in

Wild Bornean orangutans experience muscle catabolism during episodes of fruit scarcity

  • 1.

    Fleming, T. H., Breitwisch, R. & Whitesides, G. Patterns of tropical vertebrate frugivore diversity. Annu. Rev. Ecol. Syst. 18, 91–109 (1987).

    Article 

    Google Scholar 

  • 2.

    van Schaik, C. P. & Pfannes, K. R. Tropical climates and phenology: a primate perspective. In Seasonality in Primates: Studies of Living and Extinct Human and Non-Human Primates (eds Brockman, D. K. & van Schaik, C. P.) (Cambridge University Press, 2005).

    Google Scholar 

  • 3.

    Marshall, A. J., Boyko, C. M., Feilen, K. L., Boyko, R. H. & Leighton, M. Defining fallback foods and assessing their importance in primate ecology and evolution. Am. J. Phys. Anthropol. 140, 603–614 (2009).

    PubMed 
    Article 

    Google Scholar 

  • 4.

    Wich, S. A. et al. Forest fruit production is higher on Sumatra Than on Borneo. PLoS ONE 6, e21278 (2011).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 5.

    Meiri, S., Meijaard, E., Wich, S. A., Groves, C. P. & Helgen, K. M. Mammals of Borneo: small size on a large island. J. Biogeogr. 35, 1087–1094 (2008).

    Article 

    Google Scholar 

  • 6.

    Vogel, E. R. et al. Functional ecology and evolution of hominoid molar enamel thickness: Pan troglodytes schweinfurthii and Pongo pygmaeus wurmbii. J. Hum. Evol. 55, 60–74 (2008).

    PubMed 
    Article 

    Google Scholar 

  • 7.

    Vogel, E. R. et al. 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 (2017).

    Article 

    Google Scholar 

  • 8.

    Vogel, E. R. et al. Food mechanical properties, feeding ecology, and the mandibular morphology of wild orangutans. J. Hum. Evol. 75, 110–124 (2014).

    PubMed 
    Article 

    Google Scholar 

  • 9.

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

    Article 

    Google Scholar 

  • 10.

    Harrison, M. E., Morrogh-Bernard, H. C. & Chivers, D. J. Orangutan energetics and the influence of fruit availability in the nonmasting peat-swamp forest of Sabangau, Indonesian Borneo. Int. J. Primatol. 31, 585–607 (2010).

    Article 

    Google Scholar 

  • 11.

    van Schaik, C. P. The socioecology of fission-fusion sociality in Orangutans. Primates 40, 69–86 (1999).

    PubMed 
    Article 

    Google Scholar 

  • 12.

    Taylor, A. B., Vogel, E. R. & Dominy, N. J. Food material properties and mandibular load resistance abilities in large-bodied hominoids. J. Hum. Evol. 55, 604–616 (2008).

    PubMed 
    Article 

    Google Scholar 

  • 13.

    Pontzer, H., Raichlen, D. A., Shumaker, R. W., Ocobock, C. & Wich, S. A. Metabolic adaptation for low energy throughput in orangutans. Proc. Natl. Acad. Sci. 107, 14048–14052 (2010).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 14.

    Nie, Y. et al. Exceptionally low daily energy expenditure in the bamboo-eating giant panda. Science 349, 171–174 (2015).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 15.

    Zihlman, A. L., Mcfarland, R. K. & Underwood, C. E. Functional anatomy and adaptation of male gorillas (Gorilla gorilla gorilla) with comparison to male orangutans (Pongo pygmaeus). Anat. Rec. 294, 1842–1855 (2011).

    Article 

    Google Scholar 

  • 16.

    Gresl, T. A., Baum, S. T. & Kemnitz, J. W. Glucose regulation in captive Pongo pygmaeus abeli, P. p. pygmaeus, and P. p. abeli x P. p. pygmaeus orangutans. Zoo Biol. 19, 193–208 (2000).

    CAS 
    Article 

    Google Scholar 

  • 17.

    Jones, M. L. The orang utan in captivity. In The Orang Utan: Its Biology and Conservation (ed. de Boer, L. E. M.) 17–37 (Dr. W. Junk Publishers, 1982).

    Google Scholar 

  • 18.

    Knott, C. D. Energetic responses to food availability in the great apes: implications for hominin evolution. In Seasonality in Primates: Studies of Living and Extinct Human and Non-Human Primates (eds Brockman, D. K. & van Schaik, C. P.) 351–378 (Cambridge University Press, 2005).

    Google Scholar 

  • 19.

    Knott, C. D. Reproductive, physiological and behavioral responses of orangutans in Borneo to fluctuations in food availability. Doctoral Dissertation (Harvard University, 1999).

  • 20.

    Emery Thompson, M. & Knott, C. D. Urinary C-peptide of insulin as a non-invasive marker of energy balance in wild orangutans. Horm. Behav. 53, 526–535 (2008).

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • 21.

    Vogel, E. R. et al. A noninvasive method for estimating nitrogen balance in free-ranging primates. Int. J. Primatol. 33, 567–587 (2012).

    Article 

    Google Scholar 

  • 22.

    Vogel, E. R. et al. Bornean orangutans on the brink of protein bankruptcy. Biol. Lett. 8, 333–336 (2012).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 23.

    Wheatley, B. P. The evolution of large body size in orangutans: a model for hominoid divergence. Am. J. Primatol. 13, 313–324 (1987).

    PubMed 
    Article 

    Google Scholar 

  • 24.

    Emery Thompson, M., Muller, M. N. & Wrangham, R. W. Technical note: variation in muscle mass in wild chimpanzees: application of a modified urinary creatinine method. Am. J. Phys. Anthropol. 149, 622–627 (2012).

    PubMed 
    Article 

    Google Scholar 

  • 25.

    Emery Thompson, M. et al. Evaluating the impact of physical frailty during ageing in wild chimpanzees (Pan troglodytes schweinfurthii). Philos. Trans. R. Soc. B Biol. Sci. 375, 20190607 (2020).

    Article 

    Google Scholar 

  • 26.

    Bergstrom, M. L., Thompson, M. E., Melin, A. D. & Fedigan, L. M. Using urinary parameters to estimate seasonal variation in the physical condition of female white-faced capuchin monkeys (Cebus capucinus imitator). Am. J. Phys. Anthropol. 163, 707–715 (2017).

    PubMed 
    Article 

    Google Scholar 

  • 27.

    Markham, R. & Groves, C. P. Brief communication: weights of wild orang utans. Am. J. Phys. Anthropol. 81, 1–3 (1990).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 28.

    Rayadin, Y. & Spehar, S. N. Body mass of wild bornean orangutans living in human-dominated landscapes: implications for understanding their ecology and conservation. Am. J. Phys. Anthropol. 157, 339–346 (2015).

    PubMed 
    Article 

    Google Scholar 

  • 29.

    Vogel, E. R. et al. The power of protein: protein regulation, energetics, and health in wild Bornean orangutan (Pongo pygmaeus wurmbii). Am. J. Phys. Anthropol. 162, 397 (2017).

    Article 

    Google Scholar 

  • 30.

    Ashton, P. S., Givnish, T. J. & Appanah, S. Staggered flowering in the dipterocarpaceae: new insights into floral induction and the evolution of mast fruiting in the aseasonal tropics. Am. Nat. 132, 44–66 (1988).

    Article 

    Google Scholar 

  • 31.

    Cannon, C. H., Curran, L. M., Marshall, A. J. & Leighton, M. Long-term reproductive behaviour of woody plants across seven Bornean forest types in the Gunung Palung National Park (Indonesia): suprannual synchrony, temporal productivity and fruiting diversity. Ecol. Lett. 10, 956–969 (2007).

    PubMed 
    Article 

    Google Scholar 

  • 32.

    Vogel, E. R. et al. Nutritional differences between two orangutan habitats: implications for population density. PLoS ONE 10, e0138612 (2015).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 33.

    Wich, S. A. et al. Life history of wild Sumatran orangutans (Pongo abelii). J. Hum. Evol. 47, 385–398 (2004).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 34.

    van Noordwijk, M. A. et al. The slow ape: high infant survival and long interbirth intervals in wild orangutans. J. Hum. Evol. 125, 38–49 (2018).

    PubMed 
    Article 

    Google Scholar 

  • 35.

    Finney, H., Newman, D., Thakkar, H., Fell, J. & Price, C. Reference ranges for plasma cystatin C and creatinine measurements in premature infants, neonates, and older children. Arch. Dis. Child. 82, 71–75 (2000).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 36.

    Stonestreet, B. S., Bell, E. F. & Oh, W. Validity of endogenous creatinine clearance in low birthweight infants. Pediatr. Res. 13, 1012–1014 (1979).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 37.

    Kingsley, S. Causes of non-breeding and the development of the secondary sexual characteristics in the male orangutan: a hormonal study. In The Orang-Utan, Its Biology and Conservation (ed. de Boer, L. E. M.) 215–229 (Dr. W. Junk Publishers, 1982).

  • 38.

    Maggioncalda, A. N., Sapolsky, R. M. & Czekala, N. M. Reproductive hormone profiles in captive male orangutans: implications for understanding developmental arrest. Am. J. Phys. Anthropol. 109, 19–32 (1999).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 39.

    Marty, P. R. et al. Endocrinological correlates of male bimaturism in wild Bornean orangutans. Am. J. Primatol. 77, 1170–1178 (2015).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 40.

    Bhasin, S. et al. The effects of supraphysiologic doses of testosterone on muscle size and strength in normal men. N. Engl. J. Med. 335, 1–7 (1996).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 41.

    Buckley, B. J. W. Ranging behaviour of male Orang-Utans in an unfragmented Bornean habitat and implications for mating-system mechanics. Doctoral Dissertation (Cambridge University, 2015).

  • 42.

    Dunkel, L. P. et al. Variation in developmental arrest among male orangutans: a comparison between a Sumatran and a Bornean population. Front. Zool. 10, 1–11 (2013).

    Article 

    Google Scholar 

  • 43.

    Kleiber, M. Body size and metabolic rate. Physiol. Rev. 27, 511–541 (1947).

    CAS 
    PubMed 
    MATH 
    Article 

    Google Scholar 

  • 44.

    Chapman, S. et al. Compounding impact of deforestation on Borneo’s climate during El Niño events. Environ. Res. Lett. 15, 084006 (2020).

    ADS 
    Article 

    Google Scholar 

  • 45.

    Cai, W. et al. Increased variability of eastern Pacific El Niño under greenhouse warming. Nature 564, 201–206 (2018).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 46.

    R Core Team. R: A Language and Environment for Statistical Computing (R Core Team, 2019).

    Google Scholar 


  • Source: Ecology - nature.com

    MIT unveils a new action plan to tackle the climate crisis

    Niche partitioning shaped herbivore macroevolution through the early Mesozoic