Feeding ecology of Assamese macaques (Macaca assamensis) troops in Kaligandaki and Budhigandaki River basins of central Nepal
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Abstract. Ghimire SC, Khanal L, Chalise MK. 2021. Feeding ecology of Assamese macaques (Macaca assamensis) troops in Kaligandaki and Budhigandaki River basins of central Nepal. Biodiversitas 22: 2625-2634. Seasonal fluctuations in the availability of key food resources impact the foraging behavior of animals. This study aimed to examine the seasonal variations in feeding time of Assamese macaques (Macaca assamensis) in the sub-tropical deciduous riverine forest environment of central Nepal. Two troops of Nepal population of Assamese macaques, a troop from Kaligandaki River Basin (KRBT) and the next from Budhigandaki River Basin (BRBT) were studied by focal animal sampling method. Data from systematic behavioral observations were analyzed with reference to that of the vegetation surveys. Assamese macaques invested more than two-fifths (>40%) of the diurnal time on feeding. The KRBT consumed 71 plant species and the BRBT relied on 69 food plants. Leaves, mature and young, constituted the most dominant food item followed by the fruits and seeds. The two study troops inhabiting highly similar habitats of food plants (Sorensen’s Similarity Index = 0.93) didn’t have a significant difference in the selection of food-plant parts. However, the remarkable temporal difference in feeding plant parts was observed in concordance with their seasonal availability. Young leaves, when available during the spring and pre-monsoon were the major food items. Contrastingly, mature leaves were the food items during the winter on which animals were forced to rely when young leaves were scarce. We conclude that food choice and time investment on the feeding of different plant parts differ depending on the availability of food in the area. Macaques living in comparable habitats with similar food plants have analogous food choices and time investments.
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References
Adhikari K, Khanal L, Chalise MK. 2018. Status and effects of food provisioning on ecology of Assamese monkey (Macaca assamensis) in Ramdi area of Palpa, Nepal. Journal of Institute of Science and Technology 22 (2): 183-190.
Altmann J. 1974. Observational study of behavior: sampling methods. Behaviour 49 (3-4): 227-266.
Altmann J, Altmann SA, Hausfater G, McCuskey SA. 1977. Life history of yellow baboons: physical development, reproductive parameters, and infant mortality. Primates 18 (2): 315-330.
Atsalis S. 1999. Diet of the brown mouse lemur (Microcebus rufus) in Ranomafana National Park, Madagascar. International Journal of Primatology 20 (2): 193-229.
Boonratana R, Chalise M, Das J, Htun S, Timmins RJ. 2008. Macaca assamensis, Assam macaque. The IUCN Red List of Threatened Species: e.T12549A3354977. DOI: 10.2305/IUCN.UK.2008.RLTS. T12549A 3354977.en.
Cabana F, Dierenfeld E, Wirdateti W, Donati G, Nekaris KAI. 2017. The seasonal feeding ecology of the Javan slow loris (Nycticebus javanicus). American Journal of Physical Anthropology 162 (4): 768-781.
Chalise MK. 1997. Survey of primates in Makalu-Barun Conservation Area (lower parts of Apsuwa, Isuwa and Sankhuwa rivers). A research report submitted to MBCA Project, Nepal.
Chalise MK. 1999. Some behavioral and ecological aspects of Assamese monkeys (Macaca assamensis) in Makalu-Barun Area, Nepal. Nepal Journal of Science and Technology 1: 85-90.
Chalise MK. 2003. Assamese macaques (Macaca assamensis) in Nepal. Primate Conservation 19: 99-107.
Chalise MK. 2008. Primate census in Kathmandu and west parts of Nepal. Journal of Natural History Museum 23: 60-64.
Chalise MK. 2010. A study of Assamese monkey in Sebrubeshi of Langtang National Park, Nepal. Journal of Natural History Museum 25: 54-61.
Chalise MK. 2013. Fragmented primate population of Nepal. In: Marsh LK, Chapman CA (eds) Primates in Fragments: Complexity and Resilience. Springer Science+Business Media, New York 329-356.
Chalise MK, Bhattarai GP, Pandey B. 2013. Ecology and behavior of Assamese monkeys in Shivapuri Nagarjun National Park, Nepal. Journal of Natural History Museum 27: 12-24.
Chalise MK, Karki JB, Ghimire MK. 2005. Status in Nepal: Non-human Primates. Special issue on the occasion of 10th Wildlife Week, 2062. Department of National Parks & Wildlife Conservation, Kathmandu, Nepal.
Chapman CA, Chapman LJ, Wrangham RW. 1995. Ecological constraints on group size: an analysis of spider monkey and chimpanzee subgroups. Behavioral Ecology and Sociobiology 36 (1): 59-70.
Chapman CA, Chapman LJ, Struhsaker TT, Zanne AE, Clark CJ, Poulsen JR. 2005. A long-term evaluation of fruiting phenology: importance of climate change. Journal of Tropical Ecology 21: 31-45.
Clink DJ, Dillis C, Feilen KL, Beaudrot L, Marshall AJ. 2017. Dietary diversity, feeding selectivity, and responses to fruit scarcity of two sympatric Bornean primates (Hylobates albibarbis and Presbytis rubicunda rubida). PloS one 12 (3), e0173369.
Clutton?Brock TH, Harvey PH. 1977. Primate ecology and social organization. Journal of zoology 183 (1): 1-39.
Davies AG, Bennett EL, Waterman PG. 1988. Food selection by two South-east Asian colobine monkeys (Presbytis rubicunda and Presbytis melalophos) in relation to plant chemistry. Biological Journal of Linnean Society 34 (1): 33-56.
Doran D. 1997. Influence of seasonality on activity patterns, feeding behavior, ranging, and grouping patterns in Tai chimpanzees. International Journal of Primatology 18 (2): 183-206.
Dunn JC, Cristobal-Azkarate J, Vea JJ. 2010. Seasonal variations in the diet and feeding effort of two groups of Howlers in different sized forest fragments. International Journal of Primatology 31: 887-903.
Frechette JL, Hon N, Behie A, Rawson BM. 2017. Seasonal variation in the diet and activity budget of the northern yellow-cheeked crested gibbon Nomascus annamensis. Cambodian Journal of Natural History 2: 168-178.
Ghimire SC, Chalise MK. 2018. Status of crop raiding by Assamese monkeys (Macaca assamensis) along the Budhigandaki river, central Nepal. Journal of Natural History Museum 30: 294-305. DOI: 10.3126/jnhm.v30i0.27605.
Ghimire SC, Chalise MK. 2019. Crop Raiding Status by Assamese Monkeys (Macaca assamensis) along the Kaligandaki River, Western Nepal. Journal of Institute of Science and Technology 24 (1): 72-76. DOI: 10.3126/jist. v24i1.24639.
Gould L, Sussman RW, Sauther ML. 1999. Natural disasters and primate populations: The effects of a 2-year drought on a naturally occurring population of ring-tailed lemurs (Lemur catta) in southwestern Madagascar. International Journal of Primatology 20 (1): 69-84.
Grueter CC. 2016. Environmental seasonality. The international encyclopedia of primatology 1-2.
Guo S, Li B, Watanabe K. 2007. Diet and activity budget of Rhinopithecus roxellana in the Qinling Mountains, China. Primates 48: 268-276.
Hemingway CA, Bynum N. 2005. The influence of seasonality on primate diet and ranging. Cambridge Studies in Biological and Evolutionary Anthropology 44: 57-104.
Iwano T. 1973. The seasonality and nomadic life of a feral troop of Japanese monkeys. A case of the T-Ib troop of the Takagoyama area, the Boso Peninsula. Master Thesis, the University of Tokyo.
Janson CH, Chapman CA. 1999. Resources and primate community structure. Primate Communities 237-267.
Janson CH, Goldsmith ML. 1995. Predicting group size in primates: foraging costs and predation risks. Behavioral Ecology 6 (3): 326-336.
Kaplin BA, Munyaligoga V, Moermond TC. 1998. The Influence of Temporal Changes in Fruit Availability on Diet Composition and Seed Handling in Blue Monkeys (Cercopithecus mitis doggetti). Biotropica 30 (1): 56-71.
Khanal L, Chalise MK, He K, Acharya BK, Kawamoto Y, Jiang X. 2018a. Mitochondrial DNA analyses and ecological niche modeling reveal post-LGM expansion of the Assam macaque (Macaca assamensis) in the foothills of Nepal Himalaya. American Journal of Primatology 80 (3): e22748. DOI: 10.1002/ajp.22748.
Knott CD. 1998. Changes in orangutan caloric intake, energy balance, and ketones in response to fluctuating fruit availability. International Journal of Primatology 19 (6): 1061-1079.
Knott CD. 2005. Energetic responses to food availability in the great apes: implications for homonin evolution. Seasonality in primates: Studies of living and extinct human and non-human primates 44: 351-378.
Marshall AJ, Wrangham RW. 2007. Evolutionary consequences of fallback foods. International Journal of Primatology 28: 1219-1235.
Martin P, Bateson P. 1993. Measuring behaviour: an introductory guide. Cambridge University Press.
McKey DB. 1978. Soils, vegetation and seed-eating by black colobus monkeys. The ecology of arboreal folivores 423-438.
Mitani JC, Watts DP. 2005. Correlates of territorial boundary patrol behaviour in wild chimpanzees. Animal Behaviour 70 (5): 1079-1086.
Nishida T. 1976. The bark-eating habits in primates, with special reference to their status in the diet of wild chimpanzees. Folia Primatologica 25 (4): 277-287.
Norsica I, Carrai V, Borgognini-Tarli SM. 2006. Influence of dry season and food quality and quantity on behavior and feeding strategy of Propithecus verreauxi in Kirindy, Madagascar. International Journal of Primatology 27: 1001-1022.
Oates JF, Waterman PG, Choo GM. 1980. Food selection by the south Indian leaf-monkey, Presbytis johnii, in relation to leaf chemistry. Oecologia 45 (1): 45-56.
Overdorff DJ. 1993. Similarities, differences, and seasonal patterns in the diet of Eulemur rubriventer and Eulemur fulvus rufus in the Ranomafana National Park, Madagascar. International Journal of Primatology 14: 721-753.
Paudel PK. 2017. Conflict due to Assamese macaques (Macaca assamensis McClelland, 1840) and crop protection strategies in Kaligandaki river basin, western Nepal. Our Nature 14 (1): 107. DOI: 10.3126/on.v14i1.16449.
Puri GS. 1960. Indian forest ecology. A comprehensive survey of vegetation and its environment in the Indian subcontinent [Vols. I & II]. New Delhi: Oxford Books.
Remis MJ, Dierenfeld ES, Mowry CB, Carroll RW. 2001. Nutritional aspects of western lowland gorilla (Gorilla gorilla gorilla) diet during seasons of fruit scarcity at Bai Hokou, Central African Republic. International Journal of Primatology 22 (5): 807-836.
Serckx A, Kühl HS, Beudels?Jamar RC, Poncin P, Bastin JF, Huynen MC. 2015. Feeding ecology of bonobos living in forest?savannah mosaics: Diet seasonal variation and importance of fallback foods. American Journal of Primatology 77 (9): 948-962.
Simmen B, Hladik A, Ramasirisoa P. 2003. Food intake and dietary overlap in native Lemur catta and Propithecus verreauxi and introduced Eulemur fulvus at Berenty, southern Madagascar. International Journal of Primatology 24: 949-968.
Sokal RR, Rohlf FJ. 1981. Biometry. The Principles and Pratice of Statistics in Biological Research. New York, USA.
Srivastava A. 1989. Feeding ecology and behaviour of Hanuman langur (Presbytis entellus). Ph.D. Thesis, University of Jodhpur, Jodhpur, India.
Stanford CB. 1991. The capped langur in Bangladesh: behavioral ecology and reproductive tactice (Vol. 26). Karger Medical and Scientific Publishers.
Stanford CB. 1991a. The diet of the capped langur (Presbytis piliata) in a moist deciduous forest in Bangladesh. International Journal of Primatology 12 (3): 199-216.
Sugiyama Y. 1964. Group composition, population density and some sociological observations of hanuman langurs. Primates 5 (3-4): 7-37.
Terborgh J. 1986. Keystone plant resources in the tropical forest. Conservation biology: The science of scarcity and diversity 330-344.
Van Schaik CP, Van Noordwijk MA, de Boer RJ, den Tonkelaar I. 1983. The effect of group size on time budgets and social behaviour in wild long-tailed macaques (Macaca fascicularis). Behavioral ecology and sociobiology 13 (3): 173-181.
Wada K. 2005. The distribution pattern of Rhesus and Assamese monkeys in Nepal. Primates 46: 115-119.
Waterman PG, Ross JA, Bennett EL, Davies AG. 1988. A comparison of the floristics and leaf chemistry of the tree flora in two Malaysian rain forests and the influence of leaf chemistry on populations of colobine monkeys in the Old World. Biological Journal of Linnean Society 34 (1): 1-32.
Altmann J. 1974. Observational study of behavior: sampling methods. Behaviour 49 (3-4): 227-266.
Altmann J, Altmann SA, Hausfater G, McCuskey SA. 1977. Life history of yellow baboons: physical development, reproductive parameters, and infant mortality. Primates 18 (2): 315-330.
Atsalis S. 1999. Diet of the brown mouse lemur (Microcebus rufus) in Ranomafana National Park, Madagascar. International Journal of Primatology 20 (2): 193-229.
Boonratana R, Chalise M, Das J, Htun S, Timmins RJ. 2008. Macaca assamensis, Assam macaque. The IUCN Red List of Threatened Species: e.T12549A3354977. DOI: 10.2305/IUCN.UK.2008.RLTS. T12549A 3354977.en.
Cabana F, Dierenfeld E, Wirdateti W, Donati G, Nekaris KAI. 2017. The seasonal feeding ecology of the Javan slow loris (Nycticebus javanicus). American Journal of Physical Anthropology 162 (4): 768-781.
Chalise MK. 1997. Survey of primates in Makalu-Barun Conservation Area (lower parts of Apsuwa, Isuwa and Sankhuwa rivers). A research report submitted to MBCA Project, Nepal.
Chalise MK. 1999. Some behavioral and ecological aspects of Assamese monkeys (Macaca assamensis) in Makalu-Barun Area, Nepal. Nepal Journal of Science and Technology 1: 85-90.
Chalise MK. 2003. Assamese macaques (Macaca assamensis) in Nepal. Primate Conservation 19: 99-107.
Chalise MK. 2008. Primate census in Kathmandu and west parts of Nepal. Journal of Natural History Museum 23: 60-64.
Chalise MK. 2010. A study of Assamese monkey in Sebrubeshi of Langtang National Park, Nepal. Journal of Natural History Museum 25: 54-61.
Chalise MK. 2013. Fragmented primate population of Nepal. In: Marsh LK, Chapman CA (eds) Primates in Fragments: Complexity and Resilience. Springer Science+Business Media, New York 329-356.
Chalise MK, Bhattarai GP, Pandey B. 2013. Ecology and behavior of Assamese monkeys in Shivapuri Nagarjun National Park, Nepal. Journal of Natural History Museum 27: 12-24.
Chalise MK, Karki JB, Ghimire MK. 2005. Status in Nepal: Non-human Primates. Special issue on the occasion of 10th Wildlife Week, 2062. Department of National Parks & Wildlife Conservation, Kathmandu, Nepal.
Chapman CA, Chapman LJ, Wrangham RW. 1995. Ecological constraints on group size: an analysis of spider monkey and chimpanzee subgroups. Behavioral Ecology and Sociobiology 36 (1): 59-70.
Chapman CA, Chapman LJ, Struhsaker TT, Zanne AE, Clark CJ, Poulsen JR. 2005. A long-term evaluation of fruiting phenology: importance of climate change. Journal of Tropical Ecology 21: 31-45.
Clink DJ, Dillis C, Feilen KL, Beaudrot L, Marshall AJ. 2017. Dietary diversity, feeding selectivity, and responses to fruit scarcity of two sympatric Bornean primates (Hylobates albibarbis and Presbytis rubicunda rubida). PloS one 12 (3), e0173369.
Clutton?Brock TH, Harvey PH. 1977. Primate ecology and social organization. Journal of zoology 183 (1): 1-39.
Davies AG, Bennett EL, Waterman PG. 1988. Food selection by two South-east Asian colobine monkeys (Presbytis rubicunda and Presbytis melalophos) in relation to plant chemistry. Biological Journal of Linnean Society 34 (1): 33-56.
Doran D. 1997. Influence of seasonality on activity patterns, feeding behavior, ranging, and grouping patterns in Tai chimpanzees. International Journal of Primatology 18 (2): 183-206.
Dunn JC, Cristobal-Azkarate J, Vea JJ. 2010. Seasonal variations in the diet and feeding effort of two groups of Howlers in different sized forest fragments. International Journal of Primatology 31: 887-903.
Frechette JL, Hon N, Behie A, Rawson BM. 2017. Seasonal variation in the diet and activity budget of the northern yellow-cheeked crested gibbon Nomascus annamensis. Cambodian Journal of Natural History 2: 168-178.
Ghimire SC, Chalise MK. 2018. Status of crop raiding by Assamese monkeys (Macaca assamensis) along the Budhigandaki river, central Nepal. Journal of Natural History Museum 30: 294-305. DOI: 10.3126/jnhm.v30i0.27605.
Ghimire SC, Chalise MK. 2019. Crop Raiding Status by Assamese Monkeys (Macaca assamensis) along the Kaligandaki River, Western Nepal. Journal of Institute of Science and Technology 24 (1): 72-76. DOI: 10.3126/jist. v24i1.24639.
Gould L, Sussman RW, Sauther ML. 1999. Natural disasters and primate populations: The effects of a 2-year drought on a naturally occurring population of ring-tailed lemurs (Lemur catta) in southwestern Madagascar. International Journal of Primatology 20 (1): 69-84.
Grueter CC. 2016. Environmental seasonality. The international encyclopedia of primatology 1-2.
Guo S, Li B, Watanabe K. 2007. Diet and activity budget of Rhinopithecus roxellana in the Qinling Mountains, China. Primates 48: 268-276.
Hemingway CA, Bynum N. 2005. The influence of seasonality on primate diet and ranging. Cambridge Studies in Biological and Evolutionary Anthropology 44: 57-104.
Iwano T. 1973. The seasonality and nomadic life of a feral troop of Japanese monkeys. A case of the T-Ib troop of the Takagoyama area, the Boso Peninsula. Master Thesis, the University of Tokyo.
Janson CH, Chapman CA. 1999. Resources and primate community structure. Primate Communities 237-267.
Janson CH, Goldsmith ML. 1995. Predicting group size in primates: foraging costs and predation risks. Behavioral Ecology 6 (3): 326-336.
Kaplin BA, Munyaligoga V, Moermond TC. 1998. The Influence of Temporal Changes in Fruit Availability on Diet Composition and Seed Handling in Blue Monkeys (Cercopithecus mitis doggetti). Biotropica 30 (1): 56-71.
Khanal L, Chalise MK, He K, Acharya BK, Kawamoto Y, Jiang X. 2018a. Mitochondrial DNA analyses and ecological niche modeling reveal post-LGM expansion of the Assam macaque (Macaca assamensis) in the foothills of Nepal Himalaya. American Journal of Primatology 80 (3): e22748. DOI: 10.1002/ajp.22748.
Knott CD. 1998. Changes in orangutan caloric intake, energy balance, and ketones in response to fluctuating fruit availability. International Journal of Primatology 19 (6): 1061-1079.
Knott CD. 2005. Energetic responses to food availability in the great apes: implications for homonin evolution. Seasonality in primates: Studies of living and extinct human and non-human primates 44: 351-378.
Marshall AJ, Wrangham RW. 2007. Evolutionary consequences of fallback foods. International Journal of Primatology 28: 1219-1235.
Martin P, Bateson P. 1993. Measuring behaviour: an introductory guide. Cambridge University Press.
McKey DB. 1978. Soils, vegetation and seed-eating by black colobus monkeys. The ecology of arboreal folivores 423-438.
Mitani JC, Watts DP. 2005. Correlates of territorial boundary patrol behaviour in wild chimpanzees. Animal Behaviour 70 (5): 1079-1086.
Nishida T. 1976. The bark-eating habits in primates, with special reference to their status in the diet of wild chimpanzees. Folia Primatologica 25 (4): 277-287.
Norsica I, Carrai V, Borgognini-Tarli SM. 2006. Influence of dry season and food quality and quantity on behavior and feeding strategy of Propithecus verreauxi in Kirindy, Madagascar. International Journal of Primatology 27: 1001-1022.
Oates JF, Waterman PG, Choo GM. 1980. Food selection by the south Indian leaf-monkey, Presbytis johnii, in relation to leaf chemistry. Oecologia 45 (1): 45-56.
Overdorff DJ. 1993. Similarities, differences, and seasonal patterns in the diet of Eulemur rubriventer and Eulemur fulvus rufus in the Ranomafana National Park, Madagascar. International Journal of Primatology 14: 721-753.
Paudel PK. 2017. Conflict due to Assamese macaques (Macaca assamensis McClelland, 1840) and crop protection strategies in Kaligandaki river basin, western Nepal. Our Nature 14 (1): 107. DOI: 10.3126/on.v14i1.16449.
Puri GS. 1960. Indian forest ecology. A comprehensive survey of vegetation and its environment in the Indian subcontinent [Vols. I & II]. New Delhi: Oxford Books.
Remis MJ, Dierenfeld ES, Mowry CB, Carroll RW. 2001. Nutritional aspects of western lowland gorilla (Gorilla gorilla gorilla) diet during seasons of fruit scarcity at Bai Hokou, Central African Republic. International Journal of Primatology 22 (5): 807-836.
Serckx A, Kühl HS, Beudels?Jamar RC, Poncin P, Bastin JF, Huynen MC. 2015. Feeding ecology of bonobos living in forest?savannah mosaics: Diet seasonal variation and importance of fallback foods. American Journal of Primatology 77 (9): 948-962.
Simmen B, Hladik A, Ramasirisoa P. 2003. Food intake and dietary overlap in native Lemur catta and Propithecus verreauxi and introduced Eulemur fulvus at Berenty, southern Madagascar. International Journal of Primatology 24: 949-968.
Sokal RR, Rohlf FJ. 1981. Biometry. The Principles and Pratice of Statistics in Biological Research. New York, USA.
Srivastava A. 1989. Feeding ecology and behaviour of Hanuman langur (Presbytis entellus). Ph.D. Thesis, University of Jodhpur, Jodhpur, India.
Stanford CB. 1991. The capped langur in Bangladesh: behavioral ecology and reproductive tactice (Vol. 26). Karger Medical and Scientific Publishers.
Stanford CB. 1991a. The diet of the capped langur (Presbytis piliata) in a moist deciduous forest in Bangladesh. International Journal of Primatology 12 (3): 199-216.
Sugiyama Y. 1964. Group composition, population density and some sociological observations of hanuman langurs. Primates 5 (3-4): 7-37.
Terborgh J. 1986. Keystone plant resources in the tropical forest. Conservation biology: The science of scarcity and diversity 330-344.
Van Schaik CP, Van Noordwijk MA, de Boer RJ, den Tonkelaar I. 1983. The effect of group size on time budgets and social behaviour in wild long-tailed macaques (Macaca fascicularis). Behavioral ecology and sociobiology 13 (3): 173-181.
Wada K. 2005. The distribution pattern of Rhesus and Assamese monkeys in Nepal. Primates 46: 115-119.
Waterman PG, Ross JA, Bennett EL, Davies AG. 1988. A comparison of the floristics and leaf chemistry of the tree flora in two Malaysian rain forests and the influence of leaf chemistry on populations of colobine monkeys in the Old World. Biological Journal of Linnean Society 34 (1): 1-32.
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