The illegal trade in wildlife is driven by the high demand in national and international urban centers, making wildlife trafficking the third most lucrative criminal enterprise in Colombia, after the trade in weapons and drugs (CITES, 2005; Rodríguez and Echeverry, 2005). Together with the swift and pervasive destruction of tropical forests, this places many of the species reliant on these ecosystems in danger of extinction.
This report is based on our observations at the UNAU Foundation sloth rehabilitation center during its first five years of operation, from 2000 to 2005, in the city of Medellín. Here we show how independent pressures have combined to threaten the survival of sloths in Colombia.
Sloths of Colombia
Three species of sloths are known from Colombia (Wetzel, 1982). The brown-throated three-toed sloth, Bradypus variegatus (Schinz, 1825) inhabits both Pacific and Amazonian lowland rainforest and the Caribbean savanna dry forest (pers. obs.) (Fig. 1). Hoffman's two-toed sloth, Choloepus hoffmanni (Peters, 1859) is sympatric in the north with B. variegatus, sharing the Pacific rainforest and the Caribbean savanna dry forest, but is also found in Andean montane forest (pers. obs.). The southern two-toed sloth, Choloepus didactylus (Linnaeus, 1758) is sympatric in the south with B. variegatus, sharing the lowland Amazonian rainforest (Wetzel, 1982; Eisenberg, 1989; Emmons and Feer, 1999; Fonseca and Aguiar, 2004) but this species has been littlestudied in Colombia. The available habitat of these species is limited primarily by the extent of continuous canopy within natural forest (Montgomery and Sunquist, 1978).
Previous authors have assumed the distribution of B. variegatus to include nearly the entire lowland territory of Colombia (Wetzel, 1982; Eisenberg, 1989; Emmons and Feer, 1999; Fonseca and Aguiar, 2004). However, we have developed what we believe to be a more accurate and detailed assessment of its range, based on interviews with local hunters, government officials and other researchers, as well as personal observations and our efforts to track the origin of confiscated animals. Based on this information, we believe that variegated sloths are limited to some areas of the northern Caribbean region, certain localities in the inter-Andean valleys, and the Pacific and Amazonian regions. We have combined presence data from Anderson and Handley (2001) with our own unpublished data to produce a preliminary model of distribution using BIOCLIM (Busby, 1991) and DIVA-GIS (Hijmans, 2005) that we believe presents the probable current distribution of B. variegatus (Fig. 2).
C. hoffmanni has a wider distribution, ranging from the northern Caribbean coast to the south along the Pacific coast, as well as in the central Andean regions (Wetzel, 1982). In Colombia there are two distinct phenotypes of C. hoffmanni; one is found in lower, warmer areas below 1500 m, while the other is typical of higher and cooler zones between 1500 and 3000 m (Moreno, 2003b). These phenotypes may correspond to the subspecies C. h. capitalis and C. h. agustinus, respectively (Wetzel, 1982). C. didactylus has been reported from the Orinoco and Amazon regions (Wetzel, 1982; Eisenberg, 1989; Emmons and Feer, 1999), but this species has been little studied in Colombia.
Threats to Sloth Survival
Habitat destruction and fragmentation
As with too many tropical species, the greatest threat to the survival of sloths in Colombia is the destruction of their natural habitat (Chiarello, 1999). Owing to the constant expansion of ranching, agriculture and urban areas, over 100,000 ha of natural forest are destroyed every year in Colombia (IDEAM, 2004), with immense wildlife mortality as a direct result.
Sloths sometimes die in large numbers in incidents that go unreported by the media, and unnoticed or ignored by Colombian wildlife agencies and police.1 One such case was reported in the newspaper El Colombiano (Machado, 2002) in Necoclí, Department of Antioquia, where an estimated 600 B. variegatus were displaced by the destruction of their habitat, forcing them into open grassland and beaches where they suffered from starvation, dehydration and parasite infestation. People from the local communities took action to rescue the sloths on the beaches themselves, one by one, without assistance from the local authorities (R. Villarta, pers. comm.).
At the sloth rehabilitation center of the UNAU Foundation, we are often called to nearby semi-urban areas to rescue two-toed sloths (C. hoffmanni) that have been injured in a variety of ways — hit by cars, stoned by children, or suffering from electrical shocks — as well as others that appear to be dispersing from lost habitat. All these cases are ultimately related to the destruction of remnant patches of natural forests (Moreno, 2003a). We have not had rescue calls for the other two species of sloth; C. didactylus and B. variegatus do not naturally occur near the city of Medellín where the Foundation is located. We have had similar cases reported by veterinarians, however, and some individuals of these species have been sent to us from regions throughout the country.
In general, B. variegatus are more vulnerable than other sloths to habitat disruption. Their reduced mobility, small home range, and their more gregarious and diurnal habits make them more sensitive to forest loss, which may account for their disappearance from many regions of their former distribution. Unlike other arboreal mammals, a variegated sloth is likely to remain within a tree until it is cut down; this is because their instinctive reaction to a threat is to hold still rather than to flee (pers. obs.). Once on the ground, with no sheltering forest nearby, they are exposed to starvation, predators and hunting. The northern lowland rainforest and northern savannah dry forest have been widely cleared for pasture and croplands (IDEAM, 2004), seriously compromising the survival of B. variegatus in those areas. Only in the Pacific lowland rainforest are there still extensive reaches of continuous canopy.
Choloepus hoffmanni, on the other hand, has larger home ranges, is more mobile, nocturnal, solitary and aggressive, and is thus much more adaptable to habitat alteration. We have seen individuals in a diversity of habitats, frequently isolated and disturbed, such as small patches of secondary forest (less than 10 ha) near urban centers. We have also found them in patches of remnant tropical dry forest in the midst of cattle ranches. But C. hoffmanni shares the same forest habitat as B. variegatus, and so it is exposed to the same threats and alterations. Habitat loss and fragmentation affect the montane phenotype of C. hoffmanni in particular (IDEAM, 2004).
There is little published information on C. didactylus, but its distribution within Colombia follows the lowland rainforest of the upper Amazon basin (Fonseca and Aguiar, 2004), which so far has suffered comparatively little deforestation (IDEAM, 2004). Based on the extent of its remaining habitat, C. didactylus may be in the best situation of all the Colombian sloths.
Despite this flexibility, habitat fragmentation is a critical threat for all three species of sloths in Colombia. Their adaptations to an arboreal life make them exceptionally vulnerable when away from the trees, and open reaches of grassland, crops or urban infrastructure become insurmountable barriers for them. Small forest fragments are unlikely to contain viable populations due to the small genetic pool (Groom et al., 2005).
Illegal trade in sloths
Every year in Colombia, hundreds of young two-and three-toed sloths are taken from their mothers by poachers. Traffickers buy young sloths from children, who often take them from deforested areas. The mother sloths are often mistreated and sometimes killed for their meat. This is not limited to sloths alone; any wild animal that can be caught is also used, including monkeys (Alouatta, Ateles, Cebus and Saguinus), parrots (Aratinga, Pionus and Amazona), macaws (Ara) and other xenarthrans such as Tamandua and Cyclopes. Once taken from the forest, animals are brought to improvised shelters with inadequate housing, feeding and sanitary conditions, and are sold to Colombians traveling between the interior and the coast on vacation (Moreno, 2003a). The price of a young sloth starts at the local equivalent of US$30, but with a little bargaining one may be bought for less than US$5 (pers. obs.). Neither the sellers nor the buyers understand the nutritional and environmental needs of these animals, and so the stress of their capture and captivity ultimately leads to their deaths. This commerce is strictly illegal; although there are no laws in Colombia that give specific protection to sloths, all wildlife in the country is protected by a general law (Decreto 1608/1978) that prohibits the hunting, possession and traffic of Colombian wildlife.
This trade in sloths is not a new development, but the number of sloths sold on roadsides has risen in recent years. The security on national highways has improved significantly since 2003, bringing greater numbers of seasonal travelers — and hence creating greater opportunities for wildlife traffickers. Thanks in part to extensive educational efforts by the UNAU Foundation, local and national authorities have taken an increasing interest in the issues of sloth welfare, but the trade continues unabated. Sloths appear to be captured and sold mainly in the northern departments of Córdoba, Sucre, Bolívar, Atlántico and Magdalena (Fig. 3, Table 1) (Moreno and Plese, 2004). These departments are rich in natural resources — but they are also undergoing rapid transformation, with wetlands and forests converted for agriculture and cattle farming. A major highway, La Troncal del Norte, leads from the interior to the Caribbean coast, passing through the northern departments and serving as a conduit for potential buyers on vacation. Local authorities are unable to exert much control over the roadside sale of wildlife there, and many sloths change hands during the summer and winter holidays.
Departments of origin for young sloths arriving at the UNAU Foundation (March 2001–October 2004).
In 2004 in the city of Medellín alone — the second largest in the country — local police and wildlife agencies reported the confiscation of 256 mammals (Moreno et al., 2005). That same year, the UNAU Foundation received 102 sloths, of which 81 (79.4%) were B. variegatus and 21 (20.6%) were C. hoffmanni (Tables 2 and 3). Of these 102 rescued animals, about 70% were newborns or juveniles, with a body weight of less than 700 g. B. variegatus is the more appealing species for the wildlife trade; their docile nature and inherent charm, especially in infants and juveniles, make for easy sales to unwary buyers. C. didactylus is much less common in this trade; during the five years UNAU has been in operation, we have received only one individual — a juvenile rescued after its mother was killed by a car near the town of Florencia in the Amazon. The areas where C. didactylus are found are too remote and have too little tourism for traffic in this species to be common.
Number of sloths received at the UNAU Foundation sloth rehabilitation center in the first five years of its operation.
Total sloth mortality at the UNAU Foundation rehabilitation center during 2004.
To determine the departments where this traffic is most prevalent, we analyzed our records for the 274 sloths admitted to the UNAU Foundation between March 2001 and October 2004. Records without a known purchase site were not used. We also excluded records of adult individuals, as these animals come to the Foundation as result of accidents (road, electrocution) or other encounters. We sorted the remaining 61 records by department (Table 1).
The northern departments of Córdoba, Antioquia, Atlántico, Sucre, Bolívar and Magdalena are the source of 85% of the young sloths we have received, most of them victims of a chain of regular traffic. The remaining 15% come from departments of the interior. These are mostly C. hoffmanni, and according to testimonies, they were captured in chance encounters. Many of these sloths die unreported in private hands. Very few of them are given to zoos or a rehabilitation center such as UNAU.
Although the police may confiscate sloths at highway checkpoints, or in response to citizen complaints, most of those we have received were voluntarily surrendered by the buyers, concerned by their new pet's failing health — or by the trouble of keeping it alive. To some extent, buyers may also be moved by campaigns undertaken by wildlife agencies and the UNAU Foundation. Not surprisingly, the mortality of these sloths is high.
The annual increase in the number of individuals received at the center results from two factors: first, the consolidation of the rehabilitation center, and its increasing recognition by citizens and wildlife authorities; and second, the increase in the sale of sloths on the northern highways, as the improvements in overall security have brought more vacationers out on the roads.
Two factors strongly influence the success of the rehabilitation process. The first is the body weight of the animal upon arrival, which depends on its age. Mortality is very high (about 70%) for individuals weighing less than 700 g, which corresponds to their first five months of life. After this age, their chances for survival improve considerably, and older sloths show about 30% mortality (Table 4).
Sloth mortality by body weight during 2004.
The second determining factor is the physical condition of new arrivals, which is critical during their first 30 days at the rehabilitation center. Most of the mortality occurs during this period (Table 5), usually as a direct result of the treatment sloths received from poachers, salesmen and unsuspecting buyers. Before a sloth's arrival at the UNAU Foundation's rehabilitation center, it may have been in captivity for some 15 days, during which it was most likely malnourished and badly cared for. If the young sloth experiences a violent separation from its mother and is subsequently mistreated, it is in poor physical condition, often involving dehydration, starvation, trauma and disease.
Sloth mortality by time in rehabilitation during 2004.
A health survey of the 277 sloths treated by the UNAU Foundation showed that respiratory diseases, such as acute or chronic bronchopneumonia and lobar pneumonia, are by far the most common ailment, with 248 cases (90%) in total. Other illnesses include digestive problems such as diarrhea, constipation, tympanism and rumen paralysis, with 14 cases (5%); skin problems caused by fungus, bacteria (Staphylococcus aureus) and external parasites such as ticks, lice and mites (e.g., Demodex canis), with 8 cases (3%); and human-induced traumas such as nail mutilation, filed-down teeth, contusions, electric shock, burns and other wounds (5 cases; 2%). Nail polish is commonly used on sloths offered for sale: poachers use it to prevent young sloths, with their sharp nails and strong grip, from intimidating potential buyers. Other sellers will sometimes clip the nails instead of polishing them, with results as seen in Fig. 5a. C. hoffmanni have sharp, canine-like molars, and even very young individuals are able to bite down hard; thus poachers will sometimes file down the infants' teeth, with consequences that may eventually be fatal. Other generalized traumas are caused by improper confinement and careless maintenance by poachers and buyers alike.
Capture myopathy is a complex condition involving physiological and psychological factors generated by stressful handling (Kreeger et al., 2002). Infant and juvenile sloths suffer from immunodepression as a consequence of the trauma of early separation from the mother (Brieva et al., 2000). Often they will also develop digestive problems caused by an improper diet, especially infants that do not have a fully developed digestive system. There is no good substitute for a sloth mother's natural milk. Pulmonary problems may also arise, sometimes due to the inhalation of liquids into the lungs during artificial feeding. Other pulmonary difficulties may develop as well, both from overall stress and from their sudden change in climate — from the warm, lowland rainforests and savannas to the cooler Andean regions where most buyers live. Young sloths may also acquire respiratory ailments from close contact with humans.
The conservation status currently assigned to Colombian sloths by national and international authorities makes it difficult to enforce their protection. The most recognized authority, the IUCN Red List, classifies B. variegatus, C. hoffmanni and C. didactylus as LC – Least Concern (IUCN, 2006).
The Convention on International Trade in Endangered Species of Wild Flora and Fauna (CITES) lists B. variegatus in Appendix II and C. hoffmanni in Appendix III with no other restrictions, while no classification is given to C. didactylus (CITES, 2005). Appendix II includes species not necessarily threatened with extinction, but for which trade must be controlled in order to avoid uses incompatible with their survival. Appendix III contains species that are protected in at least one country and which has asked other CITES Parties for assistance in controlling the trade (CITES, 2005).
A report by the World Conservation Monitoring Centre of the United Nations Environment Programme (UNEP-WCMC) on the international trade in wildlife lists only six individuals of B. variegatus (1 body, 5 live) for the period 1995–1999, and provides no information on their origin (UNEP-WCMC, 2001). It should be noted, however, that UNEP-WCMC and CITES deal only with the international species trade, and do not address the issues of within-country wildlife commerce. We include them here to provide an international perspective on the traffic in sloths — and because conservation funds are often conditional on a species being listed by CITES.
A separate measure of conservation status, developed by the NGO NatureServe, lists B. variegatus as G5 (Secure) and both species of Choloepus as G4 (Apparently Secure) (InfoNatura, 2004). Information from all three threat classification systems is summarized in Table 6. None of the three sloth species is included on the List of Threatened Mammals of Colombia (Ministerio de Ambiente, 2005).
Sloth conservation status according to national and international listing authorities.
The international classifications of sloth conservation status are not representative of the local situation in Colombia. Other countries such as Bolivia, Costa Rica and Brazil face similar threats to their own sloth populations, and have ongoing rehabilitation programs for these species — indicating there is pressure on them as well.
The most recent distribution maps for the sloths, presented by Fonseca and Aguiar (2004), do not differ much from the maps provided by Wetzel (1982). These maps are generalized and do not represent the actual distribution of the three species in Colombia. For example, these sources indicate that B. variegatus is present throughout the territory of Colombia, in significant contrast with the preliminary results of our BIOCLIM model (Fig. 2).
Likewise, conservation assessments are sometimes based on isolated reports that may not always be representative of a species' ecology as a whole. Eisenberg and Thorington (1973) reported sloths to comprise as much as 40% of the biomass of mammals on Barro Colorado Island, and suggested that “Bradypus exists at the highest numerical density of any large, arboreal mammal” in the Neotropics. However, the situation at Barro Colorado Island is almost certainly different from conditions prevailing across the majority of the species' range. In addition, B. variegatus is sometimes gregarious, congregating in large numbers during mating seasons and at seasonal feeding grounds, giving a false impression of abundance (pers. obs.).
Thus we would caution researchers, conservationists and decision-makers on the danger of taking these generalizations too literally, as this may lead to unnoticed local extinctions. The current situation of sloths in Colombia may also hold true for other, less-noted species without organizations dedicated to their survival, such as the silky anteater (Cyclopes didactylus). At present there are very few organizations in Colombia, perhaps a dozen all told, which are working on the conservation of specific genera.
The Alexander von Humboldt Institute for the Investigation of Biological Resources (IAvH) is a public corporation, linked to the Colombian Ministry of the Environment, which tracks the threat status of all Colombian fauna. The IAvH lists 16 criteria for a species at risk of extinction (IAvH, 2005b). Six of these criteria, we believe, are applicable to Bradypus and Choloepus in Colombia:
Species whose populations are known to be declining;
Species with low population density;
Species with a reduced ability to disperse to new environments;
Species that are habitat specialists;
Species that suffer pressure from overexploitation; and
Species with close relatives extinct or currently threatened.
The Colombian Ministry of the Environment does not list any of these three sloth species as being of conservation concern (Table 6), probably because there are no long-term studies to demonstrate cause for concern. For Colombia and for the international community, sloths are not focal species because they are not listed as threatened or potentially threatened. There are no formal estimates of sloth densities in Colombia, and this would be the first step in order to present any estimates of the total population.
Funds for species protection are always scarce, and generally go to those species listed as high risk in IUCN categories, while those that are Least Concern or Data Deficient are largely ignored. This circle — in which Data Deficient species receive little attention, and lack of funding precludes new research — traps investigators in a frustrating situation, as they are witness to the worsening situation of many of these species, but are unable to address it themselves.
At a local level, the limited efforts by police and wildlife agencies to control the wildlife trade are of no substantial help. A report from the Procuraduría General de la Nación, the Colombian Attorney General's Office, denounces the lack of legal instruments to regulate the post-confiscation management of wildlife in Colombia, as well as insufficient infrastructure and the lack of reliable statistics on confiscation and illegal traffic (Rodríguez and Echeverry, 2005). This report points out that of 251,776 wild animals confiscated during the period 1996–2004, only 1,639 legal investigations were initiated. Of these, only 45 resulted in a fine, while 263 concluded with a lesser sanction.
Predictive models of species distribution, such as the one we have presented in Fig. 2, are based on easily accessed environmental data and detailed information on species localities (Phillips et al., 2006). These models can be powerful tools that should be used in species conservation assessments and to facilitate decision-making processes. Predictive models are not difficult to develop, and they can be done by researchers or NGOs with desktop computers running freeware or shareware. However, modeling also requires broadscale information, such as vegetation coverage or ecosystem type, that only government agencies have the resources to gather. Access to this information is often limited, and agreements between institutions are required to take fullest advantage of it.
Threat assessments should take into account the dangers to local populations, recognizing that many genetic, biological and ecological factors are still unknown, especially in the Neotropics. Biodiversity conservation may be most effective when efforts are focused on widespread umbrella species rather than on focal endangered species (Fleishman et al., 2000). This may be the situation with B. variegatus, which requires continuous forest canopy to survive; protecting this sloth would extend the same protection to many other species that share its rainforest habitat. Its wide distribution is an added benefit, since its range is continental in scope. Focal species, on the other hand, are generally endemic, limited to small regions and specific habitats. Concentrating efforts on the protection of focal species may create limitations on the overall conservation of biodiversity conservation, and the application of limited funds should be considered in this context.
 Colombian wildlife agencies are represented locally by “autonomous regional corporations” which have the responsibility of administering all natural resources except fish. There are 30 of these corporations throughout the country, working under the general guidelines established by the Environmental Ministry (Ministerio de Ambiente, Vivienda y Desarrollo Territorial).