimates of the threat that hunting and trade pose to some animal groups. Only one third of the species we recorded as trafficked in Ecuador are listed as threatened by IUCN [41], and only one tenth are considered as threatened under Ecuadorian law, again suggesting that the pressures affecting the conservation of many Ecuadorian species are underestimated. It is also likely that many instances of local trafficking and pet keeping will focus on abundant species, i.e., those most likely to be encountered, which, combined with other threats, could lead to them being threatened in the near future.

In addition to having a higher population density, growth rate, and presence of infrastructure compared to Ecuador’s Amazonian region, the coast of Ecuador is an area of special interest for conservation activities due to its high levels of species endemicity, and the level of threat faced by species and habitats in proximity to such anthropogenic activities [69]. The admission frequency and mortality rates we documented illustrate the intensity of anthropogenic impacts on synanthropic wildlife on the Ecuadorian coast, and particularly Guayas and Guayaquil. Almost a third of records in our study were of wild animals brought to the clinic for medical attention as a result of negative interactions with people and anthropogenic infrastructure; there was also mortality in almost a third of the animals due to the injuries they sustained during contact or through necessary euthanasia. The condition in which animals arrive at rehabilitation centers influences the mortality and release rates of animals. High levels of mortality, often surpassing 50%, are commonly observed at triage, rescue and rehabilitation facilities worldwide [48,49,70,71,72].

Human–wildlife conflict may disproportionally affect species that are already a target of wildlife trafficking. Nearly two-thirds of animals received by the clinic corresponded to species in our WSST+ list. We found that 33 previously reported WSST and 10 species identified as WSST by our study are impacted by negative interactions with people or anthropogenic infrastructure, resulting in synergistic threats of human origin. This synergy affected a number of globally and nationally threatened species. As a notable example, the Critically Endangered Ecuadorian mantled howler (A. p. ssp. aequatorialis) and the Ecuadorian capuchin (C. aequatorialis) were among the three most frequently admitted primate species, surpassed only by Humboldt’s squirrel monkeys (S. cassiquiarensis), and reported both in events of trafficking and conflict. Considering the large number of localities from which these coastal species were retrieved, including areas outside of their natural distribution, it is unlikely that the frequency of their admission is biased by the location of the clinic within their native distributions, and suggests the intense human impact on these endemic species. It was not possible to estimate the number of animals affected by human–wildlife conflict after their escape or incidental release during trafficking, but it may not be a rare situation. The large number of animals brought in by concerned citizens demonstrates the positive attitude of local populations and highlights the role of the public in mitigating anthropogenic impacts, although this itself is not enough to compensate for the synergistic threats facing many species.

5. Conclusions

Conservation strategies must consider Guayaquil as a major commercial hub in Ecuador, and the pressure that this and other coastal cities adds to synanthropic fauna. The frequent reception of Amazonian species, especially primates and testudines, at a veterinary practice in Guayaquil highlights the active national-level trafficking. The local impact is also important, as all Critically Endangered species in our database have native distributions in Ecuador’s coastal regions. Cooperation between Ecuadorian authorities and civil society is crucial to counteract this situation. Currently, an alliance between Guayaquil airport’s security agency and the Wildlife Conservation Society aims to reinforce antitrafficking work in the air transport sector, including the specialized training of custom agents to better detect and document trafficking. Frequent confiscations as a result of counter-trafficking activities can lead to problems for animal placement, easily overcrowding rescue facilities or resulting in the application of unnecessary euthanasia. The continued successful collaboration between the environmental police, Guayaquil Municipality, and Proyecto Sacha at Mansión Mascota provides a valuable solution to dealing with confiscated and rescued wildlife. The availability of appropriate facilities and trained personnel for wildlife care is associated with a higher probability of post-rescue/confiscation survival after rescue [72], and facilitates faster recuperation by animals suitable for release. Further government support for the other, mainly private, rescue centers would similarly provide greater options for the reception and rehabilitation of injured animals and those seized from the illegal pet trade. Also, the development and full implementation of strategic action plans, such as the national Action Plan for the Conservation of Primates [73] and the Ecuador–Colombia Bi-National Strategy to Control Wildlife Traffic [74], will go a long way to reducing threats to species.

The implementation of habitat protection, restoration and in situ conservation efforts promoting habitat connectivity should be prioritized to reduce the incidence of injury and death in wildlife due to vehicle collision on roads and similar threats. As a priority, actions to counter the synergistic threats to wildlife, and particularly trafficked and threatened species, should be strategically intensified, taking into account the hotspots of trafficking and human–wildlife conflict particularly in and around major population centers such as Guayaquil and other coastal cities. Environmental awareness campaigns focused on target species are needed, as have been successfully employed in Ecuadorian communities already [75]. The illegal wildlife trade in and from Latin America receives comparatively little attention compared to that of other global regions; however, mounting evidence shows that these are also severe threats and deserve more international attention [76]. Considering the significant and continuing levels of habitat loss and fragmentation in Coastal Ecuador [77], and the other anthropogenic threats to fauna we highlight, the further hunting and trapping of animals could lead to species extirpation, as seen even in areas of abundant habitat [78,79].