Introduction
Continuing, large-scale biodiversity loss is a global conservation concern and represents a major challenge for the 21st century (Butchart et al., Reference Butchart, Walpole, Collen, Van Strien, Scharlemann and Almond2010). Despite international conventions to overcome this challenge (Thomsen & Willerslev, Reference Thomsen and Willerslev2015), the dearth of information on the status and distribution of species impedes effective conservation and prioritization. Over the past few decades, anthropogenic land-cover changes have resulted in declining populations of many species (Butchart et al., Reference Butchart, Walpole, Collen, Van Strien, Scharlemann and Almond2010), with the current rate of species extinction estimated to be nearly 1,000 times the background rate (Pimm et al., Reference Pimm, Russell, Gittleman and Brooks1995, Reference Pimm, Jenkins, Abell, Brooks, Gittleman and Joppa2014). Furthermore, species conservation efforts both regionally and globally are often impeded by the lack of fine-scale range maps and accurate information on species distribution (Singh et al., Reference Singh, Singh, Kumara, Chetry and Mahato2020).
Primates are at risk of extinction globally, with 60% of species categorized as threatened on the IUCN Red List and c. 30% of non-human primate species listed as Critically Endangered (Estrada et al., Reference Estrada, Garber, Rylands, Roos, Fernandez-Duque and di Fiore2017). Nearly 75% of primate species are experiencing global population declines and the situation is particularly alarming for Asian primates, with 95% of species declining (Estrada et al., Reference Estrada, Garber, Rylands, Roos, Fernandez-Duque and di Fiore2017). Globally, populations and geographical ranges of most primate species are decreasing because of habitat loss and fragmentation caused primarily by anthropogenic activities (Rabanal et al., Reference Rabanal, Kuehl, Mundry, Robbins and Boesch2010; Wich et al., Reference Wich, Garcia-Ulloa, Kühl, Humle, Lee and Koh2014; Cotton et al., Reference Cotton, Clark, Boubli, Schwitzer, Wich and Marshall2016). Increasing human populations (Campbell et al., Reference Campbell, Kuehl, N'Goran Kouamé and Boesch2008), hunting of primates for consumption and the pet trade (Rosen & Smith, Reference Rosen and Smith2010), political instability (Kalpers et al., Reference Kalpers, Williamson, Robbins, McNeilage, Nzamurambaho, Lola and Mugiri2003) and diseases (Bermejo et al., Reference Bermejo, Rodríguez-Teijeiro, Illera, Barroso, Vilà and Walsh2006; Williams et al., Reference Williams, Lonsdorf, Wilson, Schumacher-Stankey, Goodall and Pusey2008) are additional threats affecting primate populations. These threats often act synergistically and are not mutually exclusive. Collecting baseline data on primate distribution, population sizes and trends is a key step towards effective conservation, as population monitoring enables researchers to quantify the impact of local threats and evaluate the success of any conservation measures implemented (Campbell et al., Reference Campbell, Head, Junker, Nekaris, Wich and Marshall2016). In addition, population monitoring can help to identify priority areas for primate conservation, develop conservation management strategies and eliminate threats.
Taxonomic accuracy plays a crucial role in understanding species distribution ranges, population trends, threats and conservation efforts (Mace, Reference Mace2004; Lewis & Maslin, Reference Lewis and Maslin2015). The ambiguity in the taxonomic status of some Indian primate species arises from the fact that the majority of existing classification schemes rely on plastic morphological traits, a situation that is further complicated by incompatibility between various classification systems (Nag et al., Reference Nag, Pramod and Karanth2011). Given these taxonomic uncertainties, the exact number of Indian primate species at risk of extinction remains unknown (Ashalakshmi et al., Reference Ashalakshmi, Nag and Karanth2015). There have, however, been studies employing molecular techniques in an effort to resolve this issue (Karanth et al., Reference Karanth, Singh, Collura and Stewart2008, Reference Karanth, Singh and Stewart2010a; Osterholz et al., Reference Osterholz, Walter and Roos2008; Wangchuk et al., Reference Wangchuk, Inouye and Hare2008; Ashalakshmi et al., Reference Ashalakshmi, Nag and Karanth2015). For example, studies based on molecular phylogeny and biogeography have led to the assignment of the purple-faced langur Semnopithecus vetulus and Nilgiri langur Semnopithecus johnii to the genus Semnopithecus, rather than Trachypithecus (Karanth et al., Reference Karanth, Singh, Collura and Stewart2008; Osterholz et al., Reference Osterholz, Walter and Roos2008), and maintaining the species status of the tufted gray langur Semnopithecus priam (Blyth, 1844) and black-footed gray langur Semnopithecus hypoleucos (Blyth, 1841). A study using an integrative taxonomic approach confirmed species status for the Himalayan langur Semnopithecus schistaceus (also referred to as Nepal gray langur) but did not support dividing this taxon into multiple species or subspecies (Arekar et al., Reference Arekar, Sathyakumar and Karanth2021). Similarly, a recent study ascertained the hoolock gibbon Hoolock hoolock as the only gibbon species in India (Trivedi et al., Reference Trivedi, Manu, Balakrishnan, Biswas, Asharaf and Umapathy2021), contrary to an earlier report of there being two species, the eastern Hoolock leuconedys and western Hoolock hoolock hoolock gibbons (Das et al., Reference Das, Biswas, Bhattacharjee and Mohnot2006).
Taking these ambiguities into account, a recent study reported 24 species of non-human primates in India, including two species of lorises, 10 species of langurs, 10 species of macaques and two species of small apes (Singh et al., Reference Singh, Singh, Kumara, Chetry and Mahato2020), of which 18 species are categorized as threatened on the IUCN Red List (IUCN, 2021). For many primate species in India, information on their current distribution is lacking, which impedes the assessment of their conservation status (Karanth et al., Reference Karanth, Nichols and Hines2010b). Furthermore, with the exception of a few recent studies, most surveys on Indian primates have been methodologically outdated and geographically limited (Singh et al., Reference Singh, Singh, Kumara, Chetry and Mahato2020).
To improve our understanding of the conservation status of Indian primates, we carried out a comprehensive review of the published literature, seeking to answer the following questions: (1) What do the data from recent studies indicate about population trends of Indian primates and the reasons for any observed changes? (2) How has the conservation status of Indian primates changed over time? (3) What are the reasons for such changes? (4) How do these changes vary amongst different species with respect to their habitats and the level of anthropogenic disturbance?
Methods
We undertook a systematic review using the search, appraisal, synthesis and analysis (SALSA) approach (Grant & Booth, Reference Grant and Booth2009). We followed methods described by Shrestha et al. (Reference Shrestha, Sarkar, Shrestha, Aung, Wen and Yongping2022) and included research articles dedicated either fully or in part to the study of the population status of non-human primates in India (Fig. 1). To keep our findings relevant to current species conservation efforts, we limited our search to studies published during the past 2 decades (2000–2021). We conducted a Boolean search across the Web of Science (Clarivate, Philidelphia, USA), Research Gate (ResearchGate, 2023), and Google Scholar (Google, 2023) platforms, using a combination of keywords related to the population and conservation status of Indian primates. To retrieve the relevant results, we used search operators such as AND, OR and NEAR in combination with species names and different keywords related to population status (Supplementary Table 1). We retrieved a total of 105 research publications related to Indian primates, which we examined for the presence of search query terms in the title, abstract and keywords. After this initial selection process, 41 publications accounting for 62 status reports, including multi-species studies, were retained for further analysis. For each research article in this sample (Supplementary Table 2), we recorded information on the population trend, year of survey, main threats reported, study area location, protection status of the study area and survey methods used. In the case of species for which repeated surveys had been conducted in a given area, we considered only the results from the most recent study. Although various studies have attempted to resolve the taxonomic ambiguity among Indian primates, here we considered the species taxonomy as reported by the authors in the research articles. We retrieved information on all primate species present in India, irrespective of whether or not they are threatened. We conducted all data analyses in R 4.2.2 (R Core Team, 2013) and used ArcGIS Desktop 10.8 (Esri, Redlands, USA) to map the geographical areas covered by the analysed publications.
Flow diagram of the searching, appraisal, synthesis and analysis (SALSA) method used in the literature review. The left-hand side of the diagram shows the four main processes of the review, with the components of these processes shown on the right-hand side (following Shrestha et al., Reference Shrestha, Sarkar, Shrestha, Aung, Wen and Yongping2022).
Results
Population status
We included all primate species in India, along with their conservation status and the number of studies that we found for each species, in our review. We found the highest number of studies on the rhesus macaque Macaca mulatta, but there were no reports on the population status of some species, including several langurs (Table 1). We identified five population status categories (Fig. 2) based on author inference in the reviewed articles: declining, increasing, stable, small and recovering populations. Studies that were the first to report on primate populations in a given area (and thus could not compare observed populations to previous studies) categorized populations as either small or stable/good. The majority of publications (71%) reported a declining population trend of the target species, followed by increasing (16%) and stable (13%) population trends. Declining population trends were attributed mostly to modifications of natural systems, such as habitat loss and fragmentation. Amongst the studies indicating declining population trends, 67% reported on only six primate species. For example, all nine reports on western (n = 5) and eastern (n = 4) hoolock gibbons showed declining population trends across the surveyed areas. Recovering population trends were reported for the Nicobar long-tailed macaque Macaca fascicularis umbrosus populations in coastal areas, which had been affected by a tsunami. A number of factors could affect the population dynamics of this species; for example, groups of crop-using macaques that had come into conflict with people may have moved from forest interiors to coastal areas. However, the observed population recovery is generally regarded as having been caused by the regeneration of native vegetation in coastal areas following the evacuation of people after the tsunami, which created space and suitable habitat for the species to thrive (Narasimmarajan & Raghunathan, Reference Narasimmarajan and Raghunathan2012; Velankar et al., Reference Velankar, Kumara, Pal, Mishra and Singh2016). The increasing population trend reported by 16% of the analysed studies was, however, mainly attributed to improved knowledge (i.e. increased spatial coverage compared to previous studies; Kumar et al., Reference Kumar, Kumara, Priya, Sushma, Meharabi and Udayraj2018) or to the effective protection offered to species by religious customs or cultural norms (Chaudhuri et al., Reference Chaudhuri, Murmu and Mazumdar2007). For example, the increasing population trend of the lion-tailed macaque Macaca silenus was attributed to better spatial coverage and improved enumeration techniques compared to previous studies (Kumar et al., Reference Kumar, Kumara, Priya, Sushma, Meharabi and Udayraj2018). For the Arunachal macaque Macaca munzala, which primarily inhabits the Tawang district of Arunachal Pradesh, the increasing population trend could be the result of enhanced spatial coverage and the absence of hunting attributed to the religious/cultural beliefs of the Monpa people (Kumar et al., Reference Kumar, Gama, Raghunath, Sinha and Mishra2008). Elsewhere, the species has been reported to be at risk of extirpation because of prevalent hunting practices (Sarania et al., Reference Sarania, Devi, Kumar, Sarma and Gupta2017). In the absence of hunting, the population would be expected to fluctuate, with ups and downs over the years. However, studies reported a nearly 1.5% growth per year in the number of groups recorded during 2008–2017 (from 35 to 41 groups; Kumar et al., Reference Kumar, Gama, Raghunath, Sinha and Mishra2008; Biswas et al., Reference Biswas, Borah, Das, Das, Bhattacharjee, Mohnot and Horwich2011; Sarania et al., Reference Sarania, Devi, Kumar, Sarma and Gupta2017), which we assume to be a combined effect of absence of hunting and greater spatial coverage of surveys.
Data on primate species in India, including the conservation status according to the IUCN Red List (IUCN, 2021) and the Wild Life (Protection) Act (WLPA; numerals denote schedule types under the WLPA, with lower values representing a higher protection status), the number of population studies published during 2000–2021, study site protection (PA, protected areas; NPA, non-protected areas), survey methods used, study location, main direct threats faced, local population trend (as reported in the studies) and the global population trend (according to the IUCN Red List). The numbers in parentheses indicate the number of reports. Species for which we did not find any studies are marked with asterisks (*); data on the direct threats and global population trend for these species were taken from the IUCN Red List.
The population status of Indian primates as indicated by recent studies (2000–2021).
Main threats
We assigned the various threats reported to three categories: (1) modification of natural systems, (2) human intrusions and disturbance, and (3) biological resource use according to the IUCN–CMP Unified Classification of Direct Threats (IUCN, 2023). Modification of natural systems (78%) such as habitat loss, fragmentation, modification and degradation was the main threat faced by Indian primates, forcing them to occupy isolated forest patches, including within protected areas. Other threats (Fig. 3) included biological resource use such as hunting for bushmeat and retaliatory killing because of human–wildlife conflict, and human intrusions and disturbance such as dam and road construction. The χ 2 test indicated no significant association between the types of threats and population status categories (χ 2 = 9.575, P = 0.653). Based on a comprehensive review of these studies, we found that major threats faced by Indian primates are not species-specific, but area-specific, and vary both spatially and temporally from species to species. For example, Hanuman langurs face the threat of habitat degradation within protected areas (Narasimmarajan & Raghunathan, Reference Narasimmarajan and Raghunathan2012), whereas habitat loss and hunting constitute a prevalent threat to species outside protected areas (Kumara et al., Reference Kumara, Kumar and Singh2010; Mishra et al., Reference Mishra, Sharma, Khan and Maurya2020). Similarly, trapping and deforestation have been considered major threats to rhesus macaques in the past (Southwick & Siddiqi, Reference Southwick and Siddiqi1994); however, the species is currently believed to be affected primarily by habitat loss and fragmentation (Sharma et al., Reference Sharma, Madhusudan, Sarkar, Bawri and Sinha2012; Imam & Ahmad, Reference Imam and Ahmad2013).
Number of reports indicating various threats faced by primates in India. Threats are categorized according to the IUCN–Conservation Measures Partnership threat classification scheme (IUCN, 2023).
Survey methods and duration
Most studies (83%) in our sample focused on population estimations of a single primate species. Distance sampling based on lines transects was the most commonly used method (48%) followed by the total count method (25%). Other methods used (Fig. 4) included direct sighting/random sampling (18%) and call counts (2%). Of the studies included in our analysis, only 22% were conducted during the 5 years prior to our review (2016–2021), targeting only 27% (n = 7) of the 26 Indian primate species. There has been great disparity in the distribution of population status studies across Indian primate species over the years. A few species, including rhesus macaques, bonnet macaques Macaca radiata and eastern hoolock gibbons, have received more attention from researchers than others, with the tufted gray langur, black-footed gray langur and southern pig-tailed macaque Macaca nemestrina being studied the least.
Different primate survey methods used in the studies included in our analysis.
Species coverage, temporal and spatial distribution of the studies
The population status studies on Indian primates conducted since 2010 have diversified in terms of species coverage (Fig. 5). In terms of geographical coverage, > 60% of the reports represent surveys conducted in the Western Ghats and north-eastern Himalayas (Fig. 6), and 34% of studies were conducted in non-protected areas. Unlike the studies conducted in non-protected areas, which showed stable, increasing or declining population trends, all reports (66%) conducted exclusively in protected areas reported declining population trends, except in the Chakrashila Wildlife Sanctuary, Assam (Chetry et al., Reference Chetry, Das, Phukan, Chetry, Boro and Bhattacharjee2020). In contrast, one study conducted in the upper Brahmaputra Valley of north-eastern India reported increasing population trends within and decreasing trends outside protected areas. Focused on the overall population abundance of six primate species, this study reported a 251% increase of the population within protected areas for all six species, but a dramatic decline outside protected areas caused by rapid, severe habitat loss resulting in small habitat fragments and disruption of canopy continuity (Sharma et al., Reference Sharma, Madhusudan, Sarkar, Bawri and Sinha2012).
(a) Temporal distribution of the number of publications on the population status of Indian primates and (b) total number of primate species surveyed for their population over time.
Spatial distribution of the population status studies conducted on Indian primates during 2000–2021.
Discussion
The overall trend in the population status of Indian primates mirrors the global pattern, with a population decline in 75% of primate species worldwide (Estrada et al., Reference Estrada, Garber, Rylands, Roos, Fernandez-Duque and di Fiore2017). This declining trend in the population of Indian primates has persisted for decades, with 70% of species categorized as threatened (including 35% Vulnerable and 35% Endangered) on the IUCN Red List (IUCN, 2021). Establishing reliable baseline data on species distribution and population status using appropriate methods would offer insights into population trends across a temporal scale as well as species' responses to changing habitats (Lyons et al., Reference Lyons, Runge, Laskowski and Kendall2008; Jones et al., Reference Jones, Hawes, Norton and Hawkins2019).
Routine wildlife population monitoring (Nichols & Williams, Reference Nichols and Williams2006), in addition to serving as a foundation for evaluating ecosystem functioning, conservation success and intensity of threats faced by wildlife (Stokes et al., Reference Stokes, Strindberg, Bakabana, Elkan, Iyenguet and Madzoké2010), also offers a comparative view of the effectiveness of different conservation strategies (Ferraro & Pattanayak, Reference Ferraro and Pattanayak2006). For example, population monitoring of bonnet macaques over the past 3 decades has shown a sharp decline, with a 70% reduction in population size, which has been attributed mainly to habitat loss (decreased vegetation cover and canopy connectivity) because of urbanization (Erinjery et al., Reference Erinjery, Kumar, Kumara, Mohan, Dhananjaya and Sundararaj2017). Population monitoring of rhesus macaques over 6 decades has shown varying trends, with population size decreasing by 90% during the 1960s and 1970s, followed by a partial recovery during the 1980s (Southwick & Siddiqi, Reference Southwick and Siddiqi1994) and a substantial population growth of 203% during 1995–2010 (Imam & Ahmad, Reference Imam and Ahmad2013). To evaluate population trends, a representative population of the target primate species must be identified and monitored in each habitat at least once every 3 years (Singh et al., Reference Singh, Singh, Kumara, Chetry and Mahato2020). To better understand the drivers of changing wild populations, we recommend population monitoring for all Indian primate species, with priority given to species that are threatened and/or for which we have limited or no data on their population status (e.g. the grey slender loris Loris lydekkerianus grandis and Nilgiri langur; Table 1).
Seventy-three per cent of Asian primate species are considered threatened (Estrada et al., Reference Estrada, Garber, Rylands, Roos, Fernandez-Duque and di Fiore2017). Threats to their survival are dynamic, in terms of both scope and severity, and interact with each other at various spatial and temporal scales. We found that most threats to the long-term survival of populations of Indian primates were anthropogenic in origin, with modification of natural systems, such as habitat loss and fragmentation, being of particular concern. The conversion of natural habitats to agricultural lands appears to be the main cause of habitat loss and fragmentation (Gibbs et al., Reference Gibbs, Ruesch, Achard, Clayton, Holmgren, Ramankutty and Foley2010). Destruction of habitat patches often results in the loss of all individuals in the affected area (Wich & Marshall, Reference Wich, Marshall, Wich and Marshall2016). The consequences of habitat fragmentation on primate survival are determined by several factors, including the matrix embedding the habitat fragments, fragment size and inter-patch distance, and the species' home range and diet (Michalski & Peres, Reference Michalski and Peres2005; Boyle & Smith, Reference Boyle and Smith2010; Meijaard et al., Reference Meijaard, Albar, Nardiyono, Ancrenaz and Spehar2010). Some primates exhibit behavioural and ecological resilience in the face of habitat loss, fragmentation and degradation, but population decline is a common and immediate result of habitat loss (Estrada et al., Reference Estrada, Garber, Rylands, Roos, Fernandez-Duque and di Fiore2017). To limit the threats faced by Indian primates, conservation activities must be initiated where they are absent and continued where they already exist. One encouraging example of population recovery is provided by population trend studies of rhesus macaques in northern India. Deforestation, excessive trapping and export of juvenile rhesus macaques for biomedical research reduced the population by 90% in the 1970s. However, the subsequent ban on trapping and export, coupled with a stabilizing economy and increased agricultural production, helped the population to recover and thrive in a short period of time (Southwick & Siddiqi, Reference Southwick and Siddiqi1994; Imam & Ahmad, Reference Imam and Ahmad2013).
Our results indicate that > 60% of studies concerning the population status of Indian primates were concentrated in the north-eastern Himalayas and southern Western Ghats, areas that harbour a rich diversity of primates (Srivastava, Reference Srivastava2006; Karanth et al., Reference Karanth, Nichols and Hines2010b). This spatial bias could be attributed to the fact that > 70% of Indian primates are supported by moist deciduous, evergreen, and semi-evergreen forests in these two regions, with a total of 13 species inhabiting the north-eastern Himalayas and 10 species inhabiting the Western Ghats (Choudhury, Reference Choudhury and Gupta2001; Kumara & Singh, Reference Kumara and Singh2004). Although declining population trends were observed even within protected areas, these declines may have been more pronounced had these areas not been protected. Protected areas thus continue to play a crucial role for primate conservation.
Efforts have been made to modify and improve traditional monitoring methods and to devise new methods for generating robust estimates of wildlife populations. No population survey method is entirely free of bias, and some methods can be more suitable than others in a given situation, depending on variables such as species behaviour and landscape characteristics. To utilize methodological advancements and obtain scientifically robust and reliable population estimates, given the ecological diversity of Indian primates, we suggest employing methods tailored to the target species and population to minimize bias. This includes methods not yet tested on Indian primates, for example the genetic capture–recapture method for elusive species, the double observer method for diurnal primates, cue or point count methods for species with distinctive vocalizations, lure count methods for species that respond to playback calls, and occupancy-based methods for rare species. Further studies are needed to evaluate the appropriateness and statistical soundness of such methods for the study of various primate species.
The dearth of recent population data and limited spatial coverage of most studies on Indian primate populations highlights the urgent need for a comprehensive, nationwide primate distribution and population status study as a priority for effective conservation. The threatened status and declining population trends of several Indian primates warrant immediate attention and efficient management to prevent a major extinction event in the region.
Acknowledgements
We thank the Wildlife Biology Laboratory supported by the DST-INSPIRE Faculty Award Project at the Centre of Research for Development, University of Kashmir, for providing the academic, technical and administrative support; and two anonymous reviewers for their critiques.
Author contributions
Conceptualization: SH, TB; data collection, literature review: SH; data analysis: SH, MK; writing: SH, TB; resources and supervision: TB, MNA, AK; revisions and editing: SH, TB, MK, AK.
Conflicts of interest
None.
Ethical standards
Our analysis is based on data collected from published studies. No ethical approval was required for this research, and it otherwise abides by the Oryx guidelines on ethical standards.
Data availability
The evidence supporting our findings is available on request from the corresponding author.
Open access
