P R I M A T E P O P U L A T I O N S I N C O N T I N U O U S F O R E S T A N D F O R E S T F R A G M E N T S I N C E N T R A L A M A Z O N I A . (*)
A n t h o n y B. R y l a n d s (**) A l e x i n e K e u r o g h l i a n (***)
S U M M A R Y
Population de.niAJU.eJs ofa iix. pnÁmate ipeciei [SaQutnui mLdca, VXX.he.cAa. píthexúa, Ce
bui cvpoJULa, CkinopoteA iotanai, Alouatta ienicuZui and AteleM panlicuA) wexe estimated
in continuous fao^zit and In isolated KeAexveA lone ofa 100 ha and faoux afalO ha]. Sagulnuò
demitiei In the continuous faoKeAt wexe. hound to be low, probably dueto the lack o fa edge
hab-itat and second gxowth faavouxed by them; ViXhsLCÁa., Cebuó and KteJLeA populations axe
alio low, possibly because ofa mone widely dlitxibuted and/on. leAS abundant hood souxcu
than Is txue faon othex Amazonian siegloni, although hunting An the pait, paxticulaxly ofa
Atelejs may alio be a conttU.buti.ng faactoK; and ChÃJiopotte and Alouatta dens-itiet, wexe
faound to besimllax to thoie obsexvedln othexaXeas oh Amazonai hoK.e&ts. AteZeA and
ClrvUw-potu, which occupy nangzs on the oidex o fa thxze. km1 wexe excluded fawm the 100 -ha mi->
senve at the time ofa Its isolation. UnfaoKtunately populations wexe not known pnton. to
Isolation ofa tkii JieAexve but duxing isolation thexe remained faoux groups ofa Saguinui,
two Vit.he.cla. gfioupi, one Cebuó gnoups and fatve Alouatta groups. One SagwLnui gfioup dlsap_
peatied two monthi latex, and one yeax poit-liolotion the Cehiu, gnoup alio lefat the
nz-iexve. Single AJbouatta gtioupi iuxvlve In the isolated 10-ha lesenves. SagutvuiA, pxuent
In the faoux 10-ha KUexvet, following isolation, have diiappeaxed fan,om two ofa them. One
10-ha siesexve Ketaxns a gfioup ofa Vithesiia..
I N T R O D U C T I O N
A g r i c u l t u r a l a c t i v i t i e s in the terra f i r m e tropical rain forest of Central A m a z o -nia invariably result in isolated forest f r a g m e n t s . T h e s e f r a g m e n t s , isolated by cattle p a s t u r e a n d commercial c r o p s , retain p r i m a t e p o p u l a t i o n s d i f f e r i n g in size and c o m p o -s i t i o n on the a r e a -s of the fore-st and h a b i t a t -s and f l o r i -s t i c c o m m u n i t i e -s they c o n t a i n .
In 1 9 7 9 , the W o r l d W i l d l i f e Fund - U.S. and the National Institute for A m a z o n Research
(*) P a p e r p r e s e n t e d at the S e c o n d B r a z i l i a n P r i m a t o l o g y C o n g r e s s , C a m p i n a s , São Paulo, 2 9 t h J a n u a r y to 2nd F e b r u a r y , 1 9 8 5 .
(**) I n s t i t u t o N a c i o n a l de P e s q u i s a s d a A m a z ô n i a - INPA, M a n a u s - A M .
(rtrtrt) Anthony Rylands on the Minimum Critical Size of Ecosystems Project (Currently: Biological Dynamics of Forest Fragments Project) - INPA/Smithsonian Institution, Manaus, AM.
(INPA) of Brazil initiated the M i n i m u m Critical Size of E c o s y s t e m s P r o j e c t (MCSE) in volving the study of d i f f e r e n t sized forest f r a g m e n t s resulting from the forest c 1 e a r e n c e on three farms in the Agricultural District of M a n a u s , a p p r o x i m a t e l y 80 km n o r t h of the city (Fig. l). The a i m is to e x a m i n e w h a t size of isolated forest remmant is n e c e s s a r y to m a i n t a i n the d i v e r s i t y and c o m m u n i t y s t r u c t u r e c h a r a c t e r i s t i c of the forest before its isolation and w h a t are the p r o c e s s e s involved in the ecological c h a n g e s w h i c h resul t w h e n the remnant is too small (Lovejoy e t al . , 198 3) - By agreement wi th farm o w n e r s , the areas of the forest left standing are s t a n d a r d i z e d to 1-ha , 10-ha, 1 0 0 - h a , 1 000-ha , and 1 0 , 0C0-ha. T h e s e a r e a s (hereafter called reserves) are m a r k e d out and s t u d i e d b e f o r e their isolation and left standing w h e n c l e a r a n c e a c t i v i t i e s reach that part of the f a r m .
T h e s e are nine p r i m a t e s p e c i e s w h i c h o c c u r in this r e g i o n , n o r t h of the Rio A m a z o nas a n d east of the Rio N e g r o in B r a z i l . T w o of these have not been o b s e r v e d in the farms of the project a r e a . One is the squirrel m o n k e y , Saimiri s c i u r e u s , w h i c h is typical of
flooded f o r e s t , and the w e e p e r c a p u c h i n , C e b u s n i g r i v i t t a t u s , of some u n k n o w n reason is a l s o a b s e n t . Of the remaining s e v e n , the night monkey , A o t u s trivi rgatus , al though proba bly o c c u r r i n g in the a r e a , has never been o b s e r v e d in the r e s e r v e s . The remaining six species range in size from the m i d a s (goldenhanded) t a m a r i m , S a g u i n u s m i d a s , of 4 5 0 -550 gm to the black spider m o n k e y , A t e i e s p a n i s c u s , of 7-9 kg (Table 1 ) .
S t u d i e s of the primates in the reserve area started in July 1983 , and here w e report o n o u r findings regarding their d e n s i t i e s in the s t i 1 1 - c o n t i n u o u s f o r e s t and their sur vival in a reserve of 100 ha w h i c h w a s a l r e a d y in the p r o c e s s of isolation and four r e -serves of 10 h a , isolated during 1980-1984.
M E T H O D S
T h e Study A r e a
The study w a s c a r r i e d out on three farms a p p r o x i m a t e l y 80 km north of Manaus on the M a n a u s - B o a Bista highway (BR-17*0 ( 2° 2 5 ' S , 59°W) (Fig. 1 ) . The terrain i s undu1 ating and bi sec ted by n u m e r o u s sma 1 1 streams . The predomi nant soi 1 s are nut r i en t-poor , yel 1 ow 1 atosols. The v e g e t a t i o n is tall terra firme tropical rain forest w i t h a c l o s e d canopy at 2 5 - 3 5 m and emergent trees reaching h e i g h t s of 40-50 m. T h e u n d e r s t o r y in sparse w i t h abundant stemless p a l m s . The s t r e a m v a l l e y s are c o m m o n l y abundant in p a t u ã ( J e s s e n i a batatua) or (Mauritia flexuosa) p a l m s . The annual p r e c i p i t a t i o n in the A d o l f o Ducke Forest R e s e r v e n e a r b y ( 3 ° 0 0 ' S , 59°55'W) during the y e a r s 1967-1979 w a s 2 1 7 0 - 2 9 0 0 mm w i t h a dry season from June to O c t o b e r / N o v e m b e r (monthly m e a n p r e c i p i t a t i o n 83-166 mm) and a w e t season from D e c e m b e r to May (monthly m e a n p r e c i p i t a t i o n 226-330 mm) (Marques-Filho e t a l . 1981).
T h e R e s e r v e s
Primate surveying w a s c a r r i e d out in four 100-ha r e s e r v e s , e a c h of w h i c h c o n t a i n four parallel t r a i l s , separated by 200 m a n d a fifth trail w h i c h b i s e c t s the o t h e r four down the m i d d l e of the reserve. Each trail is m a r k e d every 50 m. One of the reserves
(Porto A l e g r e , 3304) has an additional two lateral trails w h i c h w e r e a l s o s u r v e y e d . T h e total trail lengths are shown in T a b l e s 2 a n d 3 . T h e D i m o n a ( 2 3 0 3 ) , F l o r e s t a l ( 1 3 0 1 ) and km 34 (1302) reserves a r e not yet isolated a n d surveys w i t h i n them a r e c o m b i n e d for esti mating d e n s i t i e s in continuous f o r e s t . T h e P o r t o A l e g r e (3304) reserve w a s largely iso
lated during the period J u n e - A u g u s t 1983, a l t h o u g h a small isthmus of forest along a stream c o n n e c t e d it w i t h continuous forest until S e p t e m b e r 1984 w h e n a swathe w a s c u t across it, isolating the reserve c o m p l e t e l y . T h e c l e a r e d area a r o u n d the reserve w a s not b u r n e d . T h e four 10-ha reserves w e r e isolated from J u n e to A u g u s t 1980 (Colosso, 1202) April t o A u g u s t 1983 (Cidade P o w e l l , 1207 & P o r t o A l e g r e , 3209) and from June to July 1984 (Dimona, 2 2 0 6 ) . T h e felled forest w a s burned a r o u n d two of the reserves in the months following their isolation (1202 & 2206) but not a r o u n d 1207 and 3 2 0 9 .
S u r v e y T e c h n i q u e s
P r i m a t e p o p u l a t i o n d e n s i t i e s w e r e e s t i m a t e d using the m e t h o d o f repeat transect censuring ( N R C , 1 9 8 1 ) . T h e p e r p e n d i c u l a r d i s t a n c e from the path (DFP) of the f i rst m o n k e y seen at e a c h sighting w a s used to e x a m i n e the f r e q u e n c y o f sightings at d i f f e r e n t d i s t a n c e s from the p a t h , a n d , from t h i s , infer the m a x i m u m reliable s i ght i ng d i s t a n c e a n d hence the transect w i d t h (Kelker's m e t h o d , see N R C , 1 9 8 1 ) . T h e d e n s i t y e s t i m a t e s for individuals are made on the actual n u m b e r s seen during surveying rather than a v e r a g e group size
(Freese e t a l . , 1 9 8 2 ) . This results in a slight u n d e r s t i m a t i o n because it is rare that all individuals in the g r o u p a r e c o u n t e d . Results of transect s u r v e y i n g in the 100-ha isolate are c o m p a r e d w i t h the n u m b e r s of p r i m a t e s known t o o c c u r in the reserve i n o r d e r to e x a m i n e a n y bias in the m e t h o d for the d i f f e r e n t primate s p e c i e s .
RESULTS
P r i m a t e D e n s i t i e s in C o n t i n u o u s Forest
The surveys of the three 100 ha reserves w h i c h have not been i s o l a t e d ( 1 3 0 1 , 1302 & 2303) are c o m b i n e d to provide estimates of the primate d e n s i t i e s in continuous f o r e s t . The m o s t a b u n d a n t species in terms o f g r o u p s / k m2 w e r e A l o u a t t a , f o l l o w e d by S a g u i n u s (Table 2 ) . A l o u a t t a w a s also the most a b u n d a n t in terms of i n d i v i d u a l s / k m2 but C h i r o -p o t e s , w h i c h live in large g r o u -p s , w e r e the s e c o n d most a b u n d a n t , w i t h S a g u i n u s taking
third p l a c e . T h e density e s t i m a t e s by s u r v e y i n g agree q u i t e well w i t h the p i c t u r e o b -tained by e x a m i n i n g the n u m b e r of d i f f e r e n t g r o u p s w i t h home ranges partly or entirely w i t h i n the reserves (Table 4 ) , except in the case of A l o u a t t a and P i t h e c i a . T h e survey m e t h o d is e v i d e n t l y u n d e r e s t i m a t i n g A l o u a t t a n u m b e r s by o n e - h a l f to t w o - t h i r d s . This is confirmed in the P o r t o A l e g r e data w h e r e , due to isolation, it is known that the e n t i r e home ranges of 4 - 5 groups w e r e c o n t a i n e d w i t h i n 100-ha and yet density e s t i m a t e s ranged from 0.8 to 1 . 6 groups k m2 during the three survey p e r i o d s (Table 3 ) . A l o u a t t a spend long periods resting during the day in the upper canopy a n d a r e e a s i l y m i s s e d at these times. P i t h e c i a are very q u i e t , retiring a n d f a s t - m o v i n g m o n k e y s a n d t h e i r d e n s i t i e s are
probably u n d e r e s t i m a t e d by o n e - q u a r t e r to o n e - h a l f . T h e r e w e r e some a n o m a l i e s , h o w e v e r , in t h a t , in three c a s e s , species w h i c h have been seen in the reserves w e r e not recorded during s u r v e y s . All th ree rese rvcs have t he f u 1 I comp 1 einent úF spec i es but S a g u i n u s w e r e not recorded during 83.6 km of surveying in the km reserve. T w o groups have been observed w i t h their ranges just o v e r l a p p i n g the edge of the raae'rv*. {¥]'{\ •
2) . Neither P i t h e c i a nor
Cebus w e r e recorded during 7 7 . 8 km of surveying in the Florestal r e s e r v e , although both species have been o b s e r v e d there: P i t h e c i a on two o c c a s i o n s and C e b u s on only o n e o c -casion .Comparing the numbers of groups of e a c h species in the three r e s e r v e s , the results are q u i t e uniform w i t h two S a g u i n u s g r o u p in e a c h , one to two, o r p o s s i b1 e t h r e e , family groups of P i t h e c i a , one to two C e b u s , o n e to two Chi ropotes groups and three to five g roups of A l o u a t t a (Table *0 . A m i n i m u m of 6-9 A t e i e s w e r e seen in each of the r e s e r v e s , but because small subgroups are ephemeral and individuals w e r e not d i f f e r e n t i a t e d except by size and sex, the actual numbers of individuals w a s probably h i g h e r . This s u b - g r o u p i n g behaviour m a k e s it impossible to say h o w m a n y g r o u p s were using the reserves and t h e r e -fore g r o u p s / k m - were not c a l c u l a t e d ,
Primate D e n s i t i e s in an Isolated R e s e r v e o f 100 ha
O b s e r v a t i o n s of primates in the Porto A l e g r e reserve of 100 ha w e r e s ta r ted du r i ng the last staaes of its isolation in June 1983. The isolation of the reserve resulted in the imiediate loss of A t e i e s and C h i r o p o t e s .
P o p u l a t i o n s of the remaining, primates are shown in T a b l e s 3 and h. Population esti mates by surveying a g r e e q u i t e well in the O b s e r v e d situation i n the reserve f e r S a g ü i nus and C e b u s , a l t h o u g h , as. e x p l a i n e d p r e v i o u s l y , the numbers of P i t h e c i a and A l o u a t t a are u n d e r e s t i m a t e d . T h e rather high e s t i m a t e for S a g u i n u s in IS83 (Table 3) resulted froni frequent, noisy group e n c o u n t e r s over o n e of the trails (see below) during this time. The first half of 1984 u n d e r e s t i m a t e d and the second half o v e r e s t i m a t e d the density of S a g u i n u s . This is believed to have resulted from an imbalance in the total numbers of surveys of each of the trails during the respective time p e r i o d s . For C e b u s , the slight ove restimation during 1983 occurred b e c a u s e , during one period of s u r v e y i n g , the group was feeding, sometimes twice d a i l y , on two fruiting trees w h i c h w e r e right by the survey trails. T h e lower estimate for the second half of 1981* o c c u r r e d because the group w e r e leaving and re-entering the reserve (see b e l o w ) . A l o u a t t a number? vrerc one to three times higher than those e s t i m a t e d by surveying and P i t h e c i a numbers were a p p r o x i m a t e l y double those e s t i m a t e d by s u r v e y i n g . P i t h e c i a were o n l y seen on two o c c a s i o n s during the first half of 1984.
Saguinus midas
From June till August 1983 there w e r e four groups in the r e s e r v e . H o w e v e r , inter group disputes w e r e frequpntíy o b s e r v e d for two o f t h e s e , a p p r o x i m a t e l y 100 m from the e a s t e r n b o u n d a r y of the reserve. After August 1 9 8 3 , one g r o u p , w h i c h o c c u p i e d a small home range of opprnx IrnfHeiy 3-5 ha was not •'. een a g a i n . A field hand o b s e r v e d a g r o u p of
Saguínus leaving t h e reserve f r o m its e a s t e r n e d g e in late A u g u s t . T h r e e g r o u p s have r e -m a i n e d since then. T h e i r ranges c o v e r a l -m o s t the e n t i r e reserve a n d a r e est i-mated to b e a p p r o x i m a t e l y 30 h a . T w o of the g r o u p s c o n t a i n s e v e n individuals a n d the third is c o m -posed o f 9-10 i n d i v i d u a l s , a l t h o u g h in D e c e m b e r 1984 o n e o f the smaller g r o u p s a n d the large g r o u p w e r e o b s e r v e d w i t h n e w b o r n twin infants.
P i t h e c i a p i t h e c i a
During 1983 a m i n i m u m of five individuals w e r e living in the r e s e r v e : two a d u l t pairs a n d a j u v e n i l e , e s t i m a t e d t o have been aL least a year o l d . In the first half o f 1984 they w e r e seen on o n l y two o c c a s i o n s ; a n d not at all d u r i n g s u r v e y i n g . In A u g u s t 1984, h o w e v e r , a g r o u p of o n e a d u l t p a i r , a j u v e n i l e female (about six m o n t h s o l d ) , a n d a fourth u n i d e n t i f i e d s a k i , w a s seen on several o c c a s i o n s . T h e s i t u a t i o n is n o t clear but it is p o s s i b l e the o n e a d u l t p a i r h a s d i s a p p e a r e d a n d the female o f the remaining g r o u p of three g a v e b i r t h during the w e t s e a s o n o f 1 9 8 3 - 1 9 8 4 .
C e b u s a p e l l a
One group o f 1 1 - 1 2 Cebus w a s isolated w i t h the r e s e r v e . T h e y w e r e regularly seen d u r i n g 1983 until the b e g i n n i n g o f the d r y season (June 1984) w h e n they d i s a p p e a r e d . In the f i r s t half of 1984 they w e r e o b s e r v e d leaving a n d re-entering the reserve on its north a n d w e s t b o u n d a r i e s to enter n e i g h b o u r i n g f o r e s t a p p r o x i m a t e l y 1 0 0 - 2 5 0 m a w a y . T h e last sighting of this g r o u p w a s o n the 27 J u n e 1984.
A l o u a t t a s e n i c u l u s
Five g r o u p s a n d a s i n g l e m a l e w e r e o b s e r v e d in t h e reserve d u r i n g 1983. T h e single m a l e w a s o b s e r v e d in the south e a s t c o r n e r o f the reserve but in A u g u s t 1984 a group o f five individuals (one a d u l t m a l e , two a d u l t f e m a l e s , o n e s u b a d u l t male a n d o n e j u v e n i l e ) had e s t a b l i s h e d t h e m s e l v e s t h e r e . A t least four o t h e r g r o u p s , ranging in size f r o m 5-9 i n d i v i d u a l s , have remained in the reserve d u r i n g 1 9 8 4 . H o w e v e r , c h a n g e s in h o m e r a n g e s , e x t e n s i v e range o v e r l a p a n d the e s t a b l i s h m e n t of n e w g r o u p s m a k e the s i t u a t i o n a s y e t d i f f i c u l t to a s s e s s a n d m o r e d e t a i l e d s t u d i e s , p l a n n e d for 1 9 8 5 , a r e n e c e s s a r y .
P r i m a t e D e n s i t i e s in t h e Isolated R e s e r v e s o f 10 h a
T h e four isolated 10ha reserves retain p o p u l a t i o n s of A l o u a t t a . T h e C o l o s s o r e -serve ( 1 2 0 2 ) , isolated in 1 9 8 0 , retained a group of 10 h o w l e r s immediately following its
isolation (MCSE 1 9 8 0 ) . This g r o u p n u m b e r e d eight individuals (one adul t m a l e , three adult f e m a l e s , t w o s u b a d u l t m a l e s , a j u v e n i l e a n d a n infant of a p p r o x i m a t e l y five months) in December 1984. A single m a l e e s t a b l i s h e d himself in o n e part o f the reserve in e a r l y 1984 a n d by D e c e m b e r 1984 h a d a c h i e v e d a m a t e a n d a n d of fspring o f a p p r o x i m a t e l y s ix months. T h e Porto A l e g r e 10-ha reserve (3209) c o n t a i n e d a group of 6 individuals a n d the Cidade Powell reserve (1207) c o n t a i n e d a g r o u p o f 4 - 5 individuals in D e c e m b e r 1984. A g r o u p o f five h o w l e r s (one a d u l t m a l e , three females a n d a juvenile) w a s isolated in the Dimona reserve (2206) in J u n e - J u l y 1984. A f e m a l e gave birth in October 1984 a n d the g r o u p n u m b e r e d six in D e c e m b e r 1984.
rs
A group of 5-6 SaguT nus w e r e i sol ated i n the C o l o s s o reserve in 1 b u t d i s a p p e a r e d within a year. N o Saguinus groups w e r e isolated in the Dimona reserve, but ÇJroups d o sur vive in the Porto A l e q r e reserve (six individuals) a n d the C i d a d e Powe) reserve Ct-'j i n d i v i d u a l s ) . T h e felled forest around these latter tv«3 reserves w a s not b u r n e d , re-sulting in a rapid upsurge of secondary forest around it. This m a y b e the secret to the permanence of the group in the P o r t o A l e g r e reserve büt the Saguínus in the C i dade. Po^e11 reserve a l s o benefit from the fact that it w a s isolated by only tOU m . W i t h the growth of sufficient v e g e t a t i o n s to provide c o v e r , the S a g u í n u s group i s abie tc, leave a n d enter
the reserve,
Pithecia are absent from all of the 10-ha reserves except that of D i m o n a , which maintains two adult n a l e s , two adult females and a j u v e n i l e .
DISCUSSION
PRIMATE DENSITIES IN CONTINUOUS FOREST
Saguínus midas
Saguinus m i d a s densities are as I an as the ) owest es ti ma les n b t a i n e d by M u c k e n h i r n tit al . (1976) in G u y a n a , and c o n s i d e r a b l y lower than those es t i m a t e d by Thor i ngton (1 968) and M i c t e n m e i e r (1977) in S u r i n a m (Table 5 ) - Sot h Thor i rig ton {I 963) and Mi t tenueier(1977)
report that Saguinus m i d a s is m o r e common in edge hab i ta i s , den se unde rs to r I es a n d s econd growth and this is c o n f i r m e d in our o b s e r v a t i o n s of this species i n c o n t i n u o u s forest in the reserve a r e a s . This habitat preference has also been o b s e r v e d for othçr tamarin a n d m a r m o s e t , C a l l i t h r i x , species ( D a w s o n , IS79; üornsteJ n el al . , 1 976; Ry 1 atids, ) 58 I ; Branch,
1383; T e r b o r g h , 1983). For this reason the tamarins do not o c c u p y the forest uniformly and groups can be s e p a r a t e d by as m u c h as 1 km, A lack of suitable habitat in the c o n -tinuous forest probably explains the low d e n s i t i e s .
Pithecia pithecia
P i t h e c i a ore always rare (Buchanan et a l , , 1981) but d e n s i t i e s in the reserve areas are lower than in other r e g i o n s , e v e n when the undti rest i mat ion is taken into a c c o u n t . They are believed to occupy small heme ranges of less than l ü - h a , in wíiich casu their rarity wou Id i ixl i cate that they may be hab i ta t sp.se Í a 1 i s li or Q t least dependent on car tain f lor i sti c commun i t i e s , but too little is known of their behaviour and h a b i t a t preferences in the wild to support this. P i t h e d a a re h u n t e d for f oori (t he i r bushy la 1 I s n re used as dusters) and this may be a contributing factor.
Cebus a p e l l a
Cebus densities are as low aí any estimated for other regions in the A m a z o n . At Cosha C a s h u , three to four groups can be found in lDG-ha of forest, each occupyi ng ranges of 50-70 ha (Terborgh i J a n s o n , 1 9 3 3 ) . Lew densities of C e b u s in a numher of localities
be partly true for the C e b u s in the r e s e r v e s . T h i s is not be w h o l e s t o r y , h o w e v e r , because groups are n o s m a l l e r than those at C o c h a C a s h u (not hunted) (8-14 individuals) but they are e v i d e n t l y using larger home ranges (more than 600 ha) (Spironelo, 1985). T h e distri but ion a n d a b u n d a n c e o f food resources in the reserves p r o b a b l y a c c o u n t for the d i f f e r -ence .
C h i r o p o t e s s a t a n a s
B e a r d e d saki d e n s i t i e s are rather lower than those e s t i m a t e d by M u c k e n h i r n et a l . (1976) a n d van Roosmalen et a l . (1981) in Guyana a n d Surinam but s 1 ight1y higher than the d e n s i t y e s t i m a t e d by A y r e s ( 1 9 8 1 ) in the reserve areas in 1980-1981 (Table 5 ) . T h e large C h i r o p o t e s g r o u p s o c c u p y home ranges of 2 0 0 - 2 5 0 ha (van R o o s m a l e n e t a l . , 1 9 8 1 ) . Surveys of the c o n g e n e r i c w h i t e - n o s e d s a k i , C . a l b i n a s u s , at A r i p u a n i indicate d e n s i t i e s o f 0.29, 0.39 a n d 0 . 5 2 g r o u p s / k m2 along three different trails ( R y l a n d s , 1982). Density estimates for a fourth trail of 0.94 g r o u p s / k m2 w e r e inflated because a b u n d a n t fruiting trees n e a £ by d u r i n g the survey p e r i o d . C . a l b i n a s u s g r o u p s at A r i p u a n a have home ranges of 2 5 0 -350 ha (Ayres, 1981) a n d o c c u p i e d all parts of the survey a r e a . A s s u m i n g that this is a l s o true for the C h i r o p o t e s in the r e s e r v e s , a home range e s t i m a t e for 0.4 g r o u p s / k m2 w o u l d b e 250 h a . It can be c o n c l u d e d , t h e r e f o r e , that the bearded saki populations are similar to those recorded e l s e w h e r e in its r a n g e .
A l o u a t t a s e n i c u l u s
Red h o w l e r p o p u l a t i o n s are b e l i e v e d to have been u n d e r e s t i m a t e d by two to three t i m e s . T h i s being s o , d e n s i t i e s a r e similar to those e s t i m a t e d for the Sami ria basin a n d C o c h a C a s h u in Peru (Freese e t a l . , 1 9 8 2 ; T e r b o r g h & J a n s o n , 1983) a n d La M a c a r e n a a n d patches of forest in the llanos in C o l o m b i a (Klein a n d K l e i n , 1976; Defler, I 9 8 I ) (Table 5 ) . T h o r i n g t o n e t a l . (1979) b e l i e v e d that the H a t o Masaguaral p o p u l a t i o n s a r e s o high because A l o u a t t a s e n i c u l u s is best a d a p t e d to the s e a s o n a l , d r y forest patches of the V e n e z u e l a n llanos a n d D e f l e r (19¾!) suggests that the fact that they share the forests w i t h o n l y o n e o t h e r primate species m a y b e a c o n t r i b u t i n g f a c t o r . Home ranges recorded for A l o u a t t a g r o u p s in C o c h a C a s h u (Terborgh a n d J a n s o n , 1983) a n d El Tuparro (Defler, I 9 8 I ) a r e b e t w e e n 10 to 20 h a a n d this w a s o b s e r v e d t o b e t h e c a s e in the reserve a r e a s . A t H a t o Masaguaral the home ranges a r e 3.21 to 7.44 ha (Neville 1972, 1976; Sekul ic,l 982).
A t e i e s p a n i s e u s
C o m p a r i n g density e s t i m a t e s of A t e i e s w i t h those from other p a r t s o f its range indi cate that they a r e very low (Table 5 ) . A t e i e s p o p u l a t i o n s have a c o n s i d e r a b l y lower in trinsic rate o f increase c o m p a r e d to A l o u a t t a , d e s p i t e their s imi lar s i z e s . T h e gestation p e r i o d is longer 2 2 6 - 2 3 2 days (Eisenberg, 1978) c o m p a r e d to 186-194 days for A l o u a t t a s e n i c u l u s (Crockett & S e k u l i c , 1 9 8 2 ) , the period of infant d e p e n d e n c e is longer (18-28 m o n t h s (Milton, 198l) c o m p a r e d to less than a y e a r for A l o u a t t a (Mack, 1979), the inter-birth interval is longer ( 2 2- 3 6 m o n t h s ( M i l t o n , 1981) but less than a year for A l o u a t t a
(Mack, I979) a n d females reach reproductive a g e at a p p r o x i m a t e l y s i x to seven years (Mil ton, I 9 8 I ) c o m p a r e d to co u r to five years for A l o u a t t a (Froehlich e t a l ., 1 9 8 1 ) . For this
reason A t e i e s a r e more v u l n e r a b l e to h u n t i n g p r e s s u r e than A l o u a t t a , e v e n though b o t h a r e equally favoured by h u n t e r s . Hunting in the p a s t u n d o u b t e d l y , at least i n p a r t , for the low A t e i e s d e n s i t i e s , a l t h o u g h the p o s s i b i l i t y remains that a wi der d i s p e r s i o n a n d lower a b u n d a n c e of the fruits preferred by A t e i e s in the reserve areas c o m p a r e d to o t h e r regions cited in T a b l e 5 m a y a l s o be a contributing factor.
T o s u m m a r i z e , S a g u i n u s d e n s i t i e s in the c o n t i n u o u s forest a r e rather low, p r o b a b l y due to a lack o f e d g e habitat a n d the second g r o w t h p a t c h e s f a v o u r e d by them. P i t h e c i a , C e b u s a n d A t e i e s p o p u l a t i o n s are low, possibly b e c a u s e o f more w i d e l y d i s t r i b u t e d and/or less a b u n d a n t food sources than is true for o t h e r A m a z o n i a n regions a l t h o u g h h u n t i n g , p a r t i c u l a r l y in the case of A t e i e s , m a y al so be the r e a s o n . Chi ropotes a n d A l o u a t t a dens_i^ ties are similar to those o b s e r v e d in other areas o f A m a z o n i a n forest w h e r e they have been s t u d i e d .
P r i m a t e s in the isolated Forest F r a g m e n t s
A t e i e s a n d C h i r o p o t e s w e r e e x c l u d e d from the 100-ha reserve w h e n it w a s isolated and it is unlikely that they wi 1 1 recolonize i t because they a r e dependent o n widely scattered , large crops of f r u i t s , a n d both o c c u p y h o m e ranges o f m o r e than 200 ha (van R o o s m a l e n , 1 9 8 1 ; van Roosmalen e t a l . , 1981). On the basis of information regarding Cebus a p e l l a home range sizes at Cocha Cashu ( T e r b o r g h , 1983) a n d at A r i p u a n a (Rylands, 1 9 8 2 ) , it w a s e x p e c t e d that the C e b u s group w o u l d survive in the r e s e r v e , b u t they d i s a p p e a r e d a p -proximately o n e year after its i s o l a t i o n . Since then it has been found that C e b u s g r o u p s in the reserve a r e a s a r e o c c u p y i n g h o m e ranges e x c e e d i n g 600 ha (SpironeJo, I985) a n d it is probable that they w e r e facing a food s h o r t a g e .
The loss of A t e i e s a n d C h i r o p o t e s in t h e isolated 100-ha reserve is u n s u r p r i s i n g , although Bernstein et a l . (1976) found A t e i e s , as well as C e b u s , in an isolated second g r o w t h forest ( 2 - 2 0 years old) in n o r t h e r n C o l o m b i a . H o w e v e r , w h e r e a s cont inuous forest
is still predominant in the a r e a s w e a r e s t u d y i n g , this w a s u n d o u b t e d l y not so for the study a r e a o f B e r n s t e i n e t a l . ( 1 9 7 6 ) . Their forest patches w e r e those left from a rela_ tively long term d i m i n u t i o n o f o n c e large tracts w h e r e a s the isolated reserves in o u r study are patches left standing in c l e a r i n g s i n , as y e t , predomi nant 1 y cont i nuous f o r e s t . The A t e i e s a n d C e b u s groups o b s e r v e d by Bernstein et a l . (1976) a r e , t h e r e f o r e , p r o b a b l y relict p o p u l a t i o n s w i t h n o w h e r e else to g o .
S a g u i n u s , P i t h e c i a a n d A l o u a t t a remain in the reserve a n d all three s p e c i e s have bred since its i s o l a t i o n . A l o u a t t a a n d P i t h e c i a d e n s i t i e s a r e s i m i l a r to those e s t i m a t e d for continuous f o r e s t , but S a g u i n u s d e n s i t i e s are rather h i g h e r .
T h e e x c l u s i o n of o n e o f the four S a g u i n u s g r o u p s isolated in the reserve is o f interest w h e n o n e notes that two Saguinus g r o u p s a r e surviving i n t h e l O - h a r e s e r v e s . If, as is b e l i e v e d , optimal h a b i t a t s include secondary forest a n d forest edge m i x e d w i t h tall primary forest ( T h o r i n g t o n , 1368; M i t t e r m e i e r & v a n R o o s m a l e n , 1 9 8 1 ; T e r b o r g h , 1983), the m i n i m u m home range size a s well as population sizes a r e g o v e r n e d by the a m o u n t o f forest e d g e . T h e d i s c r e p a n c y b e t w e e n the s i t u a t i o n s in the )00-ha a n d 10-ha reserves m a y then be e x p l a i n e d by the greater relative a r e a o f edge h a b i t a t a n d s e c o n d g r o w t h s u r r o u n d i n g
the latter. T h i s may a l s o e x p l a i n w h y three g r o u p s s u r v i v e in the isolated 100ha r e -serve w h e r e a s the ranges of only t w o g r o u p s o v e r l a p the e d g e s of a n y o n e of the 100-ha re_ serves in c o n t i n u o u s f o r e s t (Fig. 2 ) . T h e range of o n e S a g u i n u s g r o u p overlapping the northwest corner of the D i m o n a reserve (2303) c o n t a i n s a large area of secondary growth and edge b e c a u s e the forest has been cut along the n o r t h edge a n d the home range o f the group is a p p r o x i m a t e l y 15 h a , probably because o f t h i s .
U n f o r t u n a t e l y the p o p u l a t i o n s in the Porto A l e g r e 100-ha reserve w e r e not known prior to its isolation. It m a y be that the f l o r i s t i c c o m m u n i t i e s wi th i n the reserve a r e m o r e f a v o u r a b l e to S a g u i n u s , irrespective o f edge h a b i t a t s c r e a t e d by its isolation, o r that the isolation has compressed three g r o u p s into the reserve w h i c h will not survive in the long term. Time a n d further studies will t e l l , but the indications a r e that the increase in forest e d g e , the inevitable s e c o n d a r y g r o w t h al ong the marg i ns a n d the increase in tree falls in t h e 10ha reserves (Lovejoy et a l . , 1983) resulting from the f r a g m e n t -a t i o n o f the forest will f-avor -an incre-ase in the S -a g u i n u s p o p u l -a t i o n s w h i c h r e m -a i n . A similar c o n c l u s i o n w a s reached by Bernstein et a l . , (1976) for S. l e u c o p u s .
A l o u a t t a populations in the isolated reserves a p p r o x i m a t e to those w h i c h w o u l d be e x p e c t e d from their d e n s i t i e s in c o n t i n u o u s f o r e s t . A l o u a t t a s e n i c u l u s has a very w i d e d i s t r i b u t i o n w h i c h e x t e n d s into the s e m i - d e c i d u o u s d r y forest of the 11 anos o f VenezueI a and C o l o m b i a . Defler ( 1 9 8 1 ) found four groups in a 100-ha forest patch in the C o l o m b i a n llanos e a c h w i t h home ranges of 10 to 20 h a , a n d six groups in a 150-ha p a t c h , each w i t h home ranges of 2 1 - 2 6 h a . This very similar to the situation w e have o b s e r v e d . T h e groups in the 100-ha reserves a r e using larger home ranges than those restricted to the 10-ha f r a g m e n t s . T h e two g r o u p s in the C o l o s s o 10-ha reserve (1202) indicate that they can restrict their ranges e v e n f u r t h e r . T h e smallest home ranges have been recorded f o r the p o p u l a t i o n s in forest p a t c h e s at H a t o Masaguaral in the V e n e z u e l a n llanos (3-7 h a . NeviJ_ le, 1 9 7 2 ; Sekul ic, 1982) . Preferred food sources are very abundant i n these forest p a t c h e s . S e k u l i c (1982) e s t i m a t e s that o f the three key f o o d s , Ficus o c c u r in d e n s i t i e s o f 18 t r e e s / h a , A l b i z i a c o r r e s p o n d i n g l y 12 trees/ha a n d C o p e r n i c i a palms 89 t r e e s / h a . T h e a -b u n d a n c e a n d c o n c e n t r a t i o n of A l o u a t t a food resources is u n d o u -b t e d l y very different in the m o r e d i v e r s e A m a z o n i a n forests o f t h e reserve a r e a s , but under any c i r c u m s t a n c e s , howlers a r e e v i d e n t l y very flexible regarding their home range sizes a n d this probably r e f l e c t s a c o n s i d e r a b l e f l e x i b i l i t y in their d i e t . O n e woul d e x p e c t that the howlers in the 10-ha reserves a r e including m o r e leaves a n d p o s s i b l y m o r e m a t u r e leaves in their diet than those in the isolated 100-ha reserve o r c o n t i n u o u s f o r e s t . It is possibie that the c r e a t i o n o f secondary g r o w t h forest along the m a r g i n s a n d the increase in secondary g r o w t h resulting from the increase in rate of tree falls m a y f a v o u r the survival of A l o u a t t a in the small f o r e s t patches b e c a u s e o f the a b u n d a n c e of young 1 eaves resu 11ing from
the higher net p r o d u c t i v i t y a n d rapid g r o w t h of p i o n n e r trees a n d vines (Opler, 1 9 7 8 ) . In a d d i t i o n , howlers m a y benefit from the loss of other large p r i m a t e s from the 10 a n d lOOha
reserves t h r o u g h reduced c o m p e t i t i o n for large fruit c r o p s .
P i t h e c i a g r o u p s have s u r v i v e d in the 100-ha isolated reserve a n d the 10-ha reserve i sol a ted during J u n e - J u l y o f 1 984. A s m e n t i oned prev i ous 1 y , the i r home ranges are approximately
10 ha o r less (Buchanan e t a l . 1981) a n d it is p o s s i b l e that the latter g r o u p m a y s u r -v i -v e . T h e i r a b s e n c e from the fcther 10-ha reser-ves m a y simp!y be b e c a u s e none w e r e present at the time of i s o l a t i o n . T h e f a r e vertical d i n g e r s a n d leapers (Fleagle & Mi t t e r m e i e r ,
I98O) and rarely if ever g o tó the g r o u n d (Buchanan e t a l ., 1 9 8 1 ) . They a r e therefore un likely to r e c o l o n i z e a forest p a t c h o n c e they h a v e b e c o m e e x t i n c t t h e r e . They h a v e no d i s t i n c t h a b i t a t p r e f e r e n c e s , a l t h o u g h B u c h a n a n e t a t . (1981) record that they a r e m o s t c o m m o n l y o b s e r v e d in the m i d d l e c a n o p y to u n d e r s t o r e y of high forest in S u r i n a m . T h e i r rarity, h o w e v e r , does indicate, that they a r e h a b i t a t s p e c i a l i s t s w i t h i n the forest they o c c u p y a n d their survival in %he 10-ha a n d 100-ha reserves poss i bly depends o n the p r e s e n c e of c e r t a i n , a s y e t u n d e f i n e d , 1 o r i s t i c c o m m u n i t i e s . They c a n t h r i v e in a m i x t u r e of m a t u r e f o r e s t a n d s e c o n d g r o w t h (Oliveira & L i m a , 1 9 8 l ) a n d i t p o s s i b l e that the increase in s e c o n d a r y g r o w t h a l o n g the m a r g i n s a n d in tree fall a r e a s in the isolated reserves m i g h t be f a v o u r a b l e for t h e i r survival in t h e m .
ACKNOWLEDGMENTS
T h i s paper is c o n t r i b u t i o n n ? 27 in t h e M i n i m u m Cri ti cal Size of E c o s y s t e m s Project of the W o r l d W i l d l i f e Fund - U . S . a n d the C o n s e l h o Nacional d e D e s e n v o l v i m e n t o CientTfj^ co e T e c n i l õ g i c o (CNPq) t h r o u g h the Instituto Nacional de P e s q u i s a s da A m a z o n i a ( I N P A ) , M a n a u s . T h e a u t h o r s a r e m o s t grateful to D r . R. 0. B i e r r e g a a r d (Field D i r e c t o r of the Project) f o r his help a n d s u p p o r t a n d to J u l i e Evans (Cambridge U n i v e r s i t y ) , A n a M a r g a -rida Serra N e v e s ( U n i v e r s i d a d e de S a o P a u l o , R i b e i r ã o P r e t o ) , J o n a t h a n S a x t o n (Universe ty of C a m b r i d g e ) a n d W i l s o n S p i r o n e l o ( U n i v e r s i d a d e Estadual P a u l i s t a J ú l i o M e s q u i t a Fj_ lho, R i o Claro) for their help in c o l l e c t i n g survey d a t a during 198*t. O u r thanks al so to two a n o n y m o u s reviewers for their helpful c r i t i c i s m s of an e a r l i e r d r a f t .
RESUMO
Atividades agn.ope.cua/iiao na floresta de. teAAa ^Inme via Amazonia Central resulXam Invariavelmente em faagmentoò de. hloresta* l&oladaò. Em / 9 7 9 , o fundo de. \Jlda Selvagem
(WWF-ü\S) em convênio com ozlnAtÁZuto Nacional de. Pesquisas da Amazonia (INPA - CNPq) deu Inicio ao Projeto "Dinâmica Biológica de. Fragmento* Florestais", envolvendo estudo* doò efeito* desòa fragmentação em áreas [reservas] de. tamanho* diferentes no Vlstrlto Agro-pecuário da SUFRAMA, M a n a a ó . Seis espécies de. prlmatas ocorrem na areai Sagulmiò ml~ da&, pjUheclcL pithexuxi, CeòaA apeUüi, Chiropotes òatanas, Alouatta bojujculus e Ateies panlòcuÁ. Eòte estudo descreve densidades populacionais dessas espécies na floresta con tlnua [três reservas de. Í00 ha não Isoladas), numa reserva Isolada de. 100 ha e em quatro reservas isoladas de. 10 ha. A densidade, Saguinus e baixa, provavelmente por causa da falta de. mata de. borda e de. mata secundaria preferidas peto gênero; populações de. Czbus
alimento em comparação com outras regiões amazônicas , embora a caça. no passado,
especi-almente de AteZes, talvez seja um fator contribuinte; e Cfaüiopotes e Alouatta açoitem em
densidades semelhantes às outras regiões de floresta amazônica. Grupos de Ateies e Chi
ropotes, que ocupam áreas de aproximadamente 3 km
2, foram excluídos da reservaâe 100 ha
no momento de seu Isolamento. Infelizmente, populações nessa reserva, antes destu
iso-lamento, não foram Investigadas, mas durante a Isolação permaneceram quatro grupos de
Saguinus, dois grupos de Plth&cla, um grupo de Cebus e cinco grupos de Alouatta. Um gnu
po de Saguinus desapareceu depois de um mes e o grupo de Cebaó abandonou a reserva após
um ano. Grupos únicos de Alouatta sobrevivem nas reservas Isoladas de 10 ha.
Indiví-duos de Saguinus, embora presentes nessas reservas logo após Isolação, desapareceram de
duas delas. Uma reserva de 10 ha mantém ainda um grupo de Pithecia.
F i g . 1 . The location of the three farms, Dimona, Porto Alegre and Esteio, of the Minimum C r i t i c a l Size of E c o s y s t e m s Project ( W W F - U S / I N P A ) .
100 ha R E S E R V E S
1301 2 3 0 3
R e s e r v e d 3304 is i s o l a t e d . R e s e r v e s 1 3 0 1 , 1302 and 2 3 0 3 a r e o n l y m a r k e d out in c o n t i n u o u s f o r e s t . T a b l e 1. T h e p r i m a t e s p e c i e s o c c u r r i n g i n t h e M i n i m u m Critical S i z e o f E c o s y s t e m s Project (WWF-US/INPA) reserve a r e a s . S p e c i e s A v e r a g e a d u l t m a s s (g) * D i e t CALLITRICHI DAES a g u i n u s m i d a s m i d a s G o l d e n - h a n d e d tamarin
492
Frug i vore-i nsect Í v o r e C E B 1 D A EP i t h e c i a p i t h e c i a B l a c k - a n d - w h i t e saki 1871 Frugi vore-seed p r e d a t o r C e b u s a p e l l a a p e l l a T u f t e d c a p u c h i n
3450
Omn i v o r eC h i r o p o t e s s a t a n a s c h i r o p o t e s B e a r d e d saki
2990
Frugivore-seed predator A l o u a t t a s e n i c u i u s Red h o w l e r m o n k e y7275
F r u g i v o r e - f o l i v o r e A t e i e s p a n Í s e u s p a n i s e u s Black spider m o n k e y7775
Frug i v o r eT a b l e 2. T h e p o p u l a t i o n d e n s i t y e s t i m a t e s for p r i m a t e s in c o n t i n u o u s f o r e s t . S u r v e y s in the Dimona ( 2 3 0 3 ) , Florestal (1 301) a n d km 34 (1 302) 100-ha reserves c o m b i n e d .
D i s t a n c e s u r v e y e d (km) 316..
n ° of t ra i1s 15
Total length o f trails (m) 15,68
n ° o f surveys 333 Transect G r / k m2 l n d / k m2 w i d t h S a g u i n u s 0.04 km 0.6 3.9 P i t h e c i a 0.05 k m 0.2 0.7 C e b u s 0.08 km 0.4 2.2 Chi ropotes 0.08 k m 0.4 5.5 A l o u a t t a 0.04 k m 2.0 10.5 A t e i e s 0.08 km nc 1 .0 (nc) Not c a l c u l a t e d . T a b l e 3« P o p u l a t i o n d e n s i t y e s t i m a t e s for p r i m a t e s in June I 9 8 3 .
the 100-ha reserve isolated
P o r t o A l e g r e P o r t o A l e g r e P o r t o A l e g r e 0 6 - 1 2 / 1 9 8 3 0 1- 0 6 / 1 9 8 4 07-12/1984 (3304) (3304) (3304) D i s t a n c e s u r v e y e d 4 5 . 3 3 58.96 129.99 n° of t ra i 1 5 06 06 06 Total length o f t r a i l s 5876 5876 5876 n ° o f surveys 52 70 154 T r a n s e c t G r / k m2 l n d / k m2 G r / k m2 1 n d / k m2 G r / k m2 l n d / k m2 wi d t h S a g u i n u s 0.04 k m 5.5 35.3 2.1 20.03 4.8 25.6 P i t h e c i a 0. 0 5 k m 1.3 4.8 0.0 0.0 0.5 1.7 C e b u s 0.08 k m 1.6 17.1 0.4 0.4 0.0 0.0 C h i ropotes 0.08 k m 0.0 0.0 0.0 0.0 0.0 0.0 A l o u a t t a 0.04 km 1.6 6.1 0.8 3.8 1 . 5 5.8 A t e i e s 0.08 km nc 0.0 n c 0.0 n c 0.0 (nc) Not c a l c u l a t e d .
T a b l e 4 . T h e n u m b e r s o f d i f f e r e n t p r i m a t e g r o u p s identified w i t h home ranges p a r t l y o r e n t i r e l y w i t h i n the four 100-ha r e s e r v e s .
ISOLATED FOREST C O N T I N U O U S F O R E S T P o r t o A l e g r e P o r t o A l e g r e P o r t o A l e g r e D i m o n a Florestal K m 3^ (3304) (3304) (3304) " (2303) (1301) (1302) 0 6 - 1 2 / 1 9 8 3 0 1 - 0 6/ 1 9 8 4 0 7 - 1 2 / 1 9 8 4 06/83-12/84 06/83-12/84 06/83-12/84 S a g u i n u s
4
3
3
2
2
2
P i t h e c i a12
I1
1 - 2 2 - 31
Cebus1
1
0
1 - 21
2
Chi ropotes0
00
I1
2
A l o u a t t a5
5
5
4 - 5 4 - 5 3-4A t e i e s2 0
0
0
9 ind. 6 ind. 7 ind.(1) n ° of family g r o u p s .
T a b l e 5- P o p u l a t i o n d e n s i t y e s t i m a t e s by o t h e r a u t h o r s .
Spec i e s G r / k m2 l n d / k m2 R e f e r e n c e
Saguinus m i d a s
R a l e i g h v a l l e n - V o l t z b e r b . S u r i n a m
Four locali ties in Guyana Porto P l a t o n , Brazil Pithecia pi theeia Suri n a m Four localities in Guyana C e b u s a p e l l a Cosha C a s h u , Peru Four locali t ies in Peru C o b i j a , B o I Í V i a T h r e e locali ties in Guyana La M a c a r e n a , Co)omb'ia A r i p u a n i , Brazil C h i r o p o t e s s a t a n a s R a l e i g h v a l l e n - V o l t z b e r g Suri n a m Berbice R i v e r , G u y a n a P a k a n i , G u y a n a Agricultural District M a n a u s , Brazil A l o u a t t a s e n i c u l u s S a m i r i a b a s i n , Peru Cosha C a s h u , Peru Six locali t ies in G u y a n a H a t o M a s a g u a r a 1 , Venezuela (Llanos) La M a c a r e n a , C o l o m b i a El T u p a r r o , C o l o m b i a L l a n o s A r e a 1 (100 ha) A r e a 2 (150 ha) A t e i e s p a n í s e u s C o c h a C a s h u , P e r u Pakan i, Guyana A r i p u a n i , Brazil
k
0.4-2.70 . 8 - 3 J
3.60 . 5 - 2 . 5
0.70 . 9 - 1 . 5
) . 5 - 2 . 3
0. 5 8 0.97 0. 2 5 6.1 4,S 0.3-3-6 13.3 2.3-5.8 5.65 6.8 3.2 3.4 2 3 . 5 2 . 3 - 1 3 . 9 1 6 . 4 - 3 3 . 50 . 8 - 7 . 0
2. 6 - 1 2 . 0 36.0 3.0-25.0 7.0 10.6-17.1 5 . 8 - 9. 6 9.4-40.0 7 . 8 7 . 6 1 2 . 7 3 0 . 5 24.0 1 . 6 - 1 9 . 5 1 1 8 1 . 6 - 2 9 . 0 23.0 2 7 . 0 2 2 . 4 8.1 0.6-5.6 M i t t e r m e i e r , 1977 M u c k e n h i r n e t a l . , 1976 T h o r i n g t o n , 1968 B u c h a n a n et a l . , 1981 M u c k e n h i r n e t a J ., 1976 Freese e t a l . , 1982 F r e e s e e t al ., 1982 F r e e s e e t a l . , 1982 M u c k e n h i r n e t a l . , 1976 K l e i n & K l e i n , 1976 R y l a n d s , 1982 v a n R o o s m a l e n e t a l . , 1981 M u c k e n h i r n e t a l . , 1976 M u c k e n h i r n e t a 1., 1976 A y r e s , I98I F r e e s e e t a l . , 1982 Freese e t a l . , I982 M u c k e n h i r n e t a l . , 1976 R u d r a n , 1979 K l e i n & K l e i n , 1976 D e f l e r , 1981 F r e e s e e t a l . , 1982 M u c k e n h i r n e t a l . , 1976 R y l a n d s , 1982R e f e r e n c e
A y r e s , J . M. - 1 9 8 1 . O b s e r v a ç õ e s s o b r e a e c o l o g i a e o c o m p o r t a m e n t o d o s c u x i ú s (Chiro-potes a l b i n a s u s e Chiro(Chiro-potes satanas, C e b i d a e , P r i m a t e s ) . U n p u b l i s h e d m a s t e r ' s thesis. U n i v e r s i t y of A m a z o n a s and the N a t i o n a l I n s t i t u t e f o r A m a z o n R e s e a r c h (INPA) M a n a u s .
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