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Fruiting and flushing phenology in Asian tropical and temperate forests: implications for primate ecology

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Abstract

In order to understand the ecological adaptations of primates to survive in temperate forests, we need to know the general patterns of plant phenology in temperate and tropical forests. Comparative analyses have been employed to investigate general trends in the seasonality and abundance of fruit and young leaves in tropical and temperate forests. Previous studies have shown that (1) fruit fall biomass in temperate forest is lower than in tropical forest, (2) non-fleshy species, in particular acorns, comprise the majority of the fruit biomass in temperate forest, (3) the duration of the fruiting season is shorter in temperate forest, and (4) the fruiting peak occurs in autumn in most temperate forests. Through our comparative analyses of the fruiting and flushing phenology between Asian temperate and tropical forests, we revealed that (1) fruiting is more annually periodic (the pattern in one year is similar to that seen in the next year) in temperate forest in terms of the number of fruiting species or trees, (2) there is no consistent difference in interannual variations in fruiting between temperate and tropical forests, although some oak-dominated temperate forests exhibit extremely large interannual variations in fruiting, (3) the timing of the flushing peak is predictable (in spring and early summer), and (4) the duration of the flushing season is shorter. The flushing season in temperate forests (17–28 % of that in tropical forests) was quite limited, even compared to the fruiting season (68 %). These results imply that temperate primates need to survive a long period of scarcity of young leaves and fruits, but the timing is predictable. Therefore, a dependence on low-quality foods, such as mature leaves, buds, bark, and lichens, would be indispensable for temperate primates. Due to the high predictability of the timing of fruiting and flushing in temperate forests, fat accumulation during the fruit-abundant period and fat metabolization during the subsequent fruit-scarce period can be an effective strategy to survive the lean period (winter).

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References

  • Anderson DP, Nordheim EV, Moermond TC, Gone Bi ZB, Boesch C (2005) Factors influencing tree phenology in Taï National Park, Côte d’Ivoire. Biotropica 37:631–640

    Article  Google Scholar 

  • Badgley C, Fox DL (2000) Ecological biogeography of North American mammals: species density and ecological structure in relation to environmental gradients. J Biogeogr 27:1437–1467

    Article  Google Scholar 

  • Clutton-Brock TH (1977) Primate ecology: studies of feeding and ranging behaviour in lemurs, monkeys and apes. Academic, Brighton

  • Dormann CF, McPherson JM, Araujo MB, Bivand R, Bolliger J, Carl G, Davies RG, Hirzel A, Jetz W, Kissling WD, Kuhn I, Ohlemuller R, Peres-Neto PR, Reineking B, Schroder B, Schurr FM, Wilson R (2007) Methods to account for spatial autocorrelation in the analysis of species distributional data: a review. Ecography 30:609–628

    Article  Google Scholar 

  • Eeley H, Lawes MJ (1999) Large-scale patterns of species richness and species range size in anthropoid primates. In: Fleagle J, Janson C, Reed K (eds) Primate communities. Cambridge University Press, Cambridge, pp 191–219

    Chapter  Google Scholar 

  • Fleagle JG (1999) Primate adaptation and evolution, 2nd edn. Academic, London

  • Ganesh T, Davidar P (1999) Fruit biomass and relative abundance of frugivores in a rain forest of southern Western Ghats, India. J Trop Ecol 15:399–413

    Article  Google Scholar 

  • Grueter CC, Li DY, van Schaik CP, Ren BP, Long YC, Wei FW (2008) Ranging of Rhinopithecus bieti in the Samage Forest, China. I. Characteristics of range use. Int J Primatol 29:1121–1145

    Article  Google Scholar 

  • Grueter CC, Li DY, Ren BP, Wei FW, Xiang ZF, van Schaik CP (2009) Fallback foods of temperate-living primates: a case study on snub-nosed monkeys. Am J Phys Anthropol 140:700–715

    Article  PubMed  Google Scholar 

  • Guo SG, Li BG, Watanabe K (2007) Diet and activity budget of Rhinopithecus roxellana in the Qinling Mountains, China. Primates 48:268–276

    Article  PubMed  Google Scholar 

  • Hanya G (2004) Diet of a Japanese macaque troop in the coniferous forest of Yakushima. Int J Primatol 25:55–71

    Article  Google Scholar 

  • Hanya G (2009) Effects of food type and number of feeding sites in a tree on aggression during feeding in wild Macaca fuscata. Int J Primatol 30:569–581

    Article  Google Scholar 

  • Hanya G, Aiba S (2010a) Fruit fall in five warm- and cool-temperate forests in Yakushima, Japan. For Stud China 12:184–192

    Article  Google Scholar 

  • Hanya G, Aiba S (2010b) Fruit fall in tropical and temperate forests: implications for frugivore diversity. Ecol Res 25:1081–1090

    Article  Google Scholar 

  • Hanya G, Aiba S (2011) Annual periodicity in fruiting in temperate forests in Yakushima, Japan. For Stud China 13:112–122

    Article  Google Scholar 

  • Hanya G, Bernard H (2012) Fallback foods of red leaf monkey (Presbytis rubicunda) in Danum Valley, Borneo. Int J Primatol 33:322–337

    Article  Google Scholar 

  • Hanya G, Kiyono M, Yamada A, Suzuki K, Furukawa M, Yoshida Y, Chijiiwa A (2006) Not only annual food abundance but also fallback food quality determines the Japanese macaque density: evidence from seasonal variations in home range size. Primates 47:275–278

    Article  PubMed  Google Scholar 

  • Hanya G, Kiyono M, Hayaishi S (2007) Behavioral thermoregulation of wild Japanese macaques: comparisons between two subpopulations. Am J Primatol 69:802–815

    Article  PubMed  Google Scholar 

  • Hanya G, Menard N, Qarro M, Ibn Tattou M, Fuse M, Vallet D, Yamada A, Go M, Takafumi H, Tsujino R, Agetsuma N, Wada K (2011a) Dietary adaptations of temperate primates: comparisons of Japanese and Barbary macaques. Primates 52:187–198

    Article  PubMed  Google Scholar 

  • Hanya G, Stevenson P, van Noordwijk M, Wong ST, Kanamori T, Kuze N, Aiba S, Chapman CA, van Schaik C (2011b) Seasonality in fruit availability affects frugivorous primate biomass and species richness. Ecography 34:1009–1017

    Article  Google Scholar 

  • Hendrick RL (2001) Forest types and classification. In: Evans J (ed) The forests handbook, vol 1: an overview of forest science. Blackwell, Oxford, pp 23–64

  • Hillebrand H (2004) On the generality of the latitudinal diversity gradient. Am Nat 163:192–211

    Article  PubMed  Google Scholar 

  • Hohmann G, Robbins MM, Boesch C (2006) Feeding ecology in apes and other primates. Cambridge University Press, Cambridge

    Google Scholar 

  • Iwamoto T, Dunbar RIM (1983) Thermoregulation, habitat quality and the behavioral ecology of gelada baboons. J Anim Ecol 52:357–366

    Article  Google Scholar 

  • Kanamori T, Kuze N, Bernard H, Malim TP, Kohshima S (2010) Feeding ecology of Bornean orangutans (Pongo pygmaeus morio) in Danum Valley, Sabah, Malaysia: a 3-year record including two mast fruitings. Am J Primatol 72:820–840

    Article  PubMed  Google Scholar 

  • Kay RNB, Davies AG (1994) Digestive physiology. In: Davies AG, Oates JF (eds) Colobine monkeys: their ecology, behaviour and evolution. Cambridge University Press, Cambridge, pp 229–249

    Google Scholar 

  • Lechowicz MJ (1995) Seasonality of flowering and fruiting in temperate forest trees. Can J Bot Rev Can Bot 73:175–182

    Article  Google Scholar 

  • Li BG, Chen C, Ji WH, Ren BP (2000) Seasonal home range changes of the Sichuan snub-nosed monkey (Rhinopithecus roxellana) in the Qinling mountains of China. Folia Primatol 71:375–386

    Article  PubMed  CAS  Google Scholar 

  • Martyn D (1992) Climates of the world. Elsevier, Amsterdam

    Google Scholar 

  • Muroyama Y, Kanamori H, Kitahara E (2006) Seasonal variation and sex differences in the nutritional status in two local populations of wild Japanese macaques. Primates 47:355–364

    Article  PubMed  Google Scholar 

  • Nakagawa N, Iwamoto T, Yokota N, Soumah AG (1996) Inter-regional and inter-seasonal variations of food quality in Japanese macaques: constraints of digestive volume and feeding time. In: Fa JE, Lindburg DG (eds) Evolution and ecology of macaque societies. Cambridge University Press, New York, pp 207–234

    Google Scholar 

  • Otani T (2005) Characteristics of middle-size mammals as a seed disperser of fleshy-fruited plants (in Japanese). Nagoya Univ For Sci 24:7–43

    Google Scholar 

  • Pond CM (1978) Morphological aspects and ecological and mechanical consequences of fat deposition in wild vertebrates. Annu Rev Ecol Syst 9:519–570

    Article  Google Scholar 

  • Sakai S (2002) General flowering in lowland mixed dipterocarp forests of South-East Asia. Biol J Linn Soc 75:233–247

    Google Scholar 

  • Sayers K, Norconk MA (2008) Himalayan Semnopithecus entellus at Langtang National Park, Nepal: diet, activity patterns, and resources. Int J Primatol 29:509–530

    Article  Google Scholar 

  • Stevens RD, Willig MR (2002) Geographical ecology at the community level: perspectives on the diversity of new world bats. Ecology 83:545–560

    Article  Google Scholar 

  • Takasaki H (1981) Troop size, habitat quality, and home range area in Japanese macaques. Behav Ecol Sociobiol 9:277–281

    Article  Google Scholar 

  • Takyu M, Kubota Y, Aiba S, Seino T, Nishimura T (2005) Pattern of changes in species diversity, structure and dynamics of forest ecosystems along latitudinal gradients in East Asia. Ecol Res 20:287–296

    Article  Google Scholar 

  • Ting S, Hartley S, Burns KC (2008) Global patterns in fruiting seasons. Glob Ecol Biogeogr 17:648–657

    Article  Google Scholar 

  • Tsuji Y, Takatsuki S (2012) Interannual variation in nut abundance is related to agonistic interactions of foraging female Japanese macaques (Macaca fuscata). Int J Primatol 33:489–512

    Article  Google Scholar 

  • Valdespino C (2007) Physiological constraints and latitudinal breeding season in the Canidae. Physiol Biochem Zool 80:580–591

    Article  PubMed  Google Scholar 

  • van Schaik CP, Pfannes K (2005) Tropical climates and phenology: a primate perspective. In: Brockman DK, van Schaik CP (eds) Seasonality in primates: studies of living and extinct human and non-human primates. Cambridge University Press, Cambridge, pp 23–54

    Chapter  Google Scholar 

  • van Schaik CP, Terborgh JW, Wright SJ (1993) The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annu Rev Ecol Syst 24:353–377

    Article  Google Scholar 

  • Wada K (1975) Ecology of wintering among Japanese monkeys in Shiga Heights and its adaptive significance (in Japanese). Physiol Ecol Jpn 16:9–14

    Google Scholar 

  • White LJT (1994) Patterns of fruit fall phenology in the Lopé Reserve, Gabon. J Trop Ecol 10:289–312

    Article  Google Scholar 

  • Willson MF, Irvine AK, Walsh NG (1989) Vertebrate dispersal syndromes in some Australian and New Zealand plant communities, with geographic comparisons. Biotropica 21:133–147

    Article  Google Scholar 

  • Zhao QK (1994) Seasonal changes in body weight of Macaca thibetana at Mt-Emei, China. Am J Primatol 32:223–226

    Article  Google Scholar 

  • Zhou YB, Newman C, Xu WT, Buesching CD, Zalewski A, Kaneko Y, Macdonald DW, Xie ZQ (2011) Biogeographical variation in the diet of Holarctic martens (genus Martes, Mammalia: Carnivora: Mustelidae): adaptive foraging in generalists. J Biogeogr 38:137–147

    Article  Google Scholar 

Download references

Acknowledgments

We would like to thank our friends and colleagues who helped us with our fieldwork in Japan, China, and Malaysia, which formed the basis of this paper. We thank Kevin Burns for his advice on circular statistics. This study was financed by the MEXT Grant-in-Aid (nos. 20770195, 22687002, 23657018) to GH, the 21st Century COE Program (A14), the Global COE Program “Formation of a Strategic Base for Biodiversity and Evolutionary Research: from Genome to Ecosystem,” and the Kyoto University Foundation.

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Hanya, G., Tsuji, Y. & Grueter, C.C. Fruiting and flushing phenology in Asian tropical and temperate forests: implications for primate ecology. Primates 54, 101–110 (2013). https://doi.org/10.1007/s10329-012-0341-3

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