9 Braz J Med Biol Res 34(1) 2001 Biology of the sloth Brazilian Journal of Medical and Biological Research (2001) 34: 9-25 ISSN 0100-879X Sloth biology: an update on their physiological ecology, behavior and role as vectors of arthropods and arboviruses 1Departamento de Fisiologia e Farmacologia, Universidade Federal de Pernambuco, Recife, PE, Brasil 2Institute of Biomedical and Life Sciences, University of Glasgow, Glasgow, UK D.P. Gilmore2, C.P. Da Costa1 and D.P.F. Duarte1 Abstract This is a review of the research undertaken since 1971 on the behavior and physiological ecology of sloths. The animals exhibit numerous fascinating features. Sloth hair is extremely specialized for a wet tropical environment and contains symbiotic algae. Activity shows circadian and seasonal variation. Nutrients derived from the food, particularly in Bradypus, only barely match the requirements for energy expenditure. Sloths are hosts to a fascinating array of commen- sal and parasitic arthropods and are carriers of various arthropod- borne viruses. Sloths are known reservoirs of the flagellate protozoan which causes leishmaniasis in humans, and may also carry trypano- somes and the protozoan Pneumocystis carinii. Correspondence C.P. Da Costa Departamento de Fisiologia e Farmacologia, UFPE 50670-901 Recife, PE Brasil Fax: +55-81-271-8350 E-mail: cpc@npd.ufpe.br Research supported by CNPq and FACEPE. D.P. Gilmore is the recipient of a Royal Society and Brazilian Academy of Sciences International Exchange fellowship. Received April 12, 2000 Accepted August 7, 2000 Key words �� Sloths �� Ecology �� Behavior �� Parasites �� Bradypus �� Choloepus Introduction We have recently reviewed the literature in terms of the physiological studies carried out on two- and three-toed sloths (1) since Goffart (2) published Function and Form in the Sloth 30 years ago. This paper is intended to update research undertaken since that time on other aspects of sloth biology. Topics covered include the general ecology, behav- ior, nutrition and digestion as well as the large range of arthropods associated with sloths and the number of viruses they trans- mit. Of the two living species of Megalony- chidae, Choloepus hoffmanni is found from the lowland forest to the higher altitudes of mountain forests south of Nicaragua through Central America and in Colombia, Venezu- ela, French Guiana, Ecuador, Peru, Brazil and Bolivia. The species is still common, but its numbers are fewer in areas where it coex- ists with the three-toed sloth. Its weight aver- ages 5.72 ��� 0.69 kg (3). The hair of this species is lighter than in Choloepus didacty- lus. The ears are rounded and thickened and almost always covered with hair. It has been reported (4) that the eyes can be partially retracted when the lids are tightly closed. This may make the sloth appear pop-eyed during periods of stress or prior to the onset of aggressive behavior when the lids appear to rise from their orbits. Choloepus didacty- lus is found from the delta of the Orinoco River west to the upper drainage of this river in Colombia, east through French Guiana and in Brazil to the State of Maranh��o. Its weight is 6.07 ��� 1.09 kg (3). It is less well-

10 Braz J Med Biol Res 34(1) 2001 D.P. Gilmore et al. adapted to the drier areas than is Bradypus. In 1992 its presence was recorded in the Yungas region of Bolivia, considerably fur- ther south than previously reported (5). The distribution of the present day sloths was illustrated in the earlier review (1). Bra- dypus torquatus (the maned sloth) is re- garded as an endangered species, its num- bers having fallen catastrophically with the destruction of the Atlantic coast forest (Mata Atl��ntica) in southeastern Brazil. According to Wetzel (3), Bradypus torquatus is possi- bly the South American mammalian species closest to extinction. Remnant populations are thought to survive in the remaining frag- ments of the Mata Atl��ntica from Rio Gran- de do Norte to Bahia, Esp��rito Santo, and Rio de Janeiro. Wetzel (3) reported that Bradypus tor- quatus appears to be smaller than Choloe- pus, with adults weighing about 4 kg, but Pinder (6) found the maned sloth to range from 4.05 to 6.20 kg in weight and from 520 to 672 mm in length. Infants were character- ized by the absence of a mane. The widely distributed Bradypus variegatus has an av- erage weight of 4.34 ��� 0.85 kg, whereas the pale-throated three-toed sloth, Bradypus tri- dactylus, averages 4.01 ��� 0.28 kg (3). It is obvious that human activity is the major threat to the continued existence of sloths in particular localities. One of the few natural predators of the animals is the Harpy eagle (Harpia harpyja). Izor (7) gathered the skeletal remains of about 83 prey items from a Harpy eagle nest site in southwestern French Guiana and found that sloths (predominantly Choloepus) and cebid monkeys each consti- tuted about one third of all the food prey. Beebe (8) found remnants of Bradypus tri- dactylus in the stomach of a large anaconda and in a margay cat. Izor discussed the rea- sons why sloths might constitute such a high proportion of the Harpy eagle��s diet. The usual hunting time for this bird is around sunrise when ambient temperature is at its minimum. At this time too the activity of both two- and three-toed sloths is minimal and the animals, slowed by thermal stress, are high in the trees seeking early sunshine to warm themselves (9). The sloths are thus susceptible to aerial attack by the Harpy eagles which have enormously developed feet and talons. The formidable weapons enable the birds to strike and dislodge sloths from the canopy without losing flight speed. General ecology and behavior Neither Bradypus nor Choloepus are able to tolerate cool temperature latitudes. Nev- ertheless, both Bradypus griseus = variega- tus and Choloepus hoffmanni have been re- corded living at altitudes higher than 2400 m in the Braulio Carrillo National Park (Costa Rica) and a single specimen of Choloepus hoffmanni was collected in Costa Rica from the Turrialba Volcano at 3328 m where the annual rainfall is 2284 mm and the maxi- mum annual temperature only 16.3oC (10). At higher altitudes the coat of Choloepus is appreciably thicker than in individuals liv- ing at lower altitudes (11). Bradypus has a lower thermal conductance than Choloepus because only the former has a dense woolly undercoat below the coarse guard hairs, and Bradypus also has a lower limit of thermo- neutrality (24oC) than does Choloepus (18oC). According to McNab (11), the cold temperature tolerance of some extinct ground sloths probably stemmed from their great size, larger muscle mass than their arboreal coun- terparts, thick fur and a constant food supply. This enabled them to extend their range into temperate regions of the Americas. The hair of sloths is of special interest because of the presence of symbiotic algae in it at certain times. Sloths have two distinct coats, one made up of long coarse, but silky, hair which provides the distinctive color of the animal and the other made up of short fine and soft fur lying underneath. A detailed description of the pelage of both Choloepus and Bradypus was provided by Beebe (8)

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