Local and Landscape Correlates of Primate Distribution and ......fragmentos de bosque tropical lluvioso en el Valle del Alto Brahmaputra, noreste de India. En promedio, los fragmentos

Contributed Paper

Local and Landscape Correlates of PrimateDistribution and Persistence in the Remnant LowlandRainforests of the Upper Brahmaputra Valley,Northeastern IndiaNARAYAN SHARMA,∗† ‡ M. D. MADHUSUDAN,∗† AND ANINDYA SINHA∗†∗Ecology, Behaviour and Conservation Programme and School of Natural Sciences and Engineering, National Institute of AdvancedStudies, Indian Institute of Science Campus, Bangalore 560012, India†Nature Conservation Foundation, 3076/5, 4th Cross, Gokulam Park, Mysore 570002, India

Abstract: Habitat fragmentation affects species distribution and abundance, and drives extinctions. Es-calated tropical deforestation and fragmentation have confined many species populations to habitat rem-nants. How worthwhile is it to invest scarce resources in conserving habitat remnants within denselysettled production landscapes? Are these fragments fated to lose species anyway? If not, do other ecologi-cal, anthropogenic, and species-related factors mitigate the effect of fragmentation and offer conservationopportunities? We evaluated, using generalized linear models in an information-theoretic framework, theeffect of local- and landscape-scale factors on the richness, abundance, distribution, and local extinction of 6primate species in 42 lowland tropical rainforest fragments of the Upper Brahmaputra Valley, northeasternIndia. On average, the forest fragments lost at least one species in the last 30 years but retained half theiroriginal species complement. Species richness declined as proportion of habitat lost increased but was notsignificantly affected by fragment size and isolation. The occurrence of western hoolock gibbon (Hoolockhoolock) and capped langur (Trachypithecus pileatus) in fragments was inversely related to their isolationand loss of habitat, respectively. Fragment area determined stump-tailed (Macaca arctoides) and northernpig-tailed macaque occurrence (Macaca leonina). Assamese macaque (Macaca assamensis) distribution wasaffected negatively by illegal tree felling, and rhesus macaque (Macaca mulatta) abundance increased ashabitat heterogeneity increased. Primate extinction in a fragment was primarily governed by the extent ofdivergence in its food tree species richness from that in contiguous forests. We suggest the conservation valueof these fragments is high because collectively they retained the entire original species pool and individuallyretained half of it, even a century after fragmentation. Given the extensive habitat and species loss, however,these fragments urgently require protection and active ecological restoration to sustain this rich primateassemblage.

Keywords: abundance, Assamese macaque, capped langur, habitat fragmentation, hoolock gibbon, local ex-tinction, pig-tailed macaque, species richness, stump-tailed macaque

Correlaciones Locales y de Paisaje de la Distribucion y Persistencia de Primates en los Bosques Lluviosos Rema-nentes en el Valle del Alto Brahmaputra, Noreste de India

Resumen: La fragmentacion del habitat afecta la distribucion y abundancia de especies y causa extinciones.El incremento en la deforestacion y fragmentacion en los tropicos ha confinado en los remanentes de habitata las poblaciones de muchas especies. ¿Que tan rentable es invertir recursos escasos en la conservacion deremanentes de habitat inmersos en paisajes densamente poblados? ¿Los fragmentos estan destinados a perderespecies de todos modos? Si no, ¿hay otros factores ecologicos, antropogenicos y relacionados con las especies

‡Address for correspondence: Ecology, Behaviour and Conservation Programme and School of Natural Sciences and Engineering, NationalInstitute of Advanced Studies, Bangalore, India, email [email protected] submitted October 6, 2012; revised manuscript accepted May 29, 2013.

95Conservation Biology, Volume 28, No. 1, 95–106C⃝ 2013 Society for Conservation BiologyDOI: 10.1111/cobi.12159

96 Primate Distribution in Forest Fragments

que mitigan el efecto de la fragmentacion y ofrecen oportunidades de conservacion? Evaluamos, mediantemodelos lineales generalizados enmarcados en teorıa de la informacion, el efecto de factores a escala localy de paisaje sobre la riqueza, abundancia, distribucion y extincion local de 6 especies de primates en 42fragmentos de bosque tropical lluvioso en el Valle del Alto Brahmaputra, noreste de India. En promedio, losfragmentos de bosque perdieron por lo menos una especie en los ultimos 30 anos pero retuvieron la mitad desu complemento de especies original. La riqueza de especies declino en proporcion al habitat perdido, pero nofue afectada significativamente por el tamano y aislamiento del fragmento. La ocurrencia Hoolock hoolocky Trachypithecus pileatus en fragmentos se relaciono inversamente con el aislamiento y perdida de habitat,respectivamente. El area del fragmento determino la ocurrencia de Macaca arctoides y Macaca leonina. Ladistribucion de Macaca assamensis fue afectada negativamente por la tala illegal, y la abundancia de Macacamulatta incremento a medida que incremento la heterogeneidad del habitat. La extincion de primates enun fragmento se rigio fundamentalmente por el grado de divergencia en la riqueza de especies de arbolesque le sirven de alimento en relacion con los bosques contiguos. Sugerimos que el valor de conservacion deestos fragmentos es alto porque colectivamente retuvieron al conjunto original de especies e individualmenteretuvieron la mitad, aun un siglo despues de la fragmentacion. Sin embargo, debido a perdida extensiva dehabitat y especies, estos fragmentos requieren urgentemente de proteccion y restauracion ecologica activapara sustentar este rico ensamble de primates.

Palabras Clave: abundancia, extincion local, fragmentacion de habitat, Hoolock hoolock, Macaca arctoides,M. assamensis, M. leonina, riqueza de especies, Trachypithecus pileatus

Introduction

Tropical forests have undergone extensive loss and frag-mentation (Skole & Tucker 1993), but many of thesefragments, although variable in size and isolation, arethe last refuge of numerous forest-dependent species inhuman-modified landscapes (Wilcove et al. 1986). Oneof the groups most severely affected by forest fragmenta-tion and loss are primates, most of which are forest de-pendent and highly vulnerable to environmental change(Cowlishaw & Dunbar 2000). Nearly half of all primatespecies are threatened by habitat loss, fragmentation,and hunting (IUCN 2010). With the growing extinctionrisk due to habitat fragmentation (Turner 1996; Krausset al. 2010), knowledge-based conservation strategies forspecies populations in fragmented landscapes are an ur-gent need.

The theory of island biogeography (MacArthur &Wilson 1967) has often been used as a conceptual frame-work to understand the community-level consequencesof habitat fragmentation. By treating habitat fragmentsas analogous to oceanic islands, this theory predicts thatthe species richness in a fragment is determined by a dy-namic equilibrium between extinction and colonizationrates, both functions of its size and isolation. However,in reality, the theory does not account for certain mecha-nisms governing species distribution in terrestrial habitatislands (Laurance 2008). For instance, in addition to—orindependent of—area and isolation (Prugh et al. 2008),variables such as habitat quality and anthropogenic fac-tors are key determinants of species composition, abun-dance, and distribution in habitat fragments not only forprimates (e.g., Mbora & Meikle 2004; Michalski & Peres2005; Anzures-Dadda & Manson 2007) but for other tax-

onomic groups as well (e.g., Mazerolle & Villard 1999;Michalski & Peres 2005; Sridhar et al. 2008). Moreover,the persistence of populations in fragmented terrestrialislands depends heavily on the intervening habitat ma-trix (Michalski & Peres 2005; Ewers & Didham 2006),which is seldom homogeneous (Kupfer et al. 2006) orcompletely hostile to species, whose tolerances of sucha matrix may vary considerably (Ewers & Didham 2006).

Conservation practitioners and managers, especially inthe tropics, often question how worthwhile it is to investin the conservation of habitat remnants. Are they a lostcause, fated to lose species anyway, given their small size,relatively high isolation, and continuing land-use change?To what extent can other ecological, anthropogenic, andspecies-related factors mitigate the effects of size and iso-lation and offer management opportunities that preventthe further extirpation of species and effectively conservethem?

We examined these questions by studying primates,a forest-dependent group likely to be disproportionatelyaffected by fragmentation, in the Upper Brahmaputra Val-ley in northeastern India, within the Indo-Burma globalbiodiversity hotspot, where lowland rainforest fragmentswere created over a century ago. Even after years of frag-mentation and loss, these fragments, which differ in sizeand isolation, have retained different fractions of theiroriginal primate species pool (Sharma et al. 2012a).

We explored how local and landscape factors affect pri-mate species richness, abundance, and distribution andtemporal changes in a fragment’s spatial and vegetationalattributes affect primate persistence and extinction. Wethen examined the implications of our findings for theconservation and management of primates in the frag-ments of such a landscape.

Conservation BiologyVolume 28, No. 1, 2014

Sharma et al. 97

Figure 1. Locations of the study fragments in the Upper Brahmaputra Valley in Assam, northeastern India (1,Buridehing; 2, Dangori; 3, Dehingmukh; 4, Deopani; 5, Doomdooma; 6, Duarmara; 7, Hahakhati;8, Hollogaon; 9, Jokai; 10, Joypur; 11, Kakojan; 12, Kotha; 13, Kukuramara; 14, Kumsong;15, Kundilkalia; 16, Mesaki; 17, Namdang; 18, Sadia Station North Block; 19, Sadia Station West Block; 20,Tarani; 21, Telpani; 22, Tinkopani-Namphai; 23, Tokowani; 24, Upper Dehing (East Block) Forest Complex; 25,Upper Dehing (West Block) Forest Complex).

Methods

Study Area

Our study site was in the floodplains south of the riverBrahmaputra in the Indian state of Assam (Fig. 1). Theoriginal vegetation was mainly wet evergreen forestsof the Dipterocarpus-Mesua series (Champion & Seth1968). The history of this landscape is complex. Over2 centuries, until the late 1990s, there has been heavydeforestation for agriculture and settlements and for ex-traction of timber from forests reserved for such harvest(Sharma et al. 2012b). Today, the remnant lowland rain-forests occur as fragments of different sizes spread acrossthe region (Fig. 1).

Seven primate species that vary considerably in theirecology—the rhesus macaque (Macaca mulatta), north-ern pig-tailed macaque (Macaca leonina), Assamesemacaque (Macaca assamensis), stump-tailed macaque(Macaca arctoides), western hoolock gibbon (Hoolockhoolock), capped langur (Trachypithecus pileatus), andBengal slow loris (Nycticebus bengalensis)—co-occur inthese forests. Of these, we collected data on the first 6species, which are diurnal, but not on the nocturnal slowloris because our surveys were conducted during daylighthours. The rhesus macaque is a diet and habitat general-ist, as is the Assamese macaque, which are both better-adapted to human-modified landscapes than the pig-tailedand stump-tailed macaques, capped langurs and hoolockgibbons, all of which are restricted to the forest interiors



(Roonwal & Mohnot 1977). Barring the predominantlyterrestrial stump-tailed and rhesus macaques, all the pri-mates are mostly arboreal, with the hoolock gibbon be-ing entirely so. The capped langur is mainly folivorous(Solanki et al. 2008), whereas the remaining species areprimarily frugivorous (Roonwal & Mohnot 1977). Insectsand roots, however, constitute a significant part of pig-tailed and stump-tailed macaque diets, respectively (N.S.,personal observation). The diets of these species differ,however, and may change seasonally or in response toother changes in food availability.

There are considerable differences among thesespecies in their ability to use the matrix habitat. Amongthe macaques, we observed the rhesus macaque was themost versatile in terms of its use of the surrounding habi-tats. The rhesus macaque, and to a limited extent the As-samese macaque, even moved across open paddy fields.The pig-tailed and stump-tailed macaques, on the otherhand, were rarely seen outside fragments. The cappedlangurs were able to use scattered trees in the adjacentagricultural fields and plantations for foraging and occa-sionally as sleeping sites. The hoolock gibbon was rarelyobserved visiting specific food trees in the surroundingmatrix, but only if there was a structural connectivitybetween these trees and the forest fragments.

Site Selection

We analyzed data from 25 of the 42 rainforest fragmentssurveyed in the Tinsukia and Dibrugarh Forest Divisionsof the state (Fig. 1). These ranged in size from 1.4 to 233km2. They were created approximately 100 years ago(Sharma et al. 2012a, 2012b). We defined a fragment asa forest patch separated from other such forest patcheson an ecological timescale by a river, tea plantation, agri-cultural field, human settlement, or degraded secondaryvegetation that prevented easy movement of primatesacross them. Fifteen fragments were completely isolatedin terms of their structural connectivity rather than theirbiological permeability, as determined by their presencein a simple matrix such as that of open agriculture. Ninefragments were separated from one another by a river,and one was connected to the nearest contiguous forestthrough a narrow corridor of secondary vegetation. Wedesignated 3 fragments as control sites on the basis oftheir size (>100 km2), continuity, and relatively intactforest cover. Of the 17 fragments omitted from analyses,7 fragments had been completely cleared and their pri-mates extirpated, and the remainder proved difficult tosurvey.

Primate Surveys

Between August 2006 and January 2007, we used ex-isting animal (e.g., elephant) and human trails to sur-vey fragments. We walked each trail once, after dawn

(0600–1000) or before dusk (1400–1600), when the pri-mates were most active, at approximately 2 km/h. Westopped periodically to scan the canopy and to listen forprimate presence. On detection, we identified species,enumerated groups, and categorized individuals by ageand sex. We computed fragment-wise encounter ratesonly for rhesus macaques because this species did notavoid us. For all other species, some of which could po-tentially have avoided areas of human activity includinghuman-created trails, we assessed occurrence rather thanabundance.

We also gathered information on the occurrence of allprimates, except the nocturnal slow loris, and assessedtheir distribution and extinction events in the fragmentson the basis of key-informant surveys (n = 48, 1–2 inter-views/fragment) in the adjoining villages. We selectedlocal informants who reliably recognized the primatespecies, were long-term (>30 years) residents of the area,and frequently visited the adjacent forests. Two localprimatologists helped us cross-verify the distribution ofdifferent primate species in the fragments. We preparedthe final species occurrence data for each fragment afteraggregating data from all sources.

We walked 158 trails (2–20 trails/fragment) for a totaldistance of 484 km (6.4–74.4 km/fragment). The numberof trails and sampling effort were proportional to frag-ment area (r = 0.78, P < 0.001 and r = 0.53, P < 0.01,respectively).

Fragment and Landscape Characteristics

We characterized each fragment by measuring its spatial(forested area), ecological (tree species richness, canopycover, and tree basal area) and anthropogenic (illegal treefelling and habitat loss) attributes. We used a combinationof high-resolution satellite images (large fragments) andground-based geographic position system (GPS) surveys(small fragments) to estimate actual forested area. In eachfragment, we measured all vegetation variables in circularplots with a 10-m radius (2–37 plots/fragment) locatedregularly 15 m apart to the left and right, alternately, ofeach trail. All trees with stems ≥10 cm cbh (circumfer-ence at breast height) were identified and counted oneach plot. These measurements were summarized intoestimates of tree species richness, diversity, and basal areafor each fragment. We based our estimates of species rich-ness, abundance, species diversity, and basal area of foodtrees for each primate species and all primates taken to-gether on published literature and our own observations.Canopy cover was assessed at every 100 m along the trailand on each plot with a modified ordinal 5-point scalefollowing Kakati (2004). Canopy-cover points from plotswere averaged to yield a canopy cover score for eachfragment. We also used the coefficient of variation (CV)of the canopy cover rank (estimated at regular intervals


Sharma et al. 99

Tabl

e1.

Enco

unte

rra

te,d

istr

ibut

ion,

rich

ness

,and

extin

ctio

nof

prim

ates

info

rest

frag

men

tsof

the

Uppe

rBr

ahm

aput

raVa

lley,

Assa

m,n

orth

east

ern

Indi

a.

Spec

ies

loss

Fra

gmen

tFo

rest

edFe

atu

reE

nco

un

ter

rate

ofP

rese

nce

(P)

ora

bsen

ce(A

)c

Fra

gmen

tco

dea

rea

sepa

rati

ng

2rh

esu

sm

aca

ques

Pri

ma

ten

um

ber

prop

orti

onin

Fig.

1St

udy

site

a(k

m2)

fra

gmen

tsb

(in

divi

dua

l/km

)C

LH

GA

MP

TMR

MST

Mri

chn

ess

lost

(in

%)

1B

urid

ehin

g20

.79

OA

0.42

PP

PP

PA

50

02

Dan

gori

10.9

2O

A0.

23A

PP

AP

A3

240

3D

ehin

gmuk

h29

.71

OA

5.37

AA

PA

PA

21

334

Deo

pan

i2.

7R

IV0.

00A

AA

AP

A1

150

5D

oom

doom

a24

.07

OA

1.42

PP

PP

PA

50

06

Dua

rmar

a6.

58O

A0.

00P

AA

AP

A2

133

7H

ahak

hati

2.74

RIV

1.85

AP

PA

PA

32

408

Hol

loga

on3.

25O

A1.

24A

PA

AP

A2

00

9Jo

kai

12.5

1O

A3.

87A

AP

AP

A2

00

10Jo

ypur

132.

7R

IV0.

00P

PP

PP

P6

00

11K

akoj

an21

.73

RIV

0.62

PP

PP

PA

50

012

Kot

ha8.

35O

A0.

46P

AA

AP

A2

133

13K

ukur

amar

a3.

67O

A0.

27A

PA

AP

A2

133

14K

umso

ng7.

29O

A2.

08A

PP

AP

A3

240

15K

undi

lkal

ia7.

75R

IV0.

00A

PA

AP

A2

00

16M

esak

i10

.19

RIV

0.00

AP

AA

PA

22

5017

Nam

dang

1.79

OA

2.81

AA

AA

PA

10

018

Sadi

aSt

atio

nN

orth

Blo

ck12

.61

OA

0.00

AA

AA

PA

11

5019

Sadi

aSt

atio

nW

est

Blo

ck1.

35O

A2.

54A

AA

AP

A1

150

20T

aran

i12

.84

OA

0.97

PP

PP

PA

50

021

Tel

pan

i4.

43O

A0.

71A

AP

AP

A2

00

22T

inko

pan

i-Nam

pha

i45

.48

SF0.

00P

PP

PP

P6

00

23T

okow

ani

4.98

RIV

3.15

PP

PP

PA

50

024

UD

EBFo

rest

Com

ple

x11

2.05

RIV

0.00

PP

PP

PP

60

025

UD

WB

Fore

stC

omp

lex

233.

19R

IV0.

23P

PP

PP

P6

00

aA

bbre

via

tion

s:U

DE

B,U

pper

Deh

ing

(Ea

stB

lock

);U

DW

B,U

pper

Deh

ing

(Wes

tB

lock

).bA

bbre

via

tion

s:O

A,o

pen

agr

icu

ltu

re;R

IV,r

iver

;SF,

seco

nda

ryfo

rest

.c A

bbre

via

tion

s:A

M,A

ssa

mes

em

aca

que;

CL,

capp

edla

ngu

r;H

G,h

oolo

ckgi

bbon

;PTM

,pig

-tail

edm

aca

que;

RM

,rh

esu

sm

aca

que;

STM

,stu

mp-

tail

edm

aca

que.



Table 2. Model-averaged estimates of coefficients with 95% confidenceintervals for landscape and local variables affecting primate speciesrichness.

Variable Coefficient 95% CI

Intercept 1.09 0.82 to 1.36Forested area 0.24 −0.16 to 0.64Proportion of habitat loss −0.32 −0.62 to −0.02Illegal tree felling −0.35 −0.78 to 0.08Distance to nearest forest −0.27 −0.66 to 0.11Forested area × distance to

nearest forest0.41 −0.71 to 1.53

Correlation between predictedand observed valuesa

0.80∗∗

aCoefficient of correlation (r) between model-predicted and observedvalues (∗∗correlations significant at P = 0.01).

along the trails) as a measure of horizontal heterogeneityof canopy cover.

We estimated illegal tree felling as the encounter ratealong trails of cut tree stumps ≥30 cm cbh that had beenfelled within approximately the previous year. Net habi-tat loss was estimated by comparing the original gazettedarea of each fragment with the current forested areaand computing the proportion of habitat lost in eachfragment.

The 22 fragments ranged from 1.35 to 45 km2, whereasthe 3 control sites ranged from 112 to 233 km2 (Table 2).We sampled 356 plots for vegetation in the 25 fragments.The number of plots in a fragment (4–37) was propor-tional to the size of the fragment (r = 0.49, P = 0.01).We measured 4730 stems in plots, of which 129 wereunidentified. Besides on the vegetation plots, the canopycover was also assessed in 2592 plots along the trails.

We also evaluated the spatial, ecological, and anthro-pogenic characteristics of the broader landscape sur-rounding a fragment to examine the effect of habitat frag-mentation on the community and population attributesof the primates. First, we quantified the spatial isolationof a fragment from its nearest fragment and its nearestcontiguous forest with GIS data and characterized thedominant matrix type surrounding each fragment withsatellite imagery. Of the 25 fragments, 24 were dominatedby open agriculture (paddy and tea) that lacked a treecanopy. The matrix of the remaining fragment largelycomprised a human settlement. Given the consistencyin the type of landscape matrix across fragments, webelieve that our design allowed us to hold the effectsof matrix constant and precisely address the effects ofother landscape and local factors on primate distributionand abundance. We considered the human populationdensity surrounding each fragment an important anthro-pogenic feature. This parameter was extracted for a 5-km buffer around each fragment from the Gridded Pop-ulation of the World (version 3) (CIESIN & CIAT 2005)derived from the Census of India (Government of India2001).

Although traditional hunting is widespread in north-eastern India, it was relatively low in our study areasowing to taboos against hunting primates. Yet, we wereunable to completely rule out occasional incidents ofsurreptitious hunting. We, therefore, used primate oc-currence rather than primate abundance as the responsevariable because it would be less sensitive to the possibleoccurrence of occasional hunting.

To understand the extent to which fragmentation-mediated physical and vegetation changes of a fragmentaffected local extinction of primate species over the last30 years, we estimated changes in the physical and vege-tation attributes of the fragments over this period.

To calculate change in fragment area, we used theoriginal gazetted area and present habitat area of the frag-ment. We calculated percent change per year from thehabitat area obtained for each fragment through LandsatMultispectral Scanner, Thematic Mapper, and EnhancedThematic Mapper images of 1973, 1976, 1988, and 1990(USGS 2007). We also measured changes in physical iso-lation of these fragments from contiguous forests (i.e.,fragments >100 km2) from these maps. Given that his-torical changes in vegetation structure and compositionwere difficult to obtain, we used an alternative space-for-time substitution approach (Pickett 1989) to assess suchchanges. We thus assumed that all fragments in the re-gion, having been derived from contiguous forests, weresimilar to them in terms of vegetation characteristics priorto isolation. The values of tree species richness, diversity,canopy cover, CV of canopy cover, and tree and foodtree basal area were calculated for each fragment andsubtracted from the corresponding values of continuousforests. We assumed these differences represented theextent to which a given fragment had diverged over timefrom a primary forest in terms of its vegetation.

Primate Extinctions

We defined species extirpation as the unambiguous ab-sence of a species that had been reported 30 years agowithin a fragment but which had not been seen, heard,or otherwise detected up to the time of the survey by thekey informants (Sharma et al. 2012a). In case of differ-ences between informants from the same area, we usedthe most conservative scenario. We used these data tocompute the number and proportion of primate specieslost in each fragment over time.

Statistical Analyses

From the literature and our own observations, we identi-fied 39 landscape and local variables (habitat and anthro-pogenic [Supporting Information]) that could potentiallyaffect community and population attributes of all theprimates. From among these variables and on the basis


Sharma et al. 101

of previous work (Roonwal & Mohnot 1977; Srivastava1999; Kakati 2004; Solanki et al. 2008) on primates andon established ecological mechanisms, we selected thosevariables that could affect the occurrence, species rich-ness, and abundance of primates. We also identified 12local and landscape variables, changes in which couldaffect primate extirpation in a fragment. Before modelfitting, we examined all variables for multicollinearity,and from within each pair of highly correlated variableswe retained the more ecologically meaningful one in aparticular context. Most of the independent variableswere highly correlated (Supporting Information).

To identify important local and landscape factors thataffect richness, abundance, and species distribution,we used generalized linear models (GLMs), which aresuited for modeling nonnormal data (Maindonald & Braun2007). We also used GLMs to identify factors affecting pri-mate extinction in fragments. All predictor variables werecentered and scaled to have zero means and unit standarddeviations before fitting models in order to make thevariables mutually comparable. From the primate naturalhistory and ecology literature, and our own observations,we built a set of a priori candidate models with differ-ent combinations of local and landscape variables andtheir most important interactions as predictor variablesand measures of primate occurrence, species richness,and abundance as response variables. For the responsevariables primate species richness, rhesus macaque en-counter rates, and number of extinct primates in a frag-ment we used a Poisson error structure with log-link func-tion. Because the occurrence data of individual specieswere zero-inflated, we used bias-reduced GLMs (Kosmidis2007) that involved binomial error structure and log-linkfunction for these analyses. To evaluate the factors af-fecting primate extirpation, we considered the numberof species currently present as successes and the numberof species lost as failures and used their values in com-bination as the response variable. We assume a binomialerror structure with log-link function for these models.

We analyzed and ranked candidate models on the basisof Akaike information criterion (AIC). We used Akaikeweights to identify a set of confidence models, whichcumulatively contributed at least 0.95 to the weight ofevidence (Burnham & Anderson 2002). Landscape andlocal factors that affected primate community and pop-ulation attributes and primate extinction were inferredby evaluating model-averaged estimates of their coeffi-cients from the above set of confidence models (John-son & Omland 2004). We assessed model fit by corre-lating model-predicted values of primate community andpopulation attributes and primate extinction and corre-sponding observed values (Zheng & Agresti 2000). Allanalyses were carried out with the statistical software R(version 2.12.2) (R Development Core Team 2011). Thebias-reduced GLM analysis was conducted with the aid ofthe brglm package (Kosmidis 2007).

Results

Primates in the Study Sites

We encountered 42 groups of rhesus macaques (min-imum 450 individuals), 40 groups of hoolock gibbons(minimum 129 individuals), 14 groups of Assamesemacaques (minimum 94 individuals), 8 groups of cappedlangurs (minimum 68 individuals), and 2 groups of pig-tailed macaques (minimum 21 individuals). We did notdetect stump-tailed macaques, although secondary infor-mation (e.g., questionnaires) confirmed their presence in4 relatively large forest fragments.

Mean primate species richness in fragments was 3.2(SD 1.79, range 1–6). Half the fragments retained over50% of the original species pool of the region, whereasthe other half contained 1–2 species. Mean species rich-ness was highest (mean [SD] = 6 [0]) in large fragments(>45 km2, n = 4), intermediate (3.37 [1.66]) in medium-sized fragments (10–45 km2, n = 9), and low (2.17 [1.1])in the smaller fragments (<10 km2, n = 12) (Table 1).

Approximately 57% of the fragments retained theiroriginal species pool of 30 years ago, whereas 1 or 2species were extirpated from the remaining fragments.On average a fragment lost at least one of its primatespecies over these 30 years (Table 1). The proportion ofspecies loss was highest (mean [SD] = 23.25 [21.28]) inthe smaller fragments (<10 km2) and relatively lower(19.22 [23.35]) in midsized fragments (10–30 km2),whereas the large fragments did not lose any species.

On average, a fragment lost a one-third of its forestedarea over the last century. About 16% of the fragments lostover three-fourths of their original forest, whereas 12%and 24% of fragments have been reduced to over one-halfand one-fourth of their original size, respectively.

Variables Affecting Species Richness and Presence

We compared 12 candidate GLMs for primate speciesrichness as a function of local and landscape factors.The 3 best models had habitat loss as a key explanatoryvariable (Supporting Information). The model-averagedparameter estimates showed that primate species rich-ness declined as habitat loss increased (Table 2). Primatespecies richness was also negatively related to illegal treefelling, although the 95% CI of its model-averaged param-eter estimate marginally overlapped zero.

The GLM analyses of the distribution of the 5 primatespecies were conducted as a function of the local andlandscape variables of a fragment (Table 3). Both thebest-fit model (Supporting Information) and the model-averaged coefficient showed that the likelihood of occur-rence of hoolock gibbons increased with greater prox-imity to the nearest forest. The proportion of habitatlost appeared in the first 4 best models that describedthe occurrence of capped langur, the model-averaged


102Prim

ateDistributionin

ForestFragments

Table 3. Model-averaged estimates of coefficients (coeff) with 95% confidence intervals for landscape and local variables affecting occurrence of individual primate species and encounter rate ofrhesus macaques.

Hoolock gibbon Capped langur Pig-tailed macaque Assamese macaque Stump-tailed macaque Encounter rate ofoccurrence occurrence occurrence occurrence occurrence rhesus macaque

Variable coeff 95% CI coeff 95% CI coeff 95% CI coeff 95% CI coeff 95% CI coeff 95% CI

Intercept 0.66 −0.39 to 1.70 −0.95 −3.15 to 1.24 1.71 −2.60 to 6.03 −0.98 −2.90 to 0.94 −1.41 −3.73 to 0.90 −0.06 −0.59 to 0.47Forested area 0.44 −1.94 to 2.81 2.04 −3.03 to 7.10 8.59 −2.55 to 19.73 0.00 −1.40 to 1.39 7.06 −2.00 to 16.12 −0.93 −2.21 to 0.36Coefficient of variance of

canopy cover0.34 0.03 to 0.66

Basal area of cappedlangur food plants

0.35 −0.80 to 1.51

Basal area of pig-tailedmacaque food plants

−0.10 −1.00 to 0.80

Proportion of habitat loss −0.82 −1.85 to 0.21 −1.77 −3.63 to −0.09 −1.17 −3.01 to 0.67 0.26 −1.35 to 1.87 −0.07 −2.05 to 1.92 0.36 −0.05 to 0.77Illegal tree felling −0.03 −1.05 to 0.99 −2.69 −6.25 to 0.87 −2.47 −6.22 to 1.27 −6.69 −12.54 to −0.85 0.41 −0.94 to 1.76 −0.13 −0.57 to 0.31Distance to nearest forest −1.24 −2.41 to −0.07 −1.83 −4.40 to 0.74Human population

density0.07 −0.34 to 0.48

Forested area × distanceto nearest forest

0.21 −3.74 to 4.16 −1.76 −9.63 to 6.12

Correlation betweenpredicted and observedvaluesa

0.69∗∗ 0.77∗∗ 0.90∗∗ 0.85∗∗ 0.97∗∗ 33

aCoefficient of correlation (r) between model-predicted and observed values (∗∗, correlations significant at P = 0.01).

Con

servation

Biology

Volum

e28,N

o.1,2014

Sharma et al. 103

coefficient indicated its likelihood of occurrence de-creased in fragments with greater habitat loss. Forestedarea appeared in the 3 best models and seemed to pos-itively affect the likelihood of occurrence of the pig-tailed macaque, although the model-averaged coefficientswere not significant. The likelihood of occurrence of As-samese macaques was negatively affected by illegal treefelling, whereas that of stump-tailed macaques was bestexplained by the model that included forested area (Sup-porting Information). The model-averaged coefficientssuggested, although results were not significant, likeli-hood of occurrence of the latter species increased asfragment area increased. All the predicted models for the5 primate species showed significant correlation with theobserved values.

We did not use the GLMs to explain variation in rhesusmacaque occurrence because the species was present inall fragments. Instead, we compared 8 GLMs to explainthe variation in encounter rates of rhesus macaques as afunction of both local and landscape variables. Althoughforested area was the best-fit model (Supporting Infor-mation), an examination of the model-weighted parame-ter estimates showed a positive effect of CV of canopycover and proportion of habitat loss on the abundance ofrhesus macaques (Table 2). The model-predicted value,however, showed only a weak correlation.

Variables Affecting Number and Proportion of ExtirpatedSpecies

We compared 9 candidate GLMs each for the numberand proportion of extinct species as a function of puta-tive changes in local and landscape characteristics of thefragments. The difference in food tree species richnessappeared to be a key factor in both sets of models. Themodel-averaged parameter estimates indicated the differ-ence in food tree species richness was the single-most im-portant factor affecting the proportion of primate specieslost from the sites (Table 4). The model-predicted valuesof the number of extinct primates, however, showed aweak correlation with the observed values.

Discussion

Our results indicate that primate species richness hasdeclined severely in the lowland rainforest fragments ofthe Upper Brahmaputra Valley because these fragmentshave lost, on average, one-third of their forested area overthe last century. Such extensive anthropogenic forestloss has reduced the total area of forest fragments, in-creased their isolation, and, as predicted by the theory ofisland biogeography, apparently led to a decline inspecies richness.

High levels of illegal tree felling appeared to be asso-ciated with lower primate species richness; fragments

with higher illegal tree felling lost the most primatespecies. The occurrence of some species such as theAssamese macaque was also negatively affected by illegaltree felling. Historically, these fragments were logged fortimber until it became illegal in 1996. Small-scale illegalfelling continues to degrade habitat quality by reducingthe availability of important food plants of primates (N.S.,personal observation) and by disrupting canopy continu-ity vital for arboreal primates. New canopy openings andedge creation may also facilitate the spread of invasiveplants, which, in turn, could alter the original tree com-position and diversity of a fragment.

The likelihood of occurrence of hoolock gibbons, oneof the most threatened primates in these fragments in-creased with proximity of the fragment to contiguousforests or another fragment. For these arboreal primatesthat rarely move across fragments and may not cross gapseven as small as 200 m (Choudhury 1995), the meandistance of 2.51 km between our study fragments couldbecome critical for their survival. Given the crucial im-portance of animal movement in governing species distri-butions in fragmented landscapes (Fleishman et al. 2002)and in preventing extirpation by the rescue effect (Brown& Kodric-Brown 1977), such small, completely isolatedpopulations of hoolock gibbons are likely to be extremelyvulnerable to stochastic extinctions arising from demo-graphic, genetic, or environmental factors.

The only colobine primate in our study area, thecapped langur, was extirpated from fragments that lostover half their original forested area over the last cen-tury. Folivorous primates, including the capped langur(Solanki et al. 2008), require diverse food plants in orderto limit the intake and accumulation of harmful secondarycompounds (Garber 1987). The diversity of capped lan-gur food trees was lower in fragments that had lost 50%of their forest relative to sites that had lost approximately10% of their forest.

None of the model coefficient values explained the dis-tribution of pig-tailed macaques, although forested area,distance to the nearest forest, and interactions of thesevariables contributed to the most likely model. Largerfragments may support this primate because they con-tain more food species and intact canopy cover, criticalsurvival components for this arboreal species. Distanceto the nearest forest may also be important to the lo-cal persistence for this species because it can promotedispersal among fragments.

The most important variable affecting stump-tailedmacaque distribution was forested area. Given its largehome range (400–900 ha in one fragment, the Hollon-gapar Gibbon Wildlife Sanctuary [Sharma et al. 2012a]),smaller fragments may not support populations of thisspecies, as has been reported for other wide-rangingNeotropical primates (Schwarzkopf & Rylands 1989).

Abundance of rhesus macaques was affected positivelyby canopy cover heterogeneity and negatively by forested



Table 4. Model-averaged estimates of coefficients (coef) with 95% confidence intervals for putative changes in the local and landscape variablesaffecting the number and proportion of extinct primates.

Number of extinct primates Proportion of extinct primates

Variable coeff 95% CI coeff 95% CI

Intercept −0.55 −1.2 to 0.09 −1.57 −2.3 to −0.85Difference in coefficient of variation of canopy cover 0.09 −0.46 to 0.63 0.23 −0.49 to 0.95Difference in food tree richness 0.67 −0.02 to 1.37 1.15 0.23 to 2.07Isolation −0.17 −0.92 to 0.58 −0.22 −1.22 to 0.78Total habitat loss 0.00 −0.56 to 0.57 0.43 −0.31 to 1.18Total habitat loss × isolation −0.63 −1.7 to 0.45Correlation between predicted and observed valuesa 0.43∗ 0.60∗∗

aCoefficient of correlation (r) between model-predicted and observed values (correlations significant at P = 0.01 (∗∗) and P = 0.05 (∗),respectively).

area; more heterogeneous areas supported more groups.This highly successful, generalist species is thus unique inbeing able to adapt to different types of areas and occupyvacant ecological niches in smaller fragments created bythe extirpation of other, less flexible species.

The persistence of rhesus macaques in most fragmentscould be due to their tolerance of the matrix and theirability to move between fragments. In contrast, the per-sistence of hoolock gibbons, pig-tailed macaques, andstump-tailed macaques in some of these fragments ap-peared to be negatively affected by the nature of the sur-rounding matrix, constituted predominantly by open agri-culture, which restricted movement of these species. Al-though we did not directly address movement of speciesthrough the matrix, we believe that persistence of thecapped langur and Assamese macaque in certain frag-ments may have been unaffected by the matrix becausethese 2 species sometimes use the vegetation in theseareas and the capped langur, on occasion, colonizes newforest fragments by moving across the matrix (Sharmaet al. 2012a).

The difference in species richness of food trees be-tween a fragment and contiguous forest had the greatesteffect on the number and proportion of extirpated pri-mate species in the fragment. Difference in food speciesrichness also correlated to differences in food tree diver-sity, tree species richness, tree diversity, mean canopycover, and total basal area; together these factors consti-tute habitat structure. The loss of primate species fromthe study fragments can thus be attributed to the loss ofhabitat complexity, as suggested by results from otherstudies (Heinrichs 2011), an effect possibly mediated bythe loss of feeding and sleeping trees, factors criticalfor the survival of primate populations in a fragmentedlandscape.

Our results demonstrate that the isolated fragments ofthe Upper Brahmaputra Valley are truly worth continuedconservation efforts. Many of these fragments have sur-vived 100 years amidst intense human pressure. In onesuch fragment, the Hollongapar Gibbon Wildlife Sanctu-ary, for example, primates have persisted and increasedin abundance despite over 120 years of isolation (Sharma

et al. 2012a). But given recent developments—one-thirdloss of forested area and one-fifth loss of species in allfragments—the future of these primate populations arein jeopardy.

Of the 42 forest fragments we surveyed, 7 have beencleared for human use and the rest have, on average, lostone-third of their original area. The first priority, there-fore, is to arrest further loss of forest in these fragmentsand to strengthen their protection. This is, however, aformidable challenge because legal protection for thesefragments is limited. The second priority is to restoreprimate habitat. Restoration could include increasing theavailability of food trees, particularly of keystone re-sources such as figs and other fast-growing primate foodplants. A lack of funds has limited protection and man-agement of these fragments, but we believe developmen-tal schemes, such as the Indian government’s MahatmaGandhi National Rural Employment Guarantee Act, couldeasily be linked to habitat restoration activities. This actaims to enhance the livelihood security of rural people byguaranteeing employment, and we are optimistic that bylinking it to habitat restoration, the twin goals of habitatconservation and generation of livelihood opportunitiesmay be achieved. Reestablishment of structural connec-tivity between fragments is not logistically feasible giventhe presence of an intensely modified surrounding ma-trix. We, therefore, suggest the reintroduction of speciessuch as the hoolock gibbon, which is negatively affectedby increasing isolation, after ensuring that the originalthreats that led to the extirpation of this species no longerexist and their habitat has been restored.

But, are these goals realistic in India’s current so-cioeconomic and demographic milieu? There are pos-itive signs from similar rainforest remnants in denselysettled production landscapes in the Anamalai Hills ofIndia’s Western Ghats mountains. There, many rainfor-est species, including primates, have persisted and in-creased in abundance in remnant natural areas (Umapa-thy & Kumar 2000; Sridhar et al. 2008) due to effectiveprotection and active restoration efforts (Mudappa & Ra-man 2007). Moreover, initiatives such as the ecologicalcertification of adjoining tea estates (under Sustainable


Sharma et al. 105

Agriculture Network norms) have fostered wildlife-friendly and socially responsible land use outside frag-ments to create more sustainable conservation land-scapes. Landscape and local scale conservation effortsalong similar lines are thus urgently needed to sustainthe rich primate assemblages of the Upper BrahmaputraValley.

Acknowledgments

We thank the Wildlife Conservation Society-India Pro-gram for funding this study and the Assam Forest De-partment for research permits. We especially thank Y.Suryanarayan, G. Chetry, S.K. Seal Sarma, S. Mahapatra,R.K. Gogoi, and other forest officials and guards of theAssam Forest Department without whose help this studywould not have been possible. We are grateful to K.Kakati and D. Chetry for providing valuable inputs onthe distribution records of primates in the study sites. Weacknowledge R. Kumar, U. Srinivasan, and N. Kelkar fortheir help with data analyses, our field-assistant D. Chetryfor assistance during the surveys, and S. Chakraborty,V.V. Robin, S.K. Phukan, R.R. Tariang, N. Hazarika, M.Hazarika, M. Sonowal, and J. Das for their help duringvarious stages of the project.

Supporting Information

Summary statistics of the predictor variables (AppendixS1); Pearson correlation coefficient of predictor vari-ables (Appendix S2 & S3); candidate models for primatespecies richness and abundance of rhesus macaques (Ap-pendix S4), individual primate species (Appendix S5),and number and proportion of extinct primate species(Appendix S6) are available online. The authors are solelyresponsible for the content and functionality of these ma-terials. Queries (other than absence of material) shouldbe directed to the corresponding author.

Literature Cited

Anzures-Dadda, A., and R. Manson. 2007. Patch- and landscape-scaleeffects on howler monkey distribution and abundance in rainforestfragments. Animal Conservation 10:69–76.

Brown, J. H., and A. Kodric-Brown. 1977. Turnover rates in insularbiogeography: effect of immigration on extinction. Ecology 58:445–449.

Burnham, K. P., and D. R. Anderson. 2002. Model selection andmultimodel inference: a practical information-theoretic approach.Springer Verlag, New York.

Champion, H., and S. Seth. 1968. Revised forest types of India. Govern-ment of India Press, New Delhi.

Choudhury, A. 1995. Wildlife survey in Bherjan, Borajan, and PodumoniReserved Forests of Tinsukia District, Assam, with a proposal for awildlife sanctuary. The Rhino Foundation for Nature in North-EastIndia, Guwahati, India.

CIESIN and CIAT (Center for International Earth Science InformationNetwork/Columbia University and Centro Internacional de Agricul-tura Tropical). 2005. Gridded population of the world, Version 3(GPWv3): Population density grid. NASA Socioeconomic Data andApplications Center (SEDAC), Palisades, NY. Available from http://sedac.ciesin.columbia.edu/data/set/gpw-v3-population-density (ac-cessed October 2007).

Cowlishaw, G., and R. Dunbar. 2000. Primate conservation biology.University of Chicago Press, Chicago.

Ewers, R. M., and R. K. Didham. 2006. Confounding factors in thedetection of species responses to habitat fragmentation. BiologicalReviews 81:117–142.

Fleishman, E., C. Ray, P. Sjogren-Gulve, C. L. Boggs, and D. D. Murphy.2002. Assessing the roles of patch quality, area, and isolation in pre-dicting metapopulation dynamics. Conservation Biology 16:706–716.

Garber, P. 1987. Foraging strategies among living primates. Annual Re-view of Anthropology 16:339–364.

Heinrichs, J. A. 2011. The relative influence of habitat quality on popu-lation extinction. PhD thesis, University of Calgary, Calgary.

IUCN (International Union for Conservation of Nature). 2010. IUCNRed List of Threatened Species. Version 2010.4. IUCN, Gland,Switzerland. Available from http://www.iucnredlist.org (accessedMay 2012).

Johnson, J. B., and K. S. Omland. 2004. Model selection in ecol-ogy and evolution. Trends in Ecology and Evolution 19:101–108.

Kakati, K. 2004. Impact of forest fragmentation on the hoolock gibbonin Assam, India. PhD thesis. University of Cambridge, Cambridge,United Kingdom.

Kosmidis, L. 2007. brglm: Bias reduction in binary-response GLMs. Rpackage Version 0.5–4. R Foundation for Statistical Computation,Vienna, Available from http://go.warwick.ac.uk/kosmidis/software(accessed March, 2012).

Krauss, J., R. Bommarco, M. Guardiola, R. K. Heikkinen, A. Helm,M. Kuussaari, R. Lindborg, E. Ockinger, M. Partel, and J. Pino.2010. Habitat fragmentation causes immediate and time-delayedbiodiversity loss at different trophic levels. Ecology Letters 13:597–605.

Kupfer, J. A., G. P. Malanson, and S. B. Franklin. 2006. Not seeingthe ocean for the islands: the mediating influence of matrix-basedprocesses on forest fragmentation effects. Global Ecology and Bio-geography 15:8–20.

Laurance, F. 2008. Theory meets reality: how habitat fragmentationresearch has transcended island biogeographic theory. BiologicalConservation 141:1731–1744.

MacArthur, R. H., and E. O. Wilson. 1967. The theory of island biogeog-raphy. Princeton University Press, Princeton, New Jersey.

Maindonald, J. H., and J. Braun. 2007. Data analysis and graphics usingR: an example-based approach. Cambridge University Press, Cam-bridge, United Kingdom.

Mazerolle, M. J., and M. A. Villard. 1999. Patch characteristics and land-scape context as predictors of species presence and abundance: areview. Ecoscience 6:117–124.

Mbora, D. N. M., and D. B. Meikle. 2004. Forest fragmentation andthe distribution, abundance and conservation of the Tana Riverred colobus (Procolobus rufomitratus). Biological Conservation118:67–77.

Michalski, F., and C. A. Peres. 2005. Anthropogenic determinantsof primate and carnivore local extinctions in a fragmented for-est landscape of southern Amazonia. Biological Conservation 124:383–396.

Mudappa, D., and T. R. S. Raman. 2007. Rainforest restoration andwildlife conservation on private lands in the Valparai plateau, West-ern Ghats, India. Pages 210–240 in G. Shahabuddin, and M. Rangara-jan, editors. Making conservation work. Permanent Black, Ranikhet,India.



Pickett, S. T. A. 1989. Space-for-time substitution as an alternative tolong-term studies. Pages 110–135 in G. E. Likens, editor. Long-termstudies in ecology: approaches and alternatives. Springer-Verlag,New York.

Prugh, L. R., K. E. Hodges, A. R. E. Sinclair, and J. S. Brashares. 2008. Ef-fect of habitat area and isolation on fragmented animal populations.Proceedings of the National Academy of Sciences, USA 105:20770–20775.

R Development Core Team. 2011. R: a language and environmentfor statistical computing . R Foundation for Statistical Computing,Vienna. Available from http://www.R-project.org/ (accessed March2012).

Roonwal, M. L., and S. M. Mohnot. 1977. Primates of south Asia: ecology,sociobiology, and behavior. Harvard University Press, Cambridge,Massachusetts.

Schwarzkopf, L., and A. B. Rylands. 1989. Primate species richnessin relation to habitat structure in Amazonian rainforest fragments.Biological Conservation 48:1–12.

Sharma, N., M. D. Madhusudan, P. Sarkar, M. Bawri, and A. Sinha.2012a. Trends in extinction and persistence of diurnal primatesin the fragmented lowland rainforests of the Upper BrahmaputraValley, north-eastern India. Oryx 46:308–311.

Sharma, N., M. D. Madhusudan, and A. Sinha. 2012b. Socio-economicdrivers of forest cover change in Assam: a historical perspective.Economic and Political Weekly 47:64–72.

Skole, D., and C. Tucker. 1993. Tropical deforestation and habitat frag-mentation in the Amazon: satellite data from 1978 to 1988. Science260:1905–1910.

Solanki, G., A. Kumar, and B. Sharma. 2008. Feeding ecology of Tra-chypithecus pileatus in India. International Journal of Primatology29:173–182.

Sridhar, H., T. R. S. Raman, and D. Mudappa. 2008. Mammal persistenceand abundance in tropical rainforest remnants in the southern West-ern Ghats, India. Current Science 94:748–757.

Srivastava, A. 1999. Primates of northeast India. Megadiversity Press,Bikaner, India.

Turner, I. M. 1996. Species loss in fragments of tropical rain forest: areview of the evidence. Journal of Applied Ecology 33:200–209.

Umapathy, G., and A. Kumar. 2000. The occurrence of arboreal mam-mals in the rain forest fragments in the Anamalai Hills, south India.Biological Conservation 92:311–319.

USGS (U.S. Geological Survey) Reprocessing by the GLCF. 2007. USGS,Global Land Cover Facility, College Park, Maryland. Available fromhttp://glcf.umd.edu/ (accessed March 2011).

Wilcove, D. S., C. H. McLellan, and A. P. Dobson. 1986. Habitat fragmen-tation in the temperate zone. Pages 237–256 in M. E. Soule, editor.Conservation biology: the science of scarcity and diversity. SinauerAssociates, Sunderland, Massachusetts.

Zheng, B., and A. Agresti. 2000. Summarizing the predictive power ofa generalized linear model. Statistics in Medicine 19:1771–1781.


Documents

Local and Landscape Correlates of Primate Distribution and ......fragmentos de bosque tropical lluvioso en el Valle del Alto Brahmaputra, noreste de India. En promedio, los fragmentos