Sloth Biology: an Update on Their Physiological Ecology, Behavior and Role As Vectors of Arthropods and Arboviruses

Brazilian Journal of Medical and Biological Research (2001) 34: 9-25 Biology of the sloth 9 ISSN 0100-879X

Sloth biology: an update on their physiological ecology, behavior and role as vectors of arthropods and arboviruses

D.P. Gilmore2, 1Departamento de Fisiologia e Farmacologia, C.P. Da Costa1 and Universidade Federal de Pernambuco, Recife, PE, Brasil D.P.F. Duarte1 2Institute of Biomedical and Life Sciences, University of Glasgow, Glasgow, UK

Abstract

Correspondence This is a review of the research undertaken since 1971 on the behavior Key words C.P. Da Costa and physiological ecology of sloths. The animals exhibit numerous · Sloths Departamento de Fisiologia e fascinating features. Sloth hair is extremely specialized for a wet · Ecology Farmacologia, UFPE · tropical environment and contains symbiotic algae. Activity shows Behavior 50670-901 Recife, PE · Parasites circadian and seasonal variation. Nutrients derived from the food, Brasil · Bradypus Fax: +55-81-271-8350 particularly in Bradypus, only barely match the requirements for · Choloepus E-mail: [email protected] energy expenditure. Sloths are hosts to a fascinating array of commensal and parasitic arthropods and are carriers of various arthropod- Research supported by CNPq and borne viruses. Sloths are known reservoirs of the flagellate protozoan FACEPE. D.P. Gilmore is the which causes leishmaniasis in humans, and may also carry trypano- recipient of a Royal Society and somes and the protozoan Pneumocystis carinii. Brazilian Academy of Sciences International Exchange fellowship.

Introduction ela, French Guiana, Ecuador, Peru, Brazil

Received April 12, 2000 and Bolivia. The species is still common, but Accepted August 7, 2000 We have recently reviewed the literature its numbers are fewer in areas where it coex- in terms of the physiological studies carried ists with the three-toed sloth. Its weight aver- out on two- and three-toed sloths (1) since ages 5.72 ± 0.69 kg (3). The hair of this Goffart (2) published Function and Form in species is lighter than in Choloepus didacty- the Sloth 30 years ago. This paper is intended lus. The ears are rounded and thickened and to update research undertaken since that time almost always covered with hair. It has been on other aspects of sloth biology. Topics reported (4) that the eyes can be partially covered include the general ecology, behav- retracted when the lids are tightly closed. ior, nutrition and digestion as well as the This may make the sloth appear pop-eyed large range of arthropods associated with during periods of stress or prior to the onset sloths and the number of viruses they trans- of aggressive behavior when the lids appear mit. to rise from their orbits. Choloepus didacty- Of the two living species of Megalony- lus is found from the delta of the Orinoco chidae, Choloepus hoffmanni is found from River west to the upper drainage of this river the lowland forest to the higher altitudes of in Colombia, east through French Guiana mountain forests south of Nicaragua through and in Brazil to the State of Maranhão. Its Central America and in Colombia, Venezu- weight is 6.07 ± 1.09 kg (3). It is less well-

Braz J Med Biol Res 34(1) 2001 10 D.P. Gilmore et al.

adapted to the drier areas than is Bradypus. both two- and three-toed sloths is minimal In 1992 its presence was recorded in the and the animals, slowed by thermal stress, Yungas region of Bolivia, considerably fur- are high in the trees seeking early sunshine to ther south than previously reported (5). warm themselves (9). The sloths are thus The distribution of the present day sloths susceptible to aerial attack by the Harpy was illustrated in the earlier review (1). Bra- eagles which have enormously developed dypus torquatus (the maned sloth) is re- feet and talons. The formidable weapons garded as an endangered species, its num- enable the birds to strike and dislodge sloths bers having fallen catastrophically with the from the canopy without losing flight speed. destruction of the Atlantic coast forest (Mata Atlântica) in southeastern Brazil. According General ecology and behavior to Wetzel (3), Bradypus torquatus is possibly the South American mammalian species Neither Bradypus nor Choloepus are able closest to extinction. Remnant populations to tolerate cool temperature latitudes. Nev- are thought to survive in the remaining frag- ertheless, both Bradypus griseus = variega- ments of the Mata Atlântica from Rio Gran- tus and Choloepus hoffmanni have been re- de do Norte to Bahia, Espírito Santo, and Rio corded living at altitudes higher than 2400 m de Janeiro. in the Braulio Carrillo National Park (Costa Wetzel (3) reported that Bradypus tor- Rica) and a single specimen of Choloepus quatus appears to be smaller than Choloe- hoffmanni was collected in Costa Rica from pus, with adults weighing about 4 kg, but the Turrialba Volcano at 3328 m where the Pinder (6) found the maned sloth to range annual rainfall is 2284 mm and the maxi- from 4.05 to 6.20 kg in weight and from 520 mum annual temperature only 16.3oC (10). to 672 mm in length. Infants were character- At higher altitudes the coat of Choloepus is ized by the absence of a mane. The widely appreciably thicker than in individuals liv- distributed Bradypus variegatus has an av- ing at lower altitudes (11). Bradypus has a erage weight of 4.34 ± 0.85 kg, whereas the lower thermal conductance than Choloepus pale-throated three-toed sloth, Bradypus tri- because only the former has a dense woolly dactylus, averages 4.01 ± 0.28 kg (3). undercoat below the coarse guard hairs, and It is obvious that human activity is the Bradypus also has a lower limit of thermo- major threat to the continued existence of neutrality (24oC) than does Choloepus sloths in particular localities. One of the few (18oC). According to McNab (11), the cold natural predators of the animals is the Harpy temperature tolerance of some extinct ground eagle (Harpia harpyja). Izor (7) gathered the sloths probably stemmed from their great size, skeletal remains of about 83 prey items from larger muscle mass than their arboreal coun- a Harpy eagle nest site in southwestern French terparts, thick fur and a constant food supply. Guiana and found that sloths (predominantly This enabled them to extend their range into Choloepus) and cebid monkeys each consti- temperate regions of the Americas. tuted about one third of all the food prey. The hair of sloths is of special interest Beebe (8) found remnants of Bradypus tri- because of the presence of symbiotic algae dactylus in the stomach of a large anaconda in it at certain times. Sloths have two distinct and in a margay cat. Izor discussed the rea- coats, one made up of long coarse, but silky, sons why sloths might constitute such a high hair which provides the distinctive color of proportion of the Harpy eagles diet. The the animal and the other made up of short usual hunting time for this bird is around fine and soft fur lying underneath. A detailed sunrise when ambient temperature is at its description of the pelage of both Choloepus minimum. At this time too the activity of and Bradypus was provided by Beebe (8)

Braz J Med Biol Res 34(1) 2001 Biology of the sloth 11 and updated by Goffart (2). The color pat- sloths usually has a dirty brown coloration, tern is especially variable in Bradypus, with but during long periods of rain it may show a some adult males possessing a saddle mark very appreciable greenish tinge brought about of black and white, yellow and black or by the increased presence of symbiotic al- bright orange. It has been reported (4) that in gae. According to Britton (13), the algae Choloepus hoffmanni the general coloration may already be present in the hair of animals of the body hair may be almost blonde, buff, only a few weeks old and it has been sug- tan or light brown in adults. Shading of the gested that they provide camouflage for the hair from light to dark over the head and sloths, while obtaining shelter for themselves back is sometimes observed. The facial hair (see 14). The algae have distinct distribution is characteristically lighter than that of the patterns in Choloepus and Bradypus, lying body and Choloepus hoffmanni lacks the longitudinally along the grooves in the former dark shoulder and forearm markings seen in and in short lateral tongues or lines in the Choloepus didactylus. Interestingly, the ab- latter. Algae representing four phyla have dominal hair is parted in the middle, flowing been cultured (15) from Bradypus, these outwards. This allows for the efficient run- being Chlorophyta, Chrysophyta, Cyano- off of water from the abdomen of the animal phyta and Rhodophyta. It has also been con- which spends much of its life hanging upside firmed that the algae found on the coat of down. Bradypus tridactylus lie between the cuticle In Bradypus the long hairs are oval-shaped scales (14) and that the hair changes with age with broad and narrow sides and a width of in apparently all species of Bradypus. Young 0.4 mm. The soft underfur is round and hairs are white, gray, brownish or black and never more than 0.05 mm in diameter, being do not possess the deep cracks seen in older colorless, translucent and usually wavy. In hairs. The first traces of algae appear on the two-toed sloth the long hairs are quite these young hairs as tiny dots or extremely different, having a maximum width of 0.16 narrow transverse lines. Older hairs have mm and being nearly all fluted with a series larger, wider algal colonies and obvious deep of longitudinal ridges and furrows (3-9) run- transverse cracks. When wet these cracks ning the length of each hair and attenuating close considerably, but when dry give the near the tip. This longitudinal fluting ap- effects of beads on a string. The oldest hairs pears to be unique amongst mammals. Wujek are badly deteriorated with the spongy cu- and Cocuzza (12), who examined the hair of ticle worn off on one side exposing the full sloths using scanning electron microscopy, length of the cortex. In the older hairs living found that the intricate cuticular scales in the algae are absent. It was suggested (14) that two-toed sloths hair are interrupted by either the algae colonize the very narrow grooves. Freeze-fractured sections indicated cracks in young hairs or the algae themselves that the cuticle is not continuous around the initiate the cracks. The hair of all three Bra- shaft. In Bradypus the hairs are more com- dypus species readily absorb water, but those plex and beneath the cuticle there are scat- of Choloepus do not. Aiello (14) was unsure tered fusi (shallow air pockets) which do as to whether in Choloepus the algae rested not, however, extend entirely unbroken along upon the surface of the spongy cuticle in the the shaft. Wujek and Cocuzza believe that grooves or were embedded in it. They were, the morphological differences in the hair however, confined to the grooves. Aiello lend further support to the assignment of the discussed the different possibilities as to two genera of living sloths to separate fami- why sloth hair has evolved in such a way to lies. encourage algal colonization. She does not During the dry season the hair of the believe that camouflage or thermal insula-

Braz J Med Biol Res 34(1) 2001 12 D.P. Gilmore et al.

tion are the only or necessarily the more midnight. This was followed by a resurgence important reasons and suggested that the in activity about 2 h before dawn. Most algae may provide nutrition or a particular activity had ceased by sunrise, but some trace element. Lack of healthy algal colonies animals were occasionally active until mid- could thus provide an explanation why Bra- morning. Howarth and Toole (18) also in- dypus does not survive long in captivity. vestigated the circadian rhythm of activity Meritt (4) points out that mutual groom- over nine days in a two-toed sloth (Choloe- ing of the hair in captive sloths is rare, and pus hoffmanni) using a movement-sensitive only seen between infant and mother. Self- cage. Although the animal was in captivity, grooming takes place in response to food left it was housed under natural illumination. It on the face, nose, or wedged on the roof of was observed that the sloth began to move at the mouth. In the latter instance food may be about 19:30 h (shortly after sunset) with dislodged with a foreclaw, while that on the peak activity continuing for 2 to 3 h thereaf- face and nose is removed with a claw or ter. Movement only ceased at approximately brushed off with a forelimb footpad. Ani- 5:30 h (sunrise). This nocturnal nature of mals were frequently seen to scratch the activity in Choloepus hoffmanni was also sides of the abdomen, lower neck and neck reported by Meritt (4). In contrast, Sunquist region adjacent to the chest. This type of and Montgomery (17) found that three-toed grooming, lasting 1 to 6 min, usually took sloths (Bradypus infuscatus = variegatus) place at night in sloths that had been inactive were active during both day and night. With for an extended period of time. When the the exception of a 7-h period centered ap- sloth was in a resting position, its back sup- proximately at dawn, average levels were ported the upper neck near the junction of about equal throughout the 24 h. Three-toed the jaws and the external genitalia was the sloths averaged 10.1 total hours of activity/ area most frequently scratched. day compared to 6-7 h in the two-toed spe- A large number of workers have exten- cies. Although many of the periods of activ- sively studied the flora and fauna on Barro ity were of short duration, the bulk of the Colorado Island in the Canal Zone of Panama time spent moving around was in bouts of where it appears that the three- and, to a continuous activity lasting two or more hours. lesser extent, the two-toed sloths are major It was also confirmed that three-toed sloths items (23%) of the mammalian biomass of (Bradypus variegatus), at least when in cap- the tropical rainforest (16). It has also been tivity, were active throughout the afternoon, estimated that on Barro Colorado Island the with the period of greatest activity between two-toed sloth has a larger home range than noon and 18:00 h, and the periods of deepest the three-toed animal and exists at roughly sleep between 6:00 h and noon (19). More only 25% of its density (16). In 1973 Sunquist recently, the movements of 6 adult male and Montgomery (17) examined the move- three-toed sloths (Bradypus variegatus) in ment and activity patterns of 6 adult Choloe- captivity were recorded every 5 min over a pus hoffmanni and 15 adult Bradypus varie- 48-h period (20). The animals moved about gatus on Barro Colorado Island. The two- significantly more when it was dark, particu- toed sloths were observed to be nocturnal larly between 21:00 h and midnight, than at and their activity patterns were similar to other times. those reported for other terrestrial nocturnal Working at the same location on Barro herbivores. No crepuscular activity was re- Colorado Island, Montgomery and Sunquist corded, but activity started from an hour (9) studied habitat selection and its use by after sunset. Activity levels then decreased Choloepus hoffmanni and Bradypus varie- as the night progressed to a nadir just after gatus. They found that home ranges were

Braz J Med Biol Res 34(1) 2001 Biology of the sloth 13 usually less than two hectares, and that three- lent diurnal activity behavior of these maned toed sloths were less particular about the tree sloths, and the comparatively long period species which they used, being located on 40 spent moving about, were probably related of 91 trees that grew in two study areas. to the lower ambient temperatures found in Individual three-toed sloths were found in the Atlantic forest compared to other more the same tree on successive days 38% of the equatorial regions where the animals have time, whereas in contrast two-toed sloths been studied. During the dry season (April to were seldom located on the same tree on September) the sloths spent significantly less successive days. Two-toed sloths were found time resting and more time feeding than in in about 20% of the trees used by Bradypus. the wet season (October to March), when The latter, however, tended to choose trees day range lengths were reduced. Pinder (22) more for the extent to which the crown was had previously observed that in the Poço das exposed to sunlight while Choloepus was Antas Biological Reserve in Rio de Janeiro most likely to be found in trees with masses the activity of Bradypus torquatus was es- of lianas in their crowns. It was discovered sentially nocturnal, with the sloths starting to (9) that the tendency of three-toed sloths to move about after sunset and little action use trees with open crowns was related in taking place during daylight hours. How- part to the vertical movements the animals ever, it is estimated that the temperature is made in the forest canopy into and out of around 10oC warmer in the Rio de Janeiro direct sunlight according to their thermoregu- location, which may account for this differ- latory needs. ence between the two populations. In a recent paper, Chiarello (21) has re- Beebe (8) never observed more than one ported some interesting information about adult three-toed sloth in the same tree as patterns of activity in the maned sloth Bra- another and Montgomery and Sunquist (23) dypus torquatus. Three animals were stud- reported it to be very rare for sloths of the ied using radiotelemetry over a 14-month same species to be on one tree together. period in the Santa Lucia Ecology Preserve However, an agonistic encounter between (7 km from Santa Teresa) in the State of two three-toed sloths (Bradypus variegatus) Espírito Santo. This area lies between 550 was observed at La Selva Biological Station and 1000 m above sea level and the vegeta- in Costa Rica (24). An adult male sloth was tion consists of subtropical moist lower high in a Cecropia tree eating leaves, when mountain forest. Individual home ranges var- another male ascended and struck the first ied from 0.6 to 6 hectares and sloths were from below with a forefoot. The animals recorded to travel an average of only 24 m then began to pummel each other with their during any 24-h period. Most of this move- forelegs while vocalizing frequently before ment occurred during daylight indicating a disengaging, after which the intruder de- predominantly diurnal rhythm of activity. scended and left the vicinity. The whole The sloths started to move about and feed incident lasted no longer than 3 min. between 7:00 and 8:00 h, and rested or slept for only an average of 74% of the time Nutrition and digestion during the day. The time spent active is about double that observed in other studies. Goffart (2) described in detail the anatomy Self-grooming also took place for short peri- of the sloth digestive tract, summarizing stud- ods of time. Daytime activity was maximum ies carried out by earlier workers including around 10:00-11:00 h, although feeding re- Beebe (8) and Britton (13). More recently mained relatively constant between 9:00 and esophageal pressure profiles in Bradypus 14:00 h. Chiarello suggested that the preva- variegatus were investigated by Duarte et al.

Braz J Med Biol Res 34(1) 2001 14 D.P. Gilmore et al.

(25). Three functionally distinct regions were the submucosa of these folds numerous leaf- found: a cranial one located at 7.3 ± 1.4 cm, shaped villi containing lamina propria, small a caudal one located at 27.0 ± 2.6 cm, and blood vessels and smooth muscle cells pro- another between these two. The resting pres- jected into the intestinal lumen. The epithe- sures of the cranial and caudal esophageal lium of these villi contained tall columnar sphincters were 20.5 ± 6.8 and 12.8 ± 4.9 cells with a striated border and also some mmHg, respectively. The maximal pressure goblet cells. In the duodenum the crypts of and its duration (mean ± SD) were 40.4 ± Lieberkühn were shallow and Brunners 12.4 mmHg and 2.8 ± 0.75 s (cranial) and glands were confined exclusively to the 35.7 ± 11.5 mmHg and 4.3 ± 1.2 s (caudal), lamina propria and were more abundant in respectively. These findings for the three the proximal region. The muscularis muco- distinct regions were correlated with the re- sae was poorly developed and the submu- sults of a histological study (26). cosa was straight and consisted of relatively Luis da Mota et al. (27) carried out a dense connective tissue containing large morphological and histochemical investiga- blood vessels. tion of the intestinal tract in the three-toed The same authors (27) also reported that sloth (Bradypus tridactylus = variegatus). the jejunum possessed circular folds on its The animals studied were two male and two luminal surface and that these resembled female specimens captured in the forests those seen in the duodenum except that the outside Recife. It was found that the intes- villi were longer and narrower. The villi tine averaged 198.5 cm in length and that it were lined with a simple columnar epithe- was almost totally uniform in diameter, al- lium with a well-developed striated border; though very dilated in the rectal region. The goblet cells were scattered throughout the wall of the intestine was seen to consist of epithelium. As in the duodenum the crypts mucosa, submucosa, tunica muscularis and of Lieberkühn were shallow, but sometimes serosa. The mucosa itself could be subdi- branched. In the ileum there were alternate vided into epithelium, a lamina propria (con- smooth areas, occasional branched folds and sisting of loose connective tissue containing small sinuous rugae. The mucosa was lined collagenous and elastic fibers amongst which with a simple columnar epithelium contain- were fibroblasts, small lymphocytes, eosino- ing goblet cells. The villi in this region be- phils and macrophages) and a thin layer of came shorter distally near the large intestine. smooth muscle (the muscularis mucosae). The crypts of Lieberkühn contained more The submucosa was also made up of loose goblet cells at their base than in the jejunum. connective tissue and the tunica muscularis In the sloth the large intestine has been of an inner circular and outer longitudinal seen to consist of a short colon and a dilated layer of smooth muscle between which gan- rectal pouch; no cecum exists. On the inner glion cells of Auerbachs plexus were pre- surface of the colon alternate smooth areas sent. The serosa was seen to consist of meso- and longitudinal folds are present (27). No thelial cells resting on delicate fibrous con- villi are apparent and the surface epithelium nective tissue. The duodenum was recorded is again composed of columnar cells with a as averaging 9.5 cm in length with a thicker striated border, but these are less prominent wall than the remainder of the intestine. On than in the small intestine. More goblet cells the luminal surface of its proximal third are present than in the jejunum and ileum. were five or six distinct longitudinal folds The luminal diameter of the rectal pouch is and in the medial third packed circular folds very large in comparison to the rest of the running in a sinuous fashion. The folds in the intestine and the markedly thickened walls distal third were small and irregular. From possess several well-developed folds of vary-

Braz J Med Biol Res 34(1) 2001 Biology of the sloth 15 ing size running in a sinuous manner. The the leaves, flowers, shoots and fruit of the mucosa is similar to that seen in the colon, ymbahuba (embauba) tree (Cecropia sp). It but the muscularis mucosae is very well was once believed that these were the pri- developed. The tunica muscularis, contain- mary if not only source of food for these ing many elastic fibers, is also thicker in the animals, but Montgomery and Sunquist (23), rectal pouch than in any other part of the who studied Bradypus variegatus, found that intestine. Some further details regarding the the animals ate the leaves of not less than 28 histology of the rectum in Bradypus varie- different trees and 3 vines. It was observed gatus were supplied by Padovan et al. (28), that the choice of leaves eaten by an indi- who also emphasized that water absorption vidual sloth was influenced by those eaten mainly occurs in this region of the digestive by its mother during the 6-month period tract. when it was carried by her. Leaves eaten It has been observed (27) that the longitu- from other trees included those from the dinal and circular folds seen in the intestine various species of Ficus, the wild plum (Spon- of the three-toed sloth have the same histo- dus lutea), Protium panamense, Poulsenia logical structure as those seen in most other armata, Eriobotyra japonica, Luhea and mammals. Argyrophilic and argentaffin cells Bombax longiflorum. In the Santa Lucia Ecol- are found throughout the entire length of the ogy Preserve (Espírito Santo) Chiarello (30) sloth intestine, but Paneth cells are absent. It reported that 99% of the diet of Bradypus was suggested (27) that the absence of a torquatus was composed of leaves. These cecum is probably compensated for by the were predominantly young ones and espe- enzyme activity that takes place in the large cially so during the wet season when they sacculated stomach and that the slow ab- were more abundant. Chiarello listed all the sorption of nutrients may be assisted by the plants consumed and also reported the per- numerous villi present in the small intestine. centage of time spent feeding on each. The Concentrations (ng/g wet weight of tis- most important species making up the diet sue) of 4 neuropeptides have been measured were Prunus sp, Ficus sp, Micropholus (29) in the colon of Choloepus didactylus venulosa, and the vine Mandevilla sp. Flow- and found to be as follows: VIP, 275 ± 26; ers and fruit of Mandevilla sp and Cecropia PHI, 225 ± 18; substance P, 97 ± 17, and hololeuca were consumed. The diet of these met-enkephalin, 128 ± 32. Mechanical and maned sloths, as in other species, was highly intracellular electrical activity has also been selective as less than 4% of the 476 trees recorded (29) in the smooth muscle of the recorded as present were utilized as food. colon. Spontaneous mechanical activity was Moreover, the species mostly chosen were found to consist of 5 to 6 individual phasic not those present at highest density. contractions during each 4-min period. The In captivity, citrus fruits, lettuce and ba- resting membrane potential averaged 58 ± 4 nanas are accepted by three-toed sloths, al- mV and the amplitude of the inhibitory junc- though it is very difficult to maintain the tion potential ranged from 1-3 mV with no animals alive for long periods of time. It has accompanying circular muscle relaxation. It been argued (23) that three-toed sloths may was suggested (29) that the absence of a starve to death on a full stomach if the wrong prominent inhibitory innervation may be as- selection of food is made, due to the slow sociated with low concentrations of VIP and digestion of leaves. The same workers also PHI and might account for the sloths in vivo estimated that sloths on Barro Colorado Is- pattern of colonic motility. land cropped only 0.63% of the total annual As pointed out by Goffart (2), the differ- leaf production of the forest, much less than ent species of Bradypus live principally on the 7% attributed to insects. Manganese is an

Braz J Med Biol Res 34(1) 2001 16 D.P. Gilmore et al.

element naturally occurring in the leaves to be 6 days (4). In free-living Bradypus eaten by three-toed sloths, but is not assimi- variegatus, about 56 g (dry weight) of feces lated. Nagy and Montgomery (31), by meas- was seen to be deposited every 8 days in a uring the increase in concentration of man- shallow depression punched out by the sloth ganese between the food ingested and the with its tail on the forest floor within 3 m of feces produced, estimated that three-toed a tree used by the animal (9). It was also sloths (Bradypus variegatus) on Barro Colo- reported (23) that two-toed sloths, which rado Island in the Panama Canal Zone con- lack a proper tail, usually left their feces on sumed 15 g dry food (kg/day) during the dry the soil or litter surface. In the two-toed sloth season. This is higher than the earlier esti- the feces were found to be firm and were mate of 6.9 g kg-1 day-1 (32) calculated from passed as single pellets or as a large com- measurements of oxygen consumption and pacted mass of compressed individual pel- the time budgets of free-living animals. It is lets (33). It was also observed (9) in three- also appreciably more than that of 5.1 g kg-1 toed sloths fitted with gastric fistulae that day-1 calculated (23) from measurements of young leaves were digested more rapidly feces production rates in the field with an and that the oldest leaves which were di- assumed assimilation efficiency of 50%. gested fastest were those from trees that Choloepus is much easier to maintain in were ranked highest in use by some sloths. captivity outside its normal habitat than Bra- The rates at which leaves were digested were dypus, and survives indefinitely on Cecro- much slower than those reported for other pia, bananas, oranges, figs and even meat herbivorous mammals and the rate of pas- and fish. Colonies of Choloepus hoffmanni sage of food was the slowest recorded for and Choloepus didactylus were kept healthy any mammal. Around two and a half days in Chicago on a wide variety of food includ- were required for the passage of 5% of glass ing diced apples, oranges, bananas, lettuce, beads 3 mm in diameter fed to the animals, spinach, bread, sweet potatoes, green beans, and 50 days before 95% of them were passed. peas, canned salmon, freshly ground smelt Foley et al. (34) believe that these results are and ground meat sprinkled with a powder questionable, because the beads probably containing vitamins and minerals (4,33). accumulate and are retained in the pre-py- Meritt (4) observed that daily food consump- loric region of the stomach. Foley et al. (34) tion by individual adult two-toed sloths (Cho- examined digestion near Cayenne, French loepus hoffmanni) averaged 350 g/day, i.e., Guiana, in 6 captive specimens of Bradypus 85 g/kg body weight. This was during a tridactylus fed exclusively on Cecropia period of acclimation after capture. In fully palmata. Digestive passage was measured acclimated sloths food intake averaged 250 by use of various markers dosed in liquid g/day, dropping off a little just before the form. The particulate digestive phase was periodic defecation, when 30% of the body marked with three rare earth elements ad- weight could be lost. This is not surprising, ministered in solution and the solute diges- as it has also been recently found (34) that tive phase with three complexes of ethylene- the proportion of body mass contained in the diaminetetraacetic acid. After the animals gut ranges from 17 to 37%, values similar to were killed at pre-determined intervals fol- those reported in earlier studies. It was noted lowing feeding, ranging from 6 to 288 h, (33) that in captivity the period between samples were collected from 10 regions of evacuations varied from 3 to 8 days and that the gut. By analysis of the marker content in the feces were always deposited in the same the different parts of the digestive tract it was spot. In confined two-toed sloths, the longest possible to construct cumulative excretion period between eliminations was observed curves. These indicated that the mean reten-

Braz J Med Biol Res 34(1) 2001 Biology of the sloth 17 tion time of the particulate and solid diges- basal metabolic rate in leaf-eating mammals tive markers was around 150 h. Seventy- may reduce the absorption of these sub- three per cent of this retention was in the stances. stomach and 17% (because of storage of The mean energy expenditure for Brady- feces) in the rectum. From these observa- pus has been estimated to be 95.5 kcal/day tions it was argued (34) that there is now (32). This does not agree with another study little support remaining for the earlier view (23) reporting that the daily intake of food (13) that a diverticulum acts to prolong the provided energy of only about 54.4 kcal. retention of food. Foley et al. (34) observed McNab (32) suggested that the difference that the proportion of short-chain fatty acids between these estimates of energy expendi- present in the stomach was broadly similar ture and the energy provided by the food to that present in other foregut fermenters eaten may reflect higher rates of decay in the eating fibrous diets, but the rate of fermenta- feces than assumed by other workers (9). tion measured in vitro was very slow in comparison to the latter animals. It was there- Arthropods associated with sloths fore postulated (34) that the slow fermentation rate is most likely due to the lignified Sloths act as hosts to a wide variety of nature of the Cecropia foliage the animals arthropods, which include biting and blood- were fed, but perhaps also to the low body sucking flies such as mosquitoes and sand- temperature of sloths. The same investiga- flies, triatomine bugs, lice, ticks and mites. tors further argued that although digestion in However, there is a noticeable absence of sloths is characterized by both slow rates of fleas and anoplurans associated with the ani- passage and fermentation of a large volume mals, although the flea Polygenis atopus, of digesta in the forestomach yielding en- which feeds primarily on rodents and marsu- ergy only gradually, this is feasible because pials, has been recorded from Bradypus of the sloths low energy expenditure. infuscatus = variegatus in Venezuela (36). McNab (35) examined the energetics of a Sloths also carry a highly specific commu- large variety of arboreal leaf eaters and con- nity of commensal beetles, mites and moths. firmed that the xenarthrans have low basal Waage and Best (37) investigated in detail a rates varying from 40 to 60% of the expected number of the different arthropods associ- values. Earlier the same author (35) had ated with Bradypus tridactylus, Bradypus found that the basal metabolic rate for Cho- variegatus and Choloepus didactylus in the loepus was only 45% and that of Bradypus vicinity of Manaus, while Wolda (38) car- only 42% of the values expected from their ried out a comprehensive study of the sea- respective body weights. He suggested the sonal distribution of sloth moths in Panama. following explanations as to why these low Up to 6 species of ticks of the genus basal metabolic rates may exist: a) In arbo- Ambylomma have been recorded from both real mammals muscle mass makes up only a two- and three-toed sloths in Central and relatively small proportion of the body which South America, but the opinion is (37) that therefore has a larger proportion of tissue only Ambylomma geayi and Ambylomma with low metabolic rate. b) Leaves have only varium are truly specialized for living on a low available caloric density. Since the sloths as these ticks are rarely found on other maximal daily bulk that can be processed is hosts. The other four ambylommid ticks ap- limited, the energy available from this diet is parently only occur on sloths accidentally. It low. c) A number of toxic substances includ- was also observed (37) that adult males of ing alkaloids, phenols and terpenes are pre- Ambylomma geayi may remain on their hosts sent in leaves. As mentioned earlier, the low for more than three weeks, but the females

Braz J Med Biol Res 34(1) 2001 18 D.P. Gilmore et al.

leave after engorging to oviposit. Infestation very few beetles were caught. On Barro Colo- with ticks can be extremely high. At the rado Island in Gatun Lake, higher numbers Instituto Nacional de Pesquisas da Amazonia of beetles were captured during the rainy in Manaus, Waage and Best (37) recorded season. In Fortuna (a dam site on the Chiriqui that 99% of three-toed and 86.7% of two- River and a relatively non-seasonal region) toed sloths carried Amblyomma spp. There there was a tendency towards a bimodal was no apparent correlation between the distribution in the numbers captured which, numbers of ticks at any life stage per sloth however, were comparatively low as the spe- and the seasonal difference in rainfall in cies was also rare in the area. Wolda and Manaus and nothing is known about the Estribi suggested that the beetles have dis- host-finding behavior of either Ambylomma persal flights at the beginning and end of the geayi or Ambylomma varium. Pinder (6) re- rainy season and that part of the population corded many ticks (Ambylomma varium) un- might enter reproductive diapause and dis- derneath the thighs of maned sloths (Brady- perse from the sloths to sites with some pus torquatus) examined in the Poço das moisture and then resume reproduction at Antas Biological Reserve in the State of Rio the end of the dry season and return to the de Janeiro; one specimen of Boophilus sp sloths. In Fortuna, where the rain falls either was also found. Interestingly, Pinder reported as drizzle or in tropical storms, flight activity that 83% of the ticks were males and on 60% (and therefore capture) of the beetles could of the sloths only male ticks were present. be affected. On the other hand, beetles caught A number of commensal beetles, mites in Fortuna may have been merely dispersing and moths are found in association with from elsewhere. sloths and their dung. Adults of several scarab Waage and Best (37) identified three spe- beetle species are frequently found in the fur cies of macrochelid ascarine mites (Macro- of three-toed sloths, but have not been re- cheles impae, Macrocheles uroxys and Ma- ported to be associated with Choloepus. crocheles lukoschusi) in the anus and inside Waage and Best (37) discovered more than the rectum of three-toed sloths from Curari 980 such beetles (Trichilium adisi) in the fur Island and Manaus. They also reported ear- of a single sloth (Bradypus variegatus) col- lier findings of blood-sucking mites (Lipo- lected on Curari Island in the Central Ama- nissus inheringi, Lobalges trouessarti and zon region, and stated that beetles of the Edentalges bradypus) on three-toed sloths genus Uroxys have been recorded from sloths collected in southern Brazil. Fain (40) re- in Bolivia, Brazil, Colombia and Panama. corded the mite Edentalges choloepi on Cho- The scarab beetles occur near the elbow or loepus didactylus. An interesting relation- on the flanks behind the knees buried deep ship apparently exists between the mites inside the fur. Waage and Best observed that Macrocheles impae and Macrocheles uroxys although the numbers of scarab beetles fluc- and the sloth beetles Uroxys besti and tuated during the year, seasonal factors af- Trichilium adisi on which they occur. Only fecting the populations were unknown. Beetle adult female mites have been observed and larvae feed on sloth dung and the adults may only occasionally on Trichilium adisi. Waage utilize this as food too. The presence of and Best (37) postulated that the role of the Trichilium sp has been reported in the under- beetles may be to transport the adult female fur of the lower back and thighs of Bradypus mites from a diminishing dung pile to an- torquatus (6). Wolda and Estribi (39) identi- other sloth. The third macrochelid mite (Ma- fied and counted sloth beetles (Uroxys crocheles lukoschusi) was not found in asso- gorgon) captured in light traps at five loca- ciation with the scarab beetles. tions in Panama, although in three of these Moths of the subfamily Chrysauginae

Braz J Med Biol Res 34(1) 2001 Biology of the sloth 19 spend their lives as adults in the fur of sloths, cola hahnelli is found deep inside the sloths particularly the three-toed species. It was fur where it is able to move very rapidly; found (6) that the most common ectoparasite most adults have truncated wings (presum- on maned sloths (Bradypus torquatus) was ably broken by abrasion) and are thus inca- Cryptoses sp which were found hiding in the pable of flying. Waage and Best (37) also fur. It has been suggested (38) that there the pointed out that the population sizes and sloth moths may receive some protection dynamics of the sloth moths are dependent from avian predators and possibly find nutri- on the availability of sloth dung and thus on ents in secretions of the sloths skin and/or the density of these mammals; seasonal fac- the algae present on the fur. Waage and Best tors such as rainfall may have secondary (37) reported that some three-toed sloths effects. may carry in excess of 120 moths; lower Wolda (38) investigated the seasonal dis- numbers may occasionally be seen on two- tribution of Cryptoses choloepi at three loca- toed sloths. They also pointed out that there tions in Panama where it is associated with is considerable sympatry amongst moth spe- both Bradypus infuscatus and Choloepus cies found on sloths and that several differ- hoffmanni. He used light traps to collect ent species may coexist on the same animal. moths on Barro Colorado Island, in Las Waage and Best (37) concluded that the Cumbras (a residential area near Panama most striking characteristic of the various city) and at Fortuna. Wolda observed that arthropods associated with sloths is the large although there were some notable differ- number of coprophagous species which ap- ences between the years in the seasonal pat- pear to depend on the animals for phoresis. terns of abundance of sloth moths on Barro They speculated that the great diversity of Colorado Island, numbers were generally phoretic coprophages on sloths has evolved very low during the early part of the dry because of a strong selection for phoresis season (January to mid-March). They then and the ideal conditions existing for trans- increased to peak around mid-May before port on the sloths. Larval stages of the moths declining again towards the end of the rainy live in and feed on the sloths dung, the adult season. During the dry season most moths females presumably leaving the sloths dur- were captured close to the ground, but during defecation to deposit their eggs there. ing the rainy season more were caught in the Waage and Best described how early larval canopy. At the end of the year approximately stages of the pyralid sloth moth Cryptoses equal numbers were collected from both choloepi are covered by a light silken web; situations. At Las Cumbras a broad abun- later this becomes a long silken tube within dance of moths was again seen during the which the larva feeds and then pupates. early part of the rainy season, but numbers Newly emerged moths migrate to the forest then continued to increase to peak in Janu- canopy to locate a sloth. Waage and Best ary. Numbers fell only during the very end of also reported that the sex ratio of the moth the rainy season or in the first half of the dry Cryptoses choloepi is 1:1 at emergence, but season. At Fortuna, during the early part of on Bradypus the females are outnumbered the year when the light trap was in the canopy, 3:1 by males. This led Waage and Best to more moths were captured than later in the suggest that females are possibly lost from year when it was transferred close to the the sloth-bound population when they leave ground. Wolda believes that although sea- to oviposit. The life histories of sloth moths sonal changes in rainfall may have little other than Cryptoses choloepi are less well direct effect on moth numbers, indirectly known, but several are believed to be broadly this might be very important. Wolda (38) similar to this species. However, Bradypodi- also speculated that a rise in sloth mortality

Braz J Med Biol Res 34(1) 2001 20 D.P. Gilmore et al.

during periods of increased cloudiness (due signs of illness. to interference with the animals thermoregu- Other investigations (42) in Panama have latory mechanisms) might result in more indicated that there is a high prevalence of moths becoming air-borne in search of new the St. Louis encephalitis virus in sloths, hosts. Furthermore, after a peak in sloth particularly Choloepus. This virus, which reproduction (around September) there can cause human encephalitis, occurs would be consequently more sloths defecat- throughout the Americas from Canada to ing on the forest floor making it easier for the Argentina but in the tropics is presumed to moths to find hosts. be enzootic and probably only causes sporadic human illness (42). Seymour (41) sug- Arboviruses and other diseases gested that although sloths may be important associated with sloths hosts for the St. Louis encephalitis virus, they are presumably only infrequently in- Seymour (41) has reviewed the role of fected and gradually build up antibodies over sloths as the possible hosts to a whole variety a lengthy period of time; infected animals of arthropod-borne viruses (arboviruses), cit- show no overt signs of disease. It has been ing work carried out in Belém (Brazil), and found (42) that captive two- and three-toed in Panama. However, whether or not sloths sloths responded to inoculation with the St. are essential or only incidental to the natural Louis encephalitis virus with remarkably cycle of an arbovirus, their long experimen- long-lasting viremias of high titer. The dura- tal viremias are remarkable and Seymour tion of detectable viremia ranged from 7 to suggests that these may be due to the ani- 27 days (median 11) in Choloepus hoffmanni mals low metabolic rate. and from 13 to 24 days (median 18) in Antibodies to the mosquito-borne Ven- Bradypus variegatus. Interestingly, the on- ezuela encephalitis virus, which can prove set of experimentally induced St. Louis en- fatal in horses, have been found in Bradypus cephalitis viremias was delayed and the maxi- variegatus and Choloepus hoffmanni col- mum titer levels were depressed in two sloths lected in Panama. Seymour (41) concluded concurrently infected with the Bradypus-4 that Bradypus in particular is a potential virus and an agent related to the Changuinola source of infection for this virus as it devel- virus. When mosquitoes (Culex pipiens ops higher concentrations of it in blood, quinquefasciatus) were allowed to feed on detectable for longer periods of time than for infected sloths 80% were able to transmit St. most other forest species tested. In contrast, Louis encephalitis to chicks or mice after 14- two-toed sloths had low concentrations of 27 days intrinsic incubation. Whether, how- the Venezuelan encephalitis virus in blood; ever, sloths play an important role in the the duration was unreported. Another infec- transmission of the St. Louis encephalitis tion carried by mosquitoes (the Mayaro vi- virus to humans is as yet uncertain. Some- rus) causes sporadic outbreaks of human what surprisingly, a young three-toed sloth febrile illness in forested areas of South housed with its experimentally infected non- America and Trinidad. Although sloths can lactating mother became infected with the be infected in the laboratory, this, according St. Louis encephalitis virus, indicating that to Seymour, only occasionally takes place in contact transmission is possible. Another the wild. Similarly, sloths would appear to virus antigenically related to the St. Louis play no important role in the transmission of encephalitis virus and to yellow fever is the the yellow fever virus. Although the animals Ilheus virus which occasionally causes hu- can be inoculated with it, the infection pat- man febrile illness and encephalitis. How- terns are erratic and there are no apparent ever, Seymour (41) has reported that as anti-

Braz J Med Biol Res 34(1) 2001 Biology of the sloth 21 bodies to the virus were found in only one of cluding the St. Louis encephalitis and 167 three-toed and just one of 99 two-toed Oropouche viruses) for which the role sloths sloths tested in Panama, this is a good indica- play in the natural cycles is as yet uncertain. tion that these animals are not important Simultaneous productive infections appear vectors of the disease. to be possible in these animals. Seymour (41) has reported that the It has been reported (44) that the phle- Oropouche virus (apparently transmitted by botomine sandfly is also a known vector of Culicoides midges) has been isolated from a the flagellate protozoan Leishmania which small number of sloths (Bradypus tridacty- causes cutaneous leishmaniasis in humans. lus) in Brazil. The virus is known to cause All species belonging to the genus Leishma- periodic epidemic febrile illness amongst nia are morphologically similar, except for humans in the State of Pará. Sloths are also minor differences in their size. It was also possible reservoirs for the Utinga virus also pointed out (45) that sloths are proven or carried by Culicoides midges and by Anoph- suspected reservoirs of at least five Leishma- eles mosquitoes. Seymour stated that the nia species belonging to the Leishmania bra- virus has been isolated from Bradypus tri- ziliensis complex of the subgenus Viannia, dactylus and that Bradypus variegatus and i.e., Leishmania b. colombiensis, Leishma- Choloepus hoffmanni from Panama have nia b. equatoriensis, Leishmania b. guya- been found to be positive for the virus too. nensis, Leishmania b. panamensis and Leish- However, the antibody results concerning mania b. shawi, responsible for human cuta- wild sloths are confused by possible cross- neous and/or mucosal leishmaniasis. reactions with the Utive and Pintupo viruses; Shaw et al. (46) noted that in the eastern all three, which are members of the Simbu region of the State of Pará in Brazil, south of serogroup, are sloth-specific. Antibodies to the Amazon River, Leishmania b. shawi fre- the Utive virus have been found in two- and quently infected humans, whereas north of three-toed sloths collected in Panama. the river Leishmania b. guyanensis was the According to Seymour (41), different most common cause of human leishmania- phleboviruses (carried by phlebotomine sand- sis. Leishmania b. colombiensis has also flies) have on occasion been identified in sloths. been isolated from humans, sandflies and a Strains of the Changuinola virus have been two-toed sloth (Choloepus hoffmanni) cap- isolated from both two- and three-toed sloths tured in Panama (47). Herrer and Christensen in Panama and this complex of viruses appears (48) found that in Panama Choloepus to be sloth-specific. Seymour et al. (43) also hoffmanni showed the highest infection rate reported the isolation of the previously un- with Leishmania b. guyanensis amongst all identified infectious agent (the Bradypus-4 forest mammals in which natural Leishma- virus) from a male sloth (Bradypus variega- nia infections were demonstrated. Of Leish- tus) captured in Panama. Seymour et al. (43) mania b. guyanensis infections in 95 sloths, believe this to be an RNA virus with a lipid- 33.7% were seen in the skin only, 42.1% in containing envelope; it was negative when the viscera (including blood and bone mar- tested against 216 world-wide arboviruses. row) only, and 24.2% in both regions. Infec- Seymour (41) finally concluded that the tion rates were proportional to the age of the wide variety of arboviruses isolated from animals, rates being higher in young sloths sloths can be characterized according to an- than in juveniles and adults. Herrer and tibody and virus isolation data as being sloth- Christensen (48) suggested that sloths prob- specific (Utinge, Utive and Changuinola vi- ably become infected during the first few ruses), incidental in sloths (such as the Ven- months of life and remain infected for a long ezuelan encephalitis viruses), or others (in- time, although since the parasites disappear

Braz J Med Biol Res 34(1) 2001 22 D.P. Gilmore et al.

from some animals the disease might be self- they may have evolved in the group. limiting. Herrer and Christensen (48) con- Many striking similarities exist between cluded that Choloepus hoffmanni is the prin- Leishmania and parasites of the genus Endo- cipal reservoir for Leishmania b. guyanensis trypanum which have at least three distinct in Panama and that because the animals stages in their life cycle. In sloths they exist survive infections without evidence of pa- as intra-erythrocytic epimastigotes (Endo- thology this indicates a long association trypanum schaudinni) or trypomastigotes which appears to have evolved into a com- (Endotrypanum monterogeii) while the pro- mensal relationship. Ecological and epide- mastigote stage is seen in sandflies and in miological investigations (48) also revealed culture. Shaw (51) reported that Endotry- a close relationship between geographical panum schaudinni has been recorded in Cho- distribution of human cutaneous leishmani- loepus didactylus and Choloepus hoffmanni asis and the presence of leishmanial infec- and in Bradypus variegatus and Bradypus tion in two-toed sloths. Furthermore, it was tridactylus in Costa Rica, Panama, French found (49) that Choloepus didactylus was a Guiana and Brazil. In all instances, however, reservoir for Leishmania b. guyanensis in far more two- than three-toed sloths were French Guiana in areas where dermal leish- infected with this parasite. Endotrypanum maniasis is frequent among humans. monterogeii has been isolated from two- Christensen et al. (50) carried out precip- toed sloths (Choloepus hoffmanni) in Costa itin tests on blood taken from over 2500 Rica. Another previously undescribed eryth- engorged female sandflies collected in the rocytic parasite was identified in a two-toed forest alongside the Torquato Tapajós high- sloth (Choloepus didactylus) captured in way near Manaus. The most prevalent sandfly French Guiana (52). The organism, morpho- collected was Lutzomyia umbratilis and logically related to the Babesiidae family, xenarthrans were found to be the most com- was named Babesia choloepi and is the first mon hosts of this insect and also of Lutzomyia Babesia species to be identified in a anduzei. Interestingly, the overwhelming xenarthran. majority of sandflies feeding on sloths were Flagellates of the genus Trypanosoma, found on Choloepus didactylus. Christensen which occur as trypomastigotes in their ver- et al. (50) therefore decided that this would tebrate host, have been found in a variety of implicate two-toed sloths as the major reser- xenarthrans including sloths. Shaw (51) re- voirs of Leishmania braziliensis in the north- ported that Trypanosoma mesnilbrimonti and ern Amazon region and also probably Trypanosoma preguici were isolated from throughout these animals total range (i.e., Choloepus didactylus in northern Brazil and from Nicaragua to central Brazil). Shaw (51) French Guiana. Trypanosoma preguici has also concluded that in this region the two- been identified from Choloepus hoffmanni toed sloth is the major vertebrate host of in both Costa Rica and Panama and from Leishmania b. panamensis, although Brady- Bradypus variegatus in Costa Rica. Trypa- pus variegatus is occasionally infected as nosoma leewenhoeki occurred in both Cho- well; here the sandfly Lutzomyia trapidoi is loepus hoffmanni and Bradypus variegatus the vector for the disease. In Costa Rica in Costa Rica and Panama. Moreover, Try- Leishmania herreri has been isolated from panosoma leewenhoeki has been isolated both Choloepus hoffmanni and Bradypus from Choloepus hoffmanni inhabiting the variegatus. All the Leishmania of xenarthrans Pacific coast of Colombia (53). Although that have been studied in sandflies are Trypanosoma cruzi has been recorded from peripylarians, a type of Leishmania found in Choloepus hoffmanni and Bradypus variega- New World mammals; it was suggested that tus in Panama, Shaw (51) believes they are

Braz J Med Biol Res 34(1) 2001 Biology of the sloth 23 accidental hosts and not reservoirs. Shaw The animal had been kept in captivity close (51) discussed in some detail the relation- to a group of coatimundis (Nasua narica) ship of infections to host behavior and habi- which carried the infection. Some time later tat, and pointed out that if a vector has a an apparently healthy two-toed sloth (Cho- narrower habitat preference than its verte- loepus didactylus) also captured in Pará was brate host there will consequently be unin- autopsied. Abundant division stages of fected populations of the latter. Shaw pon- Pneumocystis were found in the lungs. It was dered whether differences in behavior and concluded (55), however, that human con- the wider habitat range of Choloepus com- tact with infected wild animals in their natu- pared to Bradypus might at least partly ex- ral environment is so slight that there would plain some of the observed variations in be little chance of direct transmission, al- hemoflagellate infection rates between two- though there is an obvious risk to those and three-toed sloths. Herrer and Christensen handling captive animals. This is borne out (48) examined 498 sloths captured in the by the identification (56) of Pneumocystis Panamanian forest over a 10-year period carinii in the lungs of 23 zoo animals that and, interestingly, found that 19.3% were died in the Netherlands over an 11-year pe- infected with Leishmania braziliensis, 29.5% riod. One of these was a three-toed sloth with Endotrypanum schaudinni, 19.0% with (Bradypus tridactylus) that had been im- Trypanosoma rangeli, and just one animal ported from Surinam three months earlier. with Trypanosoma cruzi. Pneumocystis has also been isolated from a Toxoplasmosis has also been identified female three-toed sloth (Bradypus variegatus) by Shaw and Lainson (54) in a two-toed collected from the Panamanian jungle (57). sloth (Choloepus didactylus), although in Diniz and Oliveira (58), who carried out a this instance it was uncertain as to whether 20-year retrospective study on 17 two-toed the infection had been acquired in captivity and 34 three-toed sloths in the São Paulo Zoo, or in the wild. Nevertheless, these authors noted that malnutrition accounted for 45.7% did point out that the disease has been re- and respiratory disease for 13.8% of the clini- corded in other xenarthrans (the nine-banded cal disorders recorded. Digestive dysfunction armadillo Dasypus novemcinctus and lesser was responsible for 12.3% of the illnesses - anteater Tamandua tetradactyla). The sloth, just under half of these involving the presence collected from the Barcarena district of Pará, of Ascaris spp. Bacteria including Escherichia had been in the laboratory for 66 days when coli, Citrobacter freundii and Salmonella en- it was found to be infected with Toxoplasma teritidis were isolated from the feces and/or gondii. Hamsters and mice inoculated with organs of 13 sloths. homogenates of liver and spleen from this Interestingly, parasites have even been animal died within 7 days. The largest num- recorded in dung balls of the extinct Shasta ber of parasites was present in the liver, ground sloth (Nothrotheriops shastensis) lungs and spleen, but endozoites were also collected from Rampart Cave at the western detected in stained smears of blood, heart, end of the Grand Canyon in Arizona. These kidneys and peritoneal exudate. animals appear to have been completely her- The protozoan Pneumocystis carinii, bivorous and Schmidt et al. (59) identified which causes lung infections in a wide vari- juveniles of two different nematode species, ety of mammals and is implicated as a cause two morphotypes of coccidian oocysts and of pneumonia in patients with AIDS, has eggs of two species of helminths in their been found in the lungs of sloths. The dis- feces. The dung was dated to 10,000 ± 80 ease has been identified in a three-toed sloth years and, like the sloths, these parasites are (Bradypus tridactylus) in Pará, Brazil (55). now also believed to be extinct.

Braz J Med Biol Res 34(1) 2001 24 D.P. Gilmore et al.

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