An Update on the Physiology of Two- and Three-Toed Sloths

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

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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) discussed thermoregulation in the sloth in detail. 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), decreasing 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). When the pentobarbital anesthesia. They reported the animals were positioned in an experimental following values in relation to total lung chair similar values were recorded (18). In

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contrast, these same animals prior to surgi- be driven. This could be in the neighborhood cal manipulation presented heart rates of of 110 bpm. 71.8 ± 15.9 bpm when in the erect posture in Biotelemetry has been used to monitor the experimental chair. heart rate changes during a period of 24 h in There is a popular impression that sloths sloths (Bradypus variegatus) allowed to roam spend a large part of their time suspended freely in a laboratory (20). Mean heart rate from tree branches hanging upside down. values were 88 ± 8 bpm, but these showed a However, Duarte et al. (18) observed that biphasic variation pattern during the period three-toed sloths (Bradypus variegatus), of observation with the lower values (66 when left free to roam in the laboratory, bpm) being observed during daylight (9.00 spent much of their time seated with the hind h). This variation was directly related to a limbs wrapped around any vertical object decrease in motor activity seen in the ani- available and with the head down upon the mals at this time. The highest heart rate (108 chest. The forelimbs might or might not be bpm) was observed at 19.00 h. When the encircling the upright object. These same ECG pattern was determined a sinus rhythm workers found that in unrestrained condi- was present in all the records. For a mean tions the sloths heart rates were 76 ± 20.8 in heart rate of 81 ± 18 bpm the duration (in the sitting position and 79.8 ± 22.3 in the milliseconds) of the P wave was 49.18 ± suspended one. On the other hand, when 15.57, of the PR segment 71.62 ± 18.11, of these animals were placed in an experimen- the QRS complex 70.45 ± 21.64, of the ST tal chair in the supine posture (similar to segment 113.93 ± 48.46, and of the T wave when suspended in unrestrained conditions) 152.76 ± 48.71. These values for the various their heart rates were lower (79.8 ± 10.7) ECG components are near those obtained compared to those recorded under erect con- for other mammals of the same size. In the ditions (similar to when seated in unrestrained frontal plane the mean P axis was +15o (-60o conditions) which were 87.4 ± 12 bpm. In to +90o), the mean QRS axis was -20o (-100o non-surgically manipulated sloths these val- to +60o) and the T axis was 0o (-75o to +75o), ues were maintained (71.8 ± 15.9 in erect suggesting that the sloth heart lies in a versus 66.2 ± 17.8 in supine), showing that semihorizontal position. the posture adopted by these animals in the In a study (15) on cardiac mass, blood laboratory interferes with the levels of heart temperature and ventricular fibrillation in rate and indicates that they are under stress the three-toed sloth (Bradypus variegatus) after surgical manipulation. comparisons were made with the domestic Other research (19) on the autonomic cat, the latter chosen for having approxi- component in the heart rate of Bradypus mately the same heart and body size. Sloth tridactylus = variegatus demonstrated that hearts were more difficult to fibrillate and atropine raised the heart rate from 83.3 ± once fibrillation was induced it interestingly 10.8 to 96.5 ± 8.6 bpm. Propranolol slowed recovered more quickly than did the heart of the heart rate from 84.5 ± 9.9 to 65.5 ± 5.96 the cat in the same situation. When ventricu- bpm. After double blockade in one order or lar fibrillation thresholds were investigated vice versa, heart rate was 74.2 ± 5.6 bpm, in sloths (Bradypus tridactylus = variegatus) showing that in the animals under laboratory and puppies (21) by using a predetermined conditions there is a slight predominance of train of rectangular pulses the average ven- sympathetic tone at rest. The fact that atro- tricular fibrillation threshold current was 2.3 pine elevated heart rate by only 16% in the ± 0.4 mA/g for the sloth heart and when study suggests that there may be an upper fibrillation was induced 40% of the sloths limit to the rate at which the sloths heart can showed a spontaneous reversal. The average

Braz J Med Biol Res 33(2) 2000 Physiology of sloths 133 ventricular fibrillation threshold current was an extreme lability in the control of blood 0.59 ± 0.14 mA/g for the puppy heart, corre- pressure in this animal (25). Investigations sponding to a significant 4-fold difference in to evaluate the role of pressoreceptors in threshold current between the two animals. awake sloths were carried out by Lima et al. In another comparative study of myocardial (26), who analyzed the increase in blood mechanical characteristics in the sloth pressure consequent to clamping of the ca- (Bradypus tridactylus = variegatus), cat and rotid arteries. The increase in blood pressure rat (22) the time to peak tension was signif- was slow in onset and was not pronounced. icantly higher in the sloth (444 ± 33.7 ms) After removal of the occlusion, the increase than in the cat (327 ± 21.5 ms) and the rat continued for some time. The authors sug- (119 ± 9.1 ms). The df/dt maximum was also gested the possible participation of hormones different in the three species, being 2.9 ± 0.7 during the ischemic period. Further research g/s in the sloth, 5.2 ± 0.6 g/s in the cat and 6.4 would be interesting in this field. ± 0.8 g/s in the rat. Not only the contractile process but also the relaxation process were Anesthesia and sedation slow in the sloth. Cardiac output in the three-toed sloth has It has been shown (27) that Choloepus also been measured using a dye dilution hoffmanni and Choloepus didactylus can be technique (16). The values reported were immobilized by the intramuscular adminis- 0.248 ± 0.039 l/min for unanesthetized ani- tration of Sernylan (phencylidine hydrochlo- mals and 0.240 ± 0.033 l/min for anesthe- ride) at 1.65 mg/kg in combination with tized animals. The cardiac index was 0.97 ± promazine hydrochloride at 0.85 mg/kg. As 0.158 l m-2 min-1 in the unanesthetized sloth the drugs take effect, there is a relaxation of and 0.93 ± 0.13 l m-2 min-1 in the anesthe- the forelimbs accompanied by a loss of coor- tized sloth. Studies on blood pressure in the dination and of the grasping reflex; similar three-toed sloth cannulated under local an- changes in the hindlimbs follow shortly there- esthesia by the same authors found strik- after. Total immobilization is reached with a ingly high values of 176.8/128.2 mmHg. relaxation of the head and neck and partial These values fell substantially after the ad- relaxation of the jaw. Within 7 min the sloths ministration of pentobarbital anesthesia (15), suggesting that endogenous catecholamines A might promote the apparent hypertension BP (mmHg) seen in the unanesthetized sloth. This view was supported by the work of Duarte et al. 100 (23), who demonstrated that conscious sloths (Bradypus tridactylus = variegatus) were 10 s extremely sensitive to the exogenously ad- 0 ministered catecholamines. Other research B (19,24) suggested that the unanesthetized BP sloth has a mean arterial blood pressure of (mmHg) 129/86 mmHg, i.e., within the human range and not significantly greater than those seen 100 in relaxed unanesthetized laboratory animals.

However, handling and the mere approach 10 s of a person produced a rise in the sloths 0 blood pressure (Figure 2A) and in other cases Figure 2 - Changes in arterial blood pressure (BP) in Bradypus variegatus in response to the a hypotensive bout (Figure 2B), suggesting approach of a human. A, A slight rise and B, a fall.

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can be safely handled and by 21 min immo- bradycardia, although strong bradypnea was bilization is complete. No decrease occurs in sometimes seen in association with medeto- the pupillary reflex nor are there any appar- midine. Anesthesia occurred within 2.7 ± ent changes observed in the eye reflexes. 1.7 min when ketamine and xylazine were Although recovery times vary, by 5 h normal administered and within 2.5 ± 5 min when behavior returns and no undesirable side ketamine was injected along with medetomi- effects have been noted. Abdominal surgery dine. The doses of the different drugs admin- on captive adult two-toed sloths (Choloepus istered were 10 mg/kg of ketamine with 1 sp) has also been carried out using 50 mg of mg/kg of xylazine and 3 mg/kg of ketamine ketamine hydrochloride given intramuscu- with 0.04 mg/kg of medetomidine. The anes- larly (28). Maned sloths (Bradypus torquatus) thesia induced with the combination of have been tranquilized by employing a mix- ketamine and medetomidine was reversed ture of ketamine (1.3 mg/kg) and acepro- after 41.6 min by the intramuscular adminis- mazine (0.1 mg/kg) so that external exami- tration of atipamezole (0.2 mg/kg) and within nations could be carried out and blood col- 10.0 ± 7.9 min the sloths were able to attain lected (29). Two-toed sloths have been se- their normal hanging position. Intravenous dated with ketamine hydrochloride alone (2- injection of atipamezole shortened the re- 6 mg/kg) for the collection of blood (30) and covery period. Following administration of a combination of tiletamine hydrochloride the other three anesthetic combinations, the and zolazepam at a dose of 1.9-6.0 mg/kg first signs of arousal were seen between 43 has been employed to anesthetize these ani- and 51 min. Animals recovered calmly from mals before obtaining blood from the femo- the ketamine/xylazine combination and were ral artery (8). Anesthesia induction times able to support themselves after 34 min varied from 2 to 19 min, with anesthesia through grasping with at least two limbs. On lasting between 12 and 40.5 min. Recovery the other hand, with the tiletamine/zolaze- times ranged from 2 to 6 h. pam-induced anesthesia, recovery was long Recently a comprehensive review (31) and irregular averaging 76.7 ± 31.3 min; it has been published comparing the effective- was 3 h before some sloths were able to hang ness of different injectable anesthetic com- normally. binations given intramuscularly to 202 sloths (Choloepus didactylus). With acepromazine Blood chemistry (0.1 mg/kg) given along with ketamine (10 mg/kg) the animals were quickly immobi- A brief review of the blood chemistry of lized (within 2.5 ± 2.0 min), but the level of the sloth was provided by Goffart (1). Since anesthesia induced and the muscle relax- that time some further short papers have ation were both poor. Deep anesthesia within appeared which have shed further light on 1.8 ± 0.6 min with good muscle relaxation the sloths hematological characteristics. An was also obtained by this group when using examination of blood samples taken from tiletamine/zolazepam (10 mg/kg), but irregu- four specimens of Choloepus hoffmanni and lar respiration and low relative oxyhemoglo- one of Bradypus tridactylus showed that bin saturation values were often observed in cholesterol levels were high and blood urea the anesthetized sloths. Ketamine, when com- levels slightly so (32). Glucose levels were a bined with the 2 agonists xylazine or me- low in some of the animals despite an ad- detomidine, was found to be the most suit- equate diet. Serum albumin levels were low, able anesthetic providing good to excellent but those of globulin high. In another in- muscle relaxation, good analgesia, high oxy- vestigation (8) the hematocrit measured in hemoglobin saturation values, and moderate five male and two female two-toed sloths

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(Choloepus didactylus) averaged 43% (range place in Burnet Park Zoo, Syracuse, New 30-55%) and the hemoglobin varied from York, and involved a colony of animals origi- 10.7 to 17.8 g/100 ml (mean 15.3 g/100 ml). nating from Panama. Blood samples were Red blood cells ranged from 2.1 to 3.5 x 106/ collected from sloths ranging in age from mm3 (mean 2.8 x 106/mm3) and white blood one to over 16 years. A total of 15 hemato- cells from 9.9 to 33 x 103/mm3 (mean 19.33 logical and 24 biochemical parameters were x 103/mm3). The differential counts were evaluated and blood smears from five sloths found to be: basophils 1-3%, eosinophils 1- of each sex were also examined for erythro- 6%, segmented neutrophils 5-42%, lympho- cyte and leucocyte cell description and inter- cytes 16-87% (mean 73%) and monocytes 1- pretation. Detailed results of these examina- 4%. Mean corpuscular volume was 151 m3, tions were tabulated. Only serum alkaline mean corpuscular hemoglobin 55 pg and phosphatase and cholesterol appeared to be mean corpuscular hemoglobin concentration affected by gender and age. Alkaline phos- 36%. phatase was significantly elevated in juve- Meritt (6) collected blood from four two- nile females in comparison to values re- toed sloths (Choloepus hoffmanni). Hemo- corded in adult females and cholesterol lev- globin values were 11.7, 13.6, 13.6 and 13.6 els were marginally higher in juvenile fe- g/100 ml and the mean hematocrit was 35%. males in comparison to those recorded in Red blood cells ranged from 3.85 to 5.04 x juvenile males and adult females. Choles- 106/mm3 and white blood cells varied from terol values ranged widely, possibly reflect- 13.4 to 21 x 103/mm3. The differential counts ing a variation in diet. Mean sodium and for the white blood cells as a percentage of chloride values recorded of 126 and 89.7 the total present were: basophils 1 to 3, mEq/l, respectively, were slightly lower than eosinophils 0 to 5, myelocytes 0, juveniles 0, those seen in domesticated species. Potas- stab cells 0 to 3, segmented neutrophils 40 to sium levels averaged 5.8 mEq/l. Mean serum 49, lymphocytes 40 to 49 and monocytes 0 to chemistry values were as follows: glucose, 3. These values fell within the range of vari- 61 mg/dl; urea nitrogen, 16.7 mg/dl; crea- ability of previous reports. Studies (33) on tine, 0.9 mg/dl; uric acid, 2.9 mg/dl; calcium, blood from four sloths (Bradypus variegatus) 9.3 mg/dl; phosphorus, 4.6 mg/dl; triglycer- showed hemoglobin values of 11.06 ± 0.45 ides, 114.8 mg/dl; cholesterol, 194 mg/dl. g/100 ml, a hematocrit of 34.2 ± 1.42%, a The total protein content was 7.5 g/dl (albu- mean corpuscular volume of 83.02 ± 0.05 min 3.9 and globulin 3.6) and total bilirubin µm3, a mean corpuscular hemoglobin of 0.28 mg/dl. Previous ranges for hematology 27.16 ± 1.89 pg and a mean corpuscular and serum chemistry in the two-toed sloth hemoglobin concentration of 32.44 ± 0.76%. were based on much lower sample numbers, Red blood cells averaged 4.11 ± 0.29 x 106/ with consequent considerable variations. mm3 blood while white blood cells were These values (30) should stand as an excel- 12.46 ± 1.02 x 103/mm3. Differential counts lent reference for future studies in this field. were 34.8 ± 3.85% and typical lymphocytes Blood volume and iron kinetics were ex- were 56.4 ± 3.44. No basophils were found. amined in three specimens of Bradypus Recently a very detailed account (30) has tridactylus = variegatus collected near Recife been given of the hematology and serum in Pernambuco (34). The hematocrit and chemistry profiles of captive two-toed sloths hemoglobin values (37% and 9.6 g/100 ml, (Choloepus hoffmanni) and a comparison respectively) largely agreed with those of was made with the values obtained between earlier studies reported by Goffart (1). The juvenile (<3 years) and adult (>3 years) ani- average plasma volume (35.4 ml/kg body mals and between the sexes. The study took weight), as calculated by extrapolation of

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the plasma iron disappearance curve, was humans, the suggestion was made (35) that lower than that observed in humans, rats and there exists a similar period of divergent dogs, as also were the calculated blood and evolution between man and both Xenarthra red cell volumes (54.9 and 19.5 ml/kg body on the one hand and sloth and armadillo on weight). However, in the sloth it is perhaps the other. misleading to compare blood volume data to An examination (36) of the hemostatic body weight as the latter can vary enor- profiles in five specimens of Bradypus mously depending on the amount of urine variegatus found clotting time to be 6 min 21 and feces retained. It was suggested (34) ± 64 s, partial activated thromboplastin time that, in retrospect, it might have been better 45.5 ± 8.52 s and prothrombin time 7 min 2 to have correlated the values with lean body ± 39 s. Platelets numbered 324 ± 24 x 103/ mass rather than body weight. The average mm3. Bleeding time was 1 min 9 ± 42 s. iron disappearance half-time was found to Animals which had a higher platelet count be 150.6 min - approximately twice as long showed a shorter bleeding time. as in man, rat and dog. The mean iron uptake Blood gases measured (8) at 37oC in by erythrocytes was slightly less than that anesthetized two-toed sloths (Choloepus observed in man. Iron turnover rate was didactylus) were as follows: pCO2 33.2 ± -1 -1 calculated to be 165.6 µg kg day and red 2.0, pO2 89.9 ± 18.8. The pH was 7.40 ± cell iron turnover rate 102.7 µg kg-1 day-1. 0.03. Kleinschmidt et al. (35) examined the primary structure of hemoglobin collected Brain and spinal cord from Bradypus tridactylus. They used chromatography on carboxymethyl cellulose CM- Goffart (1) gave only a brief account of a 52 to separate two components, an - and a the structure of the sloth brain, but he made ß-chain at the ratio of 4:1. Also reported reference to numerous anatomical studies were the amino acid sequences and compo- carried out mainly in the nineteenth century. a sitions for the - and ß-chains. When the He did record, however, that the weight of structures were compared with the corre- the brain averaged 28.5 g in Choloepus sponding human chains it was noted that hoffmanni and pointed out that the cerebral there were 27 (19.1%) amino acid replace- hemispheres do not extend over the cerebel- a ments in the -chain and 33 (22.6%) in the ß- lum, but that the corpus callosum is well chain, necessitating at least 32 and 41 base developed. Saraiva and Magalhães-Castro substitutions in the respective genes. The (37) reported on sensory and motor repre- replacements were distributed more or less sentation in the cerebral cortex of Bradypus. randomly along the entire length of both As might be expected, the area of the cortex chains, but the number of substitutions at devoted to the representation of the forelimb functionally important positions was much and especially the forepaw was considerably a larger in the ß-chain. Whereas only one 1/ß1 larger than that for the remaining body parts. a contact was exchanged in the -chain, there The cortical area for the forelimb was fol- a were four replacements in the 1/ß1 subunit lowed in decreasing order of magnitude by interface in the ß-chain. When the hemoglo- the projections of the hindlimb, trunk and bin from Bradypus tridactylus was com- face. Visual and auditory projections occu- pared with that from the armadillo (Dasypus pied restricted areas on the caudal dorsolat- novemcinctus) it was found that there were eral surface of the neocortex. a 25 and 34 replacements in the - and ß- The anterior lobe of the cerebellum ex- chains, respectively. As there were also 25 erts a powerful tonic inhibitory influence and 32 exchanges between armadillos and over brain stem mechanisms affecting pos-

Braz J Med Biol Res 33(2) 2000 Physiology of sloths 137 ture and tone and its removal in the cat and measured using specific radioimmunoassays dog results in a marked lack of coordination. and reverse phase high performance liquid This is followed by a phase of stabilized chromatography. Concentrations (ng/g) of deficit during which significant compensa- the above peptides were tabulated in the tion takes place (38). Raccoons are seen to dorsal and ventral horns and the dorsal root compensate more rapidly after removal of ganglion as a function of the level of the this region of the brain than do cats and dogs. spinal cord in three-toed sloths and were Murphy and OLeary (38) examined hang- compared with the values recorded in the ing and climbing functions in both two- and cat, dog, owl-monkey and rhesus monkey. three-toed sloths (Choloepus hoffmanni and The findings emphasized a prominent and Bradypus tridactylus) after cerebellectomy heterogeneous distribution of peptides and compared these with the situation in the throughout the rostrocaudal and dorsoven- raccoon and cat. Attempts were made to tral regions of the spinal cord. With few follow changes in muscle tone in the sloths, exceptions, higher levels of peptides were which survived between six and eight days present in the dorsal than in the ventral horn postoperatively, by passive manipulation of and all levels (but especially those of VIP the limbs and from observations of arboreal and PHI) were elevated in the sacral cord behavior. Interestingly, cerebellectomy had compared to those in the more rostral seg- no appreciable effect on the animals ability ments. to cope with the hanging and climbing re- quirements of their arboreal environment. If Vision a rod was used to stimulate the foot pads of a clinging cerebellectomized sloth, a slowly It has been claimed that visual acuity is a developing powerful increase in the flexor requirement for successful adaptation to life tone of the limb caused the claws to grasp the in the forest canopy. However, sloths man- rod so tightly that another was required to age to survive extremely well despite pos- pry them loose. Interestingly, not a single sessing only relatively poor eyesight. Nu- clinging or hanging position was seen that merous experiments, summarized by Goffart was different between unoperated animals (1), indicate that both Bradypus and Choloe- and those which had been cerebellectomized. pus are extremely short-sighted and rely on This led to the suggestion (38) that, because additional senses for obtaining food, making sloths move with incredible slowness, mini- contact with other members of their species mal equilibratory and altitudinal controls are and avoiding danger. Goffart concluded that required to accomplish this. Thus one does the absence of a ciliary muscle and thus of not see the effects of cerebellectomy that is the ability to accommodate, a pseudoangiotic apparent, for example, in carnivores where, retina, the lack of a macula and only sparse following the operation, oscillatory head and ganglion cells and nerve fibers indicate a body tremor and truncal ataxia take place. low level of visual acuity and visual dis- A detailed survey was carried out by crimination. Yaksh et al. (39) on the longitudinal and Since Goffarts review some valuable dorsoventral distribution of a variety of pep- additional work has been carried out on vi- tides in the spinal cord of five mammals sion in sloths (40-42). Using retinoscopy, an including the two-toed sloth (Choloepus di- examination was made (40) of the ocular dactylus). Levels of substance P, vasoactive refraction of each eye in one male and seven intestinal polypeptide (VIP), cholecystoki- female sloths (Bradypus tridactylus) col- nin, neurotensin, met-enkephalin, bombesin lected near Manaus, and in a juvenile semi- and peptide-histidine-isoleucine (PHI) were domesticated female. Ophthalmoscopy was

Braz J Med Biol Res 33(2) 2000 138 D.P. Gilmore et al.

also carried out on some sloths to determine the nine sloths; three had marked hyperopia, pupil size and shape, to examine the fundus two low hyperopia, two emmetropia and two and to estimate the size of the visual fields marked hyperopic astigmatism. Anatomically and positions of the optic axes. Finally, the the eye of Bradypus tridactylus was found to eyes of two sloths were examined histologi- be nearly circular in an anterior-posterior cally. The findings generally confirmed ear- section with overall dimensions of 8.4 mm lier studies on Choloepus hoffmanni dis- axially and 8.3 mm equatorially. The cornea cussed by Goffart (1), and suggest that sloths was found to be quite convex and uniformly possess eyes that are primarily adapted for thin and wide. The radius of the thick rounded vision at low light intensities. It was reported crystalline lens was 2.35 mm in its anterior (40) that the eyes of Bradypus are some 30 surface and 1.84 mm in its posterior surface. mm apart and are relatively frontal-looking, The equatorial:axial length ratio was found being of moderate size and having a wide to be 1.36 compared to 1.7 reported for and convex cornea. The angle between the Choloepus hoffmanni by Goffart (1). It was diverging optic axes of each eye was esti- suggested (40) that because of this higher mated to be 50o and the horizontal monocu- ratio the lens of Choloepus is probably less lar and binocular visual fields were calcu- optically powerful than that of Bradypus. lated to be 70o with a binocular overlap at Furthermore, the lens is not as thick and also 35o. These latter measurements were made appears to be less round. Finally, it was on two sloths whose pupils had been some- concluded (40) that the retinal histology of what dilated with a cycloplegic drug. A wide Bradypus is similar to that reported for variation in refractive error was observed in Choloepus by Goffart (1), i.e., many slender rods with few ganglion cells are present and cones are rare or absent. Figure 3 - Distribution of gan- A Superior glion cell densities in the right Andrade-da-Costa et al. (41,42) exam- retina of a three-toed sloth 0.4 ined in detail retinal wholemounts of both Bradypus variegatus (A) and of a 0.6 two- and three-toed sloths (Choloepus two-toed sloth Choloepus didac- hoffmanni and Bradypus variegatus) for a tylus (B). Numbers next to each Nasal isodensity line represent cells/ quantitative analysis of the topographic dis- Temporal + mm2 divided by 1000. The cross 0.8 tribution and size of the retinal ganglion marks the position of the optic 1.0 1.2 cells using horseradish peroxidase (see Fig- disc. Note the different position 1.4 of the region of maximum cell ures 3 and 4). In the three-toed sloth (41), density (area centralis) between ganglion cell density was found to gradually the sloth species. In both in- increase from about 500 cells/mm2 at the stances the presence of a visual Inferior 1 mm streak in the retina is indicated periphery to a peak of around 1700 cells/ 2 by the elongated contours of the mm in a region deep in the inferior temporal isodensity lines representing in- retina localized within a range of 4.3 ± 0.53 B Superior termediate densities around the mm from the optic disc, which corresponds area centralis, this being 0.8 x 0.2 0.4 0.3 103 in Bradypus variegatus and to about 40.56 degrees of visual angle con- 0.5 0.4 x 103 in Choloepus didacty- 0.6 sidering a retinal magnification factor (RMF) 0.75 lus. of 0.106 mm/degree (Figure 3A). The region + Temporal Nasal of maximum cell density (area centralis) constituted only a weak retinal specialization with a maximum resolution power estimated to be 2.18 cycles/degree of visual angle

1 mm (Andrade-da-Costa BLS, unpublished ob- Inferior servations). Retinal cell diameters (Figure

Braz J Med Biol Res 33(2) 2000 Physiology of sloths 139

4A) ranged from 5 to 21 µm, with peaks at centralis in Choloepus didactylus (1000 cells/ 11-12, 13-14 and 15-16 µm. There was a mm2) corresponds to a maximum resolution higher frequency of the smaller cells in the power estimated as 2.38 cycles per degree, area centralis than in the superior nasal retina which is similar to that obtained for Brady- and other areas where large cells predomi- pus variegatus. Moreover, it was pointed out nated. At least three different cell popula- (42) that as the two-toed sloth does not rotate tions were identified relative to the soma its head when climbing, the area centralis size (Figure 3A). The inferior nasal and su- would then be in the appropriate part of the perior temporal retinal areas contained inter- retina for visualising the branch above (Fig- mediate cell densities in what was termed ure 5b). The organization of the retina may the visual streak, and retinal cell size was therefore be governed by the demands im- also intermediate in comparison to the area posed by the animals lifestyle and not nec- centralis and superior nasal retina. The au- essarily by how closely species are related. thors discussed the unusual position of the Figure 4 - Distribution of gan- area centralis and visual streak in the sloth 20 A glion cell diameters in two different quadrants of the retina in retina by the animals ability to rotate its 18 Bradypus variegatus (A) and o head 180 while climbing upside down along 14 Choloepus didactylus (B). The horizontal branches (Figure 5a). This would 10 relative frequency was obtained by subtracting the number of enable the sloth, by obtaining an image upon IT-SN 6 cells in the inferior temporal the inferior temporal region, to clearly visu- 2 retina (IT) of the area centralis in alize the branch directly above its head for 0 Bradypus variegatus and in the -2 accurate claw placement. superior temporal retina (ST) of Choloepus didactylus from the In the two-toed sloth (42), ganglion cell -6 Relative frequency (%) regions of lowest cell density in -10 density in the retina was found to increase the superior nasal retina (SN) of approximately 10-fold from about 100 cells/ -14 both species. An excess of cells 2 -18 for each region of the area cen- mm at the periphery to a peak of about 1000 tralis over the nasal temporal 2 cells/mm in a central region along the tem- 57 9111315171921 retina is indicated by the portion poral horizontal meridian (Figure 3B). A Cell diameter (µm) of the histogram above the 0% low cell density in the area centralis would line and the excess of cells for 8 each region of the superior na- indicate that this constitutes a region of only 6 B sal retina over the inferior tem- ST-SN 4 poral retina is indicated by the weak specialization. Surrounding the area 2 centralis a visual streak was identified. Its 0 portion of the histogram below -2 the 0% line. C is a histogram orientation was vertical, stretching from the -4 -6 obtained by subtracting the rela- 5101520 tive frequency of cell diameters upper to the lower quadrant of the temporal Relative frequency (%) retina along the vertical meridian. Interest- Cell diameter (µm) in the region of the area centralis (ST) of the retina in Choloe- ingly, no significant difference was found in pus didactylus from those in the the distribution of ganglion cell sizes through- 4 ST-IT IT and inferior nasal (IN) quad- 2 C rants. out the retina of the two-toed sloth in con- 0 -2 trast to the situation in the three-toed species -4 -6 (Figure 4B and C). The results would indi- 8 cate that the cells in the area centralis of the 6 4 two-toed sloth have a lower resolving power 2 ST-IN 0 than those of the three-toed sloth. However, -2

Relative frequency (%) -4 the much larger eye of the former would -6 -8 effectively increase its visual resolution. 5101520 Considering an RMF = 0.151 mm/degree (N Cell diameter (µm) = 3), the highest cell density in the area

Braz J Med Biol Res 33(2) 2000 140 D.P. Gilmore et al.

Mendel et al. (43) studied activity in ing situation, except that they spent less time three adult female two-toed sloths using a outside. The retinoscopic investigation indi- time lapse video recorder. After one month cated that a majority of the 11 sloths were the animals were fitted with a face mask, and myopic, but some only slightly so. It would following a period of adaptation, eye patches thus appear that the sloths rely little on vi- were added rendering the animals effectively sion to carry out their normal patterns of blind, although still able to detect light. After behavior. a further seven days to allow habituation, the animals behavior was recorded for another Sleeping and waking three weeks. Six months later additional studies on the sloths behavior were carried out Of the two genera of living sloths, the under simulated conditions of night and day. genus Bradypus is the slower moving one Retinoscopy was performed on another 11 with more quiescent behavioral patterns. two-toed sloths. Interestingly, the behavior Galvão de Moura Filho et al. (44) performed of the animals when deprived of their sight EEG recordings in Bradypus tridactylus = did not differ significantly from the preced- variegatus to study their correlation with

Figure 5 - a, Typical sequence of ab locomotion of Bradypus variegatus along a branch inclined at approximately 30o (A-F) and along another in the horizontal position (G-K). (Reproduced with permission from Mendel, 56). b, Typical sequence of locomotion of Cho- loepus hoffmanni along a branch inclined approximately 30o in relation to the horizontal. (Repro- duced with permission from Mendel, 57).

Braz J Med Biol Res 33(2) 2000 Physiology of sloths 141 observed behavior. Behavioral patterns were it eats, but in contrast it has been reported by divided into awake-exploring, awake-fixat- others that, at least in captivity, sloths do ing, awake-alert and behavioral sleep. Sloths drink appreciably. Nagy and Montgomery were found to show one or another type of (45) measured carbon dioxide production waking behavior during 30.6% of the time and water flux using doubly labeled water in and behavioral sleep during the remaining sloths (Bradypus variegatus) living on Barro time. EEG recordings were classified as A1 Colorado Island. The animals comprized (seen during awake-exploring and awake- three adult females (two of them carrying alert behavior), A2 (recorded when the ani- young) and two adult males. The two young mals were awake, but relaxed and drowsy), initially weighed 613 g and 460 g. They S1 and S2 (light sleep), S3 and S4 (deep found that water influx and efflux rates were sleep), and S5 (paradoxical sleep). Waking almost equal, averaging around 39 ml kg-1 EEGs of various types were seen 34% of the day-1 and being approximately only half of time, about 10% of this during behavioral those measured in laboratory animals. Water sleep. EEG patterns of light sleep consti- intake in the milk by young sloths varied tuted about 56% of the records made (about during different measurement periods, aver- 6% during some form of waking behavior) aging 15 ml kg-1 day-1. Interestingly, the and EEG patterns of deep sleep constituted larger young consumed milk at a significant- about 10% of the recordings; all were made ly lower rate than the smaller one, possibly during behavioral sleep. Paradoxical sleep because of supplementation of its diet with occupied 11% of the total sleep time. The leaves. It was found that the two lactating different EEG patterns were nicely illus- sloths allocated about 5% of their water trated and analyzed and are comparable to intake and 11% of their energy intake to milk those seen in other mammals (44). Although production. Water production during oxida- there was a lack of a well-developed relation of food in the sloths was estimated to be tively pure high amplitude alpha rhythm, 4.2 ml per day, leaving a daily deficit of over this deficiency is also present in most mam- 34 ml. It appeared that the remaining water mals other than primates. Low voltage activ- input came from the ingested leaves rather ity was seen in this frequency range, mixed than from the drinking of rain water. It has with other frequencies during A2 and S1. been found (6) that the average daily water True K-complexes were also lacking, al- consumption of Choloepus hoffmanni in cap- though vertex sharp waves were prominent tivity was 170 ml per animal, with measured in S2 and S3. The sleep spindles (6-7/s) seen amounts of excreted urine averaging 808 ml in the sloth were of a lower frequency than in (ranging from 340 to 1600 ml). It was also the human, cat, guinea pig and opossum, observed (6) that urine (deposited at the although only slightly lower than those re- same time as the feces) was clear and yellow corded in several species of rodents. Body to brown and had a specific gravity of 1.023. temperature did not influence the frequency It was reported earlier (46) that the urine of of the sleep spindles. the two-toed sloth has a specific gravity ranging from 1.020 to 1.031 and a pH rang- Water balance and kidney function ing from 7.0 to 9.0. Rappaport and Hochman (28) reported Goffart (1) described in detail the anatomy on the occurrence of cystic calculi in captive of the sloth kidney and discussed its concen- two-toed sloths. A male presented with a trating ability. He also pointed out how rectal prolapse which was repaired, but later Choloepus usually obtains its water require- recurred. At surgery the bladder was found ments from the leaves, fruits and vegetables to be greatly thickened and inflamed with

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several stones palpable in the lumen. Upon and left the tree, the juvenile remained at- examination these were found to be com- tached to its mothers abdomen. In contrast posed of calcium, magnesium, ammonium to the situation in Bradypus, Meritt (6) has and phosphorus. Some months later a large provided a lot of detail about Choloepus stone measuring 7-8 cm in diameter was hoffmanni, having studied captive animals removed from the bladder of a female sloth in a Chicago zoo between 1968 and 1977 that was experiencing trouble when urinat- and undertaken field work in Panama. He ing and defecating. Both sloths recovered reported that in this two-toed sloth females well and it was speculated that the stones in estrus appear to actively initiate mating. were a result of the sloths diet which con- Interbirth interval and gestation length sisted of a mixture of fresh fruit and veg- are also not well known for three-toed sloths etables along with a protein supplement. and there is still some disagreement as to whether there is a breeding season for Reproduction Bradypus, or whether the animals reproduce throughout the year. Births in Bradypus A brief update of the reproductive and variegatus have been recorded on the out- endocrine systems of the sloth summarizing skirts of Recife in August and November recent studies in these fields was provided (see 1,47). Recently, 226 female three-toed by Gilmore and Da Costa (47). Although the sloths (Bradypus tridactylus) were captured anatomy of the reproductive organs of the and examined by Richard-Hansen and Tauber sloth has been extensively investigated (see (49) over a 16-month period during the fill- 1), there is still much to be learned about the ing of the Petit-Saut dam in Guyane. They reproductive physiology and breeding of observed that young were carried from April sloths, especially Bradypus. Little indeed is to September 1994 and pregnancies were known about courtship and mating in Brady- recorded from March through September pus, which was reported to be direct and 1994 and from January 1995. However, it brief (1,48,49). Richard-Hansen and Tauber has also been stated (29) that breeding in (49) described a series of copulations be- Bradypus torquatus is not seasonal. New- tween a female three-toed sloth (Bradypus born individuals were captured along with tridactylus), carrying a young estimated to their mothers in July and two juveniles near be three to four months old, and a male weaning in August and December; another which had been sharing the same tree since juvenile of intermediate weight was cap- the previous day. Most of the initiative came tured in November. In Choloepus didactylus, from the male, who approached the female, births in captivity at the Smithsonian Institu- and face to face copulation lasting around 3 tion (Washington) were recorded every min took place. During this time the male month except April, September and Novem- was secured by his forelimbs while holding ber (50). the female, which was hanging from a branch, Beebe (51) estimated gestation in Brady- with his hindlegs. Five minutes later mating pus tridactylus to last between four and six occurred again, but this time with the male months, and Tirler (52) reported it to be on the females back. This copulation was between five and six months in Bradypus interrupted by the female which withdrew variegatus with a one-year interval between after 2 min. However, the male followed her births. Studies on Bradypus variegatus (53) and eventually they mated again face to face have indicated that the females give birth in for one and a half minutes. Throughout the successive years. Pregnancy in Choloepus whole 25-min period, from initial approach didactylus has been estimated (54) to equal to final separation when the male descended or exceed 10.5 months with a 26-month

Braz J Med Biol Res 33(2) 2000 Physiology of sloths 143 interval between births if the young sur- female was seen to attempt to solicit a male vived, but only 14 months if the newborn by pressing close in an attempt to rub her died. Goffart (1) reported that birth of the anogenital region against him. Interestingly, single young, weighing 230-250 g, takes place the male, though not aggressive, showed no on the ground or in the hanging position. real interest and exhibited no sexual behav- McCrane (50) described a birth in captivity ior. Meritt (6) described menstruation in of Choloepus didactylus. The mother was in Choloepus hoffmanni with a small amount an upside down hanging position and made of blood being present on the external geni- attempts with one forelimb to pull the infant talia; edema of the vaginal lips was also between her hind legs and on to the abdo- noted. The menstrual cycle lasted 5 to 7 men. Although approximately 20 cm of um- days. Days one to three were marked by the bilical cord was exposed, no blood of any presence of rusty-colored fluid or blood in or consequence was observed. Other sloths were on the vaginal opening. On day four the seen preventing the infant from falling and external genitalia were dry and clean, but cleaning both it and the mother by licking. slightly puffy. Genital edema was still pres- Work in Costa Rica (55) on Bradypus ent from days five to seven, but secretions tridactylus = variegatus has suggested that were absent. males are fertile throughout the year. Two Parturition in the sloth is difficult to diag- animals killed during the rainy season in July nose and observe, but Meritt (6) recorded a and two during the dry season in December number of births in Choloepus hoffmanni all displayed normal spermatogenesis, with that took place in the Chicago zoo. During the seminiferous tubules showing a sper- the postpartum period, he noted a total ab- matogenic wave similar to that seen in ro- sence of blood, blood-tinged fluids or tissue dents. However, more recent work in Per- debris in or around the genitalia, which were nambuco (48) has indicated that, although not obviously torn or distended. The single breeding may occur throughout the year, offspring, weighing 350 to 454 g, was al- only a minority of male sloths (Bradypus ways born during daylight hours and was variegatus) would appear to be sexually ac- alert and strong. The eyes were open, the ear tive at any one time. pinnae patent, the teeth present, and the claws Maturation in the sloth is a rather slow fully formed and hard. The gripping reflex process. It has been stated (52) that the three- was well developed in both front and hind toed sloth may take up to six years to reach feet, enabling the young to cling to or crawl maturity. However, in contrast, it has also about the mothers abdomen. The newborns been reported (54) that although male speci- were fully haired, except over the ventral mens of Choloepus didactylus in captivity surface, vocalized loudly and were capable are not sexually mature till four and a half of coordinated movement. Although no ob- years, females will breed at three years. Meritt vious breast development or milk flow was (6) reported a case of sexual maturity in a noticed prior to parturition, nuzzling and female two-toed sloth (Choloepus hoffmanni) suckling by the newborn stimulated the re- at two years of age; this animal died when 30 lease of milk, usually within the first 48 h months old, with a well-formed fetus in utero. (6). The mother was solicitous of the off- Estrus in the sloth is hard to detect. Two spring and spent a considerable amount of female sloths were observed (6) rubbing time vigorously licking its head and face and against one another in a near vent to vent cleaning the anogenital region, thus stimu- position during the onset of estrus; there lating elimination. The urine and feces so were, however, no changes in genital ap- produced were consumed by the mother. pearance or secretions. When in estrus a The newborns were nursed for periods of 6

Braz J Med Biol Res 33(2) 2000 144 D.P. Gilmore et al.

to 15 min at a time on several occasions each sloths were regularly feeding on solid food day. It was observed (6) that water was first away from the mother and by 6 months were consumed at seven days and food taken at 15 eliminating in typical adult fashion, but were days by a male and at 27 days by a female. still in behavioral association with the mother, Play behavior was noted at 15 and 19 days of and continued to be carried on the mothers age. The young first assumed a hanging or abdomen till 8 months. There was no sudden upside down position between 20 and 25 or dramatic break in the tie between mother days and solid food was actively sought and offspring, rather there was a gradual between 30 and 42 days. The first apparent change from maternal dependence to one of exploration away from the mother and in companionship and association as the young close proximity to other sloths was observed sloth matured. Even at two years of age a at 59 days in a female and at 65 days in a female offspring was most often found in male. As time elapsed these exploratory pe- close proximity to its mother, frequently be- riods would last longer and the distances ing active and feeding or resting in her com- away from the mother increase. If its return pany. was blocked, the infant made loud and char- acteristic bleats lasting 30 to 90 s which Acknowledgments induced the mother to respond. Sleeping in an adult position close to, but apart from the We thank Professor B. Andrade Da Costa mother, was noted at 50 days for a female for assistance in the drafting of this manu- and at 65 days for a male. By 5 months the script.

References

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