Neotropical Primates: Field Studies and Conservation : Proceedings of a Symposium on the Distribution and Abundance of Neotropical Primates (1976)

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THE NONHUMAN PRIMATE TRADE IN COLOMBIA Ken M. Green INTRODUCTION During the past several years, parameters of the pri- mate trade have been discussed in detail (Cooper, 1968; Harrisson, 1971; Roth, 1969a,b; Thorington, 1972; Middleton et al., 1972). It is the purpose of this paper to supplement this information with descriptions of (1) the present internal primate supply chain as it exists in the northern coastal region of Colombia around Barranquilla, (2) the existing Colombian regu- lations and legislation concerning primates, (3) past and present primate population pressures, and (4) the feasibility of primate conservation and management within Colombia. The author collected this informa- tion while serving with a Peace Corps primate conser- vation project, working for the governmental agency INDERENA from September 1971 to May 1973. SUPPLY CHAIN Barranquilla and Leticia, Colombia, together with Iquitos, Peru, are the three major centers exporting South American primates (Figure 1). Only 1,800 km (1,100 miles), a 3-4 hour trip by air, separates Barran- quilla from Miami, the principal U.S. port of entry for neotropical fauna. Hence, most of the primates des- tined for export from the northern coastal area of Colombia leave via Barranquilla.* There are numerous sectors within this region from which monkeys are *Colombians refer to the area of the northern Colombian coast and up to 400-km inland as "coast." gathered (Figures 2 and 3). Yet, when received in Miami, the point of origin is known only as Barran- quilla. In reality, the particular primate may have been captured 450 km or more from Barranquilla and, in some cases, in the Amazon. One supply area is the Tiquisio region. I lived there in the town of Puerto Rico (Figure 2) for about a year and will describe the region and its primate trade. The physical terrain is characterized by low mountains between 300-1,000 m in altitude that begin the north- ern tip of the central cordillera of Colombia. This range joins the eastern and western cordillera to eventually form the single Andean chain in the southern part of the country. Climatic conditions throughout the northern coast are characterized by constant tropical heat with varia- tions related largely to altitudinal differences. Much of the region lies in the Magdalena River and Cauca River valleys and is affected by seasonal inundation. The rivers rise as much as 10 m during the rainy months, and the surrounding low-lying areas become flood- plains and swamps, which are only passable by canoe or motorboat. The major rainy season is from the end of September through December, with a shorter period during April, May, and June. Years ago, almost all of the Tiquisio area was covered by continuous evergreen primary tropical rain forest. Man, being the dominant exploiting species, moved into the area from the north to log, farm, and raise cattle. The Spaniards first settled Cocos, 15 miles south of Puerto Rico, over 150 years ago, to mine the area's gold deposits. Colorado, 19 km north of Puerto 85

86 GREEN FIGURE 1 Map of Colombia.

THE NONHUMAN PRIMATE TRADE IN COLOMBIA 87 ANTIOQUIA SANTANDER Okm. I Map of the Colombian Coastal Region 150km. I FIGURE 2 Map of the Colombian coastal region. MayMeru River 25 km (fool, mule) Noroli Majagual FIGURE 3 Supply chain for primates transported to Barran- quilla. Rico, was founded 80-100 years later. From these two villages, the populations expanded and dispersed to settle Puerto Rico 18-20 years ago. Today most of the hillsides are scarred from slash and burn agricultural practices that utilize the lower lands for cattle pasture and steeper slopes for rice and corn crops. Yet, most areas are still pocketed with parts of primary forest next to well-developed second- ary forest. The existing primary and secondary forest is able to support the following endemic platyrrhine species: Alouatta seniculus, Aotus trivirgatus, Ateles belzebuth hybridus, Cebus albifrons, Saguinus leucopus, and, in more restricted mountain localities, Lagothrix lagotricha. Monkeys are not collected systematically in the Tiquisio area. In contrast to reports in the Iquitos and

88 GREEN Leticia regions (Middleton et al., 1972), blowguns are not used, and neither box, drop, nor funnel trapping occurs. It is reported that Cebus are captured by mist-nets and fishnets. Cebus live in large social group- ings of 15-20 and are infamous as crop pests. Cam- pesinos (local inhabitants) are reported sometimes to surround the area where monkeys rest and sleep, to clear all trees until the monkeys are grouped in one or two trees, and to grab the desired monkeys when they attempt to escape. Common practices for collecting Ateles are to shoot an adult female carrying an infant or young juvenile and to collect the young animal when the mother falls to the ground. Very few people seem to eat monkey meat in the Tiquisio region, and thus a potential protein source for human consumption is wasted. A number of young juvenile Ateles, Alouatta, and Saguinus were caught by campesinos who were said to have climbed trees to catch them by hand. All these species, with the exception of Lagothrix, can be found within a kilometer of Puerto Rico. Woolly monkeys inhabit the higher cooler areas further south, southeast, and southwest at a minimum distance of 20 km from the village. The woolly monkey of this region has a greyish cast over a black undercoat and is a distinct variety from the brownish Amazon race. Recently, Cooper and Hernandez-Camacho (1976) reported that the woolly monkey, Lagothrix lago- tricha, of this region represents the northernmost range of the genus and has been hunted in these sectors. This report contrasts with an earlier report by Thorington (1972) that states, "Woolly monkeys, Lagothrix lago- tricha, are not found in the vicinity of Barranquilla." Most campesinos are engaged in subsistence farming, and only a select few work land located close enough to the village to enable them to return daily. Since the only means of transportation to other parts of the country is by water, most campesinos come into Puerto Rico, as well as other villages, on Sundays to sell their crops. The crops are transported on Mondays by riverboats to Magangue and El Banco. Thus the so-called trappers are in reality campesinos who col- lect monkeys when time permits (when neither work- ing their land nor fishing). Perhaps further supply fluctuations are due to the inaccessibility of the low- land regions when flooded during the rainy season. For example, during June and July 1972, the dry season was marked by severely dry weather resulting in the loss of rice and corn seedlings. It would be interesting to note if more time than usual is given to trapping when the next harvest months of September and October come. These factors contribute to the some- times small numbers of monkeys leaving certain regions. Handling of the captured animals varies little and is considered less than desirable or very poor. Most monkeys are kept in burlap sacks when transported to a village from the countryside. A small minority of the trappers transport monkeys in unscreened and un- wired bamboo crates, which allow more circulation of air. The traveled distances may be 5-30 km, at times half a day's journey by horseback. The majority of animals suffer from exposure to the tropical sun, food deprivation during the journey, and the shock of being separated from the mother. Mortality and morbidity is common under this stress. Depending on the location, certain monkeys may be kept at the campesino's farm anywhere from 2 to 6 days before they are brought into the village to be sold. Generally the trapper sells the monkey to a store merchant, who resells the monkey to persons who will eventually sell it to an animal dealer in Magangue. One animal dealer, who buys monkeys weekly from 10 to 12 trappers, travels directly to Barranquilla, bypassing Magangue. Also of interest is the fact that most monkeys leave the region on Mondays, the day that most weekly transportation goes upriver to Magangue. To further complicate matters, there may be one or two other resellings before a particular monkey finally reaches Magangue. The riverboat journey lasts from morning to evening but may be shortened to 7-8 hours in a motorized dugout. In outboard motorboats, travel time is de- creased to 4 hours, but few campesinos have access to this rapid means of transportation. Overall, the mon- key is once again exposed to a drastic change in environment upon arrival at the deposit. At this point, depending on circumstances, most animals have passed through two to four hands. Of the three present dealers in Magangue, one has been involved in the animal trade for 20 years, the second 15-16 years, and the third only 3-4 years. Therefore, these dealers have a preferred and some- times exclusive clientele. There are no restrictions, however, and occasionally a trader will visit all three dealers several times before selling. Thus, the Magan- gue animal dealer needs only a small amount of capital to function, since he rarely ventures out to obtain the animals. In addition to the Tiquisio area, the Magangue deposits receive monkeys that originate in the regions of the upper Cauca, San Jorge, and Magdalena rivers (Figures 2 and 3). Cebus capucinus (white-faced capuchin), Saguinus oedipus (cotton-top marmoset). and Ateles fusciceps (spider monkey) have a restricted geographical distribution along the west bank of the Magdalena River. These species are trapped in the vicinity of Sucre, Guaranada, and Majagual and at

THE NONHUMAN PRIMATE TRADE IN COLOMBIA 89 times sent to Magangue. Thus, Magangue supplies two species of capuchins, marmosets, and spider monkeys to Barranquilla. It should be noted at this point that confusion exists in the use of regional names of certain species (Table 1). For example, Cebus albifrons is commonly called "cariblanca" in Tiquisio, yet in Barranquilla this name refers to C. capucinus. Similarly Aleles sp. are known as "mica," which closely resembles "mico," another name for Cebus. The worst example is "mico negro," which refers lo Lagothrix, C. capucinus, and at times Ateles fusciceps (black spider monkey) coming from the Monteria region. As can be seen from this exam- ple, sectional records kept by persons referring to common name only must be scrutinized for such circumstances. Conditions in the Magangue depositories are similar in that none have screened-in cages, the majority of which are made from wood and wire mesh. Two compounds have cages raised off the floor that allow most feces to drop through. One of these has several well-built, large, metal and wire mesh cages, 4 ft3, which hold up to a dozen Aotus each. The third has smaller cages lying on a cement floor that were rather unsanitary when observed. All are sheltered from direct sunlight and protected from rain, under a roof, and seem to be sufficiently ventilated. Food provided for the monkeys ranges from well-matured and ripe "platano" (cooking banana), the local fruits when in season (papaya, guava, orange, and mango), and boiled milk. It is questionable to what extent the cages are cleaned after monkeys leave for Barranquilla, but it is doubtful that minimum suitable health conditions are met. One dealer has a small flamethrower with which he claims to sterilize cages, but I am skeptical of its frequency of usage. Monkeys usually remain in the dealer's compound 1-6 days. Since most animals arrive Monday evening, the dealers try to transport them by bulk to Barran- quilla on Tuesday, or whenever possible early in the week. Since Magangue is a large commercial riverport for this region of the Magdalena River, it is serviced by air, land, and water. There are daily DC-3 flights to Barranquilla (1 hour), regular bus departures to Bar- ranquilla via Cartagena, covering 300 km of mostly asphalt highway (8 hours), and slower river transporta- tion. One dealer regularly sends a shipment of Aotus in well-ventilated, double-screened, wooden boxes (the same type used to export monkeys overseas) on Tues- days to Barranquilla via Avianca, the local airline. The other dealers use various modifications of the wire mesh wooden boxes, which are extremely small and confining for the animals, or the universal burlap bag. Barranquilla has 20-25 commercial animal suppliers TABLE 1 Common Neotropical Primate Names Scientific Name Lagothrix lagotricha Pithecia monachus Saimiri sciureus Cebuella pygmaea Callimico goeldii Saguinus S. leucopus S. my s tax S. nigricollis S. oedipus Local Common Name Barrigudo, mico negro, mico churrusco Mico volador Mico fraile, titi, Vizcaino Mico pielroja, titi de bosillo Leoncito Titi Titi gris Bigote bianco Bebeleche Titi bianco English Common Name Alouatta sp. Cotudos. mono, mono rojo Howler monkey Aotus trivirgatus Mai ia. mico de noche. 6wl, night monkey, martica, marteja Douroucouli Ateles Marimonda, mica, mela Spider monkey A. helzebuth hybridus Marimonda gris. marimba Long-haired spider A. fusciceps Marimonda negro, mico negro Brown-headed spider A. geoffroyi Marimonda rojo Black-handed spider Cacajao rubicundus Mico ingles Red uakari Callicebus torquatus Zogui-zogui, mico socay Dusky titi C moloch Cebus Mico, cariblanca, capuchino, monito Capuchin, ringtail C. albifrons Cariblanca, mico bayo. mico maicero Cinnamon ringtail C. capucinus Cariblanca, mico negro White-faced ringtail C. apella Mico prego, mico azul Weeper capuchin Hooded capuchin Woolly monkey Monk saki Squirrel monkey Pygmy marmoset Goeldi's marmoset Tamarin, marmoset White-footed marmoset White-moustached marmoset White-lipped marmoset Cotton-top marmoset

90 GREEN that negotiate primates and receive monkeys from regions of Magangue, El Banco, Sincelejo, and Mon- teria. These regions all have several localities similar to Magangue from which monkeys are trapped. Thus, the monkeys that arrive in Barranquilla may come from an area over 450 km away (Figures 2 and 3). I visited these facilities and questioned the dealers con- cerning their operations. It was evident that the major- ity of these suppliers had no firsthand knowledge of monkey trapping and did not know the length of time from capture to delivery at the compounds. Obviously certain information was withheld, which is under- standable: but seemingly beyond the regions such as Magangue, the Barranquilla suppliers, without excep- tion, do not know the exact geographic locations or sources of their monkeys. Most of these animal dealers receive monkeys as well as other mammals, parrots, macaws, parakeets, snakes, and lizards daily. The animals come to Bar- ranquilla via air and land, depending on the client and locality. Animals coming from Magangue have been discussed above. C. capucinus and A. fusciceps come by way of Monteria, San Marcos, and Valledupar. The cotton-top marmoset (Saguinus oedipus) comes from San Marcos and Monteria, originating in the areas of Tierra Alta, San Pedro (Antioquia), and Caucasio. Conditions of these compounds are generally good or at least a step better than the sectional animal compounds of Magangue. Most have cement floors with drains, metal and wire mesh cages raised off the floor, well-ventilated and sheltered areas, and follow adequate husbandry practices. Crowding of monkeys was not evident, yet in one compound 10 A. fusciceps were kept in a large, walk-in, 5' x 3' x 3' cage together with two foxes. A second similar cage contained five infant Tamandua, seven Sciurus granatensis, two Saguinus oedipus, and one Ateles fusciceps. It was the exception to find screened walk-in units that had smaller screened and wired cages. Most suppliers feed their monkeys a basic diet of ripe platano and fruit, supplemented with rice and milk, bread, corn, or honey. Several said they added vitamins to the water, and one stated he added tetracycline. The majority of the animal suppliers export mon- keys to either the United States or other parts of the world, or both. Some specialize in dealing with supply- ing monkeys for biomedical and other scientific re- search. There are daily airline flights from Barranquilla to Miami. All monkeys are exported in double- screened, wooden crates, with sufficient ventilation, and have adequate waste disposal through the bottom of the box floor. During transport, most have water, and some suppliers even send bread with the animal as a food source for the longer journeys. LEGISLATION AND CONTROL INDERENA, (Instituto de Desarrollo de los Recursos Naturales Renovables, i.e., Institute for Development of Renewable Natural Resources) is the Colombian governmental agency responsible for protecting the country's natural resources. Operating under the Ministry of Agriculture, it consists of several units. One, Parks and Wildlife, regulates use, hunting, man- agement, transportation, and marketing of wildlife and their products. In addition, it concerns itself with biological studies, conservation, and repopulation of those species in danger of extinction. INDERENA has a national headquarters in Bogota, with six regional offices throughout the country. The coastal region's headquarters, located in Barranquilla, has jurisdiction over the departments of Atlantico, Bolivar, Cordoba, Magdalena, and Sucre (Figure 2). Each region contains several sectional offices, which in turn control several local offices, one of which is Magangue. INDERENA has inspectors or rangers who are responsible for enforcing the various regulations in each sectional office. Magangue has three inspectors who issue licenses, collect fees, and patrol for illegal and contraband skins and animals that they have authority to confiscate. All animals transported between any points in the country must have a "salvoconducto" (license to transport). Therefore, any monkey that is trapped must possess a salvoconducto if it is to be transported to Barranquilla. This salvoconducto contains data as to the type (scientific name never used), numbers, and monetary value of each monkey and may be obtained at the local office in Magangue. A small fee is collected, which supposedly becomes part of a "special INDERENA fund" (INDERENA, Resolution No. 564, 1970) for investigative wildlife studies. Another piece of legislation (INDERENA Acuerdo No. 18, 1970) states that commercial hunters should give 10 percent of their captured animals or the equivalent monetary value that includes capture, handling, and transpor- tation to INDERENA for purposes of repopulation. (INDERENA, Resolution No. 36, 1971). This is rarely, if ever, done. There are various problems of local administration that make it difficult, and at times impossible, for inspectors to enforce the laws. Three inspectors and one boat are far from enough to cover an area of jurisdiction that includes distances 100 km away. Sec- ondly, cultural practices, political pressures, and at times graft inhibit any real regulatory efficiency. Of particular interest are the regulations and laws pertaining to primates. Since 1941, 27 years before the existence of INDERENA, the Ministry of Agriculture

THE NONHUMAN PRIMATE TRADE IN COLOMBIA 91 had a law that prohibited hunting of deer and all classes of "pelo" (mammals) from March 1 to November 1 (Decreto No. 459 de 1951). In the past this law had not been enforced. Recently, the law has been utilized to enforce a closed trapping season for the hunting of primates. A salvoconducto, theoretically, can only be issued in Magangue if an animal supplier has obtained a permit from Bogota for the capture of a certain number and species of primates. Permits are issued only if the supplier can present a certificate of need from an established biomedical or research institution overseas that is certified by a Colombian consulate. For Aotus, permits may be issued that limit the number of individuals to be captured for all suppliers to 100 a month and a total of 700 during this closed season (INDERENA, Resolution No. 225, 1971). S. oedipus had been prohibited from being hunted throughout the year (Resolution No. 574, July 1969) because of its restricted range and fears of its extinc- tion. Recent legislation (INDERENA, Resolution No. 568, 1972) amended the two previous resolutions in the northern coastal area, specifically to satisfy needs of the scientific and biomedical communities. The monthly capture limits for A. trivirgatus, S. oedipus, and C. albifrons are 100, 25, and 10, respectively, for each permit holder. For a monkey to leave the country legally it must possess (1) a salvoconducto from INDERENA, which is a prerequisite for all of the following; (2) an exporting license from the controlling export agency, INCOMEX; (3) a certificate obtained from ICA (the agency control- ling domestic and wild animal products), signed by a veterinarian or equivalent health official, stating that the animals are in good health and suitable for export; and (4) a clearance by customs when leaving the airport. In addition, there are several INDERENA in- spectors at the airport responsible for checking ani- mals destined for export to insure that all legal re- quirements have been satisfied. One would think, with such regulations, that the flow of Colombian fauna would be well controlled. But, in reality, there is much illegal transport and exportation. INDERENA has inspectors that also check each animal compound in Barranquilla for ir- regularities. Yet I observed monkeys being trans- ported illegally during the so-called closed season. Needless to say, this aspect of the primate trade is hard to document, yet there is substantial speculation as to the means of such activity. Monkeys may be shipped in crates labeled "raccoons," "anteaters," or other legally obtained animals for which a salvocon- ducto has been obtained. Thus the monkey can leave the country rather easily if controls are lax at any regulatory points. Imported fish and wildlife entering the United States are regulated by provisions issued under the CFR (Code of Federal Regulations, 1970), Title 50—Wildlife and Fisheries. Part 17, known as "Conservation of En- dangered Species and Other Fish and Wildlife." These laws, which became effective in June 1970, implement the Endangered Species Conservation Act of 1969 (83 Stat. 275), the Black Bass Act, and the Lacey Act. At arrival in Miami the monkeys must meet the requirements of four governmental agencies: Public Health Service, Department of Agriculture, Depart- ment of the Interior, and Customs. A properly exe- cuted declaration for the importation of fish and wildlife (Form 3-177) must be submitted to Customs for collection of a 3.5 percent import tariff (Table 2). Information required includes common and scientific names, numbers, country of origin, whether or not the animal is on the endangered species list, and "whether or not subject to laws or regulations in any foreign country regarding its taking, transportation or sale" (Title 50, 17.4-b). Inspectors of the Bureau of Sport Fisheries and Wildlife of the Department of the Interior examine the shipment to see that none are on the endangered species list. Listed neotropical primates include Ateles geoffroyi frontatus, A. geoffroyi panamensis, Saimiri oerstedii, Brachyteles arachnoides, Chiroptes al- binasus, Leontideus sp., Callimico goeldii, and Cacajao sp. Only the latter two are found in Colom- bia's Amazon territory. Presently, a rather shocking situation exists con- cerning Colombian exports. Monkeys enter during the closed season, yet action cannot be taken by U.S. authorities because the Bureau of Fisheries and Wildlife does not have all recent INDERENA laws on file. Title 50 further states that when wildlife is subject to foreign regulations, an export permit from an ap- propriate governmental agency, in this case INDE- RENA, must accompany the shipment. The U.S. Public Health Service is concerned primar- ily with preventing the introduction of yellow fever from Latin America. South American monkeys must be in a mosquito-proof container upon arrival and have been maintained in mosquito-proof quarters for at least TABLE 2 U.S. Customs Minimum Values Live Colombian Monkeys (in U.S. Dollars) for Aotus $5 Lagothrix $40 Ateles belzebuth $13 Saimiri $ 5 Ateles fusciceps $15 Cebuella $5 Cebus albifrons $10 Saguinus nigricollis $5 Cebus capucinus $13 Saguinus oedipus $4

92 GREEN 9 days prior to entry (Cooper, 1968). The certificate of health from ICA stating compliance with such regula- tions is sufficient evidence. These requirements are usually not followed. As mentioned earlier, animals are rarely kept in screened, mosquito-proof quarters in Barranquilla, and the ICA certificate received by Public Health cannot always be considered legitimate. The Department of Agriculture inspects the contain- ers for restricted fruits, plant matter, and insects. MOVEMENT WITHIN COLOMBIA AND EXPORTATION The number of monkeys transported within Colombia in 1970 is compiled by departments in Table 3. This table shows that 86.7 percent of the shipments were from the departments of Amazonas and Bolivar. These same two departments also supplied 56.2 percent of transported skins during 1970 (INDERENA, 1970). These figures demonstrate the concentration of faunal exploitation from the regions around Leticia and Bar- ranquilla.* During 1971, 2,381 monkeys were transported in the coastal region (Table 4). Of these, 65 percent were Aotus, 31 percent were Cebus, and 2 percent were Ateles sp. These data support earlier reports of the pre- ponderance of night monkeys. The importance of Magangue, as compared to all other regions, is demon- strated by the fact that 97 percent of the Aotus, 57 percent of the Cebus, and 72 percent of the Ateles originated there. The number of monkeys transported in the coastal region departments of Bolivar, Sucre, Cordoba, Atlan- tico, and Magdalena declined from 3,188 in 1970 (Table 3) to 2,275 in 1971 (Table 5). Colombian records shown in Table 5 identified pri- mates exported to the United States in 1970. These figures can be compared with the Fish and Wildlife Bureau's report (Paradiso and Fisher, 1972) that clas- sified imports by country. INDERENA reported more than 10,839 primates were exported specifically to the United States, while the U.S. records show 12,988 Colombia primates imported in 1970 (Paradiso and Fisher, 1972). The records for individual species differ more than total values. Curiously, U.S. records show 833 Saimiri imported compared with Colombia's figure of 5,321. Data collected by different sources frequently differ, but it is unlikely that such a large number could have entered the United States without knowledge of the authorities. Data received from one very reliable "The volume (11,734) transported nationally in 1970 according to Table 3 (INDERENA, 1971) compares favorably with the tabulation (9,142) from Table 5 (INDERENA, 1971). TABLE 3 Number of Monkeys Transported in 1970 by Department Department" Number Monkeys Percent Amazonas 8,340 71.0 Bolivar 1, 83 1 16.6 Sucre 470 4.0 Cordoba 457 3.9 Magdalena 430 3.8 Others" 206 0.7 TOTAL 11,734 100.0 SOURCE: INDERENA. Cuadro No. 40, 1971 " See Figure 1. " Antioquia, Atlantico. Caqueta. Cesar. Meta. Putamayo, Santander, Norte de Santander. animal dealer in Barranquilla shows that in 1970 he alone accounted for 80 Ateles sp., only seven short of the national total. A close look at national exports (Table 5) indicates that more Aotus, Cebus, and Saguinus were exported than transported. Table 6 illustrates the variation in governmental reports. The majority of neotropical monkeys imported into the United States in 1970 came from Peru (60.9 per- cent) (USDI, 1971). Together with Colombian ship- ments (28.0 percent), these two countries represent a mammoth 88.9 percent of neotropical imports. Of the Colombian exports arriving in the United States, the following are percentages of the most frequently ex- ported species compared with other Latin American countries (USDI, 1972): Aotus, 87.5; Ateles, 29.7; Ca/- licebus, 52.8; Cebus, 47.4; Lagothrix, 21.8; and Mar- mosets 86.5. The tamarins, 5. oedipus and S. mystax. TABLE 4 Number of Monkeys Transported in the Coastal Region in 1971 by Section Section" Aotus (marta) Cebus (mico cari- Ateles blanca, mico bayo. (marimonda, mico maicero. mico) marimba) Magangue 1. 544 416 43 El Banco 6 97 1 San Marcos 7 15 — Monteria 12 31 14 Others 20 173 2 TOTAL 1.589 732 60 SOURCE: INDERENA. 1972 a. c—Note agreement in total primates trans- ported in coastal region as reported by section (2381; INDERENA. 1971) and by species (2275; INDERENA. 1972, Table 5). " INDERENA offices that issue permits in the coastal region are located in these cities.

THE NONHUMAN PRIMATE TRADE IN COLOMBIA 93 TABLE 5 Licensed Export and Transport of Colombian Primates National Coastal Region" Exported 1970 Transported 1970 Exported 1971 Transported 1971 Scientific Name Common Name Total To U.S. To Others Alouatta Cotudo 102 Aotus Mono 2.825 4 17 Marta 1,813 45 1,213 1,580 Ateles Mico de noche 143 965 2 149 Marimba 87 28 Marimonda 28 251 Cacajao Mico ingles 20 20 Callicebus Zogui-zogui 44 44 Cebus Mico 266 807 290 Mico bayo 260 50 Mico maicero 54 127 326 Mico cariblanca 11 Mico capuchinus 33 35 13 5 Mico prego 198 108 74 Lagothrix Barrigudo 305 296 9 363 117 2 Pithecia Mico volador 18 18 Saimiri Fraile 5,546 5.321 225 8,115 2,730 Cebuella Pielroja 165 157 8 Callimico Leoncito 8 8 1 Saguinus Titi 1.925 1,905 20 86 5 Subtotal 11.265 10,839 426 9,142 5,443 2,275 Undesignated 4.932 TOTAL 16,197 10.839 426 9,142 5,443 2,275 SOURCE: National data adapted from INDERENA (1971); data for coastal region adapted from INDERENA (1972a, b, c, d). " Coastal region includes the departments of Atlantico. Bolivar. Cordoba, Magdalena. and Sucre. account for almost 90 percent of the Callitrichidae. This family roughly corresponds to one-third of all Colombian primates entering the United States for that year. Approximately 60 percent of these species im- TABLE 6 Capture and Export of Colombian Monkeys Number of Monkeys 1969 1970 Registered captures 18,572" 11,496C-20,882<1 Exported 18.522" 14,519"-16,197r 1 INDERENA, 1972. 1 INDERENA. 1972. 1 INDERENA, 1971. ported into the United States were utilized for research purposes. This is a slight increase over 1969 (Table 7). Aotus and Saimiri, together with Cebus albifrons and C. apella, were also utilized heavily. As can be seen, the number of squirrel monkeys not used for research purposes (all years) is significant. The squir- rel monkeys, 57 percent of New World imports for 1970, represent a numerical drop from previous years. Caution should be exercised, however, since the number of unspecified exports for this period as re- ported in Colombian records is 4,524. Flow into the pet market accounts for almost all of these nonresearch monkeys. Yet, imports dropped 46 percent from 1969. Most striking and unfortunate is that the number of Cebus used outside of research remained alarmingly high, close to 6,000 animals (approximately 85 per- cent). For all species the following percentages were

94 GREEN TABLE 7 Importation and Research Use of Neotropical Primates, 1968-1970 Species Common Name Imported 1 968" Used for Research Imported 1968" l969r Used for Research Imported 1969" \91<y Used for Research 1970' Alouatta Howler monkey 13 36 1 seniculus Red howler 16 12 12 palliata Mantled howler 101 93 88 Aotus trivirgatus Night monkey 4.087 5,470 5,312 3,972 4,327 4,519 Douroucouli Owl monkey A teles Spider 280 981 77 619 14 228 belzebuth Long-haired spider 142 31 87 fusciceps Brown-headed spider 34 19 geoffioyi Black-handed spider 1,105 1,548 1,870 paniscus Black spider 712 984 587 Brachyteles arachnoides Woolly spider 1 38 Cacajao melanocephalus Black-headed uakari 4 rubicundus Red uakari 127 69 14 Callicebus Titi 141 17 116 159 120 10 moloch Dusky titi 51 43 40 Cebus Capuchin 106 1,740 99 1 ,058 101 916 albifrons White-fronted 4,913 4,743 3,168 apella Black-capped 784 1,024 847 capucinus White-throated 1,768 1,574 1,762 nigrivittatus Weeper 106 78 36 Chiropotes satanas Black saki 4 6 14 Lagothrix lagotricha Humboldt's woolly 2,902 1 3,311 2,241 Pithecia monachus Monk saki 162 24 66 pithecia Pole-headed saki 10 2 2 Saimiri sciureus Squirrel 45,014 20,616 47,09 6 8,429 26,124 6,807 Not designated 114 265 SUBTOTALS (Cebidae) 62,583 28,823 66,333 14,343 41,522 12,480 Callimico goeldii Goeldi's marmoset 83 43 9 Callithra Marmoset 22 1 44 aurita White-eared 31 446 126 argentata Black-tailed 57 40 22 jacchus Common 125 52 1 Cebuella pygmaea Pygmy marmoset 197 639 192 Leontopithecus rosalia Golden lion tamarin 50 149 150 Saguinus Tamarin 89 1 graellsi Rio napo 3 6 illigeri Redmantled 289 197 labiatus Red-bellied 92 9 leui'opus White-footed 33 nigricollis Black and red 3,519 1,564 332 oedipus Cotton top 3,098 3.752 2,068 geoffioyi Geoffroy's 6 9 midas Yellow-handed 1 tamarin Negro 32 mystax White-moustached 1,780 SUBTOTAL (Callitrichidae) 7,688 3,858 6,537 2,415 4.734 2.804 TOTAL 70,271 32,799 72,870 16,758 46.256 15,284 • Jones, 1970. • ILAR. 1969. r Jones and Paradiso, 1970. " USDI, 1971. r Paradiso and Fischer. 1972. 'ILAR. 1971b.

THE NONHUMAN PRIMATE TRADE IN COLOMBIA 95 TABLE 8 Number of Animals Imported into the United States 1968« * Jones, 1970. * Jones and Paradiso, 1970. r USDI. 1971. * Paradiso and Fischer, 1972. 1969" 1970 Mammals 129,520 122,991 101, 30? Total primates 113.714 108,974 85,15r- (78,375)" New World primates 70,271 72,870 46,256* Old World primates 43.443 36,099 31,280" visited in Miami wanted a price of $175 for an infant woolly monkey. It is distressing to see how these prof- its are disproportionately inflated in the United States when Colombia, which has permanently lost this nat- ural resource, receives little of the economic gain. The campesino who traps the animal also reaps little of this eventual monetary gain, yet in local economic terms profits well. Normal weekly wages in the Tiquisio area are 30 pesos (U.S. $1.50), and the sale of one woolly monkey amounts to 2 weeks' work. It is evident that very few individual trappers and local sectional dealers have taken the main profits. The dollar volume of Colombian primate export to the United States was the following: obtained by dividing the number of research monkeys by the total number of imports: 47 percent (1968), 23 percent (1969), and 33 percent (1970). It is depressing to see the numbers that apparently reached private hands as pets, especially during 1969. To those con- cerned with the exploitation of South American pri- mates, it is important to note that the import volume in 1968 and 1969 dropped in 1970. The numbers of New World primates utilized for pet purposes in 1970 were nearly 20,000 Saimiri, 5,000 Cebus, and 2,200 Lago- ihrix (none reported to be used for research). Both New World and Old World primates accounted for 87.8, 88.6, and 84.4 percent of all mammals enter- ing the United States in 1968, 1969, and 1970, respec- tively (Table 8). Further breakdown indicates that New World monkeys were imported at consistently higher levels than Old World monkeys for the same years—61.8, 66.9, and 59.7 percent.* At the Miami port of entry, 57,921 primates entered in 1970, with neotropical primates probably comprising at least 60-70 percent. Now that a general picture of the supply chain has been presented, monetary returns at each step of the chain can be examined (Table 9). This list, as compiled by the author during the past year, is believed to be relatively accurate. Prices quoted are what the dealer pays for the animal locally, in Magangue and Barran- quilla. Also included are the export prices quoted from dealers for monkeys delivered at Miami and a rep- resentative sample of pet store prices. Undoubtedly, transport costs of $0.44 per Ib for exportation are signif- icant to the exporter, yet the margin of profit at times is believed to be close to 100 percent. One pet store 7969 1,671,400 pesos U.S. $79,543 7970 2,297,000 pesos U.S. $109,381 ($73,951)* Economically, primate exportation rated below al- ligator skins, live snakes, peccary hides, and live cats. The economic value of the monkey trade represents a very small percentage (3 percent) of Colombia's total faunal export credit. CONSERVATION As can be deduced from the facts presented in the previous pages, various pressures exist that are affect- ing the nonhuman primate population. As a result of commercial hunting and trapping for the pet and scientific community and competition with expanding human populations, such populations may be reduced in Colombia as well as throughout the world. In broader terms, the expanding human population re- sults in nonhuman primate habitat deterioration and/or destruction, reduction in the numbers of monkeys by eliminating them as agricultural pests, and utilizing them as a food source. Past reports have varied in claimed mortality rates due to trapping and transportation along the supply chain. Most of these reports lack documented evi- dence in South America, and statements such as the following do little to promote accurate information: Conservative estimates indicate a loss of 50% during the period from the capture of the animal until its final sale. (Avila-Pires, 1968) *Note in Table 8 that the 1970 import volume reported in USDI (1971) is 6.776 more than that reported in Paradiso and Fisher (1972). •Tabulated from INDERENA, 1971. Cuadro No. 3; other figures from INDERENA, 1972, Cuadro No. 38, using 21 pesos = U.S. $1.00 as conversion factor.

96 GREEN TABLE 9 Price Chain per Colombian Primate Type of Price to Local Buyer Price at Magangue Price at Barranquilla Barranquilla Export Price Price at U.S. Pet Stores Primate Pesos" U.S.$" Pesos U.S.S Pesos u.s.s Pesos U.S.S Pesos U.S.S Aotus 40-50 2-2.5 50 2.5 70 3 95-150 4.5-7 630-840 30-40 A teles 90-150 4-7 150 7 200 9.5 273-420 13-20 1,050-1.680 50-80 Alouatta 50-80 2.5-4 80-100 4-5 100-130 5-6 126-210 6-10 — — Cebus alibfrons 60-80 3-4 80 4 120 6 210-263 10-13 1,575-1,689 75-80 capucinus — — — — — — 263-420 — 1,689-2,100 — Saguinus oedipus and leucopus 20-40 0.9-2 40-45 1.9-2 50 2.5 95-170 4.5-8 735 35 Lagothrix 200-300 10-14 300-500 14-24 300-500 14-24 950 45 3,675-4,200 175-200 Saimiri Not in coastal region 168-315 8-15 735-840 35-40 1 Conversion Rate = 21 Colombian pesos/U.S.S. U.S. figures are approximated. Thorington (1972), on the other hand, has made an accurate and honest statement regarding such specula- tions: ... we are, however, unaware of the number of animals trapped in South America, those which die in trappers and dealers compounds or en route and the causes of mortality. ... (p. 18) Emphasis must be placed on the lack of clear, documentary material for determining these mortality and morbidity percentages. One reliable dealer in Barranquilla reported that Aotus had a mortality rate between 45-50 percent in his compound until he restricted his source of supply solely to Magangue, resulting in a mortality drop to 5-8 percent. The second major consideration of trapping pres- sures is the quantity of primates extracted from the various localities. Some species, such as Aotus and Saimiri sciureus, are heavily harvested yet probably are not near danger of extinction because of wide distribution and abundance. On the other hand, certain populations and species, even though trapped to a more moderate degree, may be under greater stress due to their restricted distributions. As mentioned earlier, the cotton-top marmosets are only found west of the Magdalena and north of the San Jorge rivers, and the woolly monkeys in this region are geographi- cally restricted to two small mountainous zones (Hernandez-Camacho and Cooper, 1976). Similar numbers of A teles and Lagothrix lagotricha are exported to the United States, even though woolly monkeys have a very restricted range, in contrast to Ateles, which are widely distributed within Colombia. Therefore, the numbers of animals collected in a given locality do not necessarily reflect the numbers of animals in the natural habitat. One of the greatest threats to primate populations is the alteration of environment, resulting in a reduction of suitable habitats for these species. In northern Colombia, lumbering, cutting roads, and slash and burn agricultural practices result in habitat destruc- tion. The rate of deforestation is increasing exponen- tially due to Colombian demographic expansion. The species of Alouatta, Aotus, Ateles, Cebus, and Saguinus have all been observed to inhabit various types of secondary and primary forest throughout Tiquisio and the Magdalena River valley. Frequently, populations can be found in close proximity to farm- land. Campesinos generally use such land for 2 or 3 years, then allow it to lie fallow for several years, during which time native vegetation regenerates rapidly. Reports in Tiquisio mention that C. albifrons and 5. leucopus raid the crops of many campesinos. This suggests that small numbers of these monkeys are eradicated as agricultural pests. A few monkeys are hunted for food. Since only a select number of natives possess firearms, and ammunition is expensive and in short supply, these losses are minimal. It can be seen from this discussion that in certain areas greater land use does not necessarily result in complete habitat destruction. Although the following statement may be true for parts of South America, it is not applicable to northern Colombia nor Barranquilla and probably reflects the situation in an emotional rather than realistic manner: All nonhuman primates within the hunting ranges of Iquitos. Leticia, and Barranquilla are threatened and severely decimated. (Harrisson. 1971. p. 7) It is hoped that such statements would be subjected to serious scrutiny to obviate any doubts of authenticity. With any discussion of the primate trade, one should

THE NONHUMAN PRIMATE TRADE IN COLOMBIA 97 incorporate topics that need further attention. Past reports have discussed and proposed in detail needed research similar in tone to the statement by Southwick et al. (1970) that: II becomes increasingly incumbent upon mankind in general and the scientific community in particular to undertake more vigorous research and conservation programs to protect endangered (primate) species, (p. 1051) It is believed the scientific community has been well saturated with these suggestions and demands. With respect to Colombia and that of all South America, very little has been done to promote ecological investi- gations of different species, to determine the abun- dance and natural distributions of these populations, to analyze the impact of the supply trade on remaining populations, to accumulate data to determine what level of harvest can be sustained, and to identify present irrational uses of this resource. The Colombian legislation that presently attempts to regulate and manage its primate resources has already been mentioned. INDERENA has far from an ubiquitous system of control, but many measures, even though not strictly enforced, do contribute to a reduction in primate exploitation. Unfortunately, there are certain anomalies. For instance, why does the open trapping season exist in November, December, January, and February? These winter months in the Northern Hemisphere correspond to the most stressful period of the year because of the drastic climatic change. Con- sidering that the United States receives the majority of Colombian primate exports, it seems reasonable to question this regulation. Since this decree (No. 459) was issued in 1941 with no known biological basis, it seems imperative that it be reviewed and possibly altered for better management purposes. In terms of action and control in the near future, INDERENA has considered legislating the following (Hernandez-Camacho and Cooper, 1976): • Setting aside natural reserves to protect certain threatened species, subspecies, or populations. • Limiting exploitation of its remaining natural pri- mate resources specifically to biological and biomedi- cal research. Also, a feasibility and cost-analysis study of breeding primates in captivity through programs of "zoo- criaderos" (animal farming compounds) is under con- sideration. Hence, at the local level there is genuine interest and activity to varying degrees. Besides national regulations, there should be a more acute system of coordinated action between countries such as Colombia and the United States. Previously mentioned is the absence of Colombian laws on record with the U.S. Department of the Interior. Other possi- ble measures include greater return of economic prof- its from the pet market in the United States back into the Colombian economy. Perhaps the U.S. Govern- ment should drastically reduce or completely eliminate the primate pet market altogether. But a necessary note of caution must be interjected. Such restrictive measures might stimulate undesirable and illegal activ- ity that already exists in Colombia, or even worse inhibit legitimate operations. Internationally, such organizations as the World Wildlife Fund (WWF) and the International Union for the Conservation of Nature and Natural Resources (IUCN) have action committees to propagate conserva- tion activities in all fields, including neotropical pri- mates. Basically, the practice is to set aside preserves for protection and management of critical habitats and species. It must be stressed that such advice and encouragement is helpful, but only purposeful when coupled with funds. The Fourth International Primatological Society (IPS), meeting in Portland, Ore- gon, on July 14-18, 1972, drafted an appeal for conser- vation of nonhuman primates. It is hoped that this will be a productive beginning for stronger international cooperation. ACKNOWLEDGMENTS I would like to express my gratitude to the Peace Corps for enabling me to live in Colombia during 1971 to 1973, as well as my supporting agency, INDERENA. Particularly, I would like to mention the assis- tance given by Dr. Jorge Hernandez-Camacho, chief of Wildlife, and Dr. R. W. Cooper, of the Peace Corps Conservation Program. ILAR provided the funds for travel to the conference. In Miami, Mr. John Thomas, the USDI Sport Fisheries and Wildlife inspector, was extremely helpful and cooperative. Finally, the moral support and encouragement of my wife. S. Huffman, in Colombia, was invaluable, as well as the constructive recommendations by Nancy A. Muckenhirn. REFERENCES Avila-Pires, F. D. de. 1968. Some problems concerning primates. Pages 132-141 in Proceedings of the Latin American Conference on the Conservation of Renewable Natural Resources, San Carlos de Bariloche, Argentina, 27 March-2 April. 1968. International Union for Conservation of Nature and Natural Resources (IUCN), Morges. Switzerland. Code of Federal Regulations. 1970. Conservation of endangered species and other fish or wildlife, Part 17, Title 50. Federal Register, vol. 35, no. 106. Cooper, R. W. 1968. Squirrel monkey taxonomy and supply. Pages 1-29 in L. A. Rosenblum and R. W. Cooper, eds. The squirrel monkey. Academic Press, New York. Cooper, R. W., and J. Hernandez-Camacho. 1975. A current ap- praisal of Colombia's primate resources. Pages 37-66m G. Bermant

98 GREEN and D. G. Lindburg. eds. Primate utilization and conservation. John Wiley and Sons, Inc., New York. Harrisson, B. 1971. Primates in medicine. Vol. 5. Conservation of nonhuman primates in 1970. S. Karger, Basel. 98 pp. Hernandez-Camacho, J., and R. W. Cooper. 1976. The nonhuman primates of Colombia. This volume. ILAR. 1969. Annual survey of animals used for research purposes during calendar year 1968. ILAR News I3(l):i-xi. ILAR. 1970. Annual survey of animals used for research purposes during calendar year 1969. ILAR. News 14(l):i-v. ILAR. 197la. Annual survey of animals used for research purposes during calendar year 1970. ILAR News I5(l):i-ix. ILAR. I971b. Survey of nonhuman primates being maintained as of January 1971, prepared by R. W. Thorington, Jr. ILAR News INDERENA. 1970. Cuadro No. 37. INDERENA. 1971 . Anuario de la fauna silvestre en Colombia en 1970. Oficina de Planeacion, Cuadro No. 3. 87 pp. Mimeographed report. INDERENA. 1972a. Movilizacion de los recursos faunisticos. Re- gional Costa Atlantico, Informe Estadistico, Primer Semestre, 1971. Enero-Junio, Barranquilla. Mimeographed report. INDERENA. 1972b. Exportacion de los productos faunistico. Re- gional Costa Atlantico, Informe Estadistico, Primer Semestre, 1971, Enero-Junio. Barranquilla. Mimeographed report. INDERENA. 1972c. Movilizacion de los recursos faunisticos. Re- gional Costa Atlantico, Informe Estadistico. Segundo Semestre, 1971, Julio-Diciembre, Barranquilla. Mimeographed report. INDERENA. 1972d. Exportacion de los productos faunistico. Re- gional Costa Atlantico. Informe Estadistico, Segundo Semestre, 1971. Julio-Diciembre, Barranquilla. Mimeographed report. INDERENA. 1972e. Los recursos naturales renovables del Pais en Cifras. Documento Provisional. Bogota. Jones, C. 1970. Mammals imported into the United States in 1968. Special scientific report. USDI WL-137. U.S. Government Printing Office. Washington, D.C. 30 pp. Jones, C., and J. L. Paradiso. 1970. Mammals imported into the United States in 1969. Special scientific report. USDI WL-147. U.S. Government Printing Office, Washington, D.C. 33 pp. Middleton, C. C., A. F. Moreland, and R. W. Cooper. 1972. Problems of New World primate supply. Lab. Primate Newsl. 2(2): 10-17. Paradiso, J. L., and R. D. Fisher. 1972. Mammals imported into the United States in 1970. Special scientific report. USDI WL-161. U.S. Government Printing Office, Washington, D.C. 62 pp. Roth. W. T. 1965. Editorial. Primates from trap to test tube. Lab. Anim. Care l5(4):243-246. Roth, W. T. 1969a. Primate supply today. Pages 206-210m Proceed- ings of the 2nd International Congress of Primatology, Atlanta, Georgia, 1968. Vol. 2. S. Karger, Basel. Roth, W. T. I969b. Supplying wild primates to the laboratory. Pages 1-16 in W. I. B. Beveridge, ed. Primates in medicine, vol. 2. S. Karger, Basel. Southwick, C. H., M. R. Siddiqi, and M. F. Siddiqi. 1970. Primate populations and biomedical research. Science 170:1051-1054. Thorington, R. W., Jr. 1972. Importation, breeding, and mortality of New World primates in the United States. Int. Zoo. Yearb. 12:18-23. USDI (U.S. Department of the Interior), Bureau of Sport Fisheries and Wildlife. 1971. Wildlife imported into the United States in 1970. USDI WL-495. U.S. Government Printing Office. Washing- ton. D.C.