Skip to main content

Advertisement

Log in

Seasonal variation in energy balance of wild Japanese macaques (Macaca fucata yakui) in a warm-temperate forest: a preliminary assessment in the coastal forest of Yakushima

  • Original Article
  • Published:
Primates Aims and scope Submit manuscript

Abstract

Food scarcity is a major challenge for primates living in temperate forests, where food availability varies markedly among seasons. In Japanese macaques, which are exclusively distributed in temperate zones, the fat accumulation ability has been highlighted as an adaptation for survival during the lean season and for reproductive success. However, the knowledge of energetic strategies of Japanese macaques has been mainly derived from data on cool-temperate forests, where fallback foods comprise winter buds and bark. Data on Japanese macaques in warm-temperate forests where fallback foods comprise mature leaves are still lacking. We aimed to identify seasonal variations in energy balance and the relative importance of ingestion rates (dry matter intake per feeding time), energy content of the food, and feeding time in energy intake of Japanese macaques in the coastal forest of Yakushima. We estimated energy balance of 6–12 adult females from October 2012 to October 2013. We estimated energy intake based on the data on feeding behavior and energy content of the diet and calculated energy expenditure based on the previously established relationship between body mass and total energy expenditure. We also quantified urinary C-peptide, which is a non-invasive biomarker of energetic conditions. We demonstrated that energy balance was more positive in the fruit/seed-feeding period than in the mature-leaf-feeding and fruit/fungi-feeding periods and that ingestion rates were the most important component of energy intake. The present study suggests that the fat accumulation ability is an essential adaptation in Japanese macaques even in warm-temperate forests.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Acamovic T, Brooker JD (2005) Biochemistry of plant secondary metabolites and their effects in animals. Proc Nutr Soc 64:403–412

    Article  CAS  PubMed  Google Scholar 

  • Agetsuma N (1995) Foraging strategies of Yakushima macaques (Macaca fuscata yakui). Int J Primatol 15:595–609

    Article  Google Scholar 

  • Agetsuma N, Nakagawa N (1998) Effects of habitat differences on feeding behaviors of Japanese monkeys: comparison between Yakushima and Kinkazan. Primates 39:275–289

    Article  Google Scholar 

  • Amato KR, Garber PA (2014) Nutrition and foraging strategies of the black howler monkey (Alouatta pigra) in Palenque National Park, Mexico. Am J Primatol 76:774–787

    Article  CAS  PubMed  Google Scholar 

  • Aristizabal JF, Rothman JM, García-Fería LM, Serio-Silva JC (2017) Contrasting time-based and weight-based estimates of protein and energy intake of black howler monkeys (Alouatta pigra). Am J Primatol 79:e22611

    Article  CAS  Google Scholar 

  • Brockman DK, van Schaik CP (2005) Seasonality and reproductive function. 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 269–305

    Chapter  Google Scholar 

  • Chapman CA, Chapman LJ, Rode KD, Hauck EM, McDowell LR (2003) Variation in the nutritional value of primate foods: among trees, time periods, and areas. Int J Primatol 24:317–333

    Article  Google Scholar 

  • Crockett CM, Rudran R (1987) Red howler monkey birth data I: seasonal variation. Am J Primatol 13:347–368

    Article  PubMed  Google Scholar 

  • Deschner T, Kratzsch J, Hohmann G (2008) Urinary C-peptide as a method for monitoring body mass changes in captive bonobos (Pan paniscus). Horm Behav 54:620–626

    Article  CAS  PubMed  Google Scholar 

  • Emery Thompson M, Muller MN, Wrangham RW, Lwanga JS, Potts KB (2009) Urinary C-peptide tracks seasonal and individual variation in energy balance in wild chimpanzees. Horm Behav 55:299–305

    Article  PubMed  CAS  Google Scholar 

  • Fooden J, Aimi M (2005) Systematic review of Japanese macaques, Macaca fuscata (Gray, 1870). Fieldiana Zool 104:1–198

    Google Scholar 

  • Fox J, Weisberg S (2011) An {R} companion to applied regression, 2nd Edition. Sage, Thousand Oaks. https://socserv.socsci.mcmaster.ca/jfox/Books/Companion

  • Fujita S, Sugiura H, Mitsunaga F, Shimizu K (2004) Hormone profiles and reproductive characteristics in wild female Japanese macaques (Macaca fuscata). Am J Primatol 64:367–375

    Article  CAS  PubMed  Google Scholar 

  • Furusaka S, Tochigi K, Yamazaki K, Naganuma T, Inagaki A, Koike S (2019) Estimating the seasonal energy balance in Asian black bears and associated factors. Ecosphere 10:e02891

    Article  Google Scholar 

  • Garcia C, Huffman MA, Shimizu K, Speakman JR (2011) Energetic consequences of seasonal breeding in female Japanese macaques (Macaca fuscata). Am J Phys Anthropol 146:161–170

    Article  PubMed  Google Scholar 

  • Gélin U, Coulson G, Festa-Bianchet M (2016) Heterogeneity in reproductive success explained by individual differences in bite rate and mass change. Behav Ecol 27:777–783

    Article  Google Scholar 

  • Girard-Buttoz C, Higham JP, Heistermann M, Wedegärtner S, Maestripieri D, Engelhardt A (2011) Urinary C-peptide measurement as a marker of nutritional status in macaques. PLoS ONE 6:e18042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grueter CC, Li D, Ren B, Wei F, Xiang Z, 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 

  • Grueter CC, Deschner T, Behringer V, Fawcett K, Robbins MM (2014) Socioecological correlates of energy balance using urinary C-peptide measurements in wild female mountain gorillas. Physiol Behav 127:13–19

    Article  CAS  PubMed  Google Scholar 

  • Hama N, Kanemitsu H, Sakamoto K, Oyama Y, Acosta TJ, Ishikawa O, Pengyan W, Okuda K (2008) Development and evaluation of a rapid enzyme-immunoassay system for measurement of the urinary concentration of estrone-3-glucuronide in a female giant panda (Ailuropoda melanoleuca). J Reprod Dev 54:281–285

    Article  CAS  PubMed  Google Scholar 

  • Hamada Y, Hayakawa S, Suzuki J, Watanabe K, Ohkura S (2003) Seasonal variation in the body fat of Japanese macaques Macaca fuscata. Mammal Study 28:79–88

    Article  Google Scholar 

  • Hanson AM, Hodge KT, Porter LM (2003) Mycophagy among primates. Mycologist 17:6–10

    Article  Google Scholar 

  • Hanson AM, Hall MB, Porter LM, Lintzenich B (2006) Composition and nutritional characteristics of fungi consumed by Callimico goeldii in Pando, Bolivia. Int J Primatol 27:323–346

    Article  Google Scholar 

  • Hanya G (2010) Ecological adaptations of temperate primates: population density of Japanese macaques. In: Nakagawa N, Nakamichi M, Sugiura H (eds) The Japanese macaques. Springer, Tokyo, pp 79–97

    Chapter  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Hanya G, Matsubara M, Sugiura H, Hayakawa S, Goto S, Tanaka T, Soltis J, Noma N (2004) Mass mortality of Japanese macaques in a western coastal forest of Yakushima. Ecol Res 19:179–188

    Article  Google Scholar 

  • Hanya G, Kiyono M, Takafumi H, Tsujino R, Agetsuma N (2007) Mature leaf selection of Japanese macaques: effects of availability and chemical content. J Zool 273:140–147

    Article  Google Scholar 

  • Hanya G, Tsuji Y, Grueter CC (2013) Fruiting and flushing phenology in Asian tropical and temperate forests: implications for primate ecology. Primates 54:101–110

    Article  PubMed  Google Scholar 

  • Hanya G, Fuse M, Aiba SI, Takafumi H, Tsujino R, Agetsuma N, Chapman CA (2014) Ecosystem impacts of folivory and frugivory by Japanese macaques in two temperate forests in Yakushima. Am J Primatol 76:596–607

    Article  PubMed  Google Scholar 

  • Hanya G, Otani Y, Hongo S, Honda T, Okamura H, Higo Y (2018) Activity of wild Japanese macaques in Yakushima revealed by camera trapping: patterns with respect to season, daily period and rainfall. PLoS ONE 13:e0190631

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Harris TR, Chapman CA, Monfort SL (2009) Small folivorous primate groups exhibit behavioral and physiological effects of food scarcity. Behav Ecol 21:46–56

    Article  Google Scholar 

  • Harrison ME, Morrogh-Bernard HC, Chivers DJ (2010) Orangutan energetics and the influence of fruit availability in the nonmasting peat-swamp forest of Sabangau, Indonesian Borneo. Int J Primatol 31:585–607

    Article  Google Scholar 

  • Heesen M, Rogahn S, Ostner J, Schülke O (2013) Food abundance affects energy intake and reproduction in frugivorous female Assamese macaques. Behav Ecol Sociobiol 67:1053–1066

    Article  Google Scholar 

  • Hemingway CA, Bynum N (2005) The influence of seasonality on primate diet and ranging. 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 57–104

    Chapter  Google Scholar 

  • Higham JP, Girard-Buttoz C, Engelhardt A, Heistermann M (2011) Urinary C-peptide of insulin as a non-invasive marker of nutritional status: some practicalities. PLoS ONE 6:e22398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hill DA (1997) Seasonal variation in the feeding behavior and diet of Japanese macaques (Macaca fuscata yakui) in lowland forest of Yakushima. Am J Primatol 43:305–320

    Article  CAS  PubMed  Google Scholar 

  • Hill DA, Agetsuma N (1995) Supra-annual variation in the influence of Myrica rubra fruit on the behavior of a troop of Japanese macaques in Yakushima. Am J Primatol 35:241–250

    Article  PubMed  Google Scholar 

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363

    Article  Google Scholar 

  • Hou R, He S, Wu F, Chapman CA, Pan R, Garbar PA, Guo S, Li B (2018) Seasonal variation in diet and nutrition of the northern-most population of Rhinopithecus roxellana. Am J Primatol 80:e22755

    Article  PubMed  CAS  Google Scholar 

  • Huang Z, Cui L, Scott MB, Wang S, Xiao W (2012) Seasonality of reproduction of wild black-and-white snub-nosed monkeys (Rhinopithecus bieti) at Mt. Lasha, Yunnan China. Primates 53:237–245

    Article  PubMed  Google Scholar 

  • Iwamoto T (1982) Food and nutritional condition of free ranging Japanese monkeys on Koshima Islet during winter. Primates 23:153–170

    Article  Google Scholar 

  • Iwamoto T (1988) Food and energetics of provisioned wild Japanese macaques Macaca fuscata. In: Fa JE, Southwick CH (eds) Ecology and behavior of food-enhanced primate groups. Liss, New York, pp 79–94

    Google Scholar 

  • Iwamoto T (1997) Feeding. In: Doi T, Iwamoto T, Miura S, Ikeda K (eds) Ecology of the mammals. University of Tokyo Press, Tokyo, pp 76–120 (in Japanese)

    Google Scholar 

  • Janson C, Verdolin J (2005) Seasonality of primate births in relation to climate. 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 307–350

    Chapter  Google Scholar 

  • Knott CD (1998) Changes in orangutan caloric intake, energy balance, and ketones in response to fluctuating fruit availability. Int J Primatol 19:1061–1079

    Article  Google Scholar 

  • Knott CD (2005) Energetic responses to food availability in the great apes: implications for hominin evolution. 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 351–378

    Chapter  Google Scholar 

  • Koenig A, Borries C, Chalise MK, Winkler P (1997) Ecology, nutrition, and timing of reproductive events in an Asian primate, the Hanuman langur (Presbytis entellus). J Zool 243:215–235

    Article  Google Scholar 

  • Koike S (2010) Long-term trends in food habits of Asiatic black bears in the Misaka Mountains on the Pacific coast of central Japan. Mamm Biol 75:17–28

    Article  Google Scholar 

  • Kurihara Y, Hanya G (2017) Comparison of energy balance between two different-sized groups of Japanese macaques (Macaca fuscata yakui). Primates 58:413–422

    Article  PubMed  Google Scholar 

  • Lambert JE, Rothman JM (2015) Fallback foods, optimal diets, and nutritional targets: primate responses to varying food availability and quality. Annu Rev Anthropol 44:493–512

    Article  Google Scholar 

  • Lewis RJ, Kappeler PM (2005) Are Kirindy sifaka capital or income breeders? It depends. Am J Primatol 67:365–369

    Article  CAS  PubMed  Google Scholar 

  • MacIntosh AJJ, Huffman MA, Nishiwaki K, Miyabe-Nishiwaki T (2012) Urological screening of a wild group of Japanese macaques (Macaca fuscata yakui): investigating trends in nutrition and health. Int J Primatol 33:460–478

    Article  Google Scholar 

  • Marshall AJ, Wrangham RW (2007) Evolutionary consequences of fallback foods. Int J Primatol 28:1219–1235

    Article  Google Scholar 

  • McCabe GM, Emery Thompson M (2013) Reproductive seasonality in wild Sanje mangabeys (Cercocebus sanjei), Tanzania: relationship between the capital breeding strategy and infant survival. Behaviour 150:1399–1429

    Article  Google Scholar 

  • Ménard N, Motsch P, Delahaye A, Saintvanne A, Le Flohic G, Dupé S, Vallet D, Qarro M, Tattou MI, Pierre JS (2014) Effect of habitat quality on diet flexibility in Barbary macaques. Am J Primatol 76:679–693

    Article  PubMed  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 

  • Nagy KA, Milton K (1979) Energy metabolism and food consumption by wild howler monkeys (Alouatta palliata). Ecology 60:475–480

    Article  Google Scholar 

  • Nagy KA, Girard IA, Brown TK (1999) Energetics of free-ranging mammals, reptiles, and birds. Annu Rev Nutr 19:247–277

    Article  CAS  PubMed  Google Scholar 

  • Nakagawa N (1989) Bioenergetics of Japanese monkeys (Macaca fuscata) on Kinkazan Island during winter. Primates 30:441–460

    Article  Google Scholar 

  • Nakagawa N (1997) Determinants of the dramatic seasonal changes in the intake of energy and protein by Japanese monkeys in a cool temperate forest. Am J Primatol 41:267–288

    Article  CAS  PubMed  Google Scholar 

  • Nakagawa N (2000) Foraging energetics in patas monkeys (Erythrocebus patas) and tantalus monkeys (Cercopithecus aethiops tantalus): implications for reproductive seasonality. Am J Primatol 52:169–185

    Article  CAS  PubMed  Google Scholar 

  • Nakagawa N (2009) Feeding rate as valuable information in primate feeding ecology. Primates 50:131–141

    Article  PubMed  Google Scholar 

  • Nakagawa N, Iwamoto T, Yokota N, Soumah AG (1996) Inter-regional and inter-seasonal variation 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, Cambridge, pp 207–234

    Google Scholar 

  • Nakayama Y, Matsuoka S, Watanuki Y (1999) Feeding rates and energy deficits of juvenile and adult Japanese monkeys in a cool temperate area with snow coverage. Ecol Res 14:291–301

    Article  Google Scholar 

  • National Research Council (2003) Nutrient requirements of nonhuman primates. National Academy Press, Washington DC

    Google Scholar 

  • Pekár S, Brabec M (2018) Generalized estimating equations: a pragmatic and flexible approach to the marginal GLM modelling of correlated data in the behavioural sciences. Ethology 124:86–93

    Article  Google Scholar 

  • Pichon C, Simmen B (2015) Energy management in crowned sifakas (Propithecus coronatus) and the timing of reproduction in a seasonal environment. Am J Phys Anthropol 158:269–278

    Article  PubMed  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2018) nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-137

  • Pontzer H (2015) Energy expenditure in humans and other primates: a new synthesis. Annu Rev Anthropol 44:169–187

    Article  Google Scholar 

  • Pontzer H, Raichlen DA, Gordon AD, Schroepfer-Walker KK, Hare B, O’Neill MC, Muldoon KM, Dunsworth HM, Wood BM, Isler K, Burkart J, Irwin M, Shumaker RW, Lonsdorf EV, Ross SR (2014) Primate energy expenditure and life history. Proc Natl Acad Sci USA 111:1433–1437

    Article  CAS  PubMed  Google Scholar 

  • Pontzer H, Durazo-Arvizu R, Dugas LR, Plange-Rhule J, Bovet P, Forrester TE, Lambert EV, Cooper RS, Schoeller DA, Luke A (2016) Constrained total energy expenditure and metabolic adaptation to physical activity in adult humans. Curr Biol 26:410–417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robinson AM, Williamson DH (1980) Physiological roles of ketone bodies as substrates and signals in mammalian tissues. Physiol Rev 60:143–187

    Article  CAS  PubMed  Google Scholar 

  • Rothman JM, Plumptre AJ, Dierenfeld ES, Pell AN (2007) Nutritional composition of the diet of the gorilla (Gorilla beringei): a comparison between two montane habitats. J Trop Ecol 23:673–682

    Article  Google Scholar 

  • Rothman JM, Chapman CA, Soest PJ (2012) Methods in primate nutritional ecology: a user’s guide. Int J Primatol 33:542–566

    Article  Google Scholar 

  • Rousseeuw PJ (1987) Silhouettes: a graphical aid to the interpretation and validation of cluster analysis. J Comput Appl Math 20:53–65

    Article  Google Scholar 

  • Sawada A, Sakaguchi E, Hanya G (2011) Digesta passage time, digestibility, and total gut fill in captive Japanese macaques (Macaca fuscata): effects food type and food intake level. Int J Primatol 32:390–405

    Article  Google Scholar 

  • Schmid J, Kappeler PM (2005) Physiological adaptations to seasonally in nocturnal primates. 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 129–156

    Chapter  Google Scholar 

  • Schülke O, Chalise MK, Koenig A (2006) The importance of ingestion rates for estimating food quality and energy intake. Am J Primatol 68:951–965

    Article  PubMed  CAS  Google Scholar 

  • Sha JCM, Kurihara Y, Tsuji Y, Take M, He T, Kaneko A, Suda-Hashimoto N, Morimoto M, Natsume T, Zahariev A, Blanc S, Hanya G (2018) Seasonal variation of energy expenditure in Japanese macaques (Macaca fuscata). J Therm Biol 76:139–146

    Article  PubMed  Google Scholar 

  • Sherry DS, Ellison PT (2007) Potential applications of urinary C-peptide of insulin for comparative energetics research. Am J Phys Anthropol 133:771–778

    Article  PubMed  Google Scholar 

  • Simmen B, Rasamimanana H (2018) Energy (im-) balance in frugivorous lemurs in southern Madagascar: a preliminary study in Lemur catta and Eulemur rufifrons × collaris. Folia Primatol 89:382–396

    Article  PubMed  Google Scholar 

  • Simmen B, Bayart F, Rasamimanana H, Zahariev A, Blanc S, Pasquet P (2010) Total energy expenditure and body composition in two free-living sympatric lemurs. PLoS ONE 5:e9860

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Simmen B, Pasquet P, Masi S, Koppert GJ, Wells JC, Hladik CM (2017) Primate energy input and the evolutionary transition to energy-dense diets in humans. Proc R Soc B Biol Sci 284:20170577

    Article  Google Scholar 

  • Soxhlet FV (1879) Die gewichtsanalytische bestimmung des milchfettes. Polytech J 232:461–465

    Google Scholar 

  • Sterck EHM, Watts DP, van Schaik CP (1997) The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41:291–309

    Article  Google Scholar 

  • Suzuki S, Noma N, Izawa K (1998) Inter-annual variation of reproductive parameters and fruit availability in two populations of Japanese macaques. Primates 39:313–324

    Article  Google Scholar 

  • Takahara H, Matsumoto J (2002) Climatological study of precipitation distribution in Yaku-shima Island, southern Japan. J Geogr 111:726–746 (in Japanese)

    Article  Google Scholar 

  • Takahashi H (2002) Female reproductive parameters and fruit availability: factors determining onset of estrus in Japanese macaques. Am J Primatol 57:141–153

    Article  PubMed  Google Scholar 

  • Taussky HH, Kurzmann G (1954) A microcolorimetric determination of creatine in urine by the Jaffe reaction. J Biol Chem 208:853–861

    CAS  PubMed  Google Scholar 

  • Tian J, Wang Z, Lu J, Wang B, Chen J (2013) Reproductive parameters of female Macaca mulatta tcheliensis in the temperate forest of Mount Taihangshan, Jiyuan, China. Am J Primatol 75:605–612

    Article  PubMed  Google Scholar 

  • Tsuji Y (2010) Regional, temporal, and interindividual variation in the feeding ecology of Japanese macaques. In: Nakagawa N, Nakamichi M, Sugiura H (eds) The Japanese macaques. Springer, Tokyo, pp 99–127

    Chapter  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 

  • Tsuji Y, Fujita S, Sugiura H, Saito C, Takatsuki S (2006) Long-term variation in fruiting and the food habits of wild Japanese macaques on Kinkazan Island, northern Japan. Am J Primatol 68:1068–1080

    Article  PubMed  Google Scholar 

  • Tsuji Y, Kazahari N, Kitahara M, Takatsuki S (2008) A more detailed seasonal division of the energy balance and the protein balance of Japanese macaques (Macaca fuscata) on Kinkazan Island, northern Japan. Primates 49:157–160

    Article  PubMed  Google Scholar 

  • Tsuji Y, Hanya G, Grueter CC (2013) Feeding strategies of primates in temperate and alpine forests: comparison of Asian macaques and colobines. Primates 54:201–215

    Article  PubMed  Google Scholar 

  • Tsujino R, Yumoto T (2007) Spatial distribution patterns of trees at different life stages in a warm temperate forest. J Plant Res 120:687–695

    Article  PubMed  Google Scholar 

  • van Soest PV, Robertson J, Lewis B (1991) Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J Dairy Sci 74:3583–3597

    Article  Google Scholar 

  • 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. Am J Phys Anthropol 140:716–726

    Article  PubMed  Google Scholar 

  • Vogel ER, Harrison ME, Zulfa A, Bransford TD, Alavi SE, Husson S, Morrogh-Bernard H, Santiano FT, Utami-Atmoko SS, van Noordwijk MA, Farida WR (2015) Nutritional differences between two orangutan habitats: implications for population density. PLoS ONE 10:e0138612

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vogel ER, Alavi SE, Utami-Atmoko SS, van Noordwijk MA, Bransford TD, Erb WM, Zulfa A, Sulistyo F, Farida WR, Rothman JM (2017) Nutritional ecology of wild Bornean orangutans (Pongo pygmaeus wurmbii) in a peat swamp habitat: effects of age, sex, and season. Am J Primatol 79:e22618

    Article  Google Scholar 

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

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14

    Article  Google Scholar 

Download references

Acknowledgements

We thank the Yakushima Forest Ecosystem Conservation Center and Kagoshima Prefectural Government for their permission to conduct behavioral data collection in Yakushima. We would like to express our gratitude to Drs. Hideki Sugiura and Mariko Suzuki for their warm support in the field, Dr. Shin-Ichiro Aiba for providing meteorological data, Mr. Toshihiro Saito for his help in identifying plant species, and Dr. Akiko Sawada and Ms. Yuki Shima for helping with food sample collection. We are grateful to the members of the Department of Ecology and Social Behavior in Primate Research Institute in Kyoto University for fruitful discussions. We also thank the editor, Dr. Cedric Girard-Buttoz, and the anonymous reviewer for their constructive comments, which improved our manuscript. This study was supported financially by the Cooperation Research Program of Wildlife Research Center, Kyoto University, and Daiko Foundation Scholarship to YK. Also this study was supported by Grant-in-Aid for JSPS Research Fellow and for Young Scientists (No. 16J01208 and No. 18K14490 to YK), Grant-in-Aid for Young Scientists (B) (No. 16K18482 to KK), and Grant-in-Aid for Scientific Research (B) (No. 23370099 to Dr. Naofumi Nakagawa, the Laboratory of Human Evolution Studies, Graduate School of Science, Kyoto University) from the Japan Society for the Promotion of Science.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yosuke Kurihara.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 330 kb)

Appendix

Appendix

See Table 

Table 3 Ingestion rates and nutritional content for the food items of Japanese macaques in the coastal forest of Yakushima

3.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kurihara, Y., Kinoshita, K., Shiroishi, I. et al. Seasonal variation in energy balance of wild Japanese macaques (Macaca fucata yakui) in a warm-temperate forest: a preliminary assessment in the coastal forest of Yakushima. Primates 61, 427–442 (2020). https://doi.org/10.1007/s10329-020-00797-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10329-020-00797-3

Keywords

Navigation