Oecologia Volume 90 Issue 4 1992 [Doi 10.1007%2Fbf01875446] K. M. Kool -- Food Selection by the...

8/13/2019 Oecologia Volume 90 Issue 4 1992 [Doi 10.1007%2Fbf01875446] K. M. Kool -- Food Selection by the Silver Leaf M

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Oecologia (1992) 90:527-533 Oecologia9 Springer-Verlag 1992

Food selection by the silver leaf monkeyTrachypithecus aur atu s sondaicus n relation to plant chemistryK M KoolSchool of Biological Science, The Univ ersity of New Sou th Wales, K ensington, N SW, 2033, AustraliaReceived December 6, 1990 / Accepted in revised form November 15, 1991

Summary Samples of leaves and fruits exploited as fooditems by Trachypi thecus auratus sondaicus were analysedfor nitrogen content, acid detergent f ibre (ADF), pepsincellulase digestibil i ty (CDIG), condensed tannins (CT),total phenolics (TP) and protein precipitation capacity(PP) and compared with fruits and leaves not eaten.Differences in chemical measures for i tems eaten and noteaten were not statistically signif icant but trends indicatethat leaves may have been selected for their lower f ibrecontent and greater digestibil i ty . Fruits eaten also had ah igher mean level o f CDI G and lower mean level o f ADFthan fruits not eaten but these measures are not con-sidered to be of major im portance in fruit selection asCD IG was lower and A DF h igher in fru it s ea ten than inleaves eaten. Levels of CT, TP and PP capacity werehigher in fruits eaten than in fruits not eaten but lowerin leaves eaten than in leaves not eaten. The role oftannins and phenolics in food selection is discussed.Leaves (and fruits) were not strongly selected on the basisof p ro te in con tent . Approximate ly ha l f the d ie tary in takeo f T. auratus sondaicus was leaves, a protein-r ich foodsource. Possibly, protein levels in foliage at Panga ndaranwere suff icient that selection for this nutr ient was notrequired. A nutr ient other than protein (for example,so lub le carbohydra tes) may have been maximisedthrough food se lec t ion . The pro te in /ADF ra t io mayprovide an indicator of the acceptabil i ty of foliage in ahabitat as potential food for a colobine. However, thisratio did not govern food selection by T. auratus son-daicus at Pangandaran .Key words: Trachypi thecus auratus - Colobine monkey- Plant chemistry - F oo d selection

Fo od selection is related to the typ e of digestive systemof an animal and the animal s bod y size. All colobinemonkeys are foregut fermenters. With decreasing bodysize, the energy and protein requirements of an animalincrease relative to bo dy weight (K leiber 1961) as do the

energetic costs of locomo tion (Schmidt-Nielsen 1972).Furthermore, relative gut capacity decreases with de-creasing body size (Janis 1976; van Soest 1981) as doesthe volume of the gut involved in fermentation (Chiversand Hladik 1984). The minimum body weight for aforegut fermenter has been estimated at approximately5 kg (van Soest 1981). Selection for foods of high nutr ientquali ty and low digestion-inhibitor content is thereforeexpected to be pronounced in foregut fermenters ap-proaching the lower l imit in body size for this digestivesystem. Where vegetation in the habitat is generally oflow quality , or only seasonally abundant, selection forcertain foods is expected to be particulary marked.Procolobus verus, the smallest of all colobines, with anadult m ale bo dy weight o f 4.6 kg, showed a ma rkedpreference for foods which had low fibre and tannincontents and which were therefore more digestible (Oates1988). Presbyt is rubicunda was more selective in foodchoice than the closely related P. m elalophos (Davies etal. 1988). While the t wo species have similar bod yweights (6.0-6.5 kg) and bot h selected foliage on thebasis of nitrogen con tent and digestibili ty (although onlya wea k posit ive influence was reported for P. melalophos)(Davies et al. 1988), the vegetation at Sepilok whereP. rubicunda was observed (Davies 1984) was of poorerqual i ty than a t Kuala Lompat where P. m elalophos wasstudied (Bennett 1983). Presbyt is rubicunda also selectedleaves low in f ibre content (Davies et al 1988).

Trachypithecus auratus (E. Geof froy St. Hilaire 1812)with an e stimated male bod y weight sl ightly heavier thanthe T. cristata male body weigh t o f 7 .1 kg (Roon wal andMohnot 1977), is intermediate in size for a colobine. Thediet and feeding behaviour of two T. auratus sondaicusgroups was s tudied in the Pangandaran Nature Reserve ,West Java . The hab i ta t o f one group (G RP21) consis tedof secondary forest in an advanc ed successional stageand tha t o f the o ther g roup (GRP3 ) consis ted of second-ary forest and plantation areas Tectona orandis ,Swietenia macrophyl la and Acacia auricul iformis) (Kool1989; K ool in press) . Availabil i ty of preferred food i temswas not restr icted on a seasonal basis. Dietetic diversity


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528varied li t t le from one month to the next and matureleaves were rarely eaten, ind icatin g that food was n otseasonally scarce (Kool in press) . Thus, foods may notbe s trongly selected for high nutr ient conte nt and lowdiges t ion- inhib i tor concentra t ions by T . a u r a t u s s o n -d a i c u s .

ateria ls and methods

Two sets of samples were analysed for their nitrogen, fibre, con-densed t anni n and total phenolic contents, digestibility and protein-precipitating capacity. The first set was collected on the basis thatthe plant samples looked identical to preferred food items whichwere eaten from the same plants by 7 . auratus sondaicus (Kool inpress). Nine preferred food items including four items that r ankedin the top six and that accounted for 28.8 % of the GRP3 diet (Koolin press) and five preferred food items including four items thatranked in the top seven and that accounted for 22.2% of the GRP21diet (Kool in press) were analysed. The results of these analyses arecombined to increase sample size and to consider general propertiesof food selection by T . a u ra t u s so n d a i cu s .The second set consisted of samples of matu re leaves of commonspecies, none of which was eaten by T . a u ra t u s so n d a i cu s . Twelvespecies, including 10 of the 12 most abundant species (as percentagebiomass), account ing for 71.5% of the total basal area (Kool 1989)were sampled in the GRP3 study site and nine species, including sixof the eight most abundan t species, accounting for 62.1% of basalarea (Kool 1989) were sampled in the GRP21 home-range area.After collection, leaves were sun-dried and then stored in sealedbrown paper bags. Prior to analysis, samples were ground and driedto a constant weight in an oven at 50 ~ C. Samples were analysedin duplicate. All results are expressed as percentage dry weight.Nitrogen (N) was measured using the Kjelfoss method (modifiedKjeldahl method) at Wool and Pastoral Sciences, The University ofNew South Wales. Prote in levels were calculated as N x 6.25. Otheranalyses were conducted at the Division of Wildlife and RangelandsResearch - Commonwealth Scientific and Indust rial Research Or-ganisation (CSIRO). Where possible, methods used closely ap-proximated those of P. Waterman since his laborato ry has analysedplant samples for other colobine studies (Oates et al. 1980; Water-man et al. 1980; Choo et al. 1981 ; McKey et al. 1981; Davies et al.1988; Oates 1988; Waterman et al. 1988).Fibre (lignin and cellulose) was measured as acid detergent fibre(ADF) using the van Soest (1963) method with filtrex unit s (Moir1982). The ADF method has been shown to be highly correlatedwith the neutral detergent fibre (NDF) and lignin methods (Water-man and Choo 1981).

Phenolics (and tann ins) were extracted with 50% methanol.Whilst 70% acetone (as used in P. Waterman's laboratory) mayextract a few more phenolics (Bate-Smith 1973) than methanol,methanol probably extracts more than the animal does (Mole andWaterman 1987a). Total phenolics (TP) were measured by theFolin -Denis method (Oates et al. 1980) using gallic acid as a stan-dard. Condensed tannins (CT) were measured using the vanillinmethod (Burns 1971) with catechin as a standard. This method hasshown a consistent high correlation with the Bate-Smith methodfrequently used in other studies (Waterman and Choo 1981). Asstandards were not the same for the latter two analyses, the resultsof the TP and CT assays cannot be compared directly with eachother (Oates et al. 1980; Waterman et al. 1980).Digestibility was assessed by the in vitro pepsin-cellulase digest-ibility assay (CDIG) (Choo et al. 1981). This method results in thebreakdown of all protein, cellulose and smaller carbohydrate mole-cules.The biological effects of tannins lie in their capacity to bind andprecipitate proteins (McManus et al. 1981). An absence of a correla-tion between protein-precipitating capacity and total phenolic orproanthocyanid in content has been reported and the incorporat ionof a prote in-precipi tation assay recommended, as such an assaymeasures the property of t annins in their capacity to act as plantdefensive compounds (Martin and Mart in 1982). Protein precipita-tion (PP) was measured by the Asquith and Butler (1985) method,using bovine serum albumen (BSA) covalently labelled with Re-mazol bri lliant blue R. Results were expressed as percentage oftannic acid equivalents which would precipitate BSA.Mean percentage variance in replicates was small and consider-ably lower than variance within a group. For example, the meanpercentage variance in replicates for samples of leaves eaten thatwere analysed for ADF was 2.6%, considerably less than the per-centage variance around the mean of 185 % for samples of leaves ofall species that were eaten and analysed for ADF content. Replica-tes were therefore pooled and mean values used in subsequentpresentation of results and discussion based on compari son betweengroups.

Results

There was a tende ncy for the vegetation in the GRP3home- range area to have a higher nitrogen, and thereforeprote in , content and a lower ADF content than in theGRP21 site (Table 1). However, CDIG was lower andTP and CT contents higher in mature leaves from theGRP3 home-range area. PP capacity also tended to behigher in the vegetation of the GRP3 home-r ange area

Table 1. Phytochemical analyses of mature leaves in the home-range areas of GRP3 and GRP21 bChemical analysisNitrogen ADF TP CT CDIG PP

GRP3 Mean 2.34 35.63 5.14 2.94 40.27 4.09(SD) (0.71) (9.98) (4.25) (3.45) (17.51) (3.82)Median 2.20 36.66 3.43 0.83 46.47 1.89(IQ) (1.8-2.85) (26.11-45.06) (1.53-9.06) (0.47-6.17) (25.53-52.11) (0.90-7.32)

GRP21 Mean 1.91 37.93 2.66 1.59 45.80 2.14(SD) (0.68) (10.93) (2.24) (2.71) (13.88) (1.79)Median 2.00 39.19 1.49 0.32 47.49 1.27(IQ) (1.45-2.35) (27.87-49.68) (1.12-5.30) (0.12-2.24) (32.01-54.80) (0.67-3.91)

a n = 12, basal area = 71.52%b n = 9, basal area = 62.12 %ADF = fibre, TP = total phenolics, CT = condensed tannins,CDI G = % digestibility, PP = prote in precipitating capacitySD = standard deviationIQ = interquartile range


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T a b l e 2 . W e i g h t e d v a l u e s f o r c h e m i c a l m e a s u r e s o f m a t u r e l e a v e si n t w o s t u d y s i t e s a t P a n g a n d a r a nS t u d y s i te C h e m i c a l a n a ly s i s

N P r o t A D F C D I G C T T P P PGR P3 2 .14 13 .38 34 .42 51 .06 3 .45 4 .90 4 .36GR P21 1 .80 11 .03 36 .71 46 .54 0 .96 2 .38 2 .04

R e f e r t o T a b l e 1 f o r d e f i n it i o n s o f a b b r e v i a t i o n s f o r c h e m i c a la n a l y s e s

( T a b l e 1 ). N o n e o f t h e s e d i ff e r e n c e s w e r e s i g n i f i c a n t( M a n n - W h i t n e y U ) .W e i g h t e d v a l u e s f o r e a c h c h e m i c a l m e a s u r e w e r e c a l-c u l a t e d f r o m t h e e q u a t i o n T ( p~ x J ~ ) / Z P ~ wh ere P~ i s t hep r o p o r t i o n o f th e b a s a l a r e a c o n t r i b u t e d b y s p e ci es i a n dX ~ i s th e c h e m i c a l m e a s u r e f o r s p e c i e s i ( G a r t l a n e t a l .1 9 8 0; W a t e r m a n e t a l . 1 98 8) ( T a b l e 2 ) . W e i g h t e d v a l u e sa c c o u n t f o r t h e p r o p o r t i o n o f b a sa l a r e a s a m p l e d a n da r e , t h e r e f o r e , a b e t t e r i n d i c a t o r o f t h e c h e m i c a l p ro f i l eo f t h e v e g e t a t i o n i n a g i v e n a r e a . T r e n d s i n d i f f e r e n c e sb e t w e e n t h e v e g e t a t i o n o f th e t w o s t u d y s i te s w e r e s i m i-l a r t o d i f f e r e n c e s b a s e d o n m e a n ( a n d m e d i a n ) v a l u e s( T a b l e 1 ) e x c e p t th a t m a t u r e l e a v e s i n t h e G R P 3 h o m e -r a n g e a r e a w e r e m o r e d i g e s t i b l e t h a n v e g e t a t i o n i n t h eG R P 2 1 h o m e - r a n g e a r e a w h e n b a s e d o n w e i g h te d v a lu e s(Tab l e 2 ) .T P a n d C T c o n t e n t w e r e p o si t iv e l y c o r r e l a te d f o rm a t u r e l e a v e s i n t h e G R P 3 s t u d y s i te ( rs = 0 . 73 4 , n = 1 2,P < 0 . 0 1 ) a n d i n t h e G R P 2 1 s t u d y s it e ( r s= 0 . 7 01 , n = 9 ,P < 0 .0 5 ). T h i s i n d i c a te s t h a t a c o n s i s t e n t p r o p o r t i o n o fp h e n o l i c s w e r e l a i d d o w n a s c o n d e n s e d t a n n i n s . A s i m i la rc o r r e l a t i o n h a s b e e n r e p o r t e d i n o t h e r s t u d ie s o f p l a n tc h e m i s t r y ; fo r e x a m p l e , f o r v e g e t a t i o n in S e p i lo k ( D a v i e s1 98 4). H o w e v e r , t h e r e l a t i o n s h i p b e tw e e n T P a n d C T i sn o t a l w a y s c l ea r , a s e v i d e n c e d b y t h e l a c k o f c o r r e l a t i o nb e t w e e n t h e s e t w o v a r i a b l e s i n th e v e g e t a t i o n a t K u a l aL o m p a t ( B e n n e t t 1 9 83 ).L i n e a r r e g r e s s i o n a n a l y s i s w a s u s e d t o e x a m i n e t h er e l a t i o n s h i p b e t w e e n C D I G a n d o t h e r c h e m i c a l m e a -s u re s . D a t a o n v e g e t a t i o n f r o m t h e t w o s t u d y s it es w e r ec o m b i n e d t o i n c r e a s e s a m p l e s i ze . A s i g n i f ic a n t n e g a t i v er e l a t i o n s h i p w a s f o u n d b e t w e e n C D I G a n d A D F( r = - 0 . 6 6 , F 1 , 2 o = 1 5.0 2, P < 0 . 0 1 ) . C D I G w a s n o t c o r -r e l a t e d w i t h a n y o t h e r m e a s u r e i n c l u d i n g T P a n d C T .P r e v i o u s s tu d i e s h a v e s i m i l a r ly r e p o r t e d t h a t C D I G w a sm o r e s t ro n g l y c o r r el a te d w i t h A D F t h a n a n y o t h e r m e a -s u r e , a l t h o u g h T P h a s b e e n f o u n d t o a l s o h a v e a n i n -f l ue n c e i n s o m e s t u d i es ( C h o o e t a l . 1 9 8 1; W a t e r m a net a l. 1983 ; Wa te rm an e t a l. 1988).T h e r e l a t i o n s h i p b e tw e e n P P c a p a c i t y a n d o t h e r m e a -s u r e s w a s s i m i l a r l y a s s e s s e d b y l i n e a r r e g r e s s i o n a n a l y s i s .P P w a s h i g h l y c o r r e l a t e d w i t h C T c o n t e n t ( r - - 0 .8 3 ,F 1 , 2o = 4 2 .2 4 , P < 0 . 0 0 1 ) a n d w i t h T P c o n t e n t ( r = 0 . 9 0 ,F1 .2o = 85 .11 , P < 0 .001) ; a r e f l ec t i on o f t h e co r re l a t i onb e t w e e n t h e s e t w o v a r i a b l e s a s d e s c r i b e d e a r l i e r . N oc o r r e la t io n w i t h A D F o r p r o t e in c o n t e n t w a s f o u n d .L e v e l s o f a ll si x c h e m i c a l m e a s u r e s i n f r u i t s ( e a t e n a n du n e a t e n ) a n d l e a v e s ( e a t e n a n d u n e a t e n ) w e r e c o m p a r e dw i t h M a n n - W h i t n e y U te s ts . N o n e o f th e d i ff e re n c e s

O

O

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O

64121086420 64

126 '4 '2 '0 '

529

1412

6 10~,, 6

20

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(21)

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3o-o 2o

~00

6o~ 5o

' B 403o

-o 2olO

o

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D F

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L M L Y P H U I IPROT

F i g . 1 . M e a n c o n t e n t [ a s % d r y w e i g h t ( + S D ) ] o f c h e m i c a l m e a s u r e si n l e a v e s a n d f r u i t s p r e f e r r e d b y rachyp i thecus aura tus sonda icusand in leaves and fruits available at Pangandaran but w hich werenot eaten. LM = m ature leaves, LY = young leaves. Refer to Table1 for definitions of abbrev iations for chem ical analyses. S o l i d b a r s ,not e aten; o p en b a r s , eaten

f o u n d w e r e s t a t is t ic a l ly s ig n i fi c a nt . H o w e v e r , C D I Gt e n d e d t o b e g r e a t e r i n b o t h f r u it s a n d l e av e s w h i c h w e r ee a t e n w h e n c o m p a r e d w i t h p a r t s n o t e a t e n ( F ig . 1 ). A D Fw a s l es s f o r f r u it s a n d l e a v e s e a t e n , a n d C T , T P a n d P Pc a p a c i t y t e n d e d t o b e h i g h e r i n f r u i ts e a t e n a n d l o w e r i nl e a v e s w h i c h w e r e e a t e n ( F i g . 1 ) . P r o t e i n c o n t e n t w a sh i g h e r i n f r u i t s a n d l e a v e s w h i c h w e r e e a t e n , a l t h o u g ho n l y m a r g i n a l l y g r e a t e r (1 ) f o r l e a ve s e a t e n w h e n c o m -


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530pare d wi th l eaves no t ea ten (F ig . 1 ) . Discr im inan t func-t ion ana lys i s (SPSS 1990) showed tha t l eaves tha t weren o t e a t e n h a d h i g h ADF (0 .7 3 ) a n d C T (0 .6 9 ) a n d l o wC D I G ( - 0 . 6 4 ) w h e r e a s th o s e t h at w e r e e at e n w e re h ig hi n C D I G a n d l o w in A D F a n d C T . F r u i t s e le c ti on w a ss imi la r ly ana lysed and f ru i t s tha t were no t ea ten hadc o m p a r a t i v el y h ig h A D F ( 1. 00 ) a n d l o w p r o t e in ( - 0 . 7 4 )a n d C D I G ( - 0 . 6 2 ) w h e r e a s t h o s e t h a t w e r e e a t e n w e r eh ig h in p r ot e in a n d C D I G a n d l o w in A D F . L e a v estended to have h igher l eve l s o f p ro te in , to be more d iges -t i bl e a n d h a v e l e ss A D F t h a n f ru i t s wh i l e C T , T P a n d P Pwere p resen t in h igher quan t i t i es in f ru i t s ea ten than inleaves wh ich were ea ten (F ig . 1 ) .L e a v e s m a y , t h e re fo re , h a v e b e e n s e l e c t e d fo r l o we rf ib re con ten t and , to a l es ser degree , g rea te r d iges t ib i li ty .C o n d e n s e d t a n n i n s a n d t o t a l p h e n o l i c s m a y a l s o h a v ein f luenced f ru i t and le af se lec t ion in tha t th ey were h igheri n f rui t s e a t e n a n d l o w e r i n le a v e s e a t e n wh e n c o m p a re dwi t h p a r t s n o t e a t e n . A n a l y s e s o f f lo we r s we re t o o f e w t op e rm i t c o m p a r i s o n s b e t w e e n fl o we r s e a t e n a n d t h o s e n o te a t e n. H o we v e r , c h e m i c a l c o m p o s i t i o n o f f l o we r s a n dthe i r in f luence on food se lec t ion i s genera l ly regarded asbe ing s imi la r to th a t o f l eaves (Dav ies e t a l . 1988).i s cus s ion

T h e r a ti o s o f p r o t e i n / A D F a n d p r o t e i n / ( A D F + C T ) a rec o n s i d e re d t o b e i m p o r t a n t i n th e ro l e o f p l a n t c h e m i s t ryi n i n fl u e n ci n g fo o d s e l e c t io n b y c o l o b i n e s p e c ie s (M c Ke y1 97 8; M c Ke y e t a l. 1 98 1; W a t e rm a n a n d M c K e y 1 9 8 9;Dav ies e t a l . 1988) and u l t imate ly fo r the i r in f luence onco lob ine b iomass (W ater ma n e t a l. 1988). The h igher thera t io i s then the be t te r the qua l i ty o f the l eaf . The sec ond-a ry fo re s t a t P a n g a n d a ra n (GR P 2 1 s t u d y si te ) h a d l o w e rp r o t e i n / A D F a n d p r o t e i n / ( A D F + C T ) r a t io s f o r m a t u r el e a v es th a n t h e fo r e s t a t K i b a l e wh e re P r o c o l o b u s b a d i u sa n d C o l o b u s 9 u e r e z a we re s t u d i e d (Oa t e s 1 9 77 ; Oa t e s e ta l. 1977 ; Gar t la n e t al . 1980; Wa ter ma n an d Ch oo 1981)bu t had h igher va lues than the ra t io s fo r f ive o ther s i t eswh e re c o l o b i n e s h a v e b e e n s t u d i e d (T a b l e 3 ) . R a t i o sg i v e n i n T a b l e 3 we re d e t e rm i n e d f ro m we i g h t e d v a l u e st o a c c o u n t fo r t h e p ro p o r t i o n o f b a s a l a r e a s a m p l e d .Di f fe rences in these ra t io s may re f lec t d i f fe rences inc h e m i c a l d e fe n c e o f fo li a g e a g a i n s t h e rb i v o ry .F a c t o r s wh i c h m a y i n f l u e n c e p l a n t c h e m i s t ry i n c l u d eso i l qua l i ty (Janzen 1974 ; Ne wb ery e t a l . 1986 ; W ater-ma n e t a l. 1988), l eaf l i fe -span , (B arang a 1983 ; Co ley

1983 ; Janzen and W ater ma n 1984) , topo grap hy , ra in fa l l ,a l t i tude , l igh t and tempera tu re (Waterman e t a l . 1988) .Co lon is ing spec ies, by inves t ing less in chemica l defence ,m a y c o m p r i s e r e l at i v e ly h i g h fo o d q u a l i t y (M c K e y e t a l.1981 ; Co ley 1983) when compared wi th c l imax spec ies .F o r e x a m p l e , C . 9 u e r e z a i n K i b a l e t e n d t o p r e f e r l e a v e so f co lon is ing t ree spec ies con ta in ing low er l eve ls o f f ib rea n d b e i n g m o re e a s il y d ig e s t e d th a n t h o s e o f e v e rg re enspec ies (Oa tes 1977). The com para t ive ly h igh qua l i tyc h e m i c a l p ro f il e o f t h e v e g e t a t i o n i n t h e s e c o n d a ry fo re s ta t P a n g a n d a ra n (T a b l e 3 ) m a y a c c o u n t , a t l e a s t i n p a r t ,f o r t h e r e l a t iv e c o n s t a n t a v a i l a b il i ty o f fo o d fo r T . aura-t u s s o n d a i c u s (Koo l in p ress ) . The weigh ted va luesfo r p ro t e i n / ADF a n d , t o a l e s s e r d e g re e , p ro t e i n /(A DF + C T ) fo r t h e v e g e t a ti o n in t h e GR P 3 h a b i t a t we res imi la r (0 .415 and 0 .373 , respec t ive ly ) to the GRP21s tudy s i t e (Tab le 3 ) .T h e s e c o m p a ra t i v e l y h i gh r a t i o s m a y a l s o e x pl a i n wh yfo l ia g e wa s n o t s e l ec t e d fo r p ro t e i n c o n t e n t b y T . a u r a t u ssondai cus . Poss ib ly , p ro te in l eve l s in the fo l iage a t Pan-g a n d a ra n we re s u f f i c ie n t ly h ig h fo r T . a u r a t u s s o n d a i c u sr e q u i r e m e n t s s o t h a t s e l e c t i o n fo r p ro t e i n wa s s u p e r -f luous . By se lec ting leaves lowe r in f ib re (and wi th g re a te rd iges t ib il i ty ), p ro te in ma y be e f fec t ive ly ava i lab le toT . a u r a t u s s o n d a i c u s i n a d e q u a t e a m o u n t s o v e r t i m e .In s tud ies o f co lob ine eco logy , p ro te in i s genera l lyc o n s i d e re d t o b e t h e n u t r i e n t wh i c h i s m a x i m i s e d i n d i e tse lec t ion wi th f ib re and tann ins ac t ing as cons t ra in t s inthe i r capac i ty as d iges t ion inh ib i to rs . However , on c losere x a m i n a t i o n o f t h e d a t a f ro m s t u d ie s o f c o l o b i n e s, e v -i d e n c e fo r s u p p o r t o f t h e p ro t e i n m a x i m i s a t i o n t h e o ry i sscant .

C o l o b u s s a t a n a s a t e b o t h fo l ia g e a n d s e e d s wh i c h h a da h ig h p ro t e i n c o n t e n t (M c K e y 1 9 7 8 ; M c K e y e t al . 1 9 81 )a n d P r e s b y t i s r u b i cu n d a a t e y o u n g l e a v e s wh i c h h a d h i gh -er p ro te in l eve l s (Dav ies e t a l. 1988) . Pro te in ha d a w eakpos i t ive in f luence on fo l iage se lec t ion by T . j o h n i i (W a t e r -m a n a n d C h o o 1 9 8 1 ) a n d P . m e l a l o p h o s (Dav ies e t a l .1988) . Oth er s tud ies o f co lob in e eco logy , inc lud ing thes t u d y o f T . a u r a t u s s o n d a i c u s r e p o r t e d h e re , h a v e n o tfound a s ign i f ican t co rre la t ion be tween fo l iage se lec t ionand protein levels .P r i m a t e s p e c ie s wh i c h a r e l a rg e l y f ru g i v o ro u s m a yfe e d o n y o u n g l e a v e s a n d s h o o t s t o i n c re a s e t h e d i e t a ryi n t a k e o f p ro t e i n ; h o we v e r , H l a d i k (1 97 7 ) st a t e d t h a tp ro te in con ten t i s l es s l ike ly to s t rong ly in f luence foodse lec t ion in spec ies wh ose s tap le fo od ( leaves ) i s p ro te in -

Table 3. Plant chem istry of ma ture leavesat seven sites where eolobines have beenstudied (adapted from W aterman et al.19880Study areaDo u a la - K i b a l e Ka k a c h i Ku ala S e p i l o k T i wa i P a n g an -Edea Lompat daran

b.a.c sampled 56.3 87.4a 88.1 4 9.2 78.0 46.5 62.1Protein/ADF 0.202 0.510 0.242 0.242 0.167 0.323 0.414Pro tein/ 0.187 0.492 0.207 0.214 0.146 0.234 0.405(ADF + CT)Waterm an et al. (1988) included data from the followingsources n calculations of weightedvalues: Douala-Edea (Newberyet al. 1986), Kibale (Struhsaker 1975; Oates 1977), Kakac hi(Oates et al. 1980)b Oates 1988Basal areaa W eighted data based on num ber of stems (Struhsaker 1975) as basal area data not available


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531rich. Colobus satanas, Presbytis rubicunda a n d P. melalo-phos h a d t h e l o w e s t p ro p o r t i o n o f f o li a g e i n t a k e i n t h ed ie t o f a l l co lob ine s s tud ied to da te , ex cep t P. thomasia n d Nasalis larvatus fo r w h i c h d a t a o n t h e p l a n t c h e m i s -t ry o f t h e h a b i t a t s a r e n o t a v a i l a b l e (K o o l i n p r e ss ) . Th i sm ay exp la in w hy these th ree spec ies se lec ted fo l iage wi thh i g h er p ro t e i n c o n t e n t . I n t h e a b s e n c e o f d a t a o n d i e t a ryp ro t e i n r e q u i r e m e n t s f o r c o l o b i n e s p e c ie s it is n o t k n o w nwh ether genera l l eve ls o f p ro te in in the vege ta t ion a ts o m e s t u d y s i t e s ( fo r e x a m p l e , P a n g a n d a ra n ) a r e s u f -f i c ien t ly h igh (and A D F su ff ic ien t ly low) such tha t se lec-t i o n fo r l e av e s h ig h i n p ro t e i n i s n o t w a r r a n t e d . H o w e v e r ,a n e x c e s s o f p ro t e i n i n t h e d i e t m a y c a u s e p ro b l e m slead ing to d i so rders o f the b lo od an d l iver (W ol te r 1982).W h e n v e g e t a t i o n c o n t a i n s h i g h l e v el s o f p ro t e i n ( a n d l o wleve ls o f d iges t ion inh ib i to rs ) a l eve l m ay be re achedb e y o n d w h i c h fo o d s e l e ct i on o n t h e b a s i s o f in c r e a s e dp ro t e i n c o n t e n t i s u n l i k e l y t o o c c u r a n d w o u l d a c t u a l l yb e d i s a d v a n t a g e o u s t o a c o l o b i n e .Th e ro l e o f t a n n i n s a n d p h e n o l i cs i n fo o d s e l e c t io n b ypr ima tes i s st il l a sou rce o f deba te . Som e spec ies , fo re x a m p l e , C. guereza (Oates et al . 1977), C. satanas(M c K e y e t a l. 1 98 1) a n d Procolobus verus (Oates 1988),s e le c t f o o d s l o w i n t a n n i n c o n c e n t r a t i o n . TP a n d C Tl e ve l s w e re l o w i n t h e m a j o r d i e t a ry i t e m s fo r T.johnii b u tw e re n o t r e g a rd e d a s a m a j o r f e e d i n g d e t e r r e n t a s b o t hw e re p r e s e n t i n c o n s i d e ra b l e q u a n t i t i e s i n m i n o r fo o ditems (Oates et al . 1980). Presbytis rubicunda p re f e r r e ds e e d s w i t h c o m p a ra t i v e l y h i g h t a n n i n c o n t e n t (D a v i e set al. 1988) an d T. auratus sondaicus t ended to se lec tf ru i ts h ig h e r i n C T a n d TP c o n t e n t b u t C T a n d TP l e v e lsw e re , o n a v e ra g e , l o w e r i n l e a v e s e a t e n t h a n i n l e a v es n o te a t e n fo r b o t h s p e ci e s.

Cork and Pah l (1984) sugges ted tha t such incons i s -t e n c y m a y b e d u e t o t h e e f fe c t o f to x i c c o m p o u n d s a n d / o rn o n -c o m p o s i t i o n a l f a c t o r s o v e r r i d i n g t h e b a l a n c e b e -t w e e n n i t r o g e n , f i b r e a n d t a n n i n c o n t e n t i n s o m e i n -s tances . Cork and Pah l (1984) a l so ind ica ted tha t meth -o d s o f c h e m i c a l a n a l y si s t r a d i t i o n a l ly u s e d i n a n a l y s i s o fd i e t q u a l i t y fo r g r a z i n g h e rb i v o re s m a y b e i n a d e q u a t ewhen app l ied to fo res t fo l i age and fo l ivo res . The l a t t e rseems un l ike ly to accoun t fo r d i f fe rences descr ibed info o d s e l e c t i o n b y c o l o b i n e s i n r e l a t i o n t o t a n n i n a n dp h e n o l i c c o n t e n t a s s i m i la r d i s c r e p a n c ie s h a v e b e e n n o t e dfo r g raz ing herb ivores . Reed and So l le r (1987) found tha tpheno l ics in Acacia cyanophylla had a nega t ive e f fec t onn i t ro g e n u t i l i s a t i o n i n s h e e p i n t h a t t h e y c a u s e d l o wdiges t ib il i ty , weig h t lo ss and nega t ive n i t roge n re ten t ion .C o n v e r s e l y , p h e n o l i c s i n a n o t h e r Acacia sp. A. seyal)had a pos i t ive e f fec t on n i t rogen u t i l i sa t ion (Re ed andSo l le r 1987) . Moreno-Black and Ben t (1982) emphas i sedt h e i m p o r t a n c e o f sp a t ia l , g e o g ra p h i c a l a n d t e m p o ra lv a r ia b l es o n t h e p r o d u c t i o n o f s e c o n d a r y c o m p o u n d sa n d c o n c l u d e d t h a t g i v e n t h e u n p re d i c t a b i l i ty o f se c -o n d a ry c o m p o u n d s i n th e e n v i ro n m e n t . . , d i f fe r e n t p a t -t e rn s o f a d a p t a t i o n f ro m n o t o n l y o n e p r i m a t e s p e c ie s t oa n o t h e r , b u t a l s o b e t w e e n g e o g ra p h i c a l l o c al i ti e s o f s p e-c i e s s h o u l d b e e x p e c t e d (M o re n o -B l a c k a n d B e n t 1 98 2,p. 33).I n a r e v i e w o f t h e e f f e ct s o f t a n n i n s o n f o o d s e l e ct i onb y m a m m a l i a n h e r b iv o r e s, M o l e a n d W a t e r m a n ( 1 98 7 b)n o t e d t h a t t h e r e w a s l i tt le e v i d e n c e to s u p p o r t t h e c l a imtha t t ann ins e f fec t ive ly reduce d iges t ib i l ity . CT con ten t ,

a n d t o a l e s s e r d e g re e TP c o n t e n t , w e re n e g a t i v e l y c o r -re la ted wi th d iges t ib i l i ty in two s tudy areas in Afr ica(Waterman e t a l . 1980) . These var iab les were no t co r -r e l a t e d i n p l a n t s a m p l e s c o l l e c t e d f ro m P a n g a n d a ra n .M a r t i n a n d M a r t i n (1 9 8 2 ) c o n c l u d e d f ro m t h e i rana lyses o f s ix oak spec ies tha t there was no co rre la t ionb e t w e e n P P c a p a c i t y a n d TP c o n t e n t . V e g e t a t i o n a t P a n -g a n d a ra n s h o w e d a p o s i t i v e c o r r e l a t i o n b e t w e e n P Pc a p a c i t y a n d b o t h TP a n d C T c o n t e n t . Th e s e f i n d i n g sfu r t h e r e m p h a s i s e t h e s t r u c t u r a l h e t e ro g e n e i t y o f p h e n o -l ics and tannins .W hi le h igh quan t i t i es o f t ann ins a re l ike ly to havea d v e r s e c o n s e q u e n c e s i n p r e c i p i t a t io n o f e n d o g e n o u sp ro t e i n (M o l e a n d W a t e rm a n 1 9 87 b ), l o w le v e ls o f t a n -n ins may enhance p ro te in d iges t ib i l i ty (Dav ies e t a l .1988) . Severa l poss ib i l i t i es have been sugges ted (Jonesa n d M a n g a n 1 9 7 7; M o l e a n d W a t e rm a n 1 9 8 7b ) i n c lu d -i n g a t h e o ry t h a t t a n n i n s m a y r e d u c e t h e r i sk o f a c i d o s i sb y s l ow i n g d o w n t h e r a t e o f fe r m e n t a t io n ( G o l t e n b o t h1976 ; Dav ies e t al . 1988). Th is ma y exp la in w hy CT andTP ( a n d P P ) t e n d e d t o b e h i g h e r i n f ru i t s e a t e n b yT. auratus sondaicus t h a n i n f ru i t s w h i c h w e re n o t e a t e n(Fig . 1 ) . R ipe f ru i t s a re genera l ly avo ided by co lob inesb e c a u s e a r a p i d r a t e o f f e rm e n t a t i o n m a y c a u s e h y p e r -a c i d i ty o f t h e fo r e s t o m a c h f l u id (G o l t e n b o t h 1 97 6) . R i p ef ru it s f o rm e d a c o n s i d e ra b l e p ro p o r t i o n o f th e T. auratussondaicus d ie t (Koo l in p ress ) and , poss ib ly , t ann insp l a y e d a n i m p o r t a n t r o l e i n s l o w i n g d o w n t h e r a t e o ffe rmen ta t ion when ea t ing f ru i t s .Th e s t ro n g e s t a s s o c i a t i o n b e t w e e n c o l o b i n e fo o ds e l e c t i o n a n d p l a n t c h e m i c a l p a r a m e t e r s c o m m o n l ya n a l y s e d i n s t u d i e s o f c o l o b i n e e c o l o g y is b e t w e e n f o o dse lec t ion and low leve ls o f f ib re [ fo r example , C. satanas(M cK ey 1978; M cK ey e t a l. 1981); Procolobus badiustephrosceles (S t ruh saker 1975 ; Ga r t l an e t a l. 1980 ; W a-t e rm a n a n d C h o o 1 9 8 1 ) ; T. johnii (Oates et al . 1980);Presbytis rubicunda (D avie s et al . 1988); Procolobus verus(Oates 1988) ; and T. auratus sondaicus]. A s w i t h p r e v i o u ss tud ies (van Soes t 1977 ; Waterman e t a l . 1980 ; Choo e ta l . 1981) , d iges t ib i l i ty o f p lan t s ana lysed in th is s tu dy wa sinverse ly co rre la ted wi th f ib re con ten t . F ib re i s therefo rethe d iges t ion inh ib i to r wh ich mos t cons i s ten t ly has anega t ive in f luence on food se lec t ion by co lob ines .Poss ib ly , a nu t r i en t (s ) o ther than p ro te in i s be ingm a x i m i s e d i n d i e t s e l e c t i o n b y m o s t c o l o b i n e s . S u p p o r tfo r the poss ib i l i ty tha t l eaves were se lec ted by T. auratussondaicus fo r a nu t r i en t no t examined in th i s s tudy i so b t a i n e d f ro m a n a n a l y s is o f c h em i c a l c o m p o n e n t s i nTectona grandis l eaves (Tab le 4 ). B lades o f you ng leavesa n d m a t u re l e a v e s a n d m i d r i b s o f y o u n g l e a v e s a n dm a t u re l e a v e s w e re a n a l y s e d s e p a ra t e l y . Th e p ro p o r t i o nof t ime spen t feed ing on these par t s i s a l so g iven in Tab le4 . M i d r i b s o f y o u n g T. grandis l eaves were the p lan t par t se a t e n m o s t b y G R P 3 (K o o l i n p r e s s ) b u t t h e l a rg e d i f -fe rence in t ime spen t feed ing on th i s par t , when com-p a re d w i t h t h e o t h e r p a r t s o f T. grandis leaves , is nota c c o u n t e d fo r b y a n y o f t he c h e m i c a l m e a s u re s a v a i l a b l e(Ta b l e 4 ). I f th e p ro t e i n / A D F r a t i o s t r ic t ly g o v e rn e d l e a fs e le c t io n , a g r e a t e r p ro p o r t i o n o f y o u n g l e a f b l a d e s in t h ed i e t w o u l d h a v e b e e n e x p e c t e d a s m i d r i b s h a d c o n s i d e r-a b l y le ss n i tr o g e n a n d m o re A D F t h a n y o u n g l e a f b l a d e s .I f l eaf se lec t ion was p r ima r i ly ba sed o n d iges t ib i l ity , thep ro p o r t i o n o f m a t u re l e a f m i d r i b s i n t h e d ie t w o u l d h a v e


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532Table 4. Chemical measuresa for differentparts of Tectona orandis leaves and theirrelative contributions to the diet ofTrachypithecus auratus sondaicus

ADF Prot/ CDIG CT TP PPADF feed-ing timebLY-blades 2.9 35 .9 0 .505 52. 4 0.75 6.31 1.32 1.33LM-blades 2.8 46 .7 0 .375 48.5 0.08 1.40 1.31 0.04LY-midribs 1.6 42 .7 0 .227 56.4 0.04 0.75 0.39 12.80LM-midribs 1.3 44 .4 0 .176 59.4 0.03 0.09 0.26 0.26a Definitions of abbreviations for chemical measures are given in Table 1b Kool (in press)LY = young leavesLM = mature leaves

been greater. Feeding on midribs of young teak leaveswas regarded as highly selective as mature leaves weremore abundant than young leaves and manipulation offood was required to extract the midrib from the rest ofthe leaf.

Mature T 9 r a n d i s leaves may have presente d a physi-cal limitation to T a u r a t u s s o n d a i c u s as food items as theblades had a coarse texture and midribs were woody inappearance. In a study of herbivo ry and defensiveproperties of tree species in a lowland tropical forest onBarro Colorado Island, leaf toughness was the variablemost highly correlated with levels of herbivory (Coley1983). However, this does not explain the preference ofmidribs over blades of young teak leaves as the latterwere flaccid and noticeably less tough than the midribs.Possibly, therefore, selection of leaves was governed bya mineral(s) or nutrient (for example, soluble car-bohydrates) not considered in this study. Foliage con-tains many structural carbohydrates (Davies et al. 1988)which may provide an important energy source whenbroken down by cellulose-digesting bacteria in the sto-mach (Bauchop and Martucci 1968).

Fruits eaten by T a u r a t u s s o n d a i c u s were lower inADF and higher in protein and CDIG than fruits whichwere not eaten, following the same pattern already de-scribed for leaf selection. However, these factors are notconsidered to be major components in the selection offruit as food items as CDIG and protein were lower, andADF higher, in fruits eaten when compared with leaveseaten. These findings are different to those reported forP r e s b y t i s m e l a l o p h o s and P r e s b y t i s r u b i c u n d a (Davies etal. 1988) but the conclusion that fruit selection was notrelated to the chemical measures tested, remains the same(with the possible exception of TP and CT).

The pro por ti on of fruit in the diet varies across speciescontri buting as muc h as 53 to the C s a t a n a s diet(McK ey et al. 1981). On ly for this species was ingestedfruit clearly associated with a higher protein content(McKey et al. 1981).Fruit selection, including seeds, is generally thoughtto be associated with storage carbohydrate (such asstarch) content (for example, Davies et al. 1988; Davies1991). As some fruits are usually selected by colobineswhen available, in preference to young leaves (Hladik1977; Bennett 1983 ; Davies 1984; Kool in press) this ma ybe an important nutrient in diet selection. Hladik (1977)found that S e m n o p i t h e c u s e n t e l l u s selected foods rich insoluble glucids. The possible influence of non-structural

carbohydrate content on fruit selection by other colobi-nes has not been tested. Where examined, no r elationshipbetween gross energy content a nd fruit selection has beenfound (for example, Bennett 1983; Davies 1984) but thisis not surpri sing as gross energy content does not providea measure of available energy to a colobine.

To enable a more comprehensive understanding offood selection by colobines, feeding trials of captive col-obines are needed to determine energy assimilated fromdifferent foods, and to relate this to feeding behaviour ofcolobines in the field. The effects of foregut fermen tatio non nitrogen metabolism in colobine monkeys also needto be examined (Davies et al. 1983 ; Watkins et al. 1985).Acknowledgements I wish to thank the Indonesian Institute ofSciences (LIPI) and the Nature Protection and Wildlife Manage-ment Division (PHPA) for permission to conduct research in In-donesia. Acknowledgements are due to Dr S. Cork, Mr R. Engeland Dr A. Bagnara for collaboration with chemical analyses andto Dr P.J. Waterman for advice regarding the analyses. This re-search benefitted greatly from encouragement and discussions withDrs D.B. Croft, E.L. Bennett, D.J. Chivers, A.G. Davies, Prof T.J.Dawson, Mr R.J. Fowler and Mr. A.F. Kool. Financial supportwas provided by a Commonwealth Postgraduate Research Awardand the Joyce W. Vickery Scientific Research Fund (Linnean Soci-ety of New South Wales). I am grateful to Drs D.B. Croft andC. Peres for their comments on a draft of this paper.

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Oecologia Volume 90 Issue 4 1992 [Doi 10.1007%2Fbf01875446] K. M. Kool -- Food Selection by the...

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Transcript of Oecologia Volume 90 Issue 4 1992 [Doi 10.1007%2Fbf01875446] K. M. Kool -- Food Selection by the...