Abstract
Folivorous primates have long been assumed to experience food competition less acutely than frugivores due to their ability to eat leaves, an abundant resource in most forest systems. Consequently, the behavioural responses of leaf-eating primates to variation in food availability are less well characterised than those of frugivores. Recent empirical studies have demonstrated that many colobine species are more affected by food availability and distribution than previously thought; they employ multiple strategies to survive during periods of food scarcity. We studied a population of proboscis monkeys (Nasalis larvatus) over 16 months in three forest types in West Kalimantan, Indonesia, to examine their responses to temporal fluctuation and spatial variation in food availability. We examined how feeding behaviour was influenced by the availability of plants in botanical plots to identify important and preferred foods of proboscis monkeys across months and in different forest types. Proboscis monkeys consumed foods from 68 genera, comprising 35% young leaves, 27% unripe fruit, 12% flowers and 6% mature leaves. Consumption of plant parts and genera by proboscis monkeys varied in response to monthly changes in food availability but did not vary among forest types despite substantial differences in phenology and floristics among them. The monkeys preferred unripe fruits and flowers and used young and mature leaves as fallback foods in mangrove forests. Documentation of proboscis monkey responses to variation in food availability contributes to our understanding of how monkeys respond to changes in their environments due to climate change and habitat degradation.
References
1.
Ahumada JA, Stevenson PR, Quiñones MJ (1998). Ecological response of spider monkeys to temporal variation in fruit abundance: the importance of flooded forest as a keystone habitat. Primate Conservation 18: 10–14.
2.
Altmann J (1974). Observational study of behavior – sampling methods. Behaviour 49: 227–267.
3.
Bennett EL, Sebastian AC (1988). Social organization and ecology of proboscis monkeys (Nasalis larvatus) in mixed coastal forest in Sarawak. International Journal of Primatology9: 233–255.
4.
Bernard H, Matsuda I, Hanya G, Phua MH, Oram F, Ahmad AH (2018). Feeding ecology of the proboscis monkey in Sabah, Malaysia, with special reference to plant species-poor forests. In Primates in Flooded Habitats: Ecology and Conservation(Nowak K, Barnett AA, Matsuda I, eds.), pp 89–98. Cambridge, Cambridge University Press.
5.
Boonratana R (1994). The Ecology and Behaviour of the Proboscis Monkey ( Nasalis larvatus) in the Lower Kinabatangan, Sabah. Bangkok, Mahidol University.
6.
Boonratana R (2003). Feeding ecology of proboscis monkeys (Nasalis larvatus) in the Lower Kinabatangan, Sabah, Malaysia. Sabah Parks Nature Journal 6: 1–26.
7.
Chapman CA, Chapman LJ (1999). Implications of small-scale variation in ecological conditions for the diet and density of red colobus monkeys. Primates 40: 215–231.
8.
Chapman CA, Wrangham RW, Chapman LJ (1995). Ecological constraints on group size: an analysis of spider monkey and chimpanzee subgroups. Behavioral Ecology and Sociobiology 36: 59–70.
9.
Chazdon RL, Careaga S, Webb C, Vargas O (2003). Community and phylogenetic structure of reproductive traits of woody species in wet tropical forests. Ecological Monographs 73: 331–348.
10.
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: e0173369.
11.
Clutton-Brock TH, Harvey PH (1977). Primate ecology and social organization. Journal of Zoology (London) 183: 1–40.
12.
Davies TJ, Wolkovich EM, Kraft NJ, Salamin N, Allen JM, Ault TR, et al (2013). Phylogenetic conservatism in plant phenology. Journal of Ecology 101: 1520–1530.
13.
Doran D (1997). Influence of seasonality on activity patterns, feeding behavior, ranging, and grouping patterns in Tai chimpanzees. International Journal of Primatology 18: 183–206.
14.
Feilen KL, Marshall AJ (2014). Sleeping site selection by proboscis monkeys (Nasalis larvatus) in West Kalimantan, Indonesia. American Journal of Primatology 76: 1127–1139.
15.
Feilen KL, Marshall AJ (2017). Multiple ecological factors influence the location of proboscis monkey (Nasalis larvatus) sleeping sites in West Kalimantan, Indonesia. International Journal of Primatology 38: 448–465.
16.
Freeland WJ, Janzen DH (1974). Strategies in herbivory by mammals: the role of plant secondary compounds. The American Naturalist 108: 269–289.
17.
Grueter CC, Li DY, Ren BP, Wei FW, van Schaik CP (2009a). Dietary profile of Rhinopithecus bieti and its socioecological implications. International Journal of Primatology 30: 601–624.
18.
Grueter CC, Li DY, Ren BP, Wei FW, Xiang ZF, van Schaik CP (2009b). Fallback foods of temperate-living primates: a case study on snub-nosed monkeys. American Journal of Physical Anthropology 140: 700–715.
19.
Harris TR, Chapman CA (2007). Variation in diet and ranging of black and white colobus monkeys in Kibale National Park, Uganda. Primates 48: 208–221.
20.
Hemingway CA, Bynum N (2005). The influence of seasonality on primate diet and ranging. In Seasonality in Primates: Studies of Living and Extinct Human and Non-Human Primates (Brockman DK, van Schaik C, eds.), pp 54–104. Cambridge, Cambridge University Press.
21.
Hu G (2011). Dietary breadth and resource use of François’ langur in a seasonal and disturbed habitat. American Journal of Primatology 73: 1176–1187.
22.
Isbell LA (1991). Contest and scramble competition: patterns of female aggression and ranging behavior among primates. Behavioral Ecology 2: 143–155.
23.
Isbell LA (2004). Is there no place like home? Ecological bases of female dispersal and philopatry and their consequences for the formation of kin groups. In Kinship and Behavior in Primates (Chapais B, Berman CM, eds.), pp 71–108. New York, Oxford University Press.
24.
Isbell LA, Pruetz JD, Young TP (1998). Movements of vervets (Cercopithecus aethiops) and patas monkeys (Erythrocebus patas) as estimators of food resource size, density, and distribution. Behavioral Ecology and Sociobiology 42: 123–133.
25.
Janzen DH (1974). Tropical blackwater rivers, animals, and mast fruiting by the Dipterocarpaceae. Biotropica 6: 69–103.
26.
MacArthur RH, Pianka ER (1966). On optimal use of a patchy environment. The American Naturalist 100: 603–609.
27.
Marshall AJ, Leighton M (2006). How does food availability limit the population density of white-bearded gibbons? In Feeding Ecology in Apes and Other Primates. Ecological, Physical and Behavioral Aspects (Hohmann G, Robbins H, Boesch C, eds.), pp 313–335. Cambridge, Cambridge University Press.
28.
Marshall AJ, Wich SA (2013). Characterization of primate environments through assessment of plant phenology. In Primate Ecology and Conservation: A Handbook of Techniques (Sterling E, Blair M, Bynum N, eds.), pp 103–127. Oxford, Oxford University Press.
29.
Marshall AJ, Wrangham RW (2007). Evolutionary consequences of fallback foods. International Journal of Primatology 28: 1218–1235.
30.
Marshall AJ, Boyko CM, Feilen KL, Boyko RH, Leighton M (2009). Defining fallback foods and considering their importance in primate ecology and evolution. American Journal of Physical Anthropology 140: 603–614.
31.
Matsuda I, Clauss M, Tuuga A, Sugau J, Hanya G, Yumoto T, Bernard H, Hummel J (2017). Factors affecting leaf selection by foregut-fermenting proboscis monkeys: new insight from in vitro digestibility and toughness of leaves. Scientific Reports 17: 42774.
32.
Matsuda I, Tuuga A, Higashi S (2009). The feeding ecology and activity budget of proboscis monkeys. American Journal of Primatology 71: 478–492.
33.
McKey DB, Waterman PG (1987). Seeds as a resource – the evolutionary ecology of seeds and its implications for seed-eating by primates. International Journal of Primatology 8: 433.
34.
Menon S, Poirier FE (1996). Lion-tailed macaques (Macaca silenus) in a disturbed forest fragment: activity patterns and time budget. International Journal of Primatology17: 969–985.
35.
Milton K (1984). Habitat, diet, and activity patterns of free-ranging woolly spider monkeys (Brachyteles arachnoides E-Geoffroy 1806). International Journal of Primatology 5: 491–514.
36.
Oksanen J, Blanchet FG, Kindt R, Legendre P, O’Hara RB, Simpson GL, et al (2013). vegan: community ecology package. R package (vol. version 2.0–7). http://CRAN.R-project.org/package=vegan.
37.
R Core Development Team (2013). R: a language and environment for statistical computing. Vienna, R Foundation for Statistical Computing.
38.
Roshier DA, Doerr VAJ, Doerr ED (2008). Animal movement in dynamic landscapes: interaction between behavioural strategies and resource distributions. Oecologia 156: 465–477.
39.
Salter RE, MacKenzie NA, Nightingale N, Aken KM, Chai P (1985). Habitat use, ranging behavior, and food habitat of the proboscis monkey, Nasalis larvatus (van Wurmb), in Sarawak. Primates26: 436–451.
40.
Savage RE (1931). The relationship between the feeding of the herring of the east coast of England and the plankton of the surrounding waters. Fishery Investigation, Ministry of Agriculture, Food and Fisheries Series 2: 1–88.
41.
Snaith TV, Chapman CA (2007). Primate group size and interpreting socioecological models: do folivores really play by different rules? Evolutionary Anthropology 16: 94–106.
42.
Snaith TV, Chapman CA (2008). Red colobus monkeys display alternative behavioral responses to the costs of scramble competition. Behavioral Ecology 19: 1289–1296.
43.
Soendjoto MA, Alikodra HS, Bismark M, Setijanto H (2006). Jenis dan komposisi pakan bekantan (Nasalis larvatus Wurmb) di hutan karet Kabupaten Tabalong, Kalimantan Selatan (Diet and its composition of the proboscis monkey [Nasalis larvatus Wurmb] in rubber forest of Tabalong District, South Kalimantan). Biodiversitas 7: 34–38.
44.
Steenbeek R, van Schaik CP (2001). Competition and group size in Thomas’s langurs (Presbytis thomasi): the folivore paradox revisited. Behavioral Ecology and Sociobiology 49: 100–110.
45.
Sterck EHM, Watts DP, van Schaik CP (1997). The evolution of female social relationships in nonhuman primates. Behavioral Ecology and Sociobiology 41: 291–309.
46.
Struhsaker T (2010). The Red Colobus Monkeys: Variation in Demography, Behavior, and Ecology of Endangered Species. Oxford, Oxford University Press.
47.
Van Schaik CP (1983). Why are diurnal primates living in groups? Behaviour 87: 120–144.
48.
Van Schaik CP, Terborgh JW, Wright SJ (1993). The phenology of tropical forests – adaptive significance and consequences for primary consumers. Annual Review of Ecology and Systematics24: 353–377.
49.
Vogel ER, Haag L, Mitra-Setia T, van Schaik CP, Dominy NJ (2009). Foraging and ranging behavior during a fallback episode: Hylobates albibarbis and Pongo pygmaeus wurmbii compared. American Journal of Physical Anthropology 140: 716–726.
50.
Wallace RB (2005). Seasonal variations in diet and foraging behavior of Ateles chamek in a southern Amazonian tropical forest. International Journal of Primatology 26: 1053–1075.
51.
Wrangham RW (1980). An ecological model of female-bonded primate groups. Behaviour 75: 262–300.
52.
Yeager CP (1989). Feeding ecology of the proboscis monkey (Nasalis larvatus). International Journal of Primatology 10: 497–530.
53.
Yeager CP (1991). Proboscis monkey (Nasalis larvatus) social organization: intergroup patterns of association. American Journal of Primatology 23: 73–86.
54.
Yeager CP, Kirkpatrick RC (1998). Asian colobine social structure: ecological and evolutionary constraints. Primates 39: 147–155.
© 2020 S. Karger AG, Basel
2020
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.
