Brazilian Journal of Medical and Biological Research (2000) 33: 129-146 Physiology of sloths 129 ISSN 0100-879X An update on the physiology of two- and three-toed sloths 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 Physiological and pharmacological research undertaken on sloths Key words C.P. Da-Costa during the past 30 years is comprehensively reviewed. This includes · Xenarthra Departamento de Fisiologia e the numerous studies carried out upon the respiratory and cardiovas- · Sloths Farmacologia, UFPE · cular systems, anesthesia, blood chemistry, neuromuscular responses, Bradypus 50670-901 Recife, PE · Choloepus the brain and spinal cord, vision, sleeping and waking, water balance Brasil · Physiology Fax: +55-81-271-8350 and kidney function and reproduction. Similarities and differences E-mail: [email protected] between the physiology of sloths and that of other mammals are discussed in detail. Research supported by CNPq and FACEPE. D.P. Gilmore is the recipient of a Royal Society and Brazilian Academy of Sciences Introduction tion has been proposed (3), which places the international exchange fellowship. two-toed sloths in the family Megalonychidae It is almost 30 years since Goffart (1) and the three-toed sloths in the family published Function and Form in the Sloth Bradypodidae. It is thus now generally be- Received March 31, 1999 and in the time that has now elapsed there lieved that the two living families of sloths Accepted October 14, 1999 has been no further comprehensive evalua- have quite different phylogenetic origins and tion of the biology of this mammal. It is the that Bradypus is derived from megatheroid intention of the present review to bring to- and Choloepus from megalonychid sloths, gether research reports of physiological and their separate evolution beginning about 35 pharmacological studies that have appeared million years ago in the late Oligocene. since 1971 and thereby update our knowl- The distribution of two- and three-toed edge about this intriguing animal. sloths in South America is illustrated in Fig- Sloths are included, along with the arma- ures 1A and B. Bradypus variegatus, the dillos and anteaters, in the Order Xenarthra brown-throated three-toed sloth, is one of (Edentata). Analysis of amino acid sequences the most common medium-sized mammals of the eye lens proteins (2) has confirmed in the tropical forests of Central and South earlier anatomical evidence indicating that America. Previously many workers have re- the xenarthrans are an old offshoot of the ferred to the species as Bradypus tridactylus eutherian stem that arose at least 75-80 mil- but this, the pale-throated three-toed sloth, is lion years ago. Initially all present-day sloths now regarded as the one found only in south- were considered to belong to the family ern Venezuela, the Guianas and northern Bradypodidae with two genera, Bradypus Brazil south to the Rio Amazonas. Through- and Choloepus. However, a new classifica- out this review an attempt has been made to Braz J Med Biol Res 33(2) 2000 130 D.P. Gilmore et al. distinguish between the misnamed Brady- from 32.7o to 35.5oC (4). In most, their basal pus tridactylus = variegatus and the rightful metabolic rates lie between 40 and 60% of bearer of the title. those expected from their mass on the basis All xenarthrans have low body tempera- of Kleibers rule and in the case of the tree tures compared to other mammals, ranging sloths may be directly related to the reduc- tion in muscle mass correlated with their Figure 1 - Distribution of two- A sedentary lifestyle (4). The type of food con- and three-toed sloths through- sumed would also appear to be influential in out Central and South America C. hoffmanni (A, B) (for further details see Choloepus setting the low basal metabolic rates in Wetzel (3)). xenarthrans for, firstly, the food of sloths has a low energy content and, secondly, it may C. didactylus contain poisonous compounds that require a low rate of absorption for adequate detoxifi- cation (4). The low body temperature of both Bradypus and Choloepus, which varies with that of their surroundings, is a major factor restricting their distribution. Goffart (1) dis- cussed thermoregulation in the sloth in de- tail. More recently, Silva et al. (5) recorded rectal temperatures in five adult male sloths (Bradypus variegatus) at four-hour intervals over six days. They observed a circadian rhythm in body temperature (ranging from 28o to 35oC), which was closely correlated with changes in environmental temperature. In cold conditions sloths are poor regulators of body temperature because they have little B ability to increase their metabolism due to their small muscle masses. Thus neither Bra- Bradypus dypus nor Choloepus are able to tolerate cool temperate latitudes. Bradypus has a B. tridactylus 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 B. variegatus thermoneutrality (24oC) than does Choloe- pus (18oC). B. torquatus Respiratory and cardiovascular systems The normal respiratory rate in Choloepus hoffmanni when sleeping has been reported to be 13 per minute (range 10-18), decreas- ing when the rectal temperature exceeded 37oC (6). In captive sloths, with an ambient temperature of 30oC, the respiratory rate was Braz J Med Biol Res 33(2) 2000 Physiology of sloths 131 found to be dependent upon the animals capacity: tidal volume 13.5 ± 3.4%, inspira- state. Excited or agitated sloths have been tory reserve volume 52.6 ± 8.9%, expiratory noted to breathe at a rate of between 10 and reserve volume 9.7 ± 4.7%, residual volume 30 per minute (7). In awake, but inactive, 24.2 ± 6.8%. Inspiratory capacity was 66.1 ± sloths in captivity the breathing rate was 6.6%, vital capacity 75.8 ± 6.8% and func- found to be 46 (range 38-52) breaths per tional residual capacity 33.9 ± 6.6%. In an- minute (6) and in awake and active animals other study (13) the same group analyzed the it was 73 (range 65-78). For both free-roam- active mechanical properties of these ani- ing and captive sloths in Panama, a resting mals lungs and recorded the following: rate of nine breaths per minute (range 8-11) (mean ± SD) 0.33 ± 0.10 cmH2O/l and 0.09 has been reported (6). Respiration and heart ± 0.02 cmH2O/l for resistance and active rates in anesthetized two-toed sloths (Cho- elasticity of the respiratory system. Other loepus didactylus) were 18-48 breaths per research (14) into the passive mechanical minute and 48-108 beats per minute (bpm), properties of the lung and thoracic wall in respectively (8). Félix et al. (9) carried out three-toed sloths (Bradypus variegatus) re- studies on the airway flow and pulmonary corded the following values (mean ± SD) of ventilation of Bradypus variegatus anesthe- 0.183 ± 0.030 cmH2O/ml for passive elastic- tized with sodium pentobarbital, but breath- ity of the respiratory system, 0.045 ± 0.002 ing spontaneously. They reported that the cmH2O/ml for passive elasticity of the pul- tidal volume was 57.6 ± 14.4 ml, the inspira- monary system and 0.134 ± 0.024 cmH2O/ tion time 3.8 ± 0.4 s and the expiration time ml for the thoracic wall, respectively. Active 15.9 ± 0.7 s for a respiratory rate of 3.0 ± 0.8 elasticity and active resistance were found to breaths per minute. Respiratory minute vol- be 13 and 56% higher, respectively, than the ume was 181.3 ± 27.9 ml and the expiratory passive counterparts. pause 13.1 ± 6.8 s. This long respiratory The size of the heart is adapted to the pause observed in the anesthetized animal quiet life of the sloth, but it is by no means was also noted by Santos et al. (10), who responsible for the inability of these animals monitored the breathing of four freely mov- to undertake sustained speedy movement. ing sloths (Bradypus variegatus) in the labo- The heart rate of Bradypus was initially re- ratory using an impedance technique. These ported (7) to range from 60 to 110 bpm, with animals were kept at a constant room tem- that of Choloepus being somewhat higher perature of 26oC for a period of 24 h in a 12- (70-130 bpm). A great deal more informa- h light/12-h dark cycle. The respiratory rate tion has since been obtained on cardiovascu- was 8.6 ± 5.3 breaths per minute (range 4.9- lar function in the sloth, mainly from the 20.6). Breathing was slowest at 11.30 h and group working at the Federal University of most rapid at 2.30 h when there was an Pernambuco in Recife. Research there (15, associated increase in the animals motor 16) on Bradypus tridactylus = variegatus, activity. In other data obtained recently (11), under pentobarbital anesthesia, found heart over a 2-h period from freely roaming sloths rates of 91 ± 4.5 bpm and 94.1 ± 3.3 bpm, in the laboratory at 26oC, the respiratory rate respectively. Another study (17) demon- was found to be 6.1 ± 0.81 breaths per minute strated similar values (91 bpm) in sloths and the expiratory part of the cycle 71%. under chloralose anesthesia. In conscious, Aguiar et al. (12) also determined pulmo- but restrained cannulated sloths (Bradypus nary volume and capacity in eight three-toed tridactylus = variegatus) heart rates of 89.7 sloths (Bradypus variegatus) under sodium ± 9.7 bpm were measured (16).