The large mean body size of mammalian herbivores explains the productivity paradox during the Last Glacial Maximum


Large herbivores are a major agent in ecosystems, influencing vegetation structure, and carbon and nutrient flows. During the last glacial period, a mammoth steppe ecosystem prevailed in the unglaciated northern lands, supporting a high diversity and density of megafaunal herbivores. The apparent discrepancy between abundant megafauna and the expected low vegetation productivity under a generally harsher climate with a lower CO2 concentration, termed the productivity paradox, requires large-scale quantitative analysis using process-based ecosystem models. However, most of the current global dynamic vegetation models (DGVMs) lack explicit representation of large herbivores. Here we incorporated a grazing module in a DGVM based on physiological and demographic equations for wild large grazers, taking into account feedbacks of large grazers on vegetation. The model was applied globally for present-day and the Last Glacial Maximum (LGM). The present-day results of potential grazer biomass, combined with an empirical land-use map, infer a reduction in wild grazer biomass by 79–93% owing to anthropogenic land replacement of natural grasslands. For the LGM, we find that the larger mean body size of mammalian herbivores than today is the crucial clue to explain the productivity paradox, due to a more efficient exploitation of grass production by grazers with a large body size.

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Fig. 1: Coupling between the ORCHIDEE-MICT dynamic vegetation model and the grazing module.
Fig. 2: Modelled potential large grazer biomass density for the present-day (mean of 1960–2009).
Fig. 3: Modelled LGM biome distribution and large grazer biomass density.
Fig. 4: Relationship between modelled grazer biomass and grass NPP, affected by temperature and body size.
Fig. 5: Modelled global carbon fluxes (red arrows, unit: Pg C yr−1) among different reservoirs at the LGM.


  1. 1.

    Ripple, W. J. et al. Collapse of the world’s largest herbivores. Sci. Adv. 1, e1400103 (2015).

  2. 2.

    Sandom, C., Faurby, S., Sandel, B. & Svenning, J.-C. Global late Quaternary megafauna extinctions linked to humans, not climate change. Proc. R. Soc. B 281, 20133254 (2014).

  3. 3.

    Asner, G. P. et al. Large-scale impacts of herbivores on the structural diversity of African savannas. Proc. Natl Acad. Sci. USA 106, 4947–4952 (2009).

  4. 4.

    Olofsson, J. et al. Herbivores inhibit climate-driven shrub expansion on the tundra. Glob. Change Biol. 15, 2681–2693 (2009).

  5. 5.

    Díaz, S., Noy-meir, I. & Cabido, M. Can grazing of herbaceous plants be predicted response from simple vegetative traits? J. Appl. Ecol. 38, 497–508 (2001).

  6. 6.

    Díaz, S. et al. Plant trait responses to grazing? A global synthesis. Glob. Change Biol. 13, 313–341 (2007).

  7. 7.

    Frank, D. A., Groffman, P. M., Evans, R. D. & Tracy, B. F. Ungulate stimulation of nitrogen cycling and retention in Yellowstone Park grasslands. Oecologia 123, 116–121 (2000).

  8. 8.

    Olofsson, J., Stark, S. & Oksanen, L. Reindeer influence on ecosystem processes in the tundra. Oikos 2, 386–396 (2004).

  9. 9.

    Frank, D. A. & McNaughton, S. J. Evidence for the promotion of aboveground grassland production by native large herbivores in Yellowstone National Park. Oecologia 96, 157–161 (1993).

  10. 10.

    Falk, J. M., Schmidt, N. M., Christensen, T. R. & Ström, L. Large herbivore grazing affects the vegetation structure and greenhouse gas balance in a high Arctic mire. Environ. Res. Lett. 10, 045001 (2015).

  11. 11.

    Sinclair, A. R. E. et al. Long-term ecosystem dynamics in the Serengeti: lessons for conservation. Conserv. Biol. 21, 580–590 (2007).

  12. 12.

    Gill, J. L. Ecological impacts of the late Quaternary megaherbivore extinctions. New. Phytol. 201, 1163–1169 (2014).

  13. 13.

    Gill, J. L., Williams, J. W., Jackson, S. T., Lininger, K. B. & Robinson, G. S. Pleistocene megafaunal collapse, novel plant communities, and enhanced fire regimes in North America. Science 326, 1100–1103 (2009).

  14. 14.

    Rule, S. et al. The aftermath of megafaunal extinction: ecosystem transformation in Pleistocene Australia. Science 335, 1483–1486 (2012).

  15. 15.

    Sher, A. V., Kuzmina, S. A., Kuznetsova, T. V. & Sulerzhitsky, L. D. New insights into the Weichselian environment and climate of the East Siberian Arctic, derived from fossil insects, plants, and mammals. Quat. Sci. Rev. 24, 533–569 (2005).

  16. 16.

    Guthrie, R. D Frozen Fauna of the Mammoth Steppe: The Story of Blue Babe (Univ. Chicago Press, Chicago, 1990).

  17. 17.

    Guthrie, R. D. Origin and causes of the mammoth steppe: a story of cloud cover, woolly mammal tooth pits, buckles, and inside-out Beringia. Quat. Sci. Rev. 20, 549–574 (2001).

  18. 18.

    Zimov, S. A. et al. Steppe–tundra transition: a herbivore-driven biome shift at the end of the Pleistocene. Am. Nat. 146, 765–794 (1995).

  19. 19.

    Zimov, S. A., Zimov, N. S., Tikhonov, A. N. Chapin, F. S. III. Mammoth steppe: a high-productivity phenomenon. Quat. Sci. Rev. 57, 26–45 (2012).

  20. 20.

    Kahlke, R.-D. The maximum geographic extension of Late Pleistocene Mammuthus primigenius (Proboscidea, Mammalia) and its limiting factors. Quat. Int. 379, 147–154 (2015).

  21. 21.

    Yurtsev, B. A. The Pleistocene "tundra–steppe" and the productivity paradox: the landscape approach. Quat. Sci. Rev. 20, 165–174 (2001).

  22. 22.

    Lorenzen, E. D. et al. Species-specific responses of Late Quaternary megafauna to climate and humans. Nature 479, 359–364 (2011).

  23. 23.

    Mann, D. H., Groves, P., Kunz, M. L., Reanier, R. E. & Gaglioti, B. V. Ice-age megafauna in Arctic Alaska: extinction, invasion, survival. Quat. Sci. Rev. 70, 91–108 (2013).

  24. 24.

    Owen-Smith, N. Pleistocene extinctions: the pivotal role of megaherbivores. Paleobiology 13, 351–362 (1987).

  25. 25.

    Putshkov, P. V. The impact of mammoths on their biome: clash of two paradigms. Deinsea 9, 365–379 (2003).

  26. 26.

    Hopkins, D. M., Matthews, J. V. & Schweger, C. E. Paleoecology of Beringia (Academic, New York, 1982).

  27. 27.

    Redmann, R. E. in Paleoecology of Beringia (eds Hopkins, D. M. et al.) 223–239 (Academic, New York, 1982).

  28. 28.

    Gerhart, L. M. & Ward, J. K. Plant responses to low [CO2] of the past. New. Phytol. 188, 674–695 (2010).

  29. 29.

    Prentice I. C. et al. in Terrestrial Ecosystems in a Changing World (eds Canadell, J. G. et al.) Ch. 15, 175–192 (Springer, Berlin, Heidelberg, 2007).

  30. 30.

    Pachzelt, A., Rammig, A., Higgins, S. & Hickler, T. Coupling a physiological grazer population model with a generalized model for vegetation dynamics. Ecol. Model. 263, 92–102 (2013).

  31. 31.

    Pachzelt, A., Forrest, M., Rammig, A., Higgins, S. I. & Hickler, T. Potential impact of large ungulate grazers on African vegetation, carbon storage and fire regimes. Glob. Ecol. Biogeogr. 24, 991–1002 (2015).

  32. 32.

    Krinner, G. et al. A dynamic global vegetation model for studies of the coupled atmosphere–biosphere system. Glob. Biogeochem. Cycles 19, GB1015 (2005).

  33. 33.

    Zhu, D. et al. Improving the dynamics of Northern Hemisphere high-latitude vegetation in the ORCHIDEE ecosystem model. Geosci. Model Dev. 8, 2263–2283 (2015).

  34. 34.

    Illius, A. W. & O’Connor, T. G. Resource heterogeneity and ungulate population dynamics. Oikos 89, 283–294 (2000).

  35. 35.

    Willerslev, E. et al. Fifty thousand years of Arctic vegetation and megafaunal diet. Nature 506, 47–51 (2014).

  36. 36.

    Kartzinel, T. R. et al. DNA metabarcoding illuminates dietary niche partitioning by African large herbivores. Proc. Natl Acad. Sci. USA 112, 8019–8024 (2015).

  37. 37.

    Hatton, I. A. et al. The predator–prey power law: biomass scaling across terrestrial and aquatic biomes. Science 349, aac6284 (2015).

  38. 38.

    Prins, H. H. T. & Douglas-Hamilton, I. Stability in a multi-species assemblage of large herbivores in East Africa. Oecologia 83, 392–400 (1990).

  39. 39.

    Fuller, T. K. Population dynamics of wolves in north-central Minnesota. Wildl. Monogr. 105, 3–41 (1989).

  40. 40.

    Jung, M. et al. Global patterns of land–atmosphere fluxes of carbon dioxide, latent heat, and sensible heat derived from eddy covariance, satellite, and meteorological observations. J. Geophys. Res. 116, G00J07 (2011).

  41. 41.

    Ellis, E. C., Klein Goldewijk, K., Siebert, S., Lightman, D. & Ramankutty, N. Anthropogenic transformation of the biomes, 1700 to 2000. Glob. Ecol. Biogeogr. 19, 589–606 (2010).

  42. 42.

    Harrison, S. P. & Prentice, C. I. Climate and CO2 controls on global vegetation distribution at the Last Glacial Maximum: analysis based on palaeovegetation data, biome modelling and palaeoclimate simulations. Glob. Change Biol. 9, 983–1004 (2003).

  43. 43.

    BIOME 6000 V.4.2;

  44. 44.

    Harrison, S. P. et al. Evaluation of CMIP5 palaeo-simulations to improve climate projections. Nat. Clim. Change 5, 735–743 (2015).

  45. 45.

    Mann, D. H. et al. Life and extinction of megafauna in the ice-age Arctic. Proc. Natl Acad. Sci. USA 112, 114301–114306 (2015).

  46. 46.

    Barnes, R. F. W. & Lahm, S. A. An ecological perspective on human densities in the Central African forest. J. Appl. Ecol. 34, 245–260 (1997).

  47. 47.

    Krausmann, F. et al. Global human appropriation of net primary production doubled in the 20th century. Proc. Natl Acad. Sci. USA 110, 10324–10329 (2013).

  48. 48.

    Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. & West, G. B. Toward a metabolic theory of ecology. Ecology 85, 1771–1789 (2004).

  49. 49.

    Clauss, M., Schwarm, A., Ortmann, S., Streich, W. J. & Hummel, J. A case of non-scaling in mammalian physiology? Body size, digestive capacity, food intake, and ingesta passage in mammalian herbivores. Comp. Biochem. Physiol. A 148, 249–265 (2007).

  50. 50.

    Anderson, K. J. & Jetz, W. The broad-scale ecology of energy expenditure of endotherms. Ecol. Lett. 8, 310–318 (2005).

  51. 51.

    O’Reagain, P. J. & Owen-Smith, R. N. Effect of species composition and sward structure on dietary quality in cattle and sheep grazing South African sourveld. J. Agric. Sci. 127, 261–270 (1996).

  52. 52.

    Illius, A. W. & Gordon, I. J. Modelling the nutritional ecology of ungulate herbivores: evolution of body size and competitive interactions. Oecologia 89, 428–434 (1992).

  53. 53.

    Alroy, J. Cope’s rule and the dynamics of body mass evolution in North American fossil mammals. Science 280, 731–734 (1998).

  54. 54.

    Smith, F. A. et al. The evolution of maximum body size of terrestrial mammals. Science 330, 1216–1219 (2010).

  55. 55.

    Baker, J., Meade, A., Pagel, M. & Venditti, C. Adaptive evolution toward larger size in mammals. Proc. Natl Acad. Sci. USA 112, 5093–5098 (2015).

  56. 56.

    Barnosky, A. D., Koch, P. L., Feranec, R. S., Wing, S. L. & Shabel, A. B. Assessing the causes of Late Pleistocene extinctions on the continents. Science 306, 70–75 (2004).

  57. 57.

    Waldram, M. S., Bond, W. J. & Stock, W. D. Ecological engineering by a mega-grazer: white rhino impacts on a South African Savanna. Ecosystems 11, 101–112 (2008).

  58. 58.

    Cromsigt, J. P. G. M. & te Beest, M. Restoration of a megaherbivore: landscape-level impacts of white rhinoceros in Kruger National Park, South Africa. J. Ecol. 102, 566–575 (2014).

  59. 59.

    Pringle, R. M., Palmer, T. M., Goheen, J. R., McCauley, D. J. & Keesing, F. Ecological importance of large herbivores in the Ewaso ecosystem. Smithson. Contrib. Zool. 632, 43–53 (2011).

  60. 60.

    Hempson, G. P., Archibald, S. & Bond, W. J. A continent-wide assessment of the form and intensity of large mammal herbivory in Africa. Science 350, 1056–1061 (2015).

  61. 61.

    Olofsson, J., Kitti, H., Rautiainen, P., Stark, S. & Oksanen, L. Effects of summer grazing by reindeer on composition of vegetation, productivity and nitrogen cycling. Ecography 24, 13–24 (2001).

  62. 62.

    Schweger, C. E., Matthews, J. V., Hopkins, D. M. & Young, S. B. in Paleoecology of Beringia (eds Hopkins, D. M. et al.) 425–444 (Academic, New York, 1982).

  63. 63.

    de Rosnay, P., Polcher, J., Bruen, M. & Laval, K. Impact of a physically based soil water flow and soil-plant interaction representation for modeling large-scale land surface processes. J. Geophys. Res. Atmos. 107, 4118 (2002).

  64. 64.

    Wang, F., Cheruy, F. & Dufresne, J.-L. The improvement of soil thermodynamics and its effects on land surface meteorology in the IPSL climate model. Geosci. Model Dev. 9, 363–381 (2016).

  65. 65.

    Gouttevin, I., Krinner, G., Ciais, P., Polcher, J. & Legout, C. Multi-scale validation of a new soil freezing scheme for a land-surface model with physically-based hydrology. Cryosphere 6, 407–430 (2012).

  66. 66.

    Wang, T. et al. Evaluation of an improved intermediate complexity snow scheme in the ORCHIDEE land surface model. J. Geophys. Res. Atmos. 118, 6064–6079 (2013).

  67. 67.

    Zhu, D. et al. Simulating soil organic carbon in yedoma deposits during the Last Glacial Maximum in a land surface model. Geophys. Res. Lett. 43, 5133–5142 (2016).

  68. 68.

    Koven, C. et al. On the formation of high-latitude soil carbon stocks: effects of cryoturbation and insulation by organic matter in a land surface model. Geophys. Res. Lett. 36, L21501 (2009).

  69. 69.

    Chang, J. F. et al. Incorporating grassland management in ORCHIDEE: model description and evaluation at 11 eddy-covariance sites in Europe. Geosci. Model Dev. 6, 2165–2181 (2013).

  70. 70.

    Chang, J. et al. Combining livestock production information in a process-based vegetation model to reconstruct the history of grassland management. Biogeosciences 13, 3757–3776 (2016).

  71. 71.

    Velichko, A. A. & Zelikson, E. M. Landscape, climate and mammoth food resources in the East European Plain during the Late Paleolithic epoch. Quat. Int. 126–128, 137–151 (2005).

  72. 72.

    Bliss, L. C., Heal, O. W. & Moore, J. J. (eds) Tundra Ecosystems: A Comparative Analysis (Cambridge Univ. Press, Cambridge, 1981).

  73. 73.

    Illius, A. W. & Gordon, I. J. in Herbivores: Between Plants and Predators (eds Olff, H., Brown, V. K. & Drent, R. H.) 397–427 (Blackwell, Oxford, 1999).

  74. 74.

    Eggleston, H. S. et al. (eds) 2006 IPCC Guidelines for National Greenhouse Gas Inventories (IGES, Kanagawa, 2006).

  75. 75.

    McNaughton, S. J., Ruess, R. W. & Seagle, S. W. Large mammals and process dynamics in African ecosystem. Bioscience 38, 794–800 (1988).

  76. 76.

    McNaughton, S. J. Ecology of a grazing ecosystem: the Serengeti. Ecol. Monogr. 55, 259–294 (1985).

  77. 77.

    Frank, D. A. & McNaughton, S. J. The ecology of plants, large mammalian herbivores, and drought in Yellowstone National Park. Ecology 73, 2043–2058 (1992).

  78. 78.

    Elser, J. J. et al. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol. Lett. 10, 1135–1142 (2007).

  79. 79.

    Caughley, G. The elephant problem—an alternative hypothesis. Afr. J. Ecol. 14, 265–283 (1976).

  80. 80.

    Dublin, H. T. Decline of the Mara Woodlands: The Role of Fire and Elephants. PhD thesis, Univ. British Columbia (1986).

  81. 81.

    Väisänen, M. et al. Consequences of warming on tundra carbon balance determined by reindeer grazing history. Nat. Clim. Change 4, 384–388 (2014).

  82. 82.

    Dublin, H. T., Sinclair, A. R. E. & McGlade, J. Elephants and fire as causes of multiple stable states in the Serengeti–Mara Woodlands. J. Anim. Ecol. 59, 1147–1164 (1990).

  83. 83.

    Clark, P. U. et al. The Last Glacial Maximum. Science 325, 710–714 (2009).

  84. 84.

    Hughes, P. D. & Gibbard, P. L. A stratigraphical basis for the Last Glacial Maximum (LGM). Quat. Int. 383, 174–185 (2015).

  85. 85.

    Monnin, E. et al. Atmospheric CO2 concentrations over the last glacial termination. Science 291, 112–114 (2001).

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The authors acknowledge the financial support from the European Research Council Synergy grant ERC-SyG-2013–610028 IMBALANCE-P, and from the GAP project within the French-Swedish common research and training programme on climate and environment.

Author information

D.Z. and P.C. designed the study. D.Z. led the writing and performed the analysis, with critical input from P.C. and G.K. J.C. contributed to the model development. S.P., N.V., J.P. and S.Z. enriched the discussion of the results.

Correspondence to Dan Zhu.

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Supplementary Figures 1–10, Supplementary Tables 1–2, Supplementary Notes 1–2, Supplementary Discussion, Supplementary References.

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Zhu, D., Ciais, P., Chang, J. et al. The large mean body size of mammalian herbivores explains the productivity paradox during the Last Glacial Maximum. Nat Ecol Evol 2, 640–649 (2018).

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