3.1.1 Podocnemis expansa and podocnemis unifilis (South American river turtles)
3.1.2 Geochelone carbonaria and Geochelone denticulata (tortoises)
After reviewing the patterns of use and selection criteria mentioned above (1.1) a list of 30 key groups or species of Latin American wildlife was drawn up for more detailed analysis and presentation (Table 22). It covers the animals preferred for food in the rural sector. It also includes some species of high commercial value for their hides or skins. But it underrepresents species preferred by sports hunters, e.g. doves and partridges, tinamous or Gallinaceae.
Most species included are widely distributed throughout Latin America, whereas eight are specific to South America, three are confined to Central America, and three are found only in southern or Andean South America. For each species or group the following brief data is given: the scientific name, the common names in widest use, geographical variation and distribution, elevational range, size and weight, habitat, abundance, relevant behavioural traits, feeding habits and reproduction, hunting products, and management.
South American wildlife includes 45 species of turtles (Order Chelonia): four are land turtles (tortoises), six marine turtles and the remainder freshwater turtles. Various other species, particularly of the Gopherus, Scaptochelys, Kinosternon, Staurotyphus and Claudius genera, are found in Mexico and Central America (484).
Marine turtles, especially Chelonia mydas and its eggs, are widely used in many neotropical coastal areas, but marine species are not covered in this study. Many freshwater turtles (genera Podocnemis, Peltocephalus, Phrynops, Platemys, Pseudemys, Rhinoclemmys, Kinosternon) and land species (Geochelone, Gopherus) are captured for food and other uses and may be a major local resource. Podocnemis leads the river species in this respect and, among the land genera, the main food species are Geochelone carbonaria and G. denticulata.
Common names: Podocnemis expansa: arrau (Venezuela), charapa (Colombia, Peru), tartaruga, tartaruga da Amazonia (Brazil), tortuga, tortuga del Orinoco, zamurita (Colombia, Venezuela); P. unifilis: taricaya (Peru), terecay, terecaya (Colombia, Venezuela), tracajá, tracaxá (Brazil).
Geographical variation and distribution: The original range of both species embraces the Amazon and Orinoco river basins and includes Brazil, Colombia, Peru, the Bolivian Amazon and the Colombian and Venezuelan Orinoco basin. P. unifilis apparently penetrates further into the upper reaches of rivers. Pichard and Trebbau (484) believe the species has a somewhat wider range than P. expansa, extending to Ecuador and the Guianas. Both species are monotypical (484, 631).
Other Podocnemis species are distributed as follows: P. erythrocephala (chimpire, irapuca) in the Rio Negro basin in northeastern Brazil and adjacent areas of Colombia and Venezuela; P. lewyana in the Magdalena river basin, Colombia; P. sextuberculata (Cupiso, iaca) mainly in the upper Amazon in Brazil, Colombia and Peru, and; P. vogli (galápago llanero) in the llanos of Colombia and Venezuela. P. cayennensis is co-specific with P. unifilis and P. dumerliana, often cited as Podocnemis, belonging to the genus Peltocephalus (3, 376, 392, 484, 492).
Elevational range: Restricted to tropical waters up to about 200 metres.
Size and weight: Podocnemis expansa is the biggest Latin American river turtle, with strong sexual dimorphism by size. The carapace length of adult females measured along the natural curve of the shell varies from 50-79 cm, with reported averages of 64-71 cm and an apparent top size of 89 cm. Carapace width ranges from 43-55 cm and the total weight 1 5.7 to 46 kg (average 23-26 kg). The record weight is 73 kg (491). Adult males measure 40-50 cm in carapace length and 30-38 cm in width (13, 437, 439, 459, 591, 593).
Adult female P. unifilis have a carapace length of 38-52 cm (average 44 cm), a carapace width of 33-45 cm (average 40 cm) and weigh 5.3 - 11.6 kg, averaging 8.1 kg. Adult males measure 21-39 cm in length, 19-34 cm in width and weigh 2.2-4.5 kg (189, 376, 395, 484, 552).
Habitat: Both species live in the calm waters of big rivers with marked changes in seasonal water levels. During the high-water period, they are also found in flooded forests, swamps and lagoons whereas during the dry season they concentrate in the principal riverbeds. Both species share the same habitat throughout the Amazon and Orinoco basins and their main tributaries, but P. unifilis may go further upriver, and may be found in smaller, swifter rivers (4, 376, 395, 439, 552).
Abundance: As historical accounts show, the original and very abundant population of P. expansa numbered in the millions, and was found throughout the Orinoco and Amazon basins (40, 250, 289, 542, 606, 607). But even this huge population dwindled under the massive and peremptory onslaught on egg-laying females and eggs. The current Brazilian Amazon population is estimated at 28 000 adult females on 54 nesting beaches (191). Thirty-four thousand nests were counted in 1963 on the main nesting beach (437) but only 4 700 in 1981 (459). The species is scarce in the Peruvian Amazon and the Colombian Orinoco (191, 554). IUCN (246) considers P. expansa an endangered species, and lists it on CITES Appendix II.
Data is scarce on the abundance of P. unifilis. During the 1960s the species was less common in the mid-Orinoco and Rio Branco (132) than P. expansa (Ojasti, pers. obs.) but it does seem to be fairly common in the more remote rivers of its vast range (189, 376, 395, 484, 552). IUCN considers P. unifilis a vulnerable species (246).
Behaviour: Most data on behaviour concern reproductive activities along river banks. Podocnemis seems to be diurnal in its aquatic medium, with mid-morning and afternoon peaks of activity (376, Ojasti, pers. obs.). P. unifilis likes to sun in groups on tree-trunks or stones in the middle of the river and occasionally along the shore. P. expansa females bask in the sun for only a few weeks before laying their eggs, and are very shy out of the water, diving back at the first sign of disturbance. The flight distance covered by P. unifilis is some 80 m (34).
Feeding habits: Both species feed primarily on vegetation in the flooded forests, swamps and várzea lagoons during high waters. P. expansa seems predominantly frugivorous, feeding on various fruits and seeds of flooded forest trees, particularly legumes, and rounding out its diet with green stems and leaves, freshwater sponge (Spongilla sp.), eggs, and other scraps of animal origin (191, 439, 466). P. unifilis partly shares the same diet, but green floating or submerged plants form the basis of its diet and fruits are only a supplement (376, 395, 439). During the breeding season, the stomachs of P. expansa females are either empty or contain only residual quantities of sand, decomposed wood or filamentous algae (439, 491). Newly-hatched baby turtles eat meat, fish and vegetables in captivity, but their diet in the wild is unknown. P. unifilis juveniles in captivity can collect small particles from the surface water film, and quite possibly also do this in the wild (45).
Reproduction: Both species nest along river banks in the dry season, P. expansa frequenting the same beaches in massive and widespread seasonal migrations (in the past there were concentrations of hundreds of thousands of egg-laying females (437)), whereas P. unifilis is generally solitary and more sedentary, and its nests are more dispersed.
P. expansa egg-laying coincides with dry-season low-water minima and therefore varies from site to site: January in Rio Branco, Brazil; February-March in the Orinoco, Venezuela; August-September in Rio Pacaya, Peru, and in the Madeira and Jurua rivers in Brazil; and October in Rio Trompetas, Brazil. It may vary from one year to the next at the same site as the river rises and falls (4, 132, 414, 439, 458, 491, 591). After one or two weeks of basking in the sun on the banks of the nesting beaches, the turtles come out at night to lay their eggs on selected sandy beaches along the big rivers, generally concentrating in the highest part of the beach. In a nest 60-80 cm deep, they deposit from 50 to 180 eggs, depending on female body size. The average number of nest eggs is 78-132, probably reflecting differences in size structure between the respective populations. The elastic, spherical eggs average 40 g in weight. The incubation period ranges from 45-65 days, but often the newly-hatched baby turtles remain longer in the nest, until the rains begin, when they begin to move down toward the flooded river. About 95 percent of the eggs produce viable hatchlings (11, 437). There is one male for every 30 females among the newborn (9). The hatchlings (average weight 22 g) are preyed upon by wader birds and raptors on the beach and by fish and crocodilians in the water. Some years, flooding before the end of the incubation period takes an enormous toll in mortality (13, 132, 437, 552, 554).
P. unifilis breeds approximately one month before P. expansa in the same regions: December-February in the Orinoco basin in Venezuela and Colombia, June-July in the Rio Purús in Brazil, July-August in the Samiria and Pacaya rivers in the Peruvian Amazon and September-October in the Trompetas river of Brazil. It appears to have a longer mating season than P. expansa (189, 376, 395, 550, 594), and is believed capable of producing two nests per season (189, 376, 550, 552), but there is no clear proof of this. P. unifilis prefers sandy beaches close to the water for nesting but may also use clay soil beaches, steep river banks, and even areas covered with leaf litter. P. unifilis nests alone or in small groups from evening to midnight (189, 376, 550). The nest is about 26 cm deep and contains 7 to 52 eggs, depending on female body size. The average is 30 in Peru (189, 550, 520) and 23 or 24 in two Brazilian sites (591, 594). These are oval, hard-shelled eggs weighing 15-30 g. Incubation lasts 51-70 days and the eggs hatch in 66 to 159 days (average 87) (189, 550, 552).
A good 90 percent of the eggs in undisturbed nests do hatch (132, 189, 552), but a great many nests are robbed by the local people (189, 550) even in officially protected reserves. The intensity of natural predation by Tegu lizards (Tupinambis nigropunctatus), ants, carrion birds and raptors and certain mammals averages 22 to 41 percent (189, 550, 552). Mortality from premature flooding of the nest can be very high.
Age and size: Estimates of how soon females reach breeding size vary from 4 to 5 years (491) to 8 years (6, 439, 542) to 15 (484), but the growth rate of subadults in the wild is not known. In captivity they can reach a weight of 85 g and a length of 8.5 cm the first year and 187 g and 11.2 cm the second (10). The average annual carapace length growth of tagged adult females is 0.5 cm, but smaller mature females can grow as much as 1.5 cm in one year (439).
Hunting: These turtles are hunted for their eggs, and the adult females are also caught on the nesting beaches and fished out of the water. Turtle tracks and excavations reveal the location of the nests, with the hunters probing the consistency of the sand with the bare heel or a slender rod (439, 491, 552). Massive captures of P. expansa on Orinoco beaches involve a group of "flippers", who rapidly flip over a specified number of the egg-laying females, usually after midnight on one sector of the beach. These are then shouldered or piled in baskets by "turtle carriers" and taken to the opposite shore where they are loaded into boats for transport (413, 439, 491). Outside of the breeding season, these turtles are fished in rivers with hook and line using fruit as bait. They are also hunted with harpoons and spikes in the flooded swamps and riparian forests where they feed (the area having first been baited with their favourite foods), or in areas of abundant fruit fall. Some indigenous peoples hunt them with bow and arrow and they may also be caught with trawlnets or beach seines (40, 439, 466, 491, 542). They are captured alive, and simply flipped over and/or tied, for short periods, or penned for longer periods in lagunas or ponds.
Products: Turtle meat and eggs were basic items in the diet of Amazon and Orinoco river dwellers. For indigenous peoples, the main products were the sun-dried eggs of P. expansa and meat from turtles captured on the beaches and penned alive for months in ponds. The oil extracted from the eggs became a major commercial item in colonial times, with Playa Pararuma on the Orinoco, for example, producing an annual 5 000 3-gallon jars, representing some 25 million eggs. As many as 8 000 jars came out of the upper Amazon, the product of 48 million eggs (40, 289). The subsequent development of river navigation facilitated the sale of adult turtles in the towns of the region.
The white, very flavourful meat of these turtles is a prized and very palatable food. There is no exact information on the meat/body mass yield of these chelonians with their thick carapaces and voluminous viscera. The shell is often used as a tray or cooking utensil in campesino homes.
Management: Podocnemis expansa, once one of the most abundant and valuable wildlife resources of the Amazon and Orinoco basins, is today reduced to the status of an endangered and protected species in Brazil, Colombia, Peru and Venezuela. The various forms of legal protection since colonial times have been unable to halt the gradual decline of populations ruthlessly exploited for commercial purposes in the past and still in great and constant demand for food by river-dwellers.
Venezuela has taken steps to resolve the situation. Egg-taking was banned in 1946, and the capture of adult turtles in 1962. Beaches are protected by the National Guard and flagged to deviate river traffic. Baby turtles trapped in their nests have also been rescued. These measures have failed to produce the expected results, however, and the population continues to decline (447, 449, 459). The situation looks better in Brazil, where the IBDF has embarked upon an energetic programme to recover P. expansa, protecting 54 turtle beaches (4, 191).
P. expansa's predictable nesting aggregations, its preference for the rivers of most abundant flow and the high commercial and nutritional value per unit make it more vulnerable than the more widely distributed, solitary and smaller P. unifilis, which is also subjected to the same local pressures.
Turtle management of these two species, particularly P. expansa, should concentrate on attacking the causes of population decline: this is the only way to gradually achieve real recovery. The main weapons are to list and provide real protection for the main turtle beaches, to guard egg-laying females and to avoid any disturbance that might delay egg deposition and thus risk mortality from nest flooding by rising rivers. The local inhabitants also need to be made aware of the potential future benefits of turtle protection. Because the habit of eating turtles is so ingrained and the people's protein needs are so great, the socio-economic component of this programme is highly important.
Possible additional action might include: the rescue of clutches threatened by rising rivers; protection of hatchlings against their natural predators (including keeping them for a short time in isolated lagoons and fenced-off sectors of the turtle beaches); and protection from aquatic predators during the most vulnerable phase of life (5, 10, 449, 459, 542). Excessive handling and moving of baby turtles, which might interfere with their behaviour patterns in the wild, is to be avoided.
Clutch transplants: An experimental technique for rescuing clutches apt to be flooded or raided involved transplanting eggs to artificial sand nests. In one experiment, some 85-90 percent of the P. unifilis eggs (550) and up to 95 percent of the P. expansa eggs (459) were successfully incubated and hatched, but in most trials (5, 10, 459, 554) incubation success was very low. Well-developed eggs about four weeks old apparently have no problems with transplant if they are moved swiftly and carefully and relocated in the nest in the same position and at the same depth. This is extremely important because a slight drop in incubation temperature produces clutches with a predominance of males (9).
Captive breeding: Podocnemis species adapt well in captivity and may occasionally reproduce (432). Various authors (6, 391, 542) have suggested commercial rearing of hatchlings in tanks or lagoons. Alho (6), for example, estimates that an initial lot of 5 000 baby turtles, with a 5 percent annual mortality rate and the release of 10 percent each year to beef up wild populations, would produce 1 500 adult turtles after eight years for an estimated value of 25 000 dollars. Pilot projects sufficiently long to test the validity of these proposals would therefore appear to be indicated.
Local names (generic): Jabotí, jabutí (Brazil, Argentina), morrocoy (Colombia, Trinidad, Venezuela), morroco (Colombia), motelo (Peru), secrepatos (Suriname).
Geographical distribution and variation: Geochelone carbonaria is discontinuous in distribution, ranging from easternmost Panama and parts of Colombia, Venezuela and Guianas in the north, to the mouth of the Amazon, to Bolivia, Paraguay, and the northernmost part of Argentina. G. denticulata is found throughout Amazonia and in Brazil, Bolivia, Ecuador, Guianas, Peru and Venezuela. Both species present some individual and geographic variation, but there are no recognized subspecies (484, 632). The other South American species of this genus are G. chilensis (Argentina, Paraguay) and G. elephantopus (the Galapagos archipelago in Ecuador).
Elevational range: Generally restricted to higher sections of the lowlands but may be found up to 800 m (22).
Size and weight: G. carbonaria adults in northern South America reach a linear carapace length of some 30 cm but may be 25-39 cm long. Giant specimens as big as 50 cm have occasionally been found. The weight ranges from 2 to 9.5 kg. The southernmost population is characteristically small, measuring 20-22 cm (107, 484).
G. denticulata adults reach a length of 35 cm (carapace length 29-44 cm) and a weight of 6 kg (2.5-14 kg), but giant specimens up to 70 cm long and 50 kg in weight have been reported (107, 484, 504). The males of both species are larger on the average but the giant specimens are usually female (484).
Habitat: Geochelone carbonaria lives in mosaics of deciduous and gallery forest interspersed with savannah, while G. denticulata is restricted to the moist tropical forest, often in the vicinity of water. The ecological and geographical ranges of both species overlap in some regions, however (107, 135, 411, 504).
Abundance: Tortoises seem to be fairly abundant under primary conditions (some 79 individuals/km2 for G. carbonaria and 21/km2 for G. denticulata in one area of the Roraima Territory in Brazil (411). Over one-third of the vertebrates rescued in the flooding of the Guri dam in Venezuela were tortoises. They are now far scarcer in most areas, no doubt due to frequent capture.
Behaviour: Tortoises are diurnal, solitary and slow, sometimes resting for days at a time in some small niche or burrow (G. carbonaria) or in the thickest vegetation (G. denticulata). They are apparently more active during the rainy season, in the morning and towards afternoon. They may bathe in pools, particularly during the hottest hours of the day (107).
Feeding habits: Tortoises probably feed primarily on plant matter found in the undergrowth - sprouts, shoots, fungi, flowers and ripe fruit of various kinds (Annona, Duquetia, Genipa, Spondias, Bagassa, Inga, Clarisia, Faramea). They often congregate in places where ripe fruit is falling. They also eat carrion and faeces and ingest gravel. G. carbonaria seems to adapt better to artificial diets (107, 151, 484). Captive adult G. denticulata eat up to 100-150 g/day (504).
Reproduction: Sexual activity in both species is concentrated in the rainy season. G. carbonaria are observed to mate more frequently from May to June, and G. denticulata from June to August. Both species lay their eggs from June to February in the Colombian llanos (107), but egg deposition dates vary seasonally by region (504).
G. carbonaria clutch size is usually three to five eggs weighing about 50 g each, with extremes of only one or up to seven eggs. A G. denticulata clutch ranges from four to eight eggs weighing an average 72 g, with extremes of fourteen to 12. They may produce as many as four to five clutches during the mating season at intervals of one to three weeks. The incubation period is long and variable. The incubation period for G. carbonaria is 105 to days (average 150 days) whereas the range for G. denticulata is 128-152 (average 136 days) (107, 151, 484, 504). Hatching rate success in incubation trials by Castaño and Lugo (107) was 67 percent.
Almost all the breeding data concerns animals in captivity. Under optimum conditions of confinement, G. carbonaria can reach sexual maturity in three years, but growth in the wild is probably slower. The age of 12 to 15 years for sexual maturity cited by Nogueira Neto (432) is probably excessive.
Hunting: Both campesinos and Indians capture these slow-moving easily caught tortoises wherever they find them. Sometimes they use dogs (447, 484), but other, more destructive - and unfortunately ingrained - techniques involve burning dry-season vegetation to facilitate capture (242, 396, 507). The live animals are kept penned or on their backs until they are ready to be eaten or sold.
Products: The white and very flavourful meat of the tortoise is the main product. Subsistence hunting statistics for campesinos list tortoises first numerically (Table 9) and sixth by weight. They are also important for some of the indigenous communities (Table 5). Some tortoises are intended for the family table but often at least half are sold in town. They are in great demand in southern Venezuela for traditional Holy Week dishes, spurring capture for trade in January and February (242, 396, 507). In addition to their meat, tortoises are much sought after as pets in both rural and urban areas.
Management: The importance of this species in rural diets is spurring the exploitation of wild populations. As harvesting advances, it is now suspected that these slow-growing tortoises, requiring several years to reach sexual maturity and of low reproductive capacity, are gradually dwindling in numbers (484). Compliance with the restrictions in force in various countries must be enforced - first and foremost the trade restrictions - if the survival of these chelonians is to be assured. Parallel research on tortoise biology, reproductive capacity and growth in the wild is also needed because so little is known about their population levels and ecology under field conditions.
Captive breeding: Geochelone carbonaria is easy to keep and breeds well in captivity. The situation is quite different for G. denticulata, which is harder to feed and more aggressive, particularly males during the oestrus season (107, 151, 432, 504). Tortoise breeding for food is not attractive economically in any case, due to the low reproduction rates and slow growth.
