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Herbivores increase the global availability of nutrients over millions of years

Abstract

Can the presence of herbivores increase global nutrient availability? Animals disperse vital nutrients through ecosystems, increasing the spatial availability of these nutrients. Large herbivores are especially important for the dispersal of vital nutrients due to their long food passage times and day ranges, and large herbivores from past periods (the Pleistocene) may have increased nutrient concentrations on the continental scale. However, such results have been demonstrated theoretically but not yet empirically. Models suggest that the Pennsylvanian subperiod (323−299 million years ago), with no tetrapod terrestrial herbivores, would have had fewer, less-well-distributed nutrients than the Cretaceous period (145−66 million years ago), with the largest terrestrial herbivores ever—the sauropods. Here, I show that these models are supported empirically by remnant plant material (coal deposits) from the Cretaceous (N = 680), which had significantly (P < 0.00001) increased concentrations (136%) and decreased spatial heterogeneity (22%) of plant-important rock-derived nutrients compared with the Pennsylvanian subperiod (N = 4,996). Non-biotic physical processes, such as weathering rates, cannot account for such differences, because aluminium—a nutrient not important for plants and animals, but weathered in a similar manner to the above elements—showed no significant difference between the two periods, suggesting that these large changes were driven by plant–herbivore interactions. Populations of large wild herbivores are currently at historical lows; therefore, we are potentially losing a key ecosystem service.

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Fig. 1: Maximum body size and nutrient movement.
Fig. 2: Elemental distribution in the Cretaceous and Pennsylvanian subperiod.
Fig. 3: Normalized median values in the Cretaceous and Pennsylvanian subperiod.

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References

  1. Reimchen, T. E., Mathewson, D. D., Hocking, M. D., Moran, J. & Harris, D. Isotopic evidence for enrichment of salmon-derived nutrients in vegetation, soil, and insects in Riparian zones in coastal British Columbia. Am. Fish. Soc. Symp. 34, 59–69 (2003).

    Google Scholar 

  2. Mulder, C. P. H. et al. in Seabird Islands: Ecology, Invasion, and Restoration (eds Mulder, C. P. H., Anderson, W. B., Towns, D. R. & Bellingham, P. J.) Ch. 5 (Oxford Univ. Press, Oxford, 2011).

  3. Bump, J. K., Tischler, K. B., Schrank, A. J., Peterson, R. O. & Vucetich, J. A. Large herbivores and aquatic-terrestrial links in southern boreal forests. J. Anim. Ecol. 78, 338–345 (2009).

    Article  Google Scholar 

  4. Stevenson, P. R. & Guzman-Caro, D. C. Nutrient transport within and between habitats through seed dispersal processes by woolly monkeys in north-western Amazonia. Am. J. Primatol. 72, 992–1003 (2010).

    Article  Google Scholar 

  5. Wolf, A., Doughty, C. E. & Malhi, Y. Lateral diffusion of nutrients by mammalian herbivores in terrestrial ecosystems. PLoS ONE 8, e71352 (2013).

  6. Doughty, C. E., Wolf, A. & Malhi, Y. The legacy of the Pleistocene megafauna extinctions on nutrient availability in Amazonia. Nat. Geosci. 6, 761–764 (2013).

    Article  CAS  Google Scholar 

  7. Doughty, C. E. et al. Global nutrient transport in a world of giants. Proc. Natl Acad. Sci. USA 113, 868–873 (2016).

    Article  CAS  Google Scholar 

  8. Dirzo, R. et al. Defaunation in the Anthropocene. Science 345, 401–406 (2014).

    Article  CAS  Google Scholar 

  9. Reisz, R. R. & Fröbisch, J. The oldest caseid synapsid from the Late Pennsylvanian of Kansas, and the evolution of herbivory in terrestrial vertebrates. PLoS ONE 9, e94518 (2014).

    Article  Google Scholar 

  10. Beerling, D. J. et al. The influence of Carboniferous palaeoatmospheres on plant function: an experimental and modelling assessment. Phil. Trans. R. Soc. Lond. B 353, 131–139 (1998).

    Article  Google Scholar 

  11. Taylor, L. L., Banwart, S. A., Valdes, P. J., Leake, J. R. & Beerling, D. J. Evaluating the effects of terrestrial ecosystems, climate and carbon dioxide on weathering over geological time: a global-scale process-based approach. Phil. Trans. R. Soc. B 367, 565–582 (2012).

    Article  CAS  Google Scholar 

  12. Moyersoen, B. Pakaraimaea dipterocarpacea is ectomycorrhizal, indicating an ancient Gondwanaland origin for the ectomycorrhizal habit in Dipterocarpaceae. New Phytol. 172, 753–762 (2006).

    Article  Google Scholar 

  13. Briggs, D. E. G., Plint, A. G. & Pickerill, R. K. Arthropleura trails from the Westphalian of eastern Canada. Palaeontology 27, 843–855 (1984).

    Google Scholar 

  14. Heim, N. A., Knope, M. L., Schaal, E. K., Wang, S. C. & Payne, J. L. Cope's rule in the evolution of marine animals. Science 347, 867–870 (2015).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  16. Codron, D., Carbone, C. & Clauss, M. Ecological interactions in dinosaur communities: influences of small offspring and complex ontogenetic life histories. PLoS ONE 8, e77110 (2013).

    Article  CAS  Google Scholar 

  17. Benson, R. B. J. et al. Rates of dinosaur body mass evolution indicate 170 million years of sustained ecological innovation on the avian stem lineage. PLoS ONE 12, e1001853 (2014).

    Article  Google Scholar 

  18. Palmer, C. A., Oman, C. L., Park, A. J. & Luppens, J. A. The US Geological Survey Coal Quality (COALQUAL) Database. Version 3.0 (Data Series 975, US Geological Survey, Reston, 2015); http://dx.doi.org/10.3133/ds975.

  19. Ryan, B. D. & Grieve, D. A. in Geological Fieldwork 1995 (eds Grant, B. & Newell, J. M.) 277–294 (Ministry of Energy, Mines and Petroleum Resources, Victoria, 1996).

  20. Ward, C. R., Corcoran, J. F., Saxby, J. D. & Read, H. W. Occurrence of phosphorus minerals in Australian coal seams. Int. J. Coal Geol. 30, 185–210 (1996).

    Article  CAS  Google Scholar 

  21. Ryan, B. C. & Khan, M. in Geological Fieldwork 1997 28-1–28-19 (B.C. Ministry of Employment and Investment, Victoria, 1998).

  22. Ketris, M. P. & Yudovich, Y. E. Estimations of Clarkes for Carbonaceous biolithes: world averages for trace element contents in black shales and coals. Int. J. Coal Geol. 78, 135–148 (2009).

    Article  CAS  Google Scholar 

  23. Doughty, C. E., Wolf, A., Baraloto, C. & Malhi, Y. Interdependency of plants and animals in controlling the sodium balance of ecosystems and the impacts of global defaunation. Ecography 39, 204–212 (2016).

    Article  Google Scholar 

  24. Scotese, C. R. & Ziegler, A. M. Paleozoic continental-drift reconstructions and animation. Eos Trans. Am. Geophys. Union 59, 263–263 (1978).

    Google Scholar 

  25. Poulsen, C. J., Tabor, C. & White, J. D. Long-term climate forcing by atmospheric oxygen concentrations. Science 348, 1238–1241 (2015).

    Article  CAS  Google Scholar 

  26. LePage, B. A., Currah, R. S., Stockey, R. A. & Rothwell, G. W. Fossil ectomycorrhizae from the middle Eocene. Am. J. Bot. 84, 410–412 (1997).

    Article  CAS  Google Scholar 

  27. Amatangelo, K. L. & Vitousek, P. M. Contrasting predictors of fern versus angiosperm decomposition in a common garden. Biotropica 41, 154e161 (2009).

    Article  Google Scholar 

  28. D'Emic, M. D. Comment on "Evidence for mesothermy in dinosaurs". Science 348, 982 (2015).

    Article  CAS  Google Scholar 

  29. Grady, J. M., Enquist, B. J., Dettweiler-Robinson, E., Wright, N. A. & Smith, F. A. Evidence for mesothermy in dinosaurs. Science 344, 1268–1272 (2014).

    Article  CAS  Google Scholar 

  30. Wings, O. & Sander, P. M. No gastric mill in sauropod dinosaurs: new evidence from analysis of gastrolith mass and function in ostriches. Proc. R. Soc. B 274, 635–640 (2007).

    Article  Google Scholar 

  31. Clauss, M., Steuer, P., Müller, D. W. H., Codron, D. & Hummel, J. Herbivory and body size: allometries of diet quality and gastrointestinal physiology, and implications for herbivore ecology and dinosaur gigantism. PLoS ONE 8, e68714 (2013).

    Article  CAS  Google Scholar 

  32. Okubo, A. & Levin, S. A. Diffusion and Ecological Problems: Modern Perspectives, 2nd edn (Springer, New York, 2001).

  33. Skellam, J. G. Random dispersal in theoretical populations. Biometrika 38, 196–218 (1951).

    Article  CAS  Google Scholar 

  34. Ilse, L. M. & Hellgren, E. C. Resource partitioning in sympatric populations of collared peccaries and feral hogs in southern Texas. J. Mammal. 76, 784–799 (1995).

    Article  Google Scholar 

  35. Augustine, D. J. & McNaughton, S. J. Ungulate effects on the functional species composition of plant communities: herbivore selectivity and plant tolerance. J. Wildl. Manage. 62, 1165–1183 (1998).

    Article  Google Scholar 

  36. Mcnaughton, S. J. Mineral-nutrition and spatial concentrations of African ungulates. Nature 334, 343–345 (1988).

    Article  CAS  Google Scholar 

  37. White, K. A. J., Lewis, M. A. & Murray, J. D. A model for wolf-pack territory formation and maintenance. J. Theor. Biol. 178, 29–43 (1996).

    Article  Google Scholar 

  38. Rees, P. A. Gross assimilation efficiency and food passage time in the African elephant. Afr. J. Ecol. 20, 193–198 (1982).

    Article  Google Scholar 

  39. Elser, J. J., Dobberfuhl, D. R., MacKay, N. A. & Schampel, J. H. Organism size, life history, and N:P stoichiometry: toward a unified view of cellular and ecosystem processes. Bioscience 46, 674–684 (1996).

  40. Dangerfield, J. M. & Milner, A. E. Millipede fecal pellet production in selected natural and managed habitats of southern Africa: implications for litter dynamics. Biotropica 28, 113–120 (1996).

    Article  Google Scholar 

  41. Brett-Surman, M. K., Holtz, T. R. & Farlow, J. R. The Complete Dinosaur (Indiana Univ. Press, Bloomington, 2012).

  42. Sander, P. M. et al. Biology of the sauropod dinosaurs: the evolution of gigantism. Biol. Rev. 86, 117–155 (2011).

    Article  Google Scholar 

  43. Eagle, R. A. et al. Isotopic ordering in eggshells reflects body temperatures and suggests differing thermophysiology in two Cretaceous dinosaurs. Nat. Commun. 6, 8296 (2015).

    Article  CAS  Google Scholar 

  44. Asner, G. P. & Martin, R. E. Contrasting leaf chemical traits in tropical lianas and trees: implications for future forest composition. Ecol. Lett. 15, 1001–1007 (2012).

    Article  Google Scholar 

  45. Dormann, C. F. et al. Methods to account for spatial autocorrelation in the analysis of species distributional data: a review. Ecography 30, 609–628 (2007).

    Article  Google Scholar 

  46. Pedersen, R. O., Sandel, B. & Svenning, J. C. Macroecological evidence for competitive regional-scale interactions between the two major clades of mammal carnivores (Feliformia and Caniformia). PLoS ONE 9, e100553 (2014).

    Article  Google Scholar 

Download references

Acknowledgements

C.E.D. acknowledges funding from the John Fell Fund and Google and useful advice from L. Taylor and D. Beering.

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C.E.D. conceived the idea, analysed the data and wrote the paper.

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Correspondence to Christopher E. Doughty.

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Doughty, C.E. Herbivores increase the global availability of nutrients over millions of years. Nat Ecol Evol 1, 1820–1827 (2017). https://doi.org/10.1038/s41559-017-0341-1

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