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

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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 commen- sal 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 possi- bly 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.
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