A COMPARATIVE STUDY OF BASAL METABOLISM AND THERMOREGULATION IN A FOLIVOROUS

(COLOBW GUEREZ,4) AND AN OMNIVOROUS (CERCOPITHECUS MITZS) PRIMATE SPECIES

Basal metabolic rate has been shown to be low in the prosimians (Miillcr. 1979). Simian species. on the other hand. have ;I BMR cloac to or higher than pre- dicted from body mass (Bruhn. 1934: Scholander (‘I trl.. 1950: Malinow & Wagner. 1966: Morrison & Middleton. 1967: Nakayama c,t al.. 1971). Only the night monkey (.4ot1r\ rririrqtrtus). a nocturnally active species. shows a reduced BMR (GofElrt. 1977: Lc Maho c’r ctl.. 1981).

In the prosimians some adaptive processes have been suggested as the possible reasons for the ob- set-ved low BMR (Miillcr. 1975. 1979: Miillcr & Jaksche. 1980: Whittow c’t trl.. 1977). This view could find further support if it could be shown that highly specialized arboreal folivorous simians also have a low BMR. McNab (197X) discussed the energetic con- sequences of a specialized food supply and concluded that arboreal mammals which feed on leaves should have a IO\Y BMR.

McNab’s conclusion was first tcstcd by Milton c’t trl. (1979). They measured oxygen consumption in the howlcl- monkey (.~/OULQ~U /~~~/liurr~). perhaps the most folivorous New World primate (Eisenherg PI al.. 1972). From their results the authors could not sup- port McNab’s prediction as the VOZ was 5”,, higher than expected from body mass. Howler monkeys arc day-active primates; however, experiments were con- ducted during the day when activity and body tcm- perature would be cxpectcd to be high. It seems poss- ible that the animals may not have been in their basal state.

In this study. therefore. we tested McNah’s hypoth- esis again. For the purpose we chose black and white

* Present address (to which requests for offprints should he sent): Institnt Bioloeir III. Abtcllung Phymlogische ijkologie. Unixrsitlt T;hingen. Auf dcr Morgenstelle 28 D-7300 Ttibingen I. Federal Republic of Germany.

colobus monkeys (guereras) which are mamly foli- vorous (Oates (‘I al.. I Y77 : Rose, 197X) and for a direct comparison Sykes monkeys which are more omni- vorous (Rudran. 1978: Schlichtc. 1978). The two spe- tics OCCLII- in the same habitat. In addition. we exam- ined some aspects of thermoregulation in the two spe- Clt‘S.

Tuo male colobua monkcqs ((‘olo/l~\ g~c,‘cx) ucighmg 9.4 II.5 kg and two male Sykc\ monkeys ((‘c~r,ol)irl~c,t~,., mirr\) welghmg 8 9 kg were nsed in this study. The colohus monkeys \verr I3 years old and the Sykch about 5 years old. The animals wcrc hlndly w~plicd by the Institute fw Primate Rcscarch. Tigom. Kenya. whsrc they had hccn m captivity for over 2 yxr\.

~2hdominal tcmpei-atut-c wa mea~ut-ed by telcmctrq. El\ax coated transmitters (Mini-Mittcr) \sith about 20m range wcrt‘ lmplantcd into the abdominal cavity. Surgery alas conducted under gcncral anae~lhetic (Ketamine). After sul-gory the animal\ wcrc given antlhlotics for fipe days (Penicillln,‘dihgdl-o4treptompclni. Recording of abdominal tcmpcrature and rclatcd meas~lrcmenta started two weeks after surgery. Signals from the transmitter wcrc’ caught and contInuousI> recorded by ;I modified walkie-talkie (Mini- Mltttlr). The transmitters mere calibrated In a water-bath

320 F. F. Mi’t.1.1 K c’f L/I

hefore and after the cupcrimenl. In a few cases rectal tem- perature has measured 8cm deep in one of the colobus monkeys using a Tcstothcrm. dIgital 2500. probe.

Mcaswements were done in an open-flow-system with ;I Beckman F3 Oxygen Analyzer. The experiments started hetueen 5 and 6 p.m. The fasted monkeys (food was with- drnun al Icast X hr &fore) were placed within an airtight box (73 x 4X x 50 cm) where they could sit and sleep com- fortably. Predried air (Silica-gel) was drawn through the how at constant rates from 465 6961,hr (STPD). The air flow was contmuouly measured with a calibrated Rota- meter (Rota). The animal box stood in a temper-ature con- trolled room where amblent temperatnrcs could be kept constant within + 1 C. Relative humlditv in the box varied from 60 to 95”,, depending on the &ous T,‘z. Oxygen consumpllon was contlnuouslq monitored. Normally. after the first 2 hr the monkeys slept. qOz was calculated during sleep. The Ireported $02 is the calculalcd mean for each clnlmal over a period of at least 3 hr. Experiments at T,%‘s ;~bobe 33 C took a shorter time hccnuse the animals were restless. All gas volumes were corrected to STPD.

RF31 LTS

Daily variations of Tab showed different patterns in the two species (Fig. 1). In the Sykes monkeys Tab increased in the early morning hours by about 1 C and then remained elevated until about 18 hr when it started to decrease. This pattern was the same in both Sykes. but the regulated levels of Tab differed mark- edly.

In the colobus monkeys ‘r,, increased gradually in the early and late hours of the morning culminating

39

1, 01

’ + t t ,rtv: 38

. +;’

t , t t 4

, + + t t

3

2 ; 35 ” a ’ J ’ 1 : s ’ 11 g 0 3 6 9 12 15 18 21 0 y 39

r b)

Time of dov

Fig. 1. Daily variations of abdominal temperature m two Sykes (a) and two colobus monkeys (b) as recorded hq telemetry. Given are hourly mean values _+ S.D. calculated

for each animal over periods of at least 8 full days.

.

LO-

39-

0 0

. ??

0 .

. . 0 - 3a- Y -37- . -

.* .

m 36- 0 ; 0 00 00 ‘0 3% : a L I I 1 I I I 5 5 10 15 20 25 30 35 - Ll-

bl 0

o 10-

; 39- .

0 2 38- 0 0 0 0 0. . 4 ??

77- .o . . 0 . 36- O

: - . 0

35- 0

3L- I I 1 I 1 I I 5 10 15 20 25 30 35

Amblent temperature / OC I

Fig. 2. Abdominal temperature of two Sykes (al and two colobus monkeys (b) after exposure to val-ious ambient temperaturea. At lemperaturcs from 3.5 to 31 C exposure lasted at least 5 hr: at temperatnrcs from 33.5 to 35.5 C

experiments Mere stopped after 3 hr.

Q- 31

Ll- -

in a definite peak late in the afternoon. As in the Sykes monkeys r,, started to decrease at about 18 hr.

Temperature ranges in the two species were similar being 360 38.5 C in the Sykes and 36.7-38.2 C in the colobus monkeys. The small SD in r,, of the Sykes monkeys suggests more precise control of body tem- perature in this species.

Five hour exposure to T, = 15-25 C had no effect on r,, of both species (Fig. 2). Exposure to lower r, (35 11 C) led to a slight decrease in Tab As r, in- creased from 28 to 31 C, r,, rose to 38 C in the colobus and 39’C in the Sykes monkeys. At T, 33.5-35.5 C r,, increased further in both species reaching 40 C in the colobus and 4@ 41 C in the Sykes monkeys. T,‘s above 28 C were accompanied by restlessness in both species.

Both species had a broad thermoneutral zone extending from 5 to 28 C in the colobus monkeys (Fig. 3) and to approx the same extent in the Sykes. BMR differed markedly between species: whereas in the c&bus monkeys it was SSY,, (mean 0.285 ml 0, g ’ hr I) of the value predicted from body mass. in the Sykes it was 113:;, of the predicted value (mean 0.399 ml 0, g ’ hr- ‘). At T,‘s above 30 C a v02 in- crease was observed in both species.

r,, ranges were very close in the two species. The unusual low Tab in one of the Sykes is difficult to explain. It may perhaps be due to the location of the temperature sensor. Daily variations in Tab showed

o.B r 0 / .

; bl

CL I 1 I I

5 10 15 20 25 30 35 Amblent temperature (OCI

c)bvious difl’crenccs: whereas in the Sykes T,, in- crcascd rapidly hctween 03.00 and 06.00 hr and main- tained a plateau until 18.00 hr. in the colobus the rise ill 7‘,$, wax gradual with a definite peak in the after- noon folloncd by a gradual decline thereafter. The ohscrvcd dlfferuncc explains in part the fact that Sykes monkeys have a 24 hr mean T,, greater than the colohus (38.0 vs 37.3 C). The lower ‘F,, in the col- ohus monkeys maq be a consequence of the observed lo\+ BMR.

The dlfferenccs which WC found in the diurnal vari- ations of 7’,h partly agree with previous reports on daily; feeding activity rhythms of these two primate ~~LXICS. Blue monkeys ((‘c,rc,ol’it/lc,c,~~.s rdia .stuhlmunni)

r~-om Lake Kivu, Zaire. for instance, have been t-sported to have peak maximum feeding activity at al-wnd 4 pm. with less marked peaks between 6 and 7 am. and at IO a.m. (Schlichte. 1978). lillrich (1961) obhcrved colobus monkeys at the slopes of Mt. Meru. Tanzania. and rcportcd two peak feeding times: I I XITI. 0.30 p.m. and 3.30 5 p.m. On cold misty days. the beginning of feeding activities were delayed until around ~v.xm.

Rose (197X) watched colobus monkeys in an acacia forest at Lake Naivasha. Kenya. and reported somc- v, hat diffcrcnt activity patterns. Here. the major feed- ing time was from 8 to I1 a.m. and from 4 to 7 p.m. v, ith ;I lesj marked peak from 11 to 12 a.m. It seems from thc~ studies that. irrespective of locality. all monkcb groupb had a resting period during the hot- tc\t part of the day. IL I 3 pm

It can be concluded from the above observations that in colobus monkeys the daily variations in ac- tivity do not strictly follow a species specific pattern but depend on the prevailing weather conditions in the habitat. Thus. for groups living in the mountain- ous forest regions where cold and misty weather very often persist until late in the morning, activity is delayed until ambient temperatures have become more favourable. as was the case with the Mt. Meru colobus. In the warmer East African Rift Valley. on the other hand. activities were shown to start much earlier in the morning.

The observed daily variation in Tab of the colobus monkeys correspond most to the activity pattern of the groups from Mt. Meru (Ullrich. 1961); this might be due to the fact that we used animals which had been captured in mountainous forests and wcrc kept in captivity at about 2200m above sea level. Feeding activity patterns should be expected to lead to similar patterns in body temperature. although not necess- arily in the same phase. Recording of daily activity patterns simultaneously with body temperature in free ranging colobus and Sykes monkeys would be necess- ary to resolve this problem.

It can be inferred from the early rise in T,, of the Sykes monkeys that feeding activities of these pri- mates are out of phase with those of the colobus. Since the two species share similar habitats the possi- bility of a stronger competition for the food items of the Sykes monkeys should be investigated.

Both species proved to be good thermoregulators in the cold. In the heat. however. they became uncom- fortable when T, exceeded 28 C. They became restless as shown by postural changes- lying on their sides with all limbs outstretched to facilitate heat loss. The behaviour seen in the laboratory agrees with the ob- servation that free living colobus rest and seek shade during the hottest part of the day (Ullrich. 1961; Rose. 1978). Behavioural adjustments and evaporative cooling seem to be sufficient to keep r,, below 39 C as long as 7’., does not exceed 30 C’. Higher 7;‘s (33-35 C) led to more discomfort. especially in the Sykes. and a quick rise in T,, of up to 40 C within less than 3 hr.

Sykes and colobus are ill adapted to tolerate high ambient temperatures for a long time. The thick fur coat may perhaps explain their wide TNZ which is shifted towards the colder side of the temperature scale and their inability to tolerate heat. In the natural environment, living high in the trees may aid in evaporative cooling since wind speeds increase with height. Comparative studies on monkeys living in the hotter coastal region of Kenya are envisaged.

Colobus monkeys were shown to have BMR X0,, lower than the Sykes and 15”,, below the value pre- dicted from body mass using Kleiber’s equation (Klciber. 1961). The reasons for this difference are not clear. Perhaps the difference lies in the feeding habits of the two species. This view offers support to McNab’s hypothesis that folivory favours reduction in BMR.

It still remains to be shown whether the reduced BMR of the colobus monkeys is an adaptation to folivory itself or to the specializations in the digestive processes. To answer this question. more species of the subfamily Colohinue should be investigated. In

this group the folivorous habits have Icd to a rumin- ant-like structure of the gastrointestinal tract (Kuhn. 1964; Hollihn. 1971; Bauchop 1971). As yet only few and scattered data exist about the role of fermcnta- tion in the energy budget of the leaf-eating monkeys: the data. however, suggest that the microbial produc- tion of volatile fatty acids is of greater importance (Drawert ef al.. 1962: Bauchop and Martucci. 1968; Ohwaki rt cd.. 1974: Kay et al.. 1976) and might even exceed the daily basal needs. In ruminants. as a result of the bacterial fermentation. the blood sugar level is characteristically low (Bauchop. 1978). However. in 6 colobus and 13 Sykes monkeys no obvious differences

blood glucose levels were found : Z.2 + 12mg/lOOml vs 119 + 53mg;lOOml (Suleman, per&al communication).

In howler monkeys fermentation is probably not as important and covers only 25-35”,, of the daily energy

requirements (Milton ct rrl., 1979). Nothing is known about blood sugar levels in this species.

Our sample was too small to give firm support to McNab’s hypothesis on the possible effects of folivory on BMR. We nevertheless found unexplainable differ- ences in BMR bct\veen the colobus and the Sykes monkeys. A reinvestigation of BMR in the howler monkeys should be interesting. As howler monkeys and colobus monkeys are arboreal and to a large extent folivorous with the howler monkey lacking the specializations in the digestive tract as in the colo-

bus a comparison of these two species could yield valuable data about the effects of fermentation upon the energy balance of primates.

A~~no,~,/edy~n~~,/~f.\ WC are greatly indebted to Dr J. Else. Institute for Primate Rescarch. Tigoni. Kenya. who kindly made the animals available. We are also grateful to Dr Suleman for doing the surgical implantation of the tcm- perature uwxmitters. This work was supported by a grant from the DFG (Mu 490.2a+h) to E. F. Miiller and from the Leverhulme Trust. London. to G. M. 0. Maloiy.

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