Dietary preference and feeding patterns of the urban Rhesus Macaque Macaca mulatta ( Mammalia : Primates : Cercopithecidae ) in Asola-Bhatti Wildlife Sanctuary in India

We studied the feeding patterns and discrete spatio-temporal food habitsof16 groups of the urban Rhesus Macaque Macaca mulatta following their relocation in Asola-Bhatti Wildlife Sanctuary near Delhi, India. We observed that the macaques fed on 31 plant species, with Prosopis juliflora and P. cineraria appearing in most scans. We classified the food consumed by the species into six main categories the species and recorded the average time spent on each of these throughout the year. The maximum time was spent on supplementary feeding provided by the forest department and the minimum on natural plant resources. There was a significant difference in the consumption of different food categories from morning to evening but there were no significant seasonal variations. This study showed that Rhesus Macaque adopted different foraging strategies based on the availability of resources in their new environment and that variety in food resources buffered seasonality in their diet. Information on their feeding patterns and food habits will help in developing management protocols for the primates in urban environments.


INTRODUCTION
Rhesus Macaque Macaca mulatta is the most common non-human primate in the forested and urban areas of Asia (Hasan et al. 2013).It is found throughout India in its peninsular (Madhya Pradesh, West Bengal, and Assam), northern (Jammu & Kashmir, Himachal Pradesh, Punjab, Haryana, Uttar Pradesh, Rajasthan, and Gujarat) (Seth et al. 2001), and northeastern (Assam, Meghalaya, and Arunachal Pradesh; (Molur et al. 2003) regions.Information on the feeding ecology of a species provides the detailed dietary specialization necessary for its survival and is an important part of its natural life history (Harcourt et al. 2002).Flexibility in diet patterns plays a pivotal role in the survival of non-human primate species in urban and peri-urban ecosystems through resource sharing and competition and has evolutionary implications in the long-term.Primates are known to adopt several foraging strategies (Fleagle & Gilbert 2006).Natural diet of forest Rhesus Macaques includes fruits, seeds, inflorescences, flowers, buds, leaves, young shoots, twigs, barks, roots, and pith and resin of gymnosperms, angiosperms, and fungi (Fooden 2000).Macaques are also known to consume animal food items that such as insects, spiders, worms, termites, grasshoppers, lizards, ants, beetles, molluscs, crayfish, shellfish, honeycombs, crabs, and bird eggs (Mandal 1964;Lindburg 1971;Malik 1983).In marine coastal areas, the species is mostly known to rely on seeds and fruits (Hanya et al. 2003) and also catch live fish as in the Sunderban (Majumder et al. 2012).In forested habitats,primates consume 25% to 40% of the total frugivore biomass (Chapman et al. 1995).Ingestion of fruits or young leaves with sugar and insects with protein content help to balance their diet (Janson & Chapman 1999).Feeding patterns are also associated with humanmacaque conflict-crop raiding by macaques in villages near forest areas has increased the level of negative association of the species by farmers (Air 2015).The dependency of urban macaques on anthropogenic food resources and their behaviours associated with food utilisation from urban areas often increase the risk of undesirable interactions with human beings (Sha & Hanya 2013).
In urban landscapes, the nutrition required for primates becomes highly questionable.Urban macaques largely share human food resources (Gupta 2001) and depend on cultivated crops, plants, and even garbage (Lee et al. 1986).In some cases, macaques depend on humans for being fed (Strum 1994)-the feeding patterns of primates that live in tourist sites and temples are often influenced by provisioning of food by humans.Urban macaques have also acquired behavioural adaptations in food-acquisition techniques (Mangalam & Singh 2013).Urban habitats, in contrast to natural ones, have a more direct influence on primate behaviours associated with competitive resource utilizations and foraging techniques.Several anthropogenic barriers and disturbances interfere with the feeding ecology of primates in urban environments.
Although Rhesus Macaques were assessed as a Least Concern (LC) species by IUCN (2018), primates are threatened globally by human-wildlife negative interactions, habitat loss and fragmentation, and several other anthropogenic factors (Strum 1994(Strum , 2001;;Mittermeier & Konstant 1996, 1997;Kemf & Wilson 1997;Cowlishaw & Dunbar 2000;Peterson 2003;Hill 2005).The Negative interactions between humans and macaques due to food provisioning and other anthropogenic drivers possess major challenges for the survival and persistence of the species.The need for translocation of Rhesus Macaques and the consequences were due to its proliferation in urban areas of India was suggested and studied earlier (Malik & Johnson 1991, 1994;Southwick et al. 1998).Translocation or relocation is a widely used conservation tool but it is known to induce stress, as evident in the higher level of stress hormones in females of the species during the translocation process (Aguilar-Cucurachi et al. 2010).
The reproductive capacity, inter-birth interval, and the size of social groups in primates are often determined by the amount of food they consume (Air 2015).Again, the availability of different food resources can reduce seasonal fluctuations in diet and provisioning of food regularly to urban primates may have adverse effects on their behaviour, social organization, and conservation (Sinha&Vijayakrishnan 2017).The aim of this study was to investigate the food habits and feeding patterns of urban macaques in and around (0-1 km) Asola-Bhatti Wildlife Sanctuary in Delhi.The characteristic features of this sanctuary such as the availability of food resources infringe villages and food provisioning by the public have played an influential roles in the feeding ecology of its Rhesus Macaques.Information of dietary patterns of urban macaques will enhance the knowledge of its natural history and survival and that will help in the management of the species in urban ecosystems.

Study area
Asola-Bhatti Wildlife Sanctuary is situated in South Delhi District (28.41 0 -28.49 0N and 77.19 0 N-77.27 0E) and covers a total area of about 6,874ha and there is a high density of Acacia pendula,scrub forests, and trees with a short diameters (Kushwaha et al. 2014) (Fig. 1).The forest area is located at the foothills of the Aravalli range and is about 16km long and 4.3km wide, with elevation ranging from 235-288 m.The forest is surrounded by hilly areas with shrubs, stunted trees, and moderate density forest cover and is adjacent to the urban areas of Delhi-Haryana interstate border region, Sangam Vihar, Faridabad (Surajkund Road), Pali Village, Satberi, Deragaon, Fatepurberi, and Anangpur.This protected area has semi-arid vegetation with xerophytic plants and several large, deep pits.The largest water-filled pit is Neeli-Jheel, situated 3km from Gate No. 7, where urban monkeys are intermittently released after capture since 2007.
The dominant tree species in Asola-Bhatti Wildlife Sanctuary are Prosopis juliflora, a native species introduced to counter forest degradation (Burkart 1976;Pasiecznik et al. 2001), which and present at high (7.68%),moderate (16.03%), and low (47.90%)densities,and Anogeissus pendula and Acacia nilotica, present in forest plantation, scrub vegetation (12.04%), water bodies (0.16%), and human settlements (2.92%) (Kushwaha et al. 2014).There were no Rhesus Macaques in the area before translocation began and the present population is derived entirely from relocated animals alone.This area exhibits extreme fluctuation in annual temperature, with summer highs in May (43-47 0 C) and winter lows in January (6 0 C).June to September is the wet season with an average annual rainfall of about 617mm.This sanctuary is composed of Asola Village in the north and Bhatti area in the south.It is a man-made sanctuary and the only protected area in Delhi.Most of the area of the sanctuary is degraded with the prevalence of xerophytic plants (Khanna & Sati 2003).
Vegetation shows remarkable dominance of shrubs and stunted trees (Naithani et al. 2006).

Study groups
We sighted a total of 16 groups of translocated Rhesus Macaques in the area.Observations were made from a close distance of <10m and data on demography and food habits were collected from 06.00-18.00hr daily from May 2016 to June 2017.Group size varied from 14 to 63 individuals per group (30.57±2.67)and a total of 492 (n) individuals were observed (Table 1).

Food categories
We classified the food consumed by the relocated Rhesus Macaques into categories based on variations in resource availability: i) Natural plant species: The natural plants, trees, herbs, and shrubs available in the sanctuary.
ii) Supplementary foods: Food given by the forest department daily in this sanctuary for feeding the Rhesus Macaques only (seasonal vegetables and fruits; 2500kg/ day).
iii) Provisioned food: Banana and roadside food (bread and chick-pea) thrown by the public to the macaques daily; the macaques often travel to the boundary walls, cross it, and sit on the highway it to have these itemsthe the.iv) Anthropogenic food: Garbage and human food resources (Indian bread, oily fries, and potato chips) snatched by the macaques daily from human settlements situated within 0.5km of the protected area.v) Water: Water from channelsmade in the sanctuary exclusively for Rhesus Macaques (a total of 36 in number).

Scan sampling technique
Instantaneous or scan sampling (Altmann 1974) was used to gather information on the feeding habits and food items of the macaques.Group scans were taken on all visible members of the group for 5min at every 10-minute interval.We recorded 13,740 scan samples and the type of food items eaten (young leaves,mature leaves, roots, stems, flowers, fruits, shoots, gum, bark, or animal prey).We collected the unidentified species for taxonomic identification (leaves, stem, and fruits) through herbarium in the Wildlife Institute of India, Dehradun.

Focal sampling technique
We focused on individuals (adult male/ adult female/ juvenile/ infant) and made 12 entries per hour of theiractivitiesins.We recorded the time spent by that focal individualson each food plant and the parts eaten along with thetime spent at different feeding sites.We recorded 13,874 focal samples and categorized the different plant parts eaten by the macaques.We estimated the time spent feeding on different food items in a day as per theformula by Gupta &Kumar (1994): T a = N a / N x 100, where T a is the percentage of time spent on an activity a, N a is the number of records with activity a, andN is the total number of records for the day.
Analysis: Analysis of variance (ANOVA) was used to compare the feeding time on food categories and the number of food plants eaten monthly and seasonally (Simpson et al. 1960).Independent sample t-test was used to analyse the difference in the average time spent on each category.Chi square test was performed to compare the association between groups.Microsoft Excel 2010 was used to summarize the data and Minitab version 17.0 software and web tool were used to calculate

Food categories
Food plants, plant families, parts eaten, and the average percentage of time spent feeding on each plant species are given in Table 2.The macaques were mostly found to feed on Fabaceae (8.76±2.64),Moraceae (2.60±2.06),Rhamnaceae (0.34±0.02), and Mytraceae (0.06±0.03) families.Among the plant parts (nature food items) eaten, 34.65% of feeding time was spent on leaves, followed by 31% on bark and piths, 22.90% on flowers, and 11.01% on fruits.The macaques were mostly found in the lower canopy and bottom of trees in summer (39.13%), in the upper canopy in monsoon (31.26%), and in the middle to lower canopy in the winter (19%).The species was observed to spend 79% time on the ground and only 21% time on the trees.

Seasonality and Diet
Average percentage time spent on each food category was calculated for each month.The overall mean time spent on natural plant species was 13.29±2.32, in supplementary feeding provided by forest department 50.19±3.49,in anthropogenic food category 18.18±1.41,and in provisional food by public 18.34±4 throughout the year including summer, monsoon, and winter months (Table 3).We recorded the dietary pattern and found that the maximum average time was spent on supplementary food in all seasons followed by a maximum on provisioned food in winter (26%), in summer (18%), and a minimum during monsoon (11%).The macaques were observed spending maximum time consuming natural plant species (17.68%) during the rainy season, apart from supplementary food.ANOVA analysis showed that there was no statistically significant difference in the total dietary intake pattern throughout the year (F=0.05,df=11, P>0.05).

Age-sex feeding pattern in groups
We recorded the percentage of time spent by individuals in a group on each food type (Table 4).We calculated the average percentage time spent on all food categories by adult males (25.0±8.17),adult females

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(22.01±7.13),sub-adult males (7.92±4.02),sub adult females (6.06±3.19),juveniles (0.65±0.20,) and infants (0).Adult males dominated the pattern and used up the maximum amount of food provided to them and spent the maximum time on it.Adult females were much protective and did not allow their infants to feed on artificial foods.Infants compensated their nutritional requirement through lactation only.

DISCUSSION
Non-human primates compete with human beings for resource utilisation and space, which can lead to negative interactions (Priston & Underdown 2009), especially in urban areas (Lee & Priston 2005).In India, Rhesus Macaques often co-exist with human populations and are highly dependent on them for food (Southwick et al. 1976).The high feeding dependency on anthropogenic food resources is, however, not correlated with natural resource scarcity.While natural resources such as fruits are highly variable over the year, anthropogenic food resources are potentially more stable and easily available.A study on Long-tailed Macaques Macaca fascicularis showed that the main drivers for exploitation of anthropogenic foods were natural food plant resource scarcity or an overt dependence on anthropogenic foods (Sha & Hanya 2013).Utilization of anthropogenic food resources lowered preferences of macaques on fruits and natural plants in another study (Hambali et al. 2014).The consequences of the dependency of macaques on human food resources can include food stealing, which may lead to negative interactions with humans.In our study, the relocated Rhesus Macaques were more inclined towards anthropogenic, supplementary, and provisioned food resources than natural plant resources in the forest.As this sanctuary is situated in a human-dominated landscape and human settlements are located close by (less than 50m away), Rhesus Macaques disperse from the sanctuary and consume food from nearby households, markets, and temple areas.The forest department of Delhi Government was also assigned to provide supplementary food to the rehabilitated macaques for the maintenance of a viable population in the newly introduced environment.
Our results showed that the macaques fed on natural plant species in the early morning between 06:00-09:00 hr (40.8%), after which their tendency to consume natural resources declined before rising in the late afternoon (21.75%).Food provisioning by the public was recorded mostly in the early morning (25%) and continued throughout the day in the fringes of the sanctuary.Between 09:00hr and 11:00hr, macaques gathered at feeding stations within the sanctuary near the Bhatti Range Office, reaching a peak number between 12:00hr and 15:00hr (53.75%).The macaques were reportedly given 2,500kg food per day by the forest department and this feeding pattern had a large influence on their daily activity and movement.During supplementary feeding, the macaques did not consume natural plants within the forest area.The relocated Rhesus Macaques were highly inclined towards human food outside the sanctuary and often entered nearby houses or snatched bread and vegetables from open markets in the nearby Sanjay Colony (Bhatti Mines).
Our results showed that the macaques mostly preferred leaves and stems of Prosopis juliflora (16.34%) and P. cineraria (11.09%), which were reported to be beneficial for their health.The heartwood of these two plant species contains ample antioxidants such as flavonol and mesquitol (Sirmah et al. 2009).Though numerous species of medicinal plants and fruiting trees are available in the sanctuary, the macaques did not spend much time in natural foraging but mostly depended on artificial feeding.Our results showed a high consumption of supplementary food items throughout the year with no seasonal differences and low average time spent on natural food plants.The macaques showed dependency on anthropogenic and provisioned food over natural fruit.The former included bananas, seasonal fruits and vegetables, bread, chickpeas, fried snacks, and icecreams; the macaques were even reported to steal cold water from refrigerators of houses in nearby localities at a 0.25-5 km distance (USA Today 2017).
Roadside food provisioning is a common practice across cities and villages in India.Southwick et al. (1976) documented the impact of artificial feeding on the ecology and behaviour of macaques.Our study provides information on feeding practices of Rhesus Macaques after translocation to an area containing various types of natural and anthropogenic food resources in a human-dominated landscape.An understanding of the basic natural history of primates is essential for their conservation (Caro 2007;Fashing 2007).The primary threat primates face today is habitat destruction (Wieczkowski 2004;Chapman et al. 2006).By reducing forest size and quality, habitat destruction leads to the reduction of food sources for forest-dwelling primates and, in some cases, threatens them with local extinction (Lee &Hauser 1998;Muoria et al. 2003).The increasing population of Rhesus Macaques living in proximity to human habitations has become a major issue in India.Rapid urbanisation, deforestation, and habitat fragmentation altered the natural living spaces of animals and their natural behaviour in the wild.Most primate species were severely affected by threats in anthropogenic landscapes (Sinha & Vijayakrishnan 2017).The translocation of Rhesus Macaques from city areas to forest situated at close proximity with human settlementsmight not reduce the conservation threats for the taxa.The step, however, altered their feeding strategies as the species was observed to become more dependent on supplementary and anthropogenic food resources than on natural foraging.Though artificial feeding of fruits and vegetables might increase overall nutrition, their natural frugivorous behaviour seem to be lost.The macaques were seen to snatch and steal even those anthropogenic food resources that had no health benefits, as they were used to such behaviour in human habitats (Ganguly et al. 2018).The dietary habits of Rhesus Macaques were totally different in a humandominated forest land.Previous studies showed that the species thrived in eight diverse habitats (temple, urban, village, village-cum-pond, pond, roadside, canal sides, and forest) having varying degrees of human interactions in India (Seth et al. 1986).The feeding practice seemed to increase the urban threats, diseases, and anthropogenic stress in the Rhesus Macaque population.In our study, the species was observed to spend maximum time on the ground instead of on the trees and their dependency on supplementary, provisioned, and anthropogenic food sources did not indicate conservation success.Understanding the feeding ecology in this sanctuary would help in planning the management of macaques in other urban areas.

Figure 2 .
Figure 2. Percentage of time spent on different food categories by relocated Rhesus Macaques per day from 06:00-18:00 hr in the sanctuary

Dietary preference and feeding patterns of the urban Rhesus Macaque Ganguly & Chauhan 12911 descriptive
statistics.Landsat data imageries 2016 and ArcGIS software were used to map the study area using coordinates collected during the data sampling though Garmin GPS 72H.

Table 3 . Food categories, average time spent based on seasonal variation, day length of consuming food categories, and average number of participants at a time during feeding activity
of Threatened Taxa | www.threatenedtaxa.org| 26 December 2018 | 10(15): 12907-12915