Contributed Paper Local and Landscape Correlates of Distribution and Persistence in the Remnant Lowland Rainforests of the Upper Brahmaputra Valley, Northeastern

NARAYAN SHARMA,∗†‡M.D.MADHUSUDAN,∗†ANDANINDYASINHA∗†

∗Ecology, Behaviour and Conservation Programme and School of Natural Sciences and Engineering, National Institute of Advanced Studies, 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 densely settled 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 conservation opportunities? We evaluated, using generalized linear models in an information-theoretic framework, the effect of local- and landscape-scale factors on the richness, abundance, distribution, and local extinction of 6 primate species in 42 lowland tropical rainforest fragments of the Upper Brahmaputra Valley, northeastern India. On average, the forest fragments lost at least one species in the last 30 years but retained half their original species complement. Species richness declined as proportion of habitat lost increased but was not significantly affected by fragment size and isolation. The occurrence of western hoolock gibbon (Hoolock hoolock) and capped langur (Trachypithecus pileatus) in fragments was inversely related to their isolation and loss of habitat, respectively. Fragment area determined stump-tailed (Macaca arctoides) and northern pig-tailed macaque occurrence (Macaca leonina). Assamese macaque (Macaca assamensis)distributionwas affected negatively by illegal tree felling, and rhesus macaque (Macaca mulatta) abundance increased as habitat heterogeneity increased. Primate extinction in a fragment was primarily governed by the extent of divergence in its food tree species richness from that in contiguous forests. We suggest the conservation value of these fragments is high because collectively they retained the entire original species pool and individually retained 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 primate assemblage.

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 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 habitat´ a las poblaciones de muchas especies. ¿Qu´e tan rentable es invertir recursos escasos en la conservacion´ de remanentes de habitat´ inmersos en paisajes densamente poblados? ¿Los fragmentos estan´ destinados a perder especies de todos modos? Si no, ¿hay otros factores ecologicos,´ antropog´enicos y relacionados con las especies

‡Address for correspondence: Ecology, Behaviour and Conservation Programme and School of Natural Sciences and Engineering, National Institute of Advanced Studies, Bangalore, India, email [email protected] Paper submitted October 6, 2012; revised manuscript accepted May 29, 2013. 95 Conservation Biology,Volume28,No.1,95–106 C 2013 Society for Conservation Biology ⃝ DOI: 10.1111/cobi.12159 96 Primate Distribution in Forest Fragments que mitigan el efecto de la fragmentacion´ y ofrecen oportunidades de conservacion?´ Evaluamos, mediante modelos lineales generalizados enmarcados en teor´ıa de la informacion,´ el efecto de factores a escala local y de paisaje sobre la riqueza, abundancia, distribucion´ y extincion´ local de 6 especies de primates en 42 fragmentos de bosque tropical lluvioso en el Valle del Alto Brahmaputra, noreste de India. En promedio, los fragmentos de bosque perdieron por lo menos una especie en los ultimos´ 30 anos˜ pero retuvieron la mitad de su complemento de especies original. La riqueza de especies declino´ en proporcion´ al habitat´ perdido, pero no fue afectada significativamente por el tamano˜ y aislamiento del fragmento. La ocurrencia Hoolock hoolock y Trachypithecus pileatus en fragmentos se relacionoinversamenteconelaislamientoyp´ ´erdida de habitat,´ respectivamente. El area´ del fragmento determino´ la ocurrencia de Macaca arctoides y Macaca leonina. La distribucion´ de Macaca assamensis fue afectada negativamente por la tala illegal, y la abundancia de Macaca mulatta incremento´ a medida que incremento´ la heterogeneidad del habitat.´ La extincion´ de primates en un fragmento se rigio´ fundamentalmente por el grado de divergencia en la riqueza de especies de arboles´ que le sirven de alimento en relacion´ con los bosques contiguos. Sugerimos que el valor de conservacion´ de estos fragmentos es alto porque colectivamente retuvieron al conjunto original de especies e individualmente retuvieron la mitad, aun un siglo despu´es de la fragmentacion.´ Sin embargo, debido a p´erdida extensiva de habitat´ y especies, estos fragmentos requieren urgentemente de proteccion´ y restauracion´ ecologica´ activa para sustentar este rico ensamble de primates.

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

Introduction onomic groups as well (e.g., Mazerolle & Villard 1999; Michalski & Peres 2005; Sridhar et al. 2008). Moreover, Tropical forests have undergone extensive loss and frag- the persistence of populations in fragmented terrestrial mentation (Skole & Tucker 1993), but many of these islands depends heavily on the intervening habitat ma- fragments, although variable in size and isolation, are trix (Michalski & Peres 2005; Ewers & Didham 2006), the last refuge of numerous forest-dependent species in which is seldom homogeneous (Kupfer et al. 2006) or human-modified landscapes (Wilcove et al. 1986). One completely hostile to species, whose tolerances of such of the groups most severely affected by forest fragmenta- a matrix may vary considerably (Ewers & Didham 2006). tion and loss are primates, most of which are forest de- Conservation practitioners and managers, especially in pendent and highly vulnerable to environmental change the tropics, often question how worthwhile it is to invest (Cowlishaw & Dunbar 2000). Nearly half of all primate in the conservation of habitat remnants. Are they a lost species are threatened by habitat loss, fragmentation, cause, fated to lose species anyway, given their small size, and hunting (IUCN 2010). With the growing extinction relatively high isolation, and continuing land-use change? risk due to habitat fragmentation (Turner 1996; Krauss To what extent can other ecological, anthropogenic, and et al. 2010), knowledge-based conservation strategies for species-related factors mitigate the effects of size and iso- species populations in fragmented landscapes are an ur- lation and offer management opportunities that prevent gent need. the further extirpation of species and effectively conserve The theory of island biogeography (MacArthur & them? Wilson 1967) has often been used as a conceptual frame- We examined these questions by studying primates, work to understand the community-level consequences aforest-dependentgrouplikelytobedisproportionately of habitat fragmentation. By treating habitat fragments affected by fragmentation, in the Upper Brahmaputra Val- as analogous to oceanic islands, this theory predicts that ley in northeastern India, within the Indo-Burma global the species richness in a fragment is determined by a dy- biodiversity hotspot, where lowland rainforest fragments namic equilibrium between extinction and colonization were created over a century ago. Even after years of frag- rates, both functions of its size and isolation. However, mentation and loss, these fragments, which differ in size in reality, the theory does not account for certain mecha- and isolation, have retained different fractions of their nisms governing species distribution in terrestrial habitat original primate species pool (Sharma et al. 2012a). islands (Laurance 2008). For instance, in addition to—or We explored how local and landscape factors affect pri- independent of—area and isolation (Prugh et al. 2008), mate species richness, abundance, and distribution and variables such as habitat quality and anthropogenic fac- temporal changes in a fragment’s spatial and vegetational tors are key determinants of species composition, abun- attributes affect primate persistence and extinction. We dance, and distribution in habitat fragments not only for then examined the implications of our findings for the primates (e.g., Mbora & Meikle 2004; Michalski & Peres conservation and management of primates in the frag- 2005; Anzures-Dadda & Manson 2007) but for other tax- ments of such a landscape.

Conservation Biology Volume 28, No. 1, 2014 Sharma et al. 97

Figure 1. Locations of the study fragments in the Upper Brahmaputra Valley in , 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 Seven primate species that vary considerably in their ecology—the rhesus macaque (Macaca mulatta),north- Study Area ern pig-tailed macaque (Macaca leonina), Assamese macaque , stump-tailed macaque Our study site was in the floodplains south of the river (Macaca assamensis) ,westernhoolockgibbon Brahmaputra in the Indian state of Assam (Fig. 1). The (Macaca arctoides) (Hoolock ,cappedlangur ,and original vegetation was mainly wet evergreen forests hoolock) (Trachypithecus pileatus) Bengal slow loris (Nycticebus bengalensis)—co-occur in of the Dipterocarpus-Mesua series (Champion & Seth these forests. Of these, we collected data on the first 6 1968). The history of this landscape is complex. Over species, which are diurnal, but not on the nocturnal slow 2 centuries, until the late 1990s, there has been heavy loris because our surveys were conducted during daylight deforestation for agriculture and settlements and for ex- hours. The rhesus macaque is a diet and habitat general- traction of timber from forests reserved for such harvest ist, as is the Assamese macaque, which are both better- (Sharma et al. 2012b). Today, the remnant lowland rain- adapted to human-modified landscapes than the pig-tailed forests occur as fragments of different sizes spread across and stump-tailed macaques, capped langurs and hoolock the region (Fig. 1). gibbons, all of which are restricted to the forest interiors

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(Roonwal & Mohnot 1977). Barring the predominantly (0600–1000) or before dusk (1400–1600), when the pri- terrestrial stump-tailed and rhesus macaques, all the pri- mates were most active, at approximately 2 km/h. We mates are mostly arboreal, with the hoolock gibbon be- stopped periodically to scan the canopy and to listen for ing entirely so. The capped langur is mainly folivorous primate presence. On detection, we identified species, (Solanki et al. 2008), whereas the remaining species are enumerated groups, and categorized individuals by age primarily frugivorous (Roonwal & Mohnot 1977). Insects and sex. We computed fragment-wise encounter rates and roots, however, constitute a significant part of pig- only for rhesus macaques because this species did not tailed and stump-tailed macaque diets, respectively (N.S., avoid us. For all other species, some of which could po- personal observation). The diets of these species differ, tentially have avoided areas of human activity including however, and may change seasonally or in response to human-created trails, we assessed occurrence rather than other changes in food availability. abundance. There are considerable differences among these We also gathered information on the occurrence of all species in their ability to use the matrix habitat. Among primates, except the nocturnal slow loris, and assessed the macaques, we observed the rhesus macaque was the their distribution and extinction events in the fragments most versatile in terms of its use of the surrounding habi- on the basis of key-informant surveys (n 48, 1–2 inter- tats. The rhesus macaque, and to a limited extent the As- views/fragment) in the adjoining villages.= We selected samese macaque, even moved across open paddy fields. local informants who reliably recognized the primate The pig-tailed and stump-tailed macaques, on the other species, were long-term (>30 years) residents of the area, hand, were rarely seen outside fragments. The capped and frequently visited the adjacent forests. Two local langurs were able to use scattered trees in the adjacent primatologists helped us cross-verify the distribution of agricultural fields and plantations for foraging and occa- different primate species in the fragments. We prepared sionally as sleeping sites. The hoolock gibbon was rarely the final species occurrence data for each fragment after observed visiting specific food trees in the surrounding aggregating data from all sources. matrix, but only if there was a structural connectivity We walked 158 trails (2–20 trails/fragment) for a total between these trees and the forest fragments. distance of 484 km (6.4–74.4 km/fragment). The number of trails and sampling effort were proportional to frag- ment area (r 0.78, P < 0.001 and r 0.53, P < 0.01, Site Selection respectively).= = We analyzed data from 25 of the 42 rainforest fragments surveyed in the Tinsukia and Dibrugarh Forest Divisions of the state (Fig. 1). These ranged in size from 1.4 to 233 Fragment and Landscape Characteristics km2. They were created approximately 100 years ago (Sharma et al. 2012a,2012b). We defined a fragment as We characterized each fragment by measuring its spatial a forest patch separated from other such forest patches (forested area), ecological (tree species richness, canopy on an ecological timescale by a river, tea plantation, agri- cover, and tree basal area) and anthropogenic (illegal tree cultural field, human settlement, or degraded secondary felling and habitat loss) attributes. We used a combination vegetation that prevented easy movement of primates of high-resolution satellite images (large fragments) and across them. Fifteen fragments were completely isolated ground-based geographic position system (GPS) surveys in terms of their structural connectivity rather than their (small fragments) to estimate actual forested area. In each biological permeability, as determined by their presence fragment, we measured all vegetation variables in circular in a simple matrix such as that of open agriculture. Nine plots with a 10-m radius (2–37 plots/fragment) located fragments were separated from one another by a river, regularly 15 m apart to the left and right, alternately, of and one was connected to the nearest contiguous forest each trail. All trees with stems 10 cm cbh (circumfer- through a narrow corridor of secondary vegetation. We ence at breast height) were identified≥ and counted on designated 3 fragments as control sites on the basis of each plot. These measurements were summarized into their size (>100 km2), continuity, and relatively intact estimates of tree species richness, diversity, and basal area forest cover. Of the 17 fragments omitted from analyses, for each fragment. We based our estimates of species rich- 7 fragments had been completely cleared and their pri- ness, abundance, species diversity, and basal area of food mates extirpated, and the remainder proved difficult to trees for each primate species and all primates taken to- survey. gether on published literature and our own observations. Canopy cover was assessed at every 100 m along the trail and on each plot with a modified ordinal 5-point scale Primate Surveys following Kakati (2004). Canopy-cover points from plots Between August 2006 and January 2007, we used ex- were averaged to yield a canopy cover score for each isting (e.g., elephant) and human trails to sur- fragment. We also used the coefficient of variation (CV) vey fragments. We walked each trail once, after dawn of the canopy cover rank (estimated at regular intervals

Conservation Biology Volume 28, No. 1, 2014 Sharma et al. 99 Species loss e. Primate number proportion . c (individual/km) CL HG AM PTM RM STM richness lost(in%) b )fragments 2 (km a Encounter rate, distribution, richness, and extinction of primates in forest fragments of the Upper Brahmaputra Valley, Assam, northeastern India Abbreviations: UDEB, Upper Dehing (East Block); UDWB, Upper Dehing (West Block). Abbreviations: OA, open agriculture; RIV, river; SF, secondary forest. Abbreviations: AM, Assamese macaque; CL, capped langur; HG, hoolock gibbon; PTM, pig-tailed macaque; RM, rhesus macaque; STM, stump-tailed macaqu Table 1. Fragment code1234567 Buridehing8 Dangori9Jokai12.51OA3.87AAPAPA200 Dehingmukh10 Deopani11 area Doomdooma12 Duarmara13 Hahakhati separating 214 Hollogaon 20.7915 rhesus16 macaques 29.71 Joypur17 10.92 Kakojan18 24.07 Kotha19 OA Kukuramara 2.720 Kumsong OA 6.5821 Kundilkalia OA 2.7422 Mesaki OA 3.2523 Namdang RIV24 Sadia Station North Block OA25 132.7 Sadia 0.42 Station 21.73 West RIV Block Tarani 3.67a 5.37 12.61 OA Telpanib 0.23 8.35 Tinkopani-Namphaic 1.35 7.29 1.42 7.75 Tokowani RIV P RIV 0.00 UDEB Forest A OA Complex OA 10.19 P UDWB 0.00 1.79 Forest A Complex 1.85 OA 45.48 A P OA OA RIV P 1.24 P 112.05 233.19 P A P P P RIV 12.84 0.00 P OA 0.62 A A 4.43 A P SF 0.27 A 0.00 4.98 A A P RIV A P RIV P 0.46 P P A 2.54 2.08 0.00 A P P OA P A P A P OA A A A A P A 0.00 RIV P A P 2.81 P A P A A 0.00 A A P 5 P A 0.00 P A P 0.23 2 A A A A P P P A 3 P A P 0.97 A A A 5 A A P A A 0.71 A P P P P 1 0 3.15 A P A P A P A 1 A P P 2 A P P A 3 2 A P P P P 2 A P P A A P 0 A P A P P P 0 A 1 A A 33 A P A P 6 P 1 P P 5 P 40 P 2 P 2 1 P A 0 0 P P P A 2 P 50 1 A 3 2 P P P 33 P 0 P 0 40 P 2 1 1 1 0 P A 1 A 6 1 2 6 0 A 6 0 0 33 50 2 5 0 2 33 50 40 0 5 0 0 0 50 0 0 0 0 0 0 0 0 0 0 Fragment Forested Feature Encounter rate of Presence (P) or absence (A) in Fig. 1 Study site

Conservation Biology Volume 28, No. 1, 2014 100 Primate Distribution in Forest Fragments

Table 2. Model-averaged estimates of coefficients with 95% confidence Although traditional hunting is widespread in north- intervals for landscape and local variables affecting primate species eastern India, it was relatively low in our study areas richness. owing to taboos against hunting primates. Yet, we were Variable Coefficient 95% CI unable to completely rule out occasional incidents of surreptitious hunting. We, therefore, used primate oc- Intercept 1.09 0.82 to 1.36 currence rather than primate abundance as the response Forested area 0.24 0.16 to 0.64 Proportion of habitat loss 0.32 −0.62 to 0.02 variable because it would be less sensitive to the possible Illegal tree felling −0.35 −0.78 to 0.08− occurrence of occasional hunting. Distance to nearest forest −0.27 −0.66 to 0.11 To understand the extent to which fragmentation- Forested area distance to −0.41 −0.71 to 1.53 × − mediated physical and vegetation changes of a fragment nearest forest affected local extinction of primate species over the last Correlation between predicted 0.80∗∗ and observed valuesa 30 years, we estimated changes in the physical and vege- aCoefficient of correlation (r) between model-predicted and observed tation attributes of the fragments over this period. values (∗∗correlations significant at P 0.01). To calculate change in fragment area, we used the = original gazetted area and present habitat area of the frag- ment. We calculated percent change per year from the along the trails) as a measure of horizontal heterogeneity habitat area obtained for each fragment through Landsat of canopy cover. Multispectral Scanner, Thematic Mapper, and Enhanced We estimated illegal tree felling as the encounter rate Thematic Mapper images of 1973, 1976, 1988, and 1990 along trails of cut tree stumps 30 cm cbh that had been (USGS 2007). We also measured changes in physical iso- felled within approximately the≥ previous year. Net habi- lation of these fragments from contiguous forests (i.e., tat loss was estimated by comparing the original gazetted fragments >100 km2)fromthesemaps.Giventhathis- area of each fragment with the current forested area torical changes in vegetation structure and composition and computing the proportion of habitat lost in each were difficult to obtain, we used an alternative space-for- fragment. time substitution approach (Pickett 1989) to assess such The 22 fragments ranged from 1.35 to 45 km2,whereas changes. We thus assumed that all fragments in the re- the 3 control sites ranged from 112 to 233 km2 (Table 2). gion, having been derived from contiguous forests, were We sampled 356 plots for vegetation in the 25 fragments. similar to them in terms of vegetation characteristics prior The number of plots in a fragment (4–37) was propor- to isolation. The values of tree species richness, diversity, tional to the size of the fragment (r 0.49, P 0.01). canopy cover, CV of canopy cover, and tree and food We measured 4730 stems in plots, of= which 129= were tree basal area were calculated for each fragment and unidentified. Besides on the vegetation plots, the canopy subtracted from the corresponding values of continuous cover was also assessed in 2592 plots along the trails. forests. We assumed these differences represented the We also evaluated the spatial, ecological, and anthro- extent to which a given fragment had diverged over time pogenic characteristics of the broader landscape sur- from a primary forest in terms of its vegetation. rounding a fragment to examine the effect of habitat frag- mentation on the community and population attributes of the primates. First, we quantified the spatial isolation Primate Extinctions of a fragment from its nearest fragment and its nearest contiguous forest with GIS data and characterized the We defined species extirpation as the unambiguous ab- dominant matrix type surrounding each fragment with sence of a species that had been reported 30 years ago satellite imagery. Of the 25 fragments, 24 were dominated within a fragment but which had not been seen, heard, by open agriculture (paddy and tea) that lacked a tree or otherwise detected up to the time of the survey by the canopy. The matrix of the remaining fragment largely key informants (Sharma et al. 2012a). In case of differ- comprised a human settlement. Given the consistency ences between informants from the same area, we used in the type of landscape matrix across fragments, we the most conservative scenario. We used these data to believe that our design allowed us to hold the effects compute the number and proportion of primate species of matrix constant and precisely address the effects of lost in each fragment over time. other landscape and local factors on primate distribution and abundance. We considered the human population Statistical Analyses density surrounding each fragment an important anthro- pogenic feature. This parameter was extracted for a 5- From the literature and our own observations, we identi- km buffer around each fragment from the Gridded Pop- fied 39 landscape and local variables (habitat and anthro- ulation of the World (version 3) (CIESIN & CIAT 2005) pogenic [Supporting Information]) that could potentially derived from the Census of India (Government of India affect community and population attributes of all the 2001). primates. From among these variables and on the basis

Conservation Biology Volume 28, No. 1, 2014 Sharma et al. 101 of previous work (Roonwal & Mohnot 1977; Srivastava Results 1999; Kakati 2004; Solanki et al. 2008) on primates and on established ecological mechanisms, we selected those Primates in the Study Sites variables that could affect the occurrence, species rich- We encountered 42 groups of rhesus macaques (min- ness, and abundance of primates. We also identified 12 imum 450 individuals), 40 groups of hoolock gibbons local and landscape variables, changes in which could (minimum 129 individuals), 14 groups of Assamese affect primate extirpation in a fragment. Before model macaques (minimum 94 individuals), 8 groups of capped fitting, we examined all variables for multicollinearity, langurs (minimum 68 individuals), and 2 groups of pig- and from within each pair of highly correlated variables tailed macaques (minimum 21 individuals). We did not we retained the more ecologically meaningful one in a detect stump-tailed macaques, although secondary infor- particular context. Most of the independent variables mation (e.g., questionnaires) confirmed their presence in were highly correlated (Supporting Information). 4 relatively large forest fragments. To identify important local and landscape factors that Mean primate species richness in fragments was 3.2 affect richness, abundance, and species distribution, (SD 1.79, range 1–6). Half the fragments retained over we used generalized linear models (GLMs), which are 50% of the original species pool of the region, whereas suited for modeling nonnormal data (Maindonald & Braun the other half contained 1–2 species. Mean species rich- 2007). We also used GLMs to identify factors affecting pri- ness was highest (mean [SD] 6 [0]) in large fragments mate extinction in fragments. All predictor variables were (>45 km2, n 4), intermediate= (3.37 [1.66]) in medium- centered and scaled to have zero means and unit standard sized fragments= (10–45 km2, n 9), and low (2.17 [1.1]) deviations before fitting models in order to make the in the smaller fragments (<10 km= 2, n 12) (Table 1). variables mutually comparable. From the primate natural Approximately 57% of the fragments= retained their history and ecology literature, and our own observations, original species pool of 30 years ago, whereas 1 or 2 we built a set of a priori candidate models with differ- species were extirpated from the remaining fragments. ent combinations of local and landscape variables and On average a fragment lost at least one of its primate their most important interactions as predictor variables species over these 30 years (Table 1). The proportion of and measures of primate occurrence, species richness, species loss was highest (mean [SD] 23.25 [21.28]) in and abundance as response variables. For the response the smaller fragments (<10 km2)andrelativelylower= variables primate species richness, rhesus macaque en- (19.22 [23.35]) in midsized fragments (10–30 km2), counter rates, and number of extinct primates in a frag- whereas the large fragments did not lose any species. ment we used a Poisson error structure with log-link func- On average, a fragment lost a one-third of its forested tion. Because the occurrence data of individual species area over the last century. About 16% of the fragments lost were zero-inflated, we used bias-reduced GLMs (Kosmidis over three-fourths of their original forest, whereas 12% 2007) that involved binomial error structure and log-link and 24% of fragments have been reduced to over one-half function for these analyses. To evaluate the factors af- and one-fourth of their original size, respectively. fecting primate extirpation, we considered the number of species currently present as successes and the number of species lost as failures and used their values in com- Variables Affecting Species Richness and Presence bination as the response variable. We assume a binomial error structure with log-link function for these models. We compared 12 candidate GLMs for primate species We analyzed and ranked candidate models on the basis richness as a function of local and landscape factors. of Akaike information criterion (AIC). We used Akaike The 3 best models had habitat loss as a key explanatory weights to identify a set of confidence models, which variable (Supporting Information). The model-averaged cumulatively contributed at least 0.95 to the weight of parameter estimates showed that primate species rich- evidence (Burnham & Anderson 2002). Landscape and ness declined as habitat loss increased (Table 2). Primate local factors that affected primate community and pop- species richness was also negatively related to illegal tree ulation attributes and primate extinction were inferred felling, although the 95% CI of its model-averaged param- by evaluating model-averaged estimates of their coeffi- eter estimate marginally overlapped zero. cients from the above set of confidence models (John- The GLM analyses of the distribution of the 5 primate son & Omland 2004). We assessed model fit by corre- species were conducted as a function of the local and lating model-predicted values of primate community and landscape variables of a fragment (Table 3). Both the population attributes and primate extinction and corre- best-fit model (Supporting Information) and the model- sponding observed values (Zheng & Agresti 2000). All averaged coefficient showed that the likelihood of occur- analyses were carried out with the statistical software R rence of hoolock gibbons increased with greater prox- (version 2.12.2) (R Development Core Team 2011). The imity to the nearest forest. The proportion of habitat bias-reduced GLM analysis was conducted with the aid of lost appeared in the first 4 best models that described the brglm package (Kosmidis 2007). the occurrence of capped langur, the model-averaged

Conservation Biology Volume 28, No. 1, 2014 102 Primate Distribution in Forest Fragments 0.57 to 0.31 0.05 to 0.77 2.21 to 0.36 0.59 to 0.47 0.34 to 0.48 33 − − − − − 0.13 0.93 0.06 0.34 0.03 to 0.66 0.07 − − − ∗∗ 2.05 to 1.920.94 to 1.76 0.36 3.73 to 0.90 2.00 to 16.12 lprimatespeciesandencounterrateof − − − − 0.97 0.07 1.41 − − 0.85 0.41 − ∗∗ 1.35 to 1.87 1.40 to 1.39 7.06 2.90 to 0.94 12.54 to − − − 0.85 − 6.69 0.98 0.01). − − = ∗∗ 3.01 to 0.67 0.26 6.22 to 1.27 2.60 to 6.03 4.40 to 0.74 9.63 to 6.12 1.00 to 0.80 2.55 to 19.73 0.00 − − − − − − − 0.90 1.17 2.47 1.83 1.76 0.10 − − − − − , correlations significant at P ∗∗ 0.09 − ∗∗ 6.25 to 0.87 3.03 to 7.10 8.59 3.15 to 1.24 1.71 0.80 to 1.51 3.63 to − − − − − 0.77 1.77 2.69 0.95 0.35 − − − 0.07 − ∗∗ 1.85 to 0.21 1.05 to 0.99 1.94 to 2.81 2.04 0.39 to 1.70 3.74 to 4.16 2.41 to − − − − − − 0.69 occurrence occurrence occurrence occurrence occurrence rhesus macaque Hoolock gibbon Capped langur Pig-tailed macaque Assamese macaque Stump-tailed macaque Encounter rate of 1.24 0.82 0.03 0.21 − − − distance × Model-averaged estimates of coefficients (coeff) with 95% confidence intervals for landscape and local variables affecting occurrence of individua a canopy cover macaque food plants langur food plants predicted and observed values density to nearest forest Coefficient of correlation (r) between model-predicted and observed values ( Distance to nearest forest Basal area of pig-tailed Proportion of habitat loss Illegal tree felling Coefficient of variance of Basal area of capped Forested area 0.44 Correlation between Human population a VariableIntercept coeff 0.66 95% CI coeff 95% CI coeff 95% CI coeff 95% CI coeff 95% CI coeff 95% CI Table 3. Forested area rhesus macaques.

Conservation Biology Volume 28, No. 1, 2014 Sharma et al. 103 coefficient indicated its likelihood of occurrence de- with higher illegal tree felling lost the most primate creased in fragments with greater habitat loss. Forested species. The occurrence of some species such as the area appeared in the 3 best models and seemed to pos- Assamese macaque was also negatively affected by illegal itively affect the likelihood of occurrence of the pig- tree felling. Historically, these fragments were logged for tailed macaque, although the model-averaged coefficients timber until it became illegal in 1996. Small-scale illegal were not significant. The likelihood of occurrence of As- felling continues to degrade habitat quality by reducing samese macaques was negatively affected by illegal tree the availability of important food plants of primates (N.S., felling, whereas that of stump-tailed macaques was best personal observation) and by disrupting canopy continu- explained by the model that included forested area (Sup- ity vital for arboreal primates. New canopy openings and porting Information). The model-averaged coefficients edge creation may also facilitate the spread of invasive suggested, although results were not significant, likeli- plants, which, in turn, could alter the original tree com- hood of occurrence of the latter species increased as position and diversity of a fragment. fragment area increased. All the predicted models for the The likelihood of occurrence of hoolock gibbons, one 5 primate species showed significant correlation with the of the most threatened primates in these fragments in- observed values. creased with proximity of the fragment to contiguous We did not use the GLMs to explain variation in rhesus forests or another fragment. For these arboreal primates macaque occurrence because the species was present in that rarely move across fragments and may not cross gaps all fragments. Instead, we compared 8 GLMs to explain even as small as 200 m (Choudhury 1995), the mean the variation in encounter rates of rhesus macaques as a distance of 2.51 km between our study fragments could function of both local and landscape variables. Although become critical for their survival. Given the crucial im- forested area was the best-fit model (Supporting Infor- portance of animal movement in governing species distri- mation), an examination of the model-weighted parame- butions in fragmented landscapes (Fleishman et al. 2002) ter estimates showed a positive effect of CV of canopy and in preventing extirpation by the rescue effect (Brown cover and proportion of habitat loss on the abundance of & Kodric-Brown 1977), such small, completely isolated rhesus macaques (Table 2). The model-predicted value, populations of hoolock gibbons are likely to be extremely however, showed only a weak correlation. vulnerable to stochastic extinctions arising from demo- graphic, genetic, or environmental factors. The only colobine primate in our study area, the Variables Affecting Number and Proportion of Extirpated capped langur, was extirpated from fragments that lost Species over half their original forested area over the last cen- We compared 9 candidate GLMs each for the number tury. Folivorous primates, including the capped langur and proportion of extinct species as a function of puta- (Solanki et al. 2008), require diverse food plants in order tive changes in local and landscape characteristics of the to limit the intake and accumulation of harmful secondary fragments. The difference in food tree species richness compounds (Garber 1987). The diversity of capped lan- appeared to be a key factor in both sets of models. The gur food trees was lower in fragments that had lost 50% model-averaged parameter estimates indicated the differ- of their forest relative to sites that had lost approximately ence in food tree species richness was the single-most im- 10% of their forest. portant factor affecting the proportion of primate species None of the model coefficient values explained the dis- lost from the sites (Table 4). The model-predicted values tribution of pig-tailed macaques, although forested area, of the number of extinct primates, however, showed a distance to the nearest forest, and interactions of these weak correlation with the observed values. variables contributed to the most likely model. Larger fragments may support this primate because they con- tain more food species and intact canopy cover, critical Discussion survival components for this arboreal species. Distance to the nearest forest may also be important to the lo- Our results indicate that primate species richness has cal persistence for this species because it can promote declined severely in the lowland rainforest fragments of dispersal among fragments. the Upper Brahmaputra Valley because these fragments The most important variable affecting stump-tailed have lost, on average, one-third of their forested area over macaque distribution was forested area. Given its large the last century. Such extensive anthropogenic forest home range (400–900 ha in one fragment, the Hollon- loss has reduced the total area of forest fragments, in- gapar Gibbon Wildlife Sanctuary [Sharma et al. 2012a]), creased their isolation, and, as predicted by the theory of smaller fragments may not support populations of this island biogeography, apparently led to a decline in species, as has been reported for other wide-ranging species richness. Neotropical primates (Schwarzkopf & Rylands 1989). High levels of illegal tree felling appeared to be asso- Abundance of rhesus macaques was affected positively ciated with lower primate species richness; fragments by canopy cover heterogeneity and negatively by forested

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Table 4. Model-averaged estimates of coefficients (coef) with 95% confidence intervals for putative changes in the local and landscape variables affecting 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 0.85 Difference in coefficient of variation of canopy cover− 0.09 −0.46 to 0.63− 0.23 −0.49 to− 0.95 Differenceinfoodtreerichness 0.67 −0.02 to 1.37 1.15− 0.23 to 2.07 Isolation 0.17 −0.92 to 0.58 0.22 1.22 to 0.78 Total habitat loss− 0.00 −0.56 to 0.57− 0.43 −0.31 to 1.18 Total habitat loss isolation − 0.63 −1.7 to 0.45 × a − − Correlation between predicted and observed values 0.43∗ 0.60∗∗ a Coefficient of correlation (r) between model-predicted and observed values (correlations significant at P 0.01 (∗∗)andP 0.05 (∗), respectively). = = area; more heterogeneous areas supported more groups. et al. 2012a). But given recent developments—one-third This highly successful, generalist species is thus unique in loss of forested area and one-fifth loss of species in all being able to adapt to different types of areas and occupy fragments—the future of these primate populations are vacant ecological niches in smaller fragments created by in jeopardy. the extirpation of other, less flexible species. Of the 42 forest fragments we surveyed, 7 have been The persistence of rhesus macaques in most fragments cleared for human use and the rest have, on average, lost could be due to their tolerance of the matrix and their one-third of their original area. The first priority, there- ability to move between fragments. In contrast, the per- fore, is to arrest further loss of forest in these fragments sistence of hoolock gibbons, pig-tailed macaques, and and to strengthen their protection. This is, however, a stump-tailed macaques in some of these fragments ap- formidable challenge because legal protection for these peared to be negatively affected by the nature of the sur- fragments is limited. The second priority is to restore rounding matrix, constituted predominantly by open agri- primate habitat. Restoration could include increasing the culture, which restricted movement of these species. Al- availability of food trees, particularly of keystone re- though we did not directly address movement of species sources such as figs and other fast-growing primate food through the matrix, we believe that persistence of the plants. A lack of funds has limited protection and man- capped langur and Assamese macaque in certain frag- agement of these fragments, but we believe developmen- ments may have been unaffected by the matrix because tal schemes, such as the Indian government’s Mahatma these 2 species sometimes use the vegetation in these Gandhi National Rural Employment Guarantee Act, could areas and the capped langur, on occasion, colonizes new easily be linked to habitat restoration activities. This act forest fragments by moving across the matrix (Sharma aims to enhance the livelihood security of rural people by et al. 2012a). guaranteeing employment, and we are optimistic that by The difference in species richness of food trees be- linking it to habitat restoration, the twin goals of habitat tween a fragment and contiguous forest had the greatest conservation and generation of livelihood opportunities effect on the number and proportion of extirpated pri- may be achieved. Reestablishment of structural connec- mate species in the fragment. Difference in food species tivity between fragments is not logistically feasible given richness also correlated to differences in food tree diver- the presence of an intensely modified surrounding ma- sity, tree species richness, tree diversity, mean canopy trix. We, therefore, suggest the reintroduction of species cover, and total basal area; together these factors consti- such as the hoolock gibbon, which is negatively affected tute habitat structure. The loss of primate species from by increasing isolation, after ensuring that the original the study fragments can thus be attributed to the loss of threats that led to the extirpation of this species no longer habitat complexity, as suggested by results from other exist and their habitat has been restored. studies (Heinrichs 2011), an effect possibly mediated by But, are these goals realistic in India’s current so- the loss of feeding and sleeping trees, factors critical cioeconomic and demographic milieu? There are pos- for the survival of primate populations in a fragmented itive signs from similar rainforest remnants in densely landscape. settled production landscapes in the Anamalai Hills of Our results demonstrate that the isolated fragments of India’s Western Ghats mountains. There, many rainfor- the Upper Brahmaputra Valley are truly worth continued est species, including primates, have persisted and in- conservation efforts. Many of these fragments have sur- creased in abundance in remnant natural areas (Umapa- vived 100 years amidst intense human pressure. In one thy & Kumar 2000; Sridhar et al. 2008) due to effective such fragment, the Hollongapar Gibbon Wildlife Sanctu- protection and active restoration efforts (Mudappa & Ra- ary, for example, primates have persisted and increased man 2007). Moreover, initiatives such as the ecological in abundance despite over 120 years of isolation (Sharma certification of adjoining tea estates (under Sustainable

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