Estrada y Coates 1996

8/22/2019 Estrada y Coates 1996

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International Journal of P r i m a t o l o g ) , , Vol. 17, No. 5, 1996

T r o p i c a l R a i n F o r e s t F r a g m e n t a t i o n a n d W i l dP o p u l a t i o n s o f P r i m a t e s a t L o s T u x t l a s, M e x i c oA l e j a n d r o E s t r a d a z a n d R o s a m o n d C o a t e s - E s t r a d a 1Receive d Marc h 19, 19 96; accepted June 3, 1996

In view of the extensive destruction, fragmentat ion, and conversion o f prim atehabi ta t s to anthropogenic vege ta tion , in format ion on Neo tropical pr im ateabi l it y to use a landscape cons i s t ing o f fores t f rag m ents an d agriculturalhabi tats is necessary to un derstan d the ecological f lexibi li ty of the speciesinvolved a nd i t i s of relevance to the design o f conservat ion scenarios at thel andscape le ve l. W e censused howl e r s and sp i der m o nkeys i n 126 f o re s tfrag m ents an d in 44 agricul tural s i tes at L os Tuxtlas, souther n Veracruz,Mexico , and used the IDRISI Geographic In format ion Sys tem to assess theextent of prim ate ha bi tat remaining. We con duc ted ec ono m ic surveys to assesst he p roduc t i v i ty o f s eve ra l s y s tem s o f land m anagem en t , i nc l ud ing ca t t leranching. Seventy-five perc ent o f native habitat ha s been lost at L os Tuxtlas,20% remains in the form o f iso la ted f ragments o f vegetat ion , a nd only 5%consists o f contiguous rain forest at high elevations (> 80 0 m). H owlers an dspider mon key s were present in only 60 and 8% o f the forest s i tes invest igated,respectively, attesting to extensive loca l extinction. Po pula tions o f both speciesare sma l l and fou nd in a f ragmented a nd i so la ted condi t ion throughout thelandscape. A large nu m be r o f howlers were detected in art ifactual h abi tats suchas cacao, co f fee and mixed (cacao and cof fee) p lanta t ions sha ded by ra infores t trees. Res idua l rain forest vegetat ion along streams, r ivers, an d lakesfaci l i tated the interfragment a nd interhabitat m ov em en t of howlers. E co no m icsurveys show ed th at som e o f the agricultural habi tats were more prod uct ivethan cattle ranching. C onservation o f spider m on ke ys requires large areas ofcon tiguou s forest, bu t only sma ll areas are pres ent a t high elevations. How lersare restricted to elevat ions


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760 Estrada and Coates-Estradahab i ta ts , an d pas ture l ands . S t ruc tura l aspec ts o f t he vege ta tion a ndconnectivi ty among habitat islands may be indispensable components of bothlandscape scenarios.K E Y W O R D S : A l o u a t t a t~__ ! ! i_ a.t_ a; t e l e s g e of fT r ~ y/ ; f o r e s t f r a g m e n t a t i o n ; p r i m a t e conservation;Los Tuxtlas, Mexico.

I N T R O D U C T I O NF a c e d w i th r a p i d a n d e x te n s iv e c o n v e r s i o n o f N e o t r o p i c a l r a i n f o r e s tst o a l a n d s c a p e c o n s i s ti n g m a i n l y o f p a s t u r e l a n d s a n d w i t h t h e n e e d t o

p r e s e r v e t h e r e m a i n i n g p r i m a t e w i ld l if e , i t is im p e r a t i v e t o d e t e r m i n e h o wd i f f e r e n t s p e c i es h a v e r e s p o n d e d t o s u c h a n t h r o p o g e n i c a l t e ra t i o n s o f t h e i rn a t u r a l h a b i t a t s . R e p o r t s o n h o w p r i m a t e s p e c i e s h a v e s u r v i v e d t h e d e -s t r uc t ion , f r agm en t a t i on , and i s o la t ion o f t rop i ca l r a i n f o r e s t s and how t h eya r e r e s p o n d i n g t o s u c h c h a n g e s a r e r a r e a n d e x i s t o n l y f o r f e w l o c a l i t i e si n C e n t r a l a n d S o u t h A m e r i c a ( L o v e j o y et al., 1986 ; Ga r c i a - Ch i a r e l l o ,1993a , b ; Gale t t i et al., 1994) . Mor eove r , da t a on Neo t r op i ca l p r i m a t e ab i l -i ty to u s e a l a n d s c a p e c o n s i st in g o f f o r e s t f r a g m e n t s a n d a g r i c u l tu r a lh a b i t a t s a r e a l m o s t n o n e x i s t e n t [ ( B i c c a - M a r q u e s a n d C a l e g a r o - M a r q u e s ,1994) Alouat ta caraya in Brazil].

Such i n f o r m a t i on i s neces s a r y t o un de r s t an d t h e eco l og i ca l f lex i b il it yo f t he s pec i e s invo l ved , and i t i s r e l e va n t t o t he de s i gn o f cons e r v a t i ons cena r i o s t h a t w i ll r e s u l t in l ong - t e r m co ns e r v a t i on o f gene t i ca l l y v i ab l ep o p u l a t i o n s o f p r i m a t e s i n t h e w i l d . R a r e l y a n s w e r e d a r e b a s i c q u e s t i o n ss u c h a s W h a t is th e a p p r o x i m a t e s iz e o f th e p o p u l a t i o n o f w il d p r im a t e st l i a t s t i l l ex i s t in the l andscape of in te res t? What i s the spa t i a l d i spers iono f th e p o p u l a t i o n ? W h i c h s p e ci e s h a v e b e e n m o r e a f f e c t e d b y t h e f r ag -m e n t a t i o n o f t h e o r ig i n a l h a b i ta t ? H o w a r e p r i m a t e p o p u l a t i o n s r e s p o n d i n gt o b i ogeogr aph i c va r i ab l e s s uch a s a r ea , i s o l a t i ng d i s t ance , and i s o l a t i nga g e o f t h e f o r e s t f r a g m e n t s t h e y i n h a b i t ? H o w a r e s p e c i e s r e s p o n d i n g t ot h e p r e s e n c e o f a n t h r o p o g e n i c v e g e t a t io n in t h e l a n d s c a p e ? a n d W h a t s c e -n a r io s o f l a n d m a n a g e m e n t c ou l d h e lp t o p r e s e rv e t h e r e m a i n i n g p r im a t ep o p u l a ti o n s a n d h o w c o m p a t i b le a r e t h e y w i t h t h e n e e d s o f th e h u m a np o p u l a t i o n s ?T h r e e s p e c i e s a r e p r e s e n t i n t h e t r o p i c a l f o r e s t s o f s o u t h e r n M e x i c o ;o n e s p e c i e s o f s p i d e r m o n k e y (Ateles geoffroyi) a n d t w o s p e c i e s o f h o w l e r s(Alouatta palliata a n d A. pigra), I n t h e l a s t f i v e d e c a d e s , p r i m a t e h a b i t a tde s t r uc t i on i n Mex i co ha s r e s u l t ed i n s i gn i f i c an t con t r ac t i on o f t he o r i g i na lg e o g r a p h i c d i s tr ib u t i o n o f t h e s e p r i m a t e s , a n d t o d a y h o w l e r s a n d s p i d e rm o n k e y s h a v e b e c o m e e x ti nc t in m a n y p a r ts o f s o u t h e r n M e x ic o . T h e r e-m a i n i n g p o p u l a t io n s i n h a b it f r a g m e n t s o f r a i n f o r e s t v e g e t a t i o n o f v a r ia b l e


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Primates a t L o s Tuxtlas, Mexico 761e x t e n s io n s in t h e s o u t h e r n p a r t s o f t h e c o u n t r y ( E s t r a d a a n d C o a t e s - E s -t r ada , 1988 ; W a t t s e t a l . , 1986).R e p r e s e n t a t i v e s o f A l o u a t t a p a l l i a t a a n d A t e l e s g e o f f r o y i are s t i l l p resenti n t he r eg i on o f Los Tux t l a s i n s ou t he r n Ve r ac r uz , Mex i co , whe r e t r op i ca ll owl and r a i n f o r e s t , and t he p r i m a t e s i nhab i t i ng i t , r e ach t he i r no r t he r nm os tgeogr aph i c d i s t r i bu t i on i n t he con t i nen t ( Es t r ada and Coa t e s - Es t r ada , 1988 ,1995) . The popu l a t i ons o f t he s e s pec i e s ex i s t i n a l ands cape t ha t ha s been ,a s a r e s u l t o f ho r i zon t a l expans i on o f pa s t u r e l ands f o r c a t t l e r anch i ng ,i n t ens ive l y and ex t ensi ve ly m o d i f i ed by pa s t hum an ac t iv i ty (Di r zo and Ga r -c l a, 1992 ; Es t r a da a nd Co a t e s - Es t r ada , 1995) . Th e r em a i n i ng f o r e s t s cons i s to f co l l e c t i ons o f a r ch i pe l agos o f f o r e s t f r agm en t s va r y i ng i n s i z e and i ni s o l a t i ng d i s t ance and age , and s om e a r e i nhab i t ed by howl e r s and s p i de rm o n k e y s t h a t liv e u n d e r p r e c a r i o u s d e m o g r a p h i c a n d e c o lo g i c al c o n d it i o n s( E s t r a d a a n d C o a t e s - E s t r a d a , 1 98 8; R o d r i g u e z - L u n a a n d C o r t es - O r t lz ,1994).

Tr op i ca l r a i n f o r e s t de s t r uc t i on and f r agm en t a t i on r e s u l t i n s i gn i f i c an tr educ t i ons i n t he s iz e o f the o r i g ina l an i m a l pop u l a t i ons and i n phys ica land b i o t ic i so l a ti on . Th e l a t t e r cond i t i on c r ea t e s an i n t e r r up t i on o f genef low, i nb r eed i ng dep r e s s i on , t r unca t i on o f t he h ab i t a t m a t r ix and i n t r u s i onof edges , and a r ap i d o r g r adua l de t e r i o r a t i on o f loca l e co log i ca l cond i t i onst ha t r en de r a l os s o f con t i nue d s upp l y o f r e s ou r ce s , e . g. , f ood an d m a t e s( S a u n d e r s e t a l . , 1991 ; Te r b o r gh , 1992). C on t i n ued i s o la t ion m a y a l so r e s u l ti n s a t u r a t i on o f t he f o r e s t r em nan t by s om e s pec i e s , a l t e r i ng i n t r a s pec i f i ci n t e r ac t i ons , i n ove r exp l o i t a t i on o f r e s ou r ce s , i n i nc r ea s ed com pe t i t i on andpr eda t i on , and i n changes i n f ecund i t y , al l l e ad i ng t o s i gn if ic an t redu c t i onso f t he e f f ec t i ve popu l a t i on s i ze s o f m a ny s pec ie s and t o a po t en t i a l co l l aps eo f t he r em a i n i ng popu l a t i on ( K a r r , 1990 ; An dr 6n , 1994). P r i m a t e s pec i e si n the w i ld a r e n o t exem pt f r om t he s e e f f ect s , and i t is t hus i m por t an t t ha tt he d e s i gn o f cons e r va ti on s cena r i o s f o r wi l d p r i m a t e po pu l a t i ons i n anyr e g i o n c o n s i d e r t h e r e m a i n i n g h a b i t a t i sl an d s a s f u n c t i o n a l c o m p o n e n t s o ft he l ands cape and no t a s i s o l a t ed b i o t i c en t i t i e s .

W i t h t h e o b j e c t i v e o f p r o v i d i n g i n f o r m a t i o n t o c o n t r i b u t e t o t h ea b o v e , w e p r e s e n t r e s u lt s o f s u r v ey s c o n d u c t e d d u r i n g 1 9 9 3- 19 9 5 o f p o p u -l a t i ons o f A . p a l li a ta a n d A . g e o f f r o y i i n t he r eg i on o f Los Tux t l a s . I n ad -d i ti o n , w e p r e s e n t m o r e d e t a i le d i n f o r m a t i o n o n t h e r e s p o n s e s o f t h e m o r ec o m m o n o f t h e t w o p r i m a t e s p e c i e s , n a m e l y , A . p a l l i a t a , t o a n t h r o p o g e n i cc h a n g e s i n t h e r a in f o r e s t la n d s c a p e . T h i s p a p e r is a c o m p l e m e n t t o e a r l i e rp u b l i c a t i o n s ( E s t r a d a a n d C o a t e s - E s t r a d a , 1 9 8 4 , 1 9 8 8 ) o n t h e r e s u l t s o fs h o r t- a n d l o n g - t e rm m o n i t o r i n g o f p r i m a t e h a b i t a t s a n d s p e c ie s a t L o sTuxt las .


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762 Estrada and Coates-EstradaM E T H O D S

At Lo s Tu x t l a s ( 9 5 ~ 0 0 "W, 1 8 ~ i n s o u t h e r n Ve r a c r u z , Me x i c o ,t r o p i c a l r a i n f o r e s t v e g e t a t i o n is p r e s e n t i n t h e f o r m o f c o n s t e l l a t i o n s o f f o r -e s t f r a g m e n t s t h a t v a r y i n s iz e , y e a r s o f i s o l at i o n a n d i s o l at i n g d i s t a n c e ( F ig .1 ) . In th i s r eg ion the r ema in ing t rop ica l r a in fo res t vege ta t ion i s t echn ica l lyk n o wn a s t a l l e v e r g r e e n r a i n f o r e s t ( P e n n i n g t o n a n d S a r u k h f i n , 1 9 6 8 ) . Me a nannu a l r a in fa l l i s 4900 mm , wi th a d r i e r sea son (X = 111.7 _+ 11 .7 (SD ) m mp e r mo n t h ] f r o m Ma r c h t o Ma y a n d a we t t e r s e a s o n ( X = 4 8 6. 2 5 + 8 7 .0m m p e r m o n t h ) f r o m J u n e t o F eb r u ar y , a nd m e a n a n n u al t e m p e r a t u r e is2 7 ~ ( E s t r a d a et al., 1 9 8 5 ) . Th e a l t i t u d i n a l g r a d i e n t r a n g e s f r o m s e a l e v e lto 1600 m a .s. l. , an d 7 0% of the land is ab ov e 300 m a .s. l (Fig . 1) .

C u r r e n t D i s t r i b u t i o n o f th e T r o p i c a l R a i n F o r e s t i n L o s T u x t l a s

W e c o m b i n e d , w it h th e a id o f t h e I D R I S I G e o g r a p h i c I n f o r m a t i o nS y s te m s o f tw a r e p a c k a g e ( G r a d u a t e S c h o ol o f G e o g r a p h y , C l a r k U n i v e r -

Fig. 1. Region of Los Tuxtlas. Dark areas represent remaining rain forest. 1 and 2 areareas into which the r e# on was divided to assess forest loss along altitudinal gradient.The intersection of coordinates at 1 (Vo lcan de San M artin Tux tla) and 2 (VolcanSanta Martha) is highest in elevation, at 1600 m a.s.l. 3, Lake Catemaco.


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P r i m a t e s a t L o s T u x t l a s , M e x i co 7 6 3

sity), the most recent satellite images (1993) with a topographic map ofthe region to obtain two types of information. (1) A grid formed by 4 4-kin2 cells was superimposed on the resulting image. Each cell of the gridwas in turn divided into 0.5 km 2 squares in which we counted the numberof 0.5-km2 cells occupied by rain forest vegetation. This provided an esti-mate of the proportion of contiguous rain forest in existence and theproportion of rain forest in a fragmented condition. (2) To estimate theloss of forest along the altitudinal gradient (sea level to 1600 m), the regionwas divided in two areas for examination, one north (Area 1) and the othersouth (Area 2) of Lake Catemaco (Fig. 1). For each area we used thehighest elevations as the intersection of two lines following the cardinalpoints. Such intersection created four divisions, in each of which we super-imposed five grided transects (2 km wide, each cell = 0.5 km2), followingthe altitudinal gradient to sea level. In each of the five transects in eachdivision, we counted the number of 0.5-km 2 squares ceils occupied by rainforest (Fig. 1).

C e n s u s e s o f P r im a t e P o p u l a t io n sWe censused Ateles and Alouatta in 126 forest fragments dispersed in

the region in the two areas indicated above. These sites varied in altitudefrom sea level to 1600 m, in age of isolation from 1 to 40 years, in sizefrom 2 to 1000 ha, and in isolating distance (straight line distance to theedge of the nearest forest fragment) from 0.1 to 8.0 km (Fig. 1).

We further completed surveys of Alouatta and Ateles in eight replicatesof each of the following artifactual habitats: cacao and coffee plantations,mixed plantations (cacao and coffee), and citrus and allspice groves. Theyvaried in size from 2 to 10 ha and in age from 12 to 15 years and wereall fruit productive. Distance to the nearest forest patch varied from 200to 6000 m and distance to other plantations varied from 200 to 1000 m.In the case of plantations such as cacao, coffee, and mixtures of cacao andcoffee, the shade required by the cultivated plants was provided by tall(>15-m) rain forest trees left by the farmers for this purpose.

We accomplished all primate censuses by visual means with the aidof binoculars at all sites and habitats investigated by walking slowly (ca. 1krn/hr) using existing trails or trails opened by us. Their lengths varied withthe size o f the forest fragment as follows: 400 m for sites


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764 Estrada and Coates-EstradaWe selected the routes for these censuses to avoid overlaps from one

day to the next and to minimize the probability of observing the same troopor individuals more than once. With each contact we recorded the numberof individuals observed, their general age (adults, immatures), and, if adults,their sex. We recorded the height at which they were found and the per-pendicular distance to the census trail with the aid of a range finder. Wenoted the general activity of the troop--traveling, resting, feeding, other--and any special natural body markings such as patches of light hair on thebacks, tails, and/or feet of the monkeys to improve identification of thetroops observed. We transversed trails twice a day, between 0600 and 1800hr, on 2 consecutive days at each site.

C e n s u s o f th e V e g e t a t io nWe surveyed the vegetation at each of the sites by recording all trees>10 cm in diameter at breast height (dbh) and _>1.5 m in he ight in six 10x 10-m plots. We located the plots randomly within the a rea where we

sampled the primates; the plots were at least 30-40m from each other. Foreach tree, we recorded the species, maximum height, and circumference.We measured vertical foliage density at four randomly selected spots withineach of the six plots by scoring vegetation intercepts along a vertical poleat the following intervals: 04).5, 0.51-1.0, 1.1-2, 2.1-3, 3.1-5, 5.1-8, 8.1-10,10.1-15, and >15 m (Schemske and Brokaw, 1981). We expressed inter-cepts at each height interval as the proportion of total intercepts recordedper site in each habitat. We further measured the height and the dbh ofthe trees occupied by howlers during the censuses.

E c o n o m i c S u r v e y sWe conducted economic surveys in five private ranches and five com-

munal farms --eji dos--t o determine the average number of cattle sustainedper hectare and the selling price of standing beef. We also monitored reve-nues from milk production sold to the Nestle company and incorporatedthese into a gross estimate of the total revenues per hectare per year pro-vided by cattle ranching. In the case of the plantations we interviewed theowners to determine the productivity of the cash crop (kg/ha) and moni-tored the selling prices of the cash crops in the region over 3 years toestimate average earnings grossly on a per hectare per year basis. We cal-culated the number of man/days invested in the field for each agriculturalactivity and for cattle ranching from our surveys and interviews.


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P r i m a t e s a t Los Tuxtlas, Mexico 765S t a t i s ti c a l T r e a t m e n t o f t h e D a t a

W e u s e d e s c r i p t i v e s t a t i s t i c s ( m e a n + S D ) t h r o u g h o u t t h e p a p e r a n dc o m p u t e d t h e S p e a r m a n c o r r e l a t i o n c o e f f i c i e n t ( r s ) , p a r t i a l c o r r e l a t i o n c o -e f f i c i e n t , a n d t t e s t f o r d e p e n d e n t s a m p l e s w h e n v a r i a b l e s a n d m e a n s w e r ec o m p a r e d b e t w e e n g r o u p s o f d a t a ( F it c h, 1 9 92 ). W e e x p r e s s e d f o l ia g e v e r-t ic a l d iv e r si ty v i a t h e S h a n n o n - W e a v e r i n f o rm a t i o n i n d e x ( H ' ) ( L u d w i g a n dR e y n o l d s , 1 9 8 8 ) a n d h o r i z o n t a l p l a n t d i v e rs it y p e r h a b i t a t a s t h e m e a nn u m b e r o f t r e e s p e c i e s c e n s u s e d p e r s it e i n e a c h h a b i t at . F r o m t h e p r i m a t ec e n s u s d a t a w e e s t i m a t e d e c o l o g i ca l d e n si ty f o r A . p a l l i a t a a n d f o r A . g e o f -f r o y i a n d w e u s e d t h e s e f i g u r e s t o e s t i m a t e t h e s iz e o f t h e c u r r e n tp o p u l a t i o n s o f h o w l e rs a n d s p i d e r m o n k e y s i n L o s T u x tl a s.

R E S U L T SH a b i t a t L o s s a n d F r a g m e n t a t i o n

O u r d a t a i n d i c a t e a c o n s i d e r a b l e r e d u c t io n o f th e o r i g i n a l e x t e n s io n(ca 2548 km 2 ) o f t he t r op i ca l r a i n f o r e s t a t Los Tux t l a s . O ur e s t im a t e s o fn a t iv e h a b i t a t r e m a i n i n g u s in g t h e G I S s h o w e d t h a t c a . 1 9 2 2 k m 2 ( 7 5 % o fthe t o t a l ) is w i tho u t f o r e s t , c a . 514 km 2 (20% o f t o t a l ) cons i s t s o f f o r e s tf r agm en t s o f va r i ous s i z e s, and on ly ca . 110 km 2 (5% o f t o t a l ) con t a in scon t i guous fo r e s t a t h igh e l eva t i ons (F ig . 1 ) . The a symmet r i ca l d i s t r i bu t i ono f f o r e s t fr a g m e n t s o f d i f fe r e n t s iz e s i n d ic a t es a p r e d o m i n a n c e o f f o r e s tf r agmen t s < 200 ha i n s i z e i n t he l andscape (F ig . 2 ) . Da t a a l so show thea l m o s t t o t a l d i s a p p e a r a n c e o f c o n ti g u o u s p r im a t e h a b i t a t a l o n g t h e a l ti tu -d i n a l g r a d i e n t i n t h e r e g i o n . C u r r e n t l y , o n l y s o m e s e c t i o n s o f t h es o u t h e a s t e r n s l o p e in A r e a 1 a n d s o u t h w e s t e r n s l o p e i n A r e a 2 , o f t h emo un ta in r ange , show, in som e sec ti ons , a s ca t t e r ed d i s t r i bu t i on o f f o r e s tf r agm en t s a l ong t he g r ad i en t (F ig s . 1 and 3 ) .

T o t a l N u m b e r o f P r i m a t e s C e n s u s e dOur censuse s i n 126 fo r e s t f r agmen t s de t ec t ed i nd iv idua l s o f A l o u a t t a

i n 60% o f t he s i te s , 40% were w i thou t how le rs . I n t he fo r e s t s i t e s w i thA l o u a t t a , we censused 422 i nd iv idua l s d i s t r i bu t ed i n 60 t r oops and a l so de -t ec t ed 20 so l i t a ry i nd iv idua l s ( 15 ma le s and 5 f ema le s ) . Mean t r oop s i ze i s7 ( range , 3 -1 4 ) . Th e m ean age and s ex com pos i t i on i s 1.9 adu l t ma l e s , 3.3adu l t f ema le s , 1 .3 j uven i l e s (> 1 yea r ) , and 1 .7 i n f an ts (< 1 yea r ) (A ppe nd ixT a b l e A I ) .


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766 Es trada and Coates-Est rada

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0 , . . . . . . . . . . . . . .I I 9 a. i l a I a I I I I l25 75 125 175 225 275 350 6 0 0

S I Z E O F F R A G M E N T S ( H A )Fig. 2. Size distribution of forest fragm ents rem aining in the region (approxi-mately 514 kin2).

We detected Ateles in only 8% of the 126 forest sites investigated. Atthese sites, we censused 32 spider monkeys. Three of them were solitaryanimals (two males and one female); the rest were distributed in eightgroups. Group size ranged from two to eight individuals, with the followingaverage composition: 1 adult male, 2.1 adult females, 1 juvenile, and 1 in-fant (Appendix Table AI). We detected individuals of Ateles in only 4 ofthe 40 agricultural sites, which represent the following artifactual habitats:cacao, coffee, and mixed plantations. We censused 12 Ateles at these sites:1 was a solitary male, and the rest were distributed in three troops rangingfrom three to five individuals (Appendix Table AII).

E s t i m a t e d S i z e o f P o p u l a t i o n s o f A / ou a tt a a n d Ate les

Our censuses indicate a gross ecological density for Alouatta of 2.9individuals per km 2 and 0.22 individual per km2 for Ateles. These figuresresult in an estimated population size for Alouatta of 1500-1800 individu-als and of 400-600 individuals for Ateles. Such populations are found, as


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t h e i r n a t i v e h a b i t a t , i n a f r a g m e n t e d a n d i s o l a t e d c o n d i t i o n i n t h e l a n d -s c a p e .


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Fig. 5. Relationship between num ber o f individuals of Alouatta de-tected in our cen sus and biogeograph ie variables.p l a n t a t i o n s ( c o f f e e a n d c a c a o ) . A t t h e s e s i te s w e c o u n t e d 1 1 7 i n d i v id u a l sof Alouatta, o f w h i c h 1 11 w e r e d i s t r i b u t e d in 1 8 t r o o p s a n d t h e r e s t w e r es o l i t a r y a n i m a l s ( 4 m a l e s a n d 2 f e m a l e s ) . A v e r a g e t r o o p s i z e i n t h e s e h a b i -t a t s i s 6 . 2 ( r a n g e , 3 - 8 ) a n d a v e r a g e t r o o p c o m p o s i t i o n i s 1 . 5 a d u l t m a l e s ,


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M E A N N O . O F T R E E S P E C I E SFig . 6 . Re la t ionship be tween t ree spec ies d ive rs i ty and ve r t i ca lfol iage divers i ty in the focal habi ta ts . F , undis turbed large fores ts( > 1 0 0 h a ) ; D F , d i s t u r b e d fo r e st s ( < 5 0 h a ) , O G , o l d s e c o n dgrowths; YG , you ng second growths ; C A, cacao p lan ta t ion ; CF ,cof fee p lan ta t ion ; M, mixed p lan ta t ion (cacao and cof fee ) .

3 .1 a d u l t f e m a l e s , 1 .2 j u v e n i l e s , a n d 1 i n f a n t ( A p p e n d i x T a b l e A I I I ) . M e a nt r o o p s iz e is s i g n if i c a n tl y h i g h e r a t t h e m i x e d - c r o p p l a n t a t i o n s 7 . 6 (+ 1 . 8 )t h a n a t t h e o t h e r t w o a r ti f a c t u a l h a b i t a t s ( c a c a o , 5 .3 0 . 8 ; c o f f e e , 5 .5 +1 .0 ; c a c a o a n d m i x e d t = - 3 . 4 , d f 5 , P = 0 . 0 1 ; c o f f e e a n d m i x e d t = - 4 . 0 ,d f 5 , P = 0 . 0 1 ) .

S t r u c t u r e a n d D i v e r s i t y o f t h e V e g e t a t i o n a n d S i z e o f P o p u l a t i o n s o fA / o u a t t a

R e s u l t s o f t h e v e g e t a t i o n a l c e n s u s e s a t t h e fo c a l h a b i t a t s i n d i c a t e as t r o n g a s s o c i a t i o n b e t w e e n h o r i z o n t a l t r e e d i v e r s i t y a n d v e r t i c a l f o l i a g e d i -v e r s i t y (r s = 0 . 6 9 , P = 0 . 0 4 ; F i g . 6 ) . A c c o r d i n g l y , t h e h a b i t a t s w i t h t h eh i g h e s t c o m p l e x i t y i n t h e v e g e t a t i o n i n t h e s e t w o d i m e n s i o n s a r e l a r g e f o r -e s t fr a g m e n t s f o l l o w e d b y o l d g r o w t h s a n d m i x e d p l a n ta t i o n s. D i s t u r b e df o r e s t f r a g m e n t s a r e t h e l e a s t c o m p l e x a c c o r d i n g t o th i s m e a s u r e ( F ig . 6 ) .T h e m e a n n u m b e r o f i nd iv id u al s o f Alouatta c e n s u s e d p e r s i te i s s t r o n g l ya s s o c i a t e d w i t h h o r i z o n t a l p l a n t d i v e r s i t y (r s = 0 . 9 8 , P = 0 . 0 2 ) a n d w i t hv e r t i c a l d i v e rs i t y o f t h e v e g e t a t i o n (rs = 0 . 7 6 , P = 0 . 0 0 0 5 ). H o w e v e r , p a r t i a lc o r r e l a t i o n a n a l y s is s h o w s t h a t t h e o n l y s i g n i f ic a n t e f f e c t i s t h a t o f h o r i-


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DBH (cm)F i g . 7 . R e l a t i o n s h i p b e t w e e n d b h a n d t r e e h e i g h t o f t r e e s u s e d b y A loua t t a a t t h efocal fores t s i tes .

zonta i p lan t d ivers i ty ( r = 0 .83 , P = 0 .009) . H ow lers d i sp lay a s t rong pref -e r ence fo r l a rge t r e e s a s suppor t i ng s t r uc tu r e s i n t he foca l hab i t a t s , v i z . ,t r e e s r ang ing i n he igh t f r om 10 t o 43 m (mean , 22 .5 + 6 .0 cm) and i n dbhf rom 25 t o 310 cm (mean , 98 .3 + 61 .9 cm) (F ig . 7 ) .

E c o n o m i c V a l u e o f t h e A g r ic u l tu r a l H a b i t a t s S t u d i e dO u r e c o n o m i c su r v ey s i n d i c a te t h a t s o m e c r o p s p r o d u c e h i g h e r e c o -

nomic bene f i t s t han ca t t l e r anch ing (F ig . 8 ) . Cacao , a l l sp i ce and mixedp l a n t a ti o n s s e e m t o b e h ig h ly p r o d u c t i v e o p t io n s o f l an d m a n a g e m e n t , w i t han ave rag e y i e ld o f U .S . $2 ,346 pe r h a pe r yea r . On e o f t he m a jo r d i f f e r -e n c e s b e t w e e n c a t t le r a n c h in g a n d t h e s e c r o p s is t h e n u m b e r o f m a n / d a y sr e q u i r e d i n t h e f i e l d t o p r o d u c e t h e c r o p . F o r e x a m p l e , t h e a r b o r e a l c r o p sa s a g r o u p r e q u i r e d a n a v e r a g e o f 6 2 m a n / d a y s i n t h e f i e ld t o o p e r a t e , w i tha r ange o f 50 days ( c it r u s ) t o 75 days ( cacao ) . Con t r a r i l y , c a t t l e r anch ingrequ i r e s an ave rag e o f 40 days . M ixed c rop p l an t a t i ons , w i th t he h ighes teconomic y i e ld pe r hec t a r e pe r yea r , a r e ve ry l abo r i n t ens ive , r equ i r i ngabou t 140 man /days i n t he f i e l d (F ig . 8 ) .


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772 Estrada and Coates-Estrada

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Fig. 8. Economic yield per hectare per year of the focal habitats. Note the higheryield of some cash crops compared to cattle ranching.

Z

D I S C U S S I O NDisappearance and fragmentation of the lowland rain forest in Los

Tuxtlas have resulted in 80-90% reduction of area of natural habitat avai l -a b l e t o A loua t t a a n d Ateles a n d t h e t r en d i s c o n t i n u e d c o n t r a c t i o n ,fragmentat ion and i so la t ion o f the remain ing habi ta t . Our es t imates o fpopulat ion dens i ty for A loua t t a and Ate les - -2 .9 individuals per kn'l2 and0.22 individual per kn'l2 respect ive ly - -are lower than those reported ear lier(Estrada and Coates-Estrada, 1988) from surveys conducted in the regionabout 10 years ago (1981 -198 6) - - 3 .6 ind ividuals per k i n 2 for A loua t t a and0.66 individual per km 2 for Ate les) - -suggest ing important dec l ines in thepopulat ion as a resu l t o f cont inued i so la t ion o f the fores t and human ac-t ivity in the form of further forest removal , se lect ive logging and hunting.This and the fact that A loua t t a and Ate les were absent in 40 and 90% ofthe focal forest s i tes , respect ively , attest to the extensive local ext inct ion ofboth species in the region. We est imated that only about 16% of the origi-na l e s t imated populat ion o f A l oua t ta (ca. 10,000 individuals) and about 26%o f A teles (ca. 1500 individuals) st i l l exist in the region (Estrada and Coates-


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Primates a t L o s Tuxtlas, Mexico 77 3Es t r ada , 1988 ) . Cu r r en t popu l a t i ons o f A l o u a t t a a n d A t e l e s cons i s t o f i so -l a t ed co l l e c t ions o f i nd iv idua ls an d sma l l g roups l iv ing i n sm a l l and l a rgef o r e s t i s la n d s s u r r o u n d e d b y a s e a o f p a s t u r e a n d o t h e r a n t h r o p o g e n i c v e g e -t a t i on .A r e a a n d i s o la t in g d i s ta n c e o f f o r e s t f r a g m e n t s e e m e d t o b e i m p o r t a n tv a r i a b l e s i n f l u e n c i n g t h e n u m b e r o f A l o u a t t a pre sen t a t a g iven s i t e . Sma l la r e a a n d g r e a t e r i s o l a t i o n f r o m o t h e r f o r e s t f r a g m e n t s m a y r e s u l t i n e x t e n -s ive changes i n eco log i ca l cond i t i ons o f t he i so l a t ed hab i t a t , f o r example ,g r e a t e r p e n e t r a t i o n o f w i n d t o t h e i n t e ri o r a n d h i g h e r d e s i c c a t i o n a t t h eedges , wh ich may r e su l t i n a g r ea t e r mor t a l i t y o f t r e e s , t hus d imin i sh ingre sou rce s f o r t he ex i s t i ng p r ima te s (Love joy e t a l . , 1986 ; Lau rance , 1991 ) .O u r s t u d y s h o w e d t h a t l a rg e r f r a g m e n t s s u p p o r t e d l a r g e r s e g m e n t s o f th ed i v i d e d p o p u l a t i o n o f A l o u a t t a , b u t t h e s e f r ag m e n t s a r e n o t v e r y c o m m o nwi th in t he a l t it ud ina l r ange oc cup i e d by A l o u a t t a a t Los Tux t l a s . Sho r t i n -t e r f r a g m e n t d i s t an c e s m a y f a v o r t h e m o v e m e n t o f h o w l er s o n t h e g r o u n dt h r o u g h t h e p a s t u r e l a n d f r o m o n e h a b i t a t i s l a n d t o a n o t h e r . W e h a v e s e e nhow le r s mov ing on t he g roun d and t r ave li ng d i s tances r ang ing f rom 10 t o2 0 0 m t o r e a c h o t h e r f o r e s t f r a g m e n t s . H o w e v e r , t h i s h a s b e e n a n i n f r e -quen t l y obse rved behav io r , sugges t i ng t ha t t he r e a r e l im i t s t o t he d i s t anceshowle r s a r e w i l l i ng t o t r ave l on t he open g round , p robab ly a s a r e su l t o fp o t e n t i a l d a n g e r f r o m d o g s a n d h u m a n s .

R e s i d u a l r a in f o r e s t v e g e t a t i o n a l o n g t h e e d g e s o f l a k es , s e a s o n a l a n dp e r m a n e n t s t re a m s , a n d r iv e r s f o r m i n g s tr ip s o f c o n n e c t i n g v e g e t a t i o na m o n g i s o l a te d f o r e s t f r a g m e n t s s e e m s to f a v o r t h e i n t e r f ra g m e n t m o v e -m e n t s o f p r i m a t e t r o o p s a n d i n d iv i du a ls . W e o b s e r v e d m o r e m o v e m e n t so f h o w l e r s al o n g t h e s e c o r r id o r s t h a n t h r o u g h t h e o p e n p a s t u r e , a t t e s ti n gt o t h e v a l u e o f su c h r e s i d u a l v e g e t a t i o n f o r t h e p r im a t e s . T h e p r e s e n c e a n dc o n s e r v a t i o n o f t h e s e c o r r id o r s o f v e g e t a t i o n m a y s u s ta i n c o n n e c t i v i t ya m o n g t h e i s o l a t e d s e g m e n t s o f t h e r e m a i n i n g h o w l e r p o p u l a t i o n ( N o s s ,1991; P imente l e t a l . , 1992 ; Na iman e t a l . , 1993).

H o w l e r tr o o p s a n d i n d iv i d u a ls s h o w i n g a n a v e r s i o n t o l e a v e th e i r f o r -e s t f r a g m e n t m a y e v e n t u a l l y b e c o m e e x t i n c t b e c a u s e t h e f r a g m e n t i s t o os m a l l, i t m a y n o t c o n t a i n t h e n e c e s s a r y r e s o u r c e s t o s u p p o r t t h e m , i ts i so -l a t io n m a y b e s o g r e a t ( l a rg e i n t e r f r a g m e n t d i s t a n c e a n d l a c k o f c o r r i d o r s )t h a t i t i m p e d e s t h e i r t e m p o r a r y a n d / o r p e r m a n e n t s e l f - r e l o c a t i o n t o o t h e rh a b i t a t i s l an d s ( B u r k e y , 1 9 88 ; A n d r 6 n a n d A n g e l s t a m , 1 9 8 8) , o r e x p o s u r et o p r e d a t i o n b y h u m a n s , d o g s , an d r a p t o r s m a y b e h i g h e r a t t h e s e s i t e st h a n a t l a r g e r h a b i t a t i s l a n d s ( E s t r a d a , u n p u b l i s h e d d a t a ) . I n a d d i t i o n ,s o m e o f t h e s e o t h e r h a b i ta t i s la n d s m a y b e o c c u p i e d b y o t h e r h o w l e rs ,t h u s e x e r t i n g m o r e p r e s s u r e o n t h e l i m i t e d r e s o u r c e s a v a i l a b l e ( E s t r a d ae t a l . , 1994).


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774 E s t r a d a a n d C o a t e s - E s t r a d a

O u r s u r v e y s i n d i c a t e t h a t h o w l e r s s o m e t i m e s i n h a b i t a n t h r o p o g e n i cv e g e t a t i o n . W h i l e a s ig n if ic a n t n u m b e r o f m o n k e y s w e r e p r e s e n t i n t h e a r -b o r e a l a g r i c u l t u r a l h a b i t a t s , n o t a ll o f t h e s e h a b i t a t s a r e e q u a l in t h eo p p o r t u n i t i e s t h e y m a y o f f e r t o t h e m . F o r e x a m p l e , s h a d e d h a b i t a t s w e r ethe on ly a r t i f a c tua l hab i t a t s w i th howle r s , p robab ly t he r e su l t o f t he p r e s -e n c e o f r a in f o r e s t tr e e s. U n s h a d e d a g r i cu l tu r a l h a b i t a t s - - c i t r u s a n da l l s p i c e - - l a c k t a l l p l a n t c o v e r , w h i c h c o u p l e d w i t h t h e w i d e i n t e r r o w s p a c eb e t w e e n t h e c u l t i v a t e d p l a n t s a n d t h e s p a r s e v e g e t a t i o n , m e a n s a l a c k o fs u i t a b l e s t r u c t u r e s f o r p r i m a t e l o c o m o t i o n , p r o t e c t i v e c o v e r , a n d f o o d r e -s o u r c e s , a n d t h u s h o w l e r s d o n o t s e e m t o v i s i t t h e s e h a b i t a t s .

T h e p r e s e n c e a t t h e s h a d e d a g r i c u lt u r al h a b i t a ts u s e d b y h o w l e r s o ft a ll ( > 2 0 - m ) r a i n f o r e s t t r e e s o f p l a n t f a m i l ie s su c h a s M o r a c e a e ( F i c u sspp . , P o u l s e n i a a r m a t a , B r o s i m u m a l i c a s t r u m ) , L e g u m i n o s a e (P te ro c a rp u sro rh i i , L o n c h o c a rp u s g u a te m a le n s i s ) , S a p o t a c e a e ( M a n i l k a r a z a p o t a , P o u t e r iac a m p e c h i a n a ) , A n a c a r d i a c e a e ( S p o n d ia s ra d lk o f e r i ) , L a u r a c e a e (N e c t a n d r aa m b i g e n s , O c o t e a s p p. ), a n d A n n o n a c e a e ( R o l li n i a j i m e n e z i i ) a m o n g o t h e r s ,p e r m i t s t h e e x i s t e n c e o f a c o n t i g u o u s c a n o p y f o r t h e s e m o b i l e a r b o r e a lm a m m a l s . S o m e o f t h e s e t r e e s p e c i e s a r e a l s o a n i m p o r t a n t s o u r c e o f l e a v e sa n d o f f r u i t f o r t h e m o n k e y s ( E s t r a d a , 1 98 4; E s t r a d a a n d C o a t e s - E s t r a d a ,1993) .T h e t a ll p l a n t c o v e r p r o v i d e d b y t h e r a i n f o r e s t t r e e s a t t h e s e p l a n t a -t i o n s c o u p l e d w i t h t h e h i g h t r e e d i v e r s i t y i n t h e v e g e t a t i o n p r o v i d i n g s h a d et o t h e c u l t i v a te d p l a n t s a n d t h e a b s e n c e o f h u n t in g o f h o w l e r s i n t h e s eh a b i t a t s b y l o c al h u m a n s h a s a l l o w e d t h e p e r s i s t e n c e o f i s o l a t ed t r o o p s o fh o w l e r s a n d m a y a l s o e x p l a in t h e h i g h m e a n t r o o p s i z e d e t e c t e d a t t h e s ehab i t a t s . I n some in s t ances , we obse rved t roops and so l i t a ry an ima l s v i s i t i ngc a c a o , c o f f e e , a n d m i x e d p l a n t a ti o n s b y m o v i n g t h r o u g h t h e t r e e s o f n a r r o ws t ri p s o f f o r e s t v e g e t a t i o n a l o n g s t r e a m s a n d r iv e r s. I n s o m e c a s e s , t h et r o o p s w e r e p r e s e n t w i t h o t h e r t r o o p s a t t h e s e p l a n t a t i o n s .

O u r o b s e r v a t i o n s a n d i n t e r v i e w s w i t h t h e f a r m e r s i n d i c a t e t h a t h o w l e r sd o n o t f e e d o n t h e e c o n o m i c a l l y i m p o r t a n t f r u it s b u t , i n s t e a d , c o n c e n t r a t ethe i r f e ed in g on l e aves and f ru i ts o f t he t a l l r a in fo r e s t t r e e s . The f eed inga c ti v it ie s o f h o w l e r s a t t h e s e h a b i t a ts m a y f a v o r p r i m a r y p r o d u c t i v i ty i n a r -t i f a c tua l hab i t a t s , a cce l e r a t i ng t he f l ow o f nu t r i en t s and t he conv e r s ion o fm a t t e r a n d e n e r g y ( E s t r a d a a n d C o a t e s - E s t r a d a , 1 9 9 3) . L i k e w i s e, t h e i n -g e s t i o n o f f r u i t s m a y f a v o r th e d i s p e r s a l o f r a i n f o r e s t s e e d s t o l e s scompe t i t i ve s i t e s f o r t he i r e s t ab l i shmen t , con t r i bu t i ng t hus t o su s t a in ing t hea r b o r e a l s p e c i e s p r e s e n t a t t h e p l a n t a t i o n s , w h i c h c o u l d a l s o b e m a n a g e db y p e o p l e ( E s t r a d a a n d C o a t e s - E s tr a d a , 1 98 4, 1 9 86 ). T h e m o v e m e n t o fs e e d s m a y b e e n h a n c e d b y t h e u s e o f c o r r id o r s o f r e s id u a l v e g e t a t io n b yt h e m o n k e y s w h e n m o v i n g f r o m a f o r e s t f r a g m e n t t o a n a r t i f a c tu a l h a b i t a t ,a n d v i c e v e r s a ( E s t r a d a et al . , 1993) .


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P r i m a t e s a t L o s T u x t l a s , Mex i c o 7 7 5

A l t h o u g h < 3 % o f t h e l a n d a t L o s T u x t l a s is d e d i c a t e d t o th e c u l t i -v a t i o n o f a r b o r e a l c r o p s u n d e r t h e s h a d e o f r a in f o r e st c a n o p y t r e e s a n dm o s t o f t h e t i m e s u c h p l a n t a t i o n s a r e v i r tu a l i s la n d s o f v e g e t a t i o n s u r -r o u n d e d b y p a s tu r e s , t h e f e w o c c u r re n c e s i n v e s ti g a te d m a y a l lo w u s t oc o n t e m p l a t e s c e n a r i o s o f l a nd m a n a g e m e n t t h a t c o u l d b e m o r e b e n i g n f o rt h e c o n s e r v a t i o n o f t h e r e m a i n in g p r i m a t e p o p u l a t i o n s ( E s t r a d a a n dC o a t e s - E s t r a d a , 1 9 95 ). I n t h is c a se , a l a n d s c a p e a r r a n g e m e n t i n w h i c h a r -b o r e a l a n d s h a d e d a g r ic u l tu r a l h a b i t a ts o c c u p y s o m e o f th e p a s t u r e s e p a -r a t i n g a r c h i p e l a g o s o f f o r e s t f r a g m e n t s , i n c lu d i n g f o r e s t s i n p r o c e s s o fr e g e n e r a t i o n , m a y r e d u c e i s o la t in g d i s t a n ce s , t h e r e b y f a c i l it a ti n g t h e f l o wo f p r im a t e s t h r o u g h s p a c e . In s o m e i n s ta n c e s t h e a g r i c u l tu r a l p l o t s c o u l db e u s e d t o p r o t e c t t h e e d g e s o f fo r e s t fr a g m e n t s f r o m e x p o s u r e t o w i n da n d h ig h t e m p e r a t u r e s a n d t o i n c r e a s e t h e a r e a o f v e g e t a t i o n a v a i l a b l e t oh o w l e r s . I n t h i s s c e n a r i o , c o r r i d o r s o f r e s i d u a l f o r e s t v e g e t a t i o n a l o n gs t r e a m s a n d r i v e r s c o u l d e n h a n c e f a u n a l c o n n e c t i o n b e t w e e n f o r e s t a n da g r i c u lt u r a l i s la n d s in th e l a n d s c a p e . S u c h m a n a g e m e n t o f t h e l a n d m a yh a v e s e v e r a l i m p o r t a n t a d d e d b e n e f i t s i n c lu d i n g r e t e n t i o n o f s o il a n d o fs o il fe r ti li t y a n d p r e s e r v a t i o n o f w a t e r r e s o u r c e s ( G l e i s s m a n et al., 1981;Morowi t z , 1991 ; Or r , 1991 ) .W e a l s o n e e d t o c o n s i d e r t h a t Alouat ta a n d At e l e s m a y n o t b e e q u a l l ye l a s t i c i n t he i r r e sponse t o env i ronmen ta l change . Fo r example , we s t i l ll a c k su f f ic i e n t k n o w l e d g e a b o u t t h e c a p a c i t y o f s p i d e r m o n k e y s t o u s e a n -t h r o p o g e n i c h a b i t a t s s u c h a s th e c o f f e e , c a c a o a n d m i x e d p l a n ta t i o n s . W ed e t e c t e d v e r y f e w s p i d e r m o n k e y s a t t h e s e h a b i t at s . I n t h e c a s e o f A l oua t t a ,t h e i r p r e s e n c e a t t h e s e h a b i t a ts m a y b e f a c i li t at e d b y th e c a p a c i t y o f t h espec i e s t o e a t t he l e aves o f t he r a in fo r e s t tr e e s p rov id ing shad e t o t hecu l t i va t ed p l an ts . I n ex t r em e cond i t i ons o f hum ar , hab i t a t m od i f i c a t i on , i so -l a t ed t r o ops o f howle r s have u sed t he l e aves and f ru it s o f cu l ti va t ed p l an t ss u c h a s Citrus s p p . ( B i c c a - M a r q u e s a n d C a l e g a r o - M a r q u e s , 1 9 9 4 ) . I n t h ec a s e o f Ate les , i t s h igh dependence on r i pe f ru i t a s a p r inc ipa l i t em in i t sd i e t i m p o s e s l a r g e r d e m a n d s o f a r e a a n d r e s o u r c e s ( M i t t e r m e i e r a n d v a nR o o s m a l e n , 1 9 8 1 ) . T h u s w h i l e a t r o o p o f Al oua t t a c o m p o s e d o f 1 0 i n d i -v idua l s c an ex i st f o r s eve ra l yea r s w i thou t ap pa re n t p ro b l em s in a 10 -ham i x e d p l a n t a ti o n ( E s t r a d a , u n p u b l i s h e d d a t a ) , s h a d e d b y r a in f o r e s t v e g e -t a ti o n , a n e q u i v a l e n t b i o m a s s o f sp i d e r m o n k e y s w o u l d r e q u i r e 1 00 t im e stha t a r ea (Chapman , 1988 ) .T h u s t h e c o n s e r v a t i o n o f Ate les i n r eg ions such a s Los Tux t l a s mayd e p e n d o n t h e c o n s e r v a t io n o f l a rg e t r a c t s o f r a i n f o r e s t i n w h i c h g e n e t i c a ll yv i ab l e popu la t i ons can be p r e se rved (Sha f f e r , 1987 ) . A g ros s e s t ima te (2 .5 -5 . 0 k m 2 p e r 1 0 in d i v id u a l s) o f t h e a r e a r e q u i r e d i n t h is c a s e w o u l d b e250-50 0 km 2 fo r 500 i nd iv idua ls of A te les . In t he ca se o f A l oua t ta , t h e g r o s se s t ima te y i e ld s (0 .3 -0 .6 k m 2 pe r 10 i nd iv idua l s ) a bo u t 15 -20 km 2 o f co n -


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7 7 6 E s t r a d a a n d C o a t e s - E s t r a d a

t i g u o u s r a i n f o r e s t . C u r r e n t l y i n L o s T u x t l a s t h e r e is a b o u t 6 2 4 k m 2 o f r a i nf o r e s t l e ft , b u t 8 2 % o f it is in a n e x t e n s iv e s t a t e o f f r a g m e n t a t i o n . F u r t h e r ,m os t o f t he fo r e s t f r om sea l eve l t o ab ou t 700 m a .s .1 , ha s be en l o s t . Th i sm e a n s i m p o r t a n t c h a n g e s in t h e d i st r ib u t i o n o f th e t w o p r i m a t e s p e c i e sa l o n g t h e g r a d i e n t .

T h e f a c t t h a t A . pa l l ia ta i s r a r e l y f o u n d a b o v e 8 0 0 m a . s . l , i n M e x i c o( H o r w i c h a n d J o h n s o n , 1 9 86 ) s u g g e s ts t h e p r e s e n c e o f c e rt a in l i m i ta t io n so n t h e d i s t r i b u t i o n o f t h e s p e c i e s i n t h e m o u n t a i n o u s r e g i o n o f L o sT u x t l a s . T h e s e l i m i t a t i o n s c o u l d b e d u e t o s p e c i f i c e c o l o g i c a l r e q u i r e -m e n t s , c o l d e r c l i m a t e , a n d / o r b e h a v i o r a l r e s t r i c t i o n s t h a t d e t e r A l o u a t t af r o m o c c u p y i n g t h e n a t iv e v e g e t a t i o n f o u n d a t h i g h e r a l ti t u d e s . T h i sm e a n s t h a t , a t L o s T u x tl a s, a s ig n i fi c an t p r o p o r t i o n o f th e r e m a i n i n gp o p u l a t i o n o f A l o u a t t a i s s e r io u s l y at r i sk b e c a u s e m o s t o f t h e l o w l a n dr a in f o r e s t h a s d i s a p p e a r e d a t t h e e l e v a t io n w h e r e t h e s p e c i e s is u s u a l l yf o u n d . T h e p e r s i s t e n c e o f A l o u a t t a u n d e r t h is s c e n a r io m a y b e d u e t o i tsa b i l it y to u s e l e a v e s a s f o o d , t h u s e x is t in g , f o r a t i m e , i n v e r y s m a l l h a b i t a ti s l a n d s o r , o n o c c a s i o n , i n s o m e a r t i f a c t u a l h a b i t a t s . I n c o n t r a s t , Ate le sc a n o c c u p y h i g h e r e l e v a t i o n s i n t h e d i s t r i b u t i o n o f v a r i a n t s o f t h e r a i nf o r e s t v e g e t a t i o n a l o n g t h e a l t i t u d i n a l g r a d i e n t o f L o s T u x t l a s , b u t a s ar e s u lt o f it s la r g e a r e a r e q u i r e m e n t s a n d e x p l o i t a ti o n o f p a t c h y r e s o u r c e s ,i t h a s b e e n m u c h m o r e s e n s i t i v e t h a n A l o u a t t a t o t h e g e n e r a l d i s a p p e a r -a n c e o f i ts h a b i t a t a n d c a n n o t p e r s i s t in s m a l l p a t c h e s o f v e g e t a t i o n . T h i s ,p l u s in t e n s iv e h u n t i n g b y h u m a n s o v e r s e v e r a l d e c a d e s h a s r e s u l t e d i nd r a m a t i c d e c l i n e s o f s p i d e r m o n k e y p o p u l a t i o n ( E s t r a d a a n d C o a t e s - E s -t r ada , 1988 ) .I n t h e c a s e o f L o s T u x t la s , w e n e e d t o r e c o g n i z e t h a t t h e n a t u r a lh a b i t a t o f b o t h p r i m a t e s p e c i e s is n o w , a l o n g s e v e r a l e c o lo g i c a l a n d g e o -g r a p h i c a l d i m e n s i o n s , a l i m i t e d r e s o u r c e a n d t h a t c o n t i n u e d i s o l a t i o n m a yr e s u lt i n f u r t h e r d e c r e a s e s in th e r e m a i n i n g h o w l e r a n d s p i d e r m o n k e yp o p u l a t i o n s . T h i s s u gg e s ts t h e i n d i s p e n s a b l e n e s s o f t re a t i n g t h e p r o b l e mo f p r im a t e c o n s e r v a t i o n a t t h e l e v e l o f t h e l a n d s c a p e . F o r e x a m p l e , i nt h e c a s e o f A l o u a t t a , a c o m b i n a t i o n o f a r c h ip e l a g o s o f f o r e s t fr a g m e n t si n c o m b i n a t i o n w i t h s o m e t y p e s o f a g r ic u l tu r a l h a b i t a t s m a y b e u s e f u l t op r e s e r v e t h e re m a i n i n g p o p u l a t i o n - - v a r i e g a t e d m o d e l s ( M c l n t y r e a n dB a r r e t , 1 9 9 2 ) . I n t h e c a s e o f Ate les , i t w o u l d b e i n d i s p e n s a b l e t o e n s u r et h e p r e s e r v a t i o n o f th e l a r g e s t t r a c t s o f r a in f o r e s t s ti ll e x i st i n g in t h er e g i o n . I n b o t h c a s e s , t h e p r e s e r v a t i o n a n d u s e o f r e s i d u a l v e g e t a t i o na l o n g s t r e a m s , r i v e r s , l a k e s , a n d l a g o o n s w o u l d b e n e c e s s a r y t o e n s u r ea n d t o e n h a n c e p h y s i c al a n d b i o t i c c o n n e c t i v i t y . I n th i s s c e n a r i o w e a l s om a y n e e d t o c o n s i d e r a r c h i t e c t u r a l a s p e c t s o f t h e v e g e t a t i o n i n s u c h c o r -


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P r i m a t e s a t L o s T u x t l a s , M e x i co 7 7 7

r id o r s. F o r e x a m p l e , o u r d a t a s u g g e s t t h a t s m a l l - - l o w - h e i g h t a n d s m a l l -d b h - - t r e e s m a y n o t b e a d e q u a t e t o fa c il it at e t h e m o v e m e n t s o f h o w le r st h r o u g h t h e c a n o p y .O u r e c o n o m i c s u r v ey s s h o w t h a t, i n c o n t r a s t t o c a t t le r a n c h in g , t h ec u l ti v a ti o n o f s o m e o f t h e c r o p s m a y b e a m o r e e c o n o m i c a l l y p r o d u c t i v em o d e t o m a n a g e t ro p i c a l l a n d. S u c h m a n a g e m e n t o f t h e l a n d , in a d d i ti o nto be ing l e s s s ens i t i ve t o f l uc tua t i ons i n t he marke t va lue o f t he d i f f e r en tc a s h c r o p s i n v o l v e d , m a y h a v e s e v e r a l i m p o r t a n t a d d e d b e n e f i t s , a m o n gw h i c h s t a n d o u t r e t e n t i o n o f s o il a n d o f so il fe r ti li ty a n d p r e s e r v a t i o n o fw a t e r r e s o u r c e s ( G l e i s s m a n e t a l . , 1981). The c h i e f obs t ac l e t o a change o fl a n d m a n a g e m e n t s t r a te g y m a y b e e c o n o m i c . F i rs t, t h e c r o p s i n v e s t ig a t e da r e , in c o n t r a s t t o p a s t u r e s , l a b o r i n t en s i v e a n d r e s o u r c e s w o u l d b e r e q u i r e dt o h i r e t h e e x t r a h u m a n l a b o r . S e c o n d , c r o p s s u c h a s c a c a o a n d c o f f e er equ i r e t e chno logy , e . g . , p ropane d rye r s t o d ry t he s eeds , t o r each h ighp r o d u c t i v i t y l e v e l s f o r p r o c e s s i n g b e f o r e t h e y c a n b e m a r k e t e d . A l t h o u g ho n l y a f e w f a r m e r s a t L o s T u x t la s h a v e h a d e n o u g h r e s o u r c e s t o c u l ti v a t ec rops w i th a h igh marke t va lue and have d ive r s i f i ed t he i r p r i va t e e conomies ,w e r e c o m m e n d a c h a n g e i n t h i s d i r e c t i o n , r a t h e r t h a n t o c o n t i n u e w i t h t h eho r i zon t a l expa ns ion o f c a t t l e r anch ing , wh ich cou ld r e su l t i n g r ea t e r e co -n o m i c b e n e f i t s t o t h e l o c a l e c o n o m i e s .

F i n a l l y , a s c o n s e r v a t i o n a l p r i m a t o l o g i s t s w e n e e d t o r e c o n s i d e r t h ep r o b l e m o f p r i m a t e c o n s e r v a ti o n n o t ju s t f r o m a b a s i c e c o lo g i c a l v i ew -p o i n t b u t , i n s t e a d , a s a m u l t i d i m e n s i o n a l s o c i a l p r o b l e m . T h i s s c e n a r i od e m a n d s t h e d e v e l o p m e n t o f i n te r d is c ip l in a r y r e s e a r c h p r o j e c t s t h at c a nt a c k l e t h e p r o b l e m a t d i f f e r e n t l e v e l s . O n e w o u l d b e p r o j e c t s t h a t c o u l dc o n t r i b u t e t o i n c r e a s e d p r o d u c t i v i t y o f th e p a s t u r e l a n d s t o d i m i n is h p r e s -s u r e o n t h e r e m a i n i n g p r i m a t e h a b i t a t s . T h u s , fo r e x a m p l e , w e m a y n e e dt o i n v e s t i g a te h o w t o i m p r o v e b o v i n e g e n e t i c s v i a i n t r o d u c t i o n o f d i f f e r e n tb r e e d s o f c a t t l e o r a r ti fi c ia l i n s e m i n a t i o n , t o c h a n g e t h e t y p e s o f p l a n t e dg r a s s s p e c i e s f o r c a tt l e g r a zi n g , t o i n t r o d u c e r o t a t i n g a n d s t r ip g r a z i n ga n d c u l t i v a ti o n o f f o r a g e s , a n d t o i m p r o v e p r e v e n t i v e v e t e r i n a r y c a r e(He r r and Reed , 1991 ; Benne t t , 1995 ; Cas se l l 1995 ) . Un le s s r ad i ca l l y d i f -f e r e n t m o d e l s o f la n d m a n a g e m e n t t h at i n v ol ve r e c e n t p r o g r e s s ina g r o f o r e s t r y a n d v e t e r i n a r y s c i e n c e a r e i m p l e m e n t e d i n t r o p i c a l r e g i o n ss u c h a s L o s T u x t l a s , t h e c o n t i n u e d g r o w t h o f t r a d i ti o n a l c a t t l e r a n c h i n gt h r o u g h h o r i z o n t a l e x p a n s i o n o f p a s t u r e l a n d s , a t t h e e x p e n s e o f t h e r e -m a i n i n g f o r e s t , w i l l c o n t i n u e t o c a u s e t h e l o c a l a n d r e g i o n a l e x t i n c t i o no f th e r e m n a n t p r i m a t e p o p u l a t io n s , a n d p r o d u c t iv i t y o f t h e l o ca l e c o n o -m i e s w i ll c o n t i n u e t o b e i n s u f fi c i en t t o i m p r o v e t h e q u a l i t y o f l if e o f t h el o c a l h u m a n i n h a b i t a n t s .


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7 7 8 E s t r a d a a n d C o a t e s - E s tr a d a

A P P E N D I XTable AL Individuals of A loua t t a Detected in the Focal Forest Fragments

Altitude Years of DistanceSite N Males Femal es Juv. Inf. (m a.s.I.) Ha isolation (kin)1 1 1 30 2 12 0.52 1 1 40 2 11 0.53 1 1 80 2 16 0.54 1 1 30 3 15 0.75 4 1 2 1 100 5 8 0.76 1 1 320 8 18 0.77 1 1 220 8 15 0.78 2 2 320 8 9 8.09 1 1 30 10 17 1.5

10 4 1 2 1 25 18 20 0.511 1 1 30 20 16 3.012 2 1 1 600 20 11 6.013 2 1 1 55 20 14 2.014 2 2 140 20 13 3.015 5 1 2 2 250 20 10 0.516 1 1 50 30 14 2.417 2 1 1 70 30 10 5.518 7 2 4 1 170 35 18 4.419 8 3 4 1 135 35 13 0.520 4 1 3 35 40 6 2.021 1 1 45 45 15 0.222 2 1 1 90 50 9 4.023 6 1 3 1 1 180 50 18 0.424 1 1 80 60 12 3.525 1 1 300 60 11 3.526 3 1 2 20 60 6 1.527 5 1 4 150 60 8 0.328 8 2 4 2 50 60 15 0.329 2 1 1 60 80 7 3.530 2 2 50 80 12 4.031 5 2 2 1 120 80 18 0.432 6 1 3 1 1 380 80 10 0.533 7 1 4 2 30 80 2 0.334 4 2 1 1 150 85 15 3.035 5 1 2 2 25 85 4 0.636 4 1 2 1 75 110 20 3.037 5 2 2 1 250 110 4 0.738 3 1 2 400 120 10 1.039 7 2 3 2 460 120 3 0.640 8 2 4 2 500 120 10 0.541 8 2 3 1 2 250 130 2 0.342 6 1 2 1 2 180 150 10 0.343 8 2 4 1 1 280 150 2 0.144 5 2 3 450 160 10 0.545 5 2 2 1 280 170 11 0.546 8 3 4 1 360 180 8 0.547 8 2 4 2 220 180 14 0.348 4 2 2 160 220 9 3.049 5 1 2 1 1 600 220 17 3.0


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P r i m a t e s a t L o s T u x t l a s , M e x i c oT a b l e AI. Continued

7 7 9

Altitude Years of DistanceSite N Males Females Juv. Inf. (m a.s.i.) Ha isolation (kin)50 7 2 3 2 400 220 11 0.551 5 2 3 260 230 15 3.052 9 3 5 1 700 230 10 0.453 10 3 4 1 2 370 230 12 0.754 3 1 2 246 240 10 0.955 8 1 4 3 460 245 5 2.056 10 2 5 2 1 320 250 7 0.457 8 2 3 1 2 360 267 10 2.058 6 1 3 1 1 300 270 12 0.559 8 2 4 1 1 350 270 10 0.760 8 2 3 1 2 180 280 8 0.461 5 1 2 1 I 80 300 4 0.562 7 2 3 2 340 310 15 1.063 2 2 140 330 15 2.064 14 3 6 2 3 400 350 10 0.465 5 1 3 1 260 360 15 2.166 11 3 5 1 2 270 360 8 0.267 12 3 5 2 2 300 450 10 0.568 13 3 5 2 3 250 450 9 0.769 12 4 5 1 2 350 500 10 0.770 12 3 6 2 1 300 700 7 1.771 11 3 5 1 2 270 800 6 0.272 12 3 5 2 2 300 600 11 0.273 12 4 5 1 2 250 700 8 0.574 12 3 6 2 1 350 1000 8 0.775 13 3 5 2 3 300 900 6 0.776 14 3 6 2 3 350 800 6 1.7

Total 442 129 202 39 72

T a b l e AII. Number of Spider Monkeys Detected at the Focal Forest Fragments andArtifactual HabitatsAltitude Years of DistanceSite N Males Females Juv. Inf. (m a.s.l.) Ha isolation (kin) Vege tat ion

1 1 1 200 60 30 3.0 For est2 1 1 450 100 20 4.0 Forest3 1 1 1000 600 35 4.0 Forest4 2 1 1 850 300 25 3.0 Forest5 3 1 2 100 270 20 3.0 Forest6 3 1 2 1300 350 18 1.0 Forest7 4 1 2 1 900 500 28 0.2 Forest8 5 1 2 1 1 1200 380 30 0.3 F orest9 6 1 3 1 I 960 700 35 0.8 Forest10 6 1 3 1 1 500 1000 32 0.6 ForestTotal 32 9 16 3 4


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7 8 0 E s t r a d a a n d C o a t e s - E s t r a d a

Table All. ContinuedAltitude Years of Distance

Site N Males Femal es Juv. Inf. (m a.s.I.) Ha isolation (km) Veget atio nHuman-made habitats

1 1 1 400 10 20 0.3 Cacao2 3 1 2 500 10 25 0.5 Cacao3 5 1 2 1 1 600 8 18 0.8 Coffee4 3 1 2 400 8 15 0.6 Mixed

Total 12 4 6 1 1

Table AIII. Agricultural Sites with A loua t t aAltitude DistanceSite N Males Femal es Juv. Inf. (m a.s.I.) Ha Years (km) Vegeta tion

1 4 1 ! 1 1 150 I0 25 0.3 Cacao2 6 1 3 1 1 200 10 25 0.2 Cacao3 5 1 3 1 250 10 25 0.3 Cacao4 6 1 3 1 1 150 10 25 0.3 Cacao5 6 1 4 1 1 200 10 25 0.2 Cacao6 5 2 3 250 10 25 0.3 Cacao7 10 3 5 1 1 250 3 15 0.2 Mixed8 8 2 3 2 1 200 3 15 0.1 Mixed9 5 1 3 1 50 15 15 0.9 Mixed

10 6 2 3 1 100 15 15 0.4 Mixed11 8 2 3 2 1 150 15 15 0.3 Mixed12 9 2 4 1 2 200 5 15 0.2 Mixed13 6 2 3 1 150 5 5 0.6 Cof fee14 6 1 3 1 1 100 5 5 0.5 C off ee15 5 1 3 1 200 5 5 0.6 Cof fee16 5 1 3 1 250 5 5 0.4 Cof fee17 7 2 3 1 1 300 5 5 0.3 C off ee18 4 1 2 1 350 5 5 0.8 Cof feeTota l 111 27 55 14 16

Solitary animals19 1 1 80 8 15 0.4 Cacao20 1 1 350 4 18 0.6 Cacao21 1 1 60 5 20 0.8 Cof fee22 1 1 40 4 17 0.2 Coff ee23 1 1 230 4 20 0.3 Mixed24 1 1 50 2 17 0.2 MixedTotal 6 4 2


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Primates at Los Tuxtlas, Mexico 781AC KNOW L E DGME NT S

We than k the Linco ln Park Zool ogica l Socie ty and i ts Scot t Fundf or Ne o t r o p i c a l R e se a r c h f o r su p p o r t t o l a u n c h t h is r e s e a r c h p r o g r a ma n d f o r it s c o n t i n u e d su p p o r t . T h e C e n t e r f o r Fi e l d R e se a r c h , E a r t h -wa t c h , a n d T h e E x p l o r e r s C l u b o f Ne w Yo r k p r o v i d e d a d d i t i o n a lsuppor t . Univ e rs idad Nac iona l Aut6noma de M6xico p rov ided e ssen t i a llogist ical aid.

R E FE R E NC E SAndr6n, H. (1994). Effects of habitat fragmentation on birds and mammals in landscapes withdifferent proportions of suitable habitat: A review. Oikos 71: 355-366.Andr6n, H., and Angelstam, P. (1988). Elevated predation rates as an edge effect in habitatislands: Experimental evidence. Ecology 69: 544-547.Bennett, M. (1995). Intensive rotational grazing. Jersey J. Oct.: 49-52.Bicca-Marques, J. L., and Calegaro-Marques, C. (1994). Exotic plant species can serve asstaple food sources for wild howler populations. Folia Primatol. 63: 209-211.Burkey, T. V. (1988). Extinction in nature reserves: the effects of fragmentation and theimportance of migration between reserve fragments. Oikos 55: 75-81.Cassell, B. (1995). Genetic progress is not automatic. Hoard's Dairyman 12: 1127-1128.Chapman, C. A. (1988). Patterns of foraging and range use by three species of Neotropicalprimates. Primates 29: 177-194.Dirzo, R., and Garcia, M. C. (1992). Rates of deforestation in Los Tuxtlas, a neotropical areain southern Mexico. Conserv. BioL 6: 84-90.Estrada, A. (1984). Resource use by howler monkeys in the rain forest of Los Tuxtlas,Veracruz, Mexico. Int. Z Primatol. 5: 105-131.Estrada, A., and Coates-Estrada, R. (1984a). Fruit-eating and seed dispersal by howlingmonkeys in the tropical rain forest of Los Tuxtlas, Mexico. Am. J . Pr imato t 6: 77-91.Estrada, A., and Coates-Estrada, R.(1984b). Some observations on the present distributionand conservation of Aloua t ta an d Ate l e s in southern Mexico. Am. J . Pr imato l . 7:133-137.Estrada, A., and Coates-Estrada, R.(1986). Frugivory by howling monkeys (Alouatta palliata)at LOs Tuxtlas, Mexico: Dispersal and fate of seeds. In Estrada, A., and Fleming T. H.(eds.), Frugivores and Seed D/spersa/, W. Junk, The Hague, pp. 93-104.Estrada, A., and Coates-Estrada, R. (1988). Tropical rain forest conversion and perspectivesin the conservation of wild primates (Alouatta and Ateles) in Mexico. Am. Z PrimatoL

14: 315-327.Estrada, A., and Coates-Estrada, R. (1993). Aspects of ecological impact of howling Monkeys(Alouatta palliata) on their habitat: a review. In Estrada, A., Rodriguez-Luna, E.,Lopez-Wilchis, R., and Coates-Estrada, R. (eds.), Avarices en Estudios P rimatologicos enMex ico 1 , Asociaci6n Mexicana de Primatologia, A.C. y Patronatto Pro-UniversidadVeracruzana, A.C. Xalapa, Veracruz, Mexico, pp. 87-117.Estrada, A., and Coates-Estrada, R. (1995)./..as Selvas Tropicales Humedas de Mexico: RecursoPoderoso pero Vulnerable, Fondo de Cultura Economica, Mexico.Estrada, A., Coates-Estrada, R., and Martinez, M. (1985). La Estaci6n de Biologia LosTuxtlas: un recurso para el estudio y conservaci6n de las selvas del tr6pico hfimedo enM6xico. In del Amo, S., and Gomez-Pompa, A. (eds.), Regeneracion de Selvas II, InstitutoNational de Investigaciones sobre Recursos Bioticos, Editorial Alhambra Mexicana, S.A.de C.V. Mexico, pp. 379-393.


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78 2 E s t r a d a a n d C o a t e s - E s t r a d aE st rada , A. , Coa t e s -E s t r ada , R . , Mer r i t , D . , J r . , Mont i e i , S . , and Cur i e l , D . (1993) . Pa t t e rns

o f f rug ivore spec i e s ri chness and abu ndance i n fo re s t is lands and i n ag r i cu l t u ra l hab i t a tsa t L os T ux t l a s , Mex ico . In F l em ing , T . H. , and E s t r ada , A . ( eds . ) , Frugivores and SeedDispersal: Ecological an d Evolutionary Aspects, K l u w e r A c a d e m i c G r o u p , D o r d r e c h t , T h eNether lands, pp. 245-257.E s t r ada , A . , Coa t e s -E s t r ada , R . , and Mer i t t , D . , J r. (1994) . N on f l ying m am m al s and l andscapechanges i n t he t rop i ca l r a in fo re s t r eg ion o f L os T ux t l a s , Mex ico . Ecography.Fi t ch , R . (1992) . WinST AT , T he Statist ics Program for W'mdows, K a l m i a , C a m b r i d g e , M A .Garc i a Ch ia re l l o , A . (1993a ). Ac t iv i ty pa t t e rns o f the b row n ho wle r m on key Alouatta fusca,Geof f roy i 1812 , i n a fo re s t f r agm ent o f Sou theas t e rn Braz i l . Primates 34: 289-293.Ga rc i a Ch ia reUo , A. (1993b) . Hom e range o f t he b rown howle r m onkey (Alouatta fusca) ina fo re s t f r agm ent i n sou the rn Braz i l . Fol ia P r imatot 60: 173-175.Ga le t t i , M. , Pedron i , F . , and Mo re l l a to , L . P . C . (1994). Die t o f t he b row n ho wle r m on key(Alouatta fusca) i n a fo re s t f r agm ent i n sou theas t e rn Braz i l . M am m al ia 1: 111-118.Gle i ssm an , S . R . , Ga rc i a , R . and A m ad or , M . (1981). T he eco log i ca l ba s is fo r t he ap p l i ca t i ono f t r a d i t i o n a l a g r i c u l t u r e t e c h n o l o g y i n t h e m a n a g e m e n t o f t r o p i c a l e c o s y s t e m s .Agro-ecosystems 7: 173-185.H e r r , C . M . , an d R e e d , K . C . (1 9 9 1) . M i c r o m a n i p u l a t i o n o f b o v i n e e m b r y o s f o r s e xde t e rm ina t i on . Theriogenology 35: 45.Horw ich , R . , and J ohnso n , E . D. (1986). Geo graph ic d i s tr i bu t ion o f t he b l ack howle r (Alouattapigra) i n Cen t ra l Am er i ca . Primates 27: 53-62.Ka r r , J . R . (1990). Av ian surviva l r a t e s and t he ex t i nc t i on p rocess on B a r ro Co lo rado I s l and ,P a n a m a . Conserv. Biol. 4: 391-397.L aurance , W . F . (1991). E dge e f fec t s i n t rop i ca l fo re s t f r agm ent s : App l i ca t i ons o f a m ode lfo r t he de s ign o f na tu re r e se rves . BIOL Conserv. 57: 205-219.L ove joy , T . E . , B i e r regaa rd , R . O. , J r . , Ry lands , A . B . , Ma lcom , J . R . , Q u in t e l a , C . F . , Ha rpe r ,L . H. , Brown, IC S . , Powe l l , A . H . , Powe l l , G . V. N. , Schuba r t , H . O. R . , and H ays , M.B. (1986). E dg e and o the r e f f ec t s o f iso l a t ion on Am azon fo re s t f r agm ent s . In Sou le , M .E. (ed.), Conservation B ioloD,: The Science o f Scarcity and Diversity, Sinaue r , Sunde r l and ,MA, pp. 257-285.Ludwig, J . A. , and Reynolds, J . F. (1988) . Statistical Ecolog y, J o h n W i l e y a n d S o n s , N e w Y o r k .Mc ln ty re , S . , and Ba r re t , G . W. (1992) . Hab i t a t va r i ega t i on , an a l t e rna t i ve t o f r agm enta t i on .Conserv. Biol. 1: 146-147.M i t t e rm e ie r , R . A. , and van Roo sm a len , M. G. M . (1981). Pre l im ina ry obse rva t i ons on hab i t a tu t i l i z a t i on and d i e t i n e igh t Sur inam m onkeys . Folia Primatol. 36: 1-39.Morow i t z , H . J . (1991) . Ba l anc ing spec ie s p re se rva t i on and econo m ic cons ide ra t i ons . Science253: 752-75,LN a i m a n , R . J . , D e c a m p s , H . , a n d P o l l o c k , M . ( 1 9 9 3 ) . T h e r o l e o f r i p a r i a n c o r r i d o r s i nmainta ining regional biodiversi ty . Ecol. Appl. 3: 209-212.Noss , R . F . (1991) . L anD scape connec t i v i ty : Di f f e ren t func t ions a t d i f f e ren t scal es . In H udso n ,W. E . ( ed . ) , Landscape Linkages and Biodiversity, I s l and Pre ss , Wash ing ton , DC, pp .110-130.

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(ed.), I/ ' tab/e Populations for Conservation, Cambr idge Univ . P res s , Cambr idge , pp . 69-86 .Terb orgh , J . (1992) . M ain te nan ce of d ive rs i ty in t ropica l fores ts . Biotropica 24: 283-292.W at t s , E . S ., R ico-Gray , V . , and Chan , C . (1986). M onkey s of the Y uca tan Pen insula , Mexico:Pre l im inary survey of the i r d i s t r ibu t ion and s t a tus . P r /mate Conserv. 7: 17-22.

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