Mammal diversity influences the carbon cycle through trophic interactions in the Amazon

Subjects

Abstract

Biodiversity affects many ecosystem functions and services, including carbon cycling and retention. While it is known that the efficiency of carbon capture and biomass production by ecological communities increases with species diversity, the role of vertebrate animals in the carbon cycle remains undocumented. Here, we use an extensive dataset collected in a high-diversity Amazonian system to parse out the relationship between animal and plant species richness, feeding interactions, tree biomass and carbon concentrations in soil. Mammal and tree species richness is positively related to tree biomass and carbon concentration in soil—and the relationship is mediated by organic remains produced by vertebrate feeding events. Our research advances knowledge of the links between biodiversity and carbon cycling and storage, supporting the view that whole community complexity—including vertebrate richness and trophic interactions—drives ecosystem function in tropical systems. Securing animal and plant diversity while protecting landscape integrity will contribute to soil nutrient content and carbon retention in the biosphere.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Map of the study area in Guyana (WGS 84/UTM zone 21N; short lines indicate surveyed transects) and diagram of hypothesized ecological interactions that link atmospheric, biotic and soil carbon pools.
Fig. 2: Results of the richness–carbon relationships.
Fig. 3: Results of the structural equation model analysing the relationship of mammal richness, tree richness, feeding interactions and organic remains with carbon concentration in soil, carbon per tree and tree carbon per area.

Change history

  • 19 October 2017

    In the version of this Article originally published, the surname of Ted K. Raab was misspelt. This error has now been corrected in all versions of the Article.

References

  1. 1.

    Cardinale, B. J. et al. Biodiversity loss and its impact on humanity. Nature 486, 59–67 (2012).

    CAS  Article  Google Scholar 

  2. 2.

    Aarssen, L. W. High productivity in grassland ecosystems: effected by species diversity or productive species? Oikos 80, 183–184 (1997).

    Article  Google Scholar 

  3. 3.

    Tilman, D., Lehman, C. L. & Thomson, K. T. Plant diversity and ecosystem productivity: theoretical considerations. Proc. Natl Acad. Sci. USA 94, 1857–1861 (1997).

    CAS  Article  Google Scholar 

  4. 4.

    Cardinale, B. J. et al. The functional role of producer diversity in ecosystems. Am. J. Bot. 98, 572–592 (2011).

    Article  Google Scholar 

  5. 5.

    Fornara, D. A. & Tilman, D. Plant functional composition influences rates of soil carbon and nitrogen accumulation. J. Ecol. 96, 314–322 (2008).

    CAS  Article  Google Scholar 

  6. 6.

    Cong, W. F. et al. Plant species richness promotes soil carbon and nitrogen stocks in grasslands without legumes. J. Ecol. 102, 1163–1170 (2014).

    CAS  Article  Google Scholar 

  7. 7.

    Poorter, L. et al. Diversity enhances carbon storage in tropical forests. Glob. Ecol. Biogeogr. 24, 1314–1328 (2015).

    Article  Google Scholar 

  8. 8.

    Estes, J. A. et al. Trophic downgrading of planet Earth. Science 333, 301–306 (2011).

    CAS  Article  Google Scholar 

  9. 9.

    Lange, M. et al. Plant diversity increases soil microbial activity and soil carbon storage. Nat. Commun. 6, 6707 (2015).

    CAS  Article  Google Scholar 

  10. 10.

    Fierer, N. et al. Reconstructing the microbial diversity and function of pre-agricultural tallgrass prairie soils in the United States. Science 342, 621–624 (2013).

    CAS  Article  Google Scholar 

  11. 11.

    Marichal, R. et al. Soil macroinvertebrate communities and ecosystem services in deforested landscapes of Amazonia. Appl. Soil. Ecol. 83, 177–185 (2014).

    Article  Google Scholar 

  12. 12.

    Allgeier, J. E., Layman, C. A., Mumby, P. J. & Rosemond, A. D. Biogeochemical implications of biodiversity and community structure across multiple coastal ecosystems. Ecol. Monogr. 85, 117–132 (2015).

    Article  Google Scholar 

  13. 13.

    Bello, C. et al. Defaunation affects carbon storage in tropical forests. Sci. Adv. 1, e1501105 (2015).

    Article  Google Scholar 

  14. 14.

    Dos Santos Neves, N., Feer, N., Salmon, S., Chateil, C. & Ponge, C. J. F. The impact of red howler monkey latrines on the distribution of main nutrients and on topsoil profiles in a tropical rainforest. Austral Ecol. 35, 549–559 (2010).

    Article  Google Scholar 

  15. 15.

    Sitters, J., Maechler, M. J., Edwards, P. J., Suter, W. & Venterink, H. O. Interactions between C:N:P stoichiometry and soil macrofauna control dung decomposition of savanna herbivores. Funct. Ecol. 28, 776–786 (2014).

    Article  Google Scholar 

  16. 16.

    Barton, P. S., Cunningham, S. A., Lindenmayer, D. B. & Manning, A. D. The role of carrion in maintaining biodiversity and ecological processes in terrestrial ecosystems. Oecologia 171, 761–772 (2013).

    Article  Google Scholar 

  17. 17.

    Parmenter, R. R. & MacMahon, J. A. Carrion decomposition and nutrient cycling in a semiarid shrub-steppe ecosystem. Ecol. Monogr. 79, 637–661 (2009).

    Article  Google Scholar 

  18. 18.

    Hawlena, D., Strickland, M. S., Bradford, M. A. & Schmitz, O. J. Fear of predation slows plant-litter decomposition. Science 336, 1434–1438 (2012).

    CAS  Article  Google Scholar 

  19. 19.

    Lehmann, J. & Kleber, M. The contentious nature of soil organic matter. Nature 528, 60–68 (2015).

    CAS  Article  Google Scholar 

  20. 20.

    Frank, D. A., Depriest, T., McLauchlan, K. & Risch, A. C. Topographic and ungulate regulation of soil C turnover in a temperate grassland ecosystem. Glob. Change Biol. 17, 495–504 (2011).

    Article  Google Scholar 

  21. 21.

    Ritchie, M. E. Plant compensation to grazing and soil carbon dynamics in a tropical grassland. PeerJ 2, e233 (2014).

    Article  Google Scholar 

  22. 22.

    McSherry, M. E. & Ritchie, M. E. Effects of grazing on grassland soil carbon: a global review. Glob. Change Biol. 19, 1347–1357 (2013).

    Article  Google Scholar 

  23. 23.

    Hooper, D. U., Schulze, E. D. & Mooney, H. A. Biodiversity and Ecosystem Function (Springer, Berlin, 1993).

    Google Scholar 

  24. 24.

    Fragoso, J. M. V. & Huffman, J. M. Seed-dispersal and seedling recruitment patterns by the last Neotropical megafaunal element in Amazonia, the tapir. J. Trop. Ecol. 16, 369–385 (2000).

    Article  Google Scholar 

  25. 25.

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

    Article  Google Scholar 

  26. 26.

    Nichols, E. et al. Ecological functions and ecosystem services provided by Scarabaeinae dung beetles. Biol. Conserv. 141, 1461–1474 (2008).

    Article  Google Scholar 

  27. 27.

    Kurten, E. L. Cascading effects of contemporaneous defaunation on tropical forest communities. Biol. Conserv. 163, 22–32 (2013).

    Article  Google Scholar 

  28. 28.

    Kurten, E. L., Wright, S. J. & Carson, W. P. Hunting alters seedling functional trait composition in a neotropical forest. Ecology 96, 1923–1932 (2015).

    Article  Google Scholar 

  29. 29.

    Hoehn, P., Tscharntke, T., Tylianakis, J. M. & Steffan-Dewenter, I. Functional group diversity of bee pollinators increases crop yield. Proc. R. Soc. B 275, 2283–2291 (2008).

    Article  Google Scholar 

  30. 30.

    Lefcheck, J. S. et al. Biodiversity enhances ecosystem multifunctionality across trophic levels and habitats. Nat. Commun. 6, 6936 (2015).

  31. 31.

    Iwamura, T., Lambin, E. F., Silvius, K. M., Luzar, J. B. & Fragoso, J. M. V. Agent-based modeling of hunting and subsistence agriculture on indigenous lands: understanding interactions between social and ecological systems. Environ. Model. Softw. 58, 109–127 (2014).

    Article  Google Scholar 

  32. 32.

    Read, J. M. et al. Space, place, and hunting patterns among indigenous peoples of the Guyanese Rupununi region. J. Lat. Am. Geogr. 9, 213–243 (2010).

    Article  Google Scholar 

  33. 33.

    Luzar, J. B. et al. Large-scale environmental monitoring by indigenous peoples. BioScience. 6, 771–781 (2011).

    Article  Google Scholar 

  34. 34.

    Luzar, J. B., Silvius, K. M. & Fragoso, J. M. V. Church affiliation and meat taboos in indigenous communities of Guyanese Amazonia. Hum. Ecol. 40, 833–845 (2012).

    Article  Google Scholar 

  35. 35.

    Fragoso, J. M. V. et al. Line transect surveys underdetect terrestrial mammals: implications for the sustainability of subsistence hunting. PLoS ONE 11, e0152659 (2016).

    Article  Google Scholar 

  36. 36.

    Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005).

    Article  Google Scholar 

  37. 37.

    Anderson, D. R., Laake, J. L., Crain, B. R. & Burnham, K. P. Guidelines for line transect sampling of biological populations. J. Wildlife Manage. 43, 70–78 (1979).

    Article  Google Scholar 

  38. 38.

    Butt, N., Epps, K., Overman, H., Iwamura, T. & Fragoso, J. M. V. Assessing carbon stocks using indigenous peoples’ field measurements in Amazonian Guyana. Forest Ecol. Manage. 338, 191–199 (2015).

    Article  Google Scholar 

  39. 39.

    Batjes, N. H. Total carbon and nitrogen in the soils of the world. Eur. J. Soil Sci. 47, 151–163 (1996).

    CAS  Article  Google Scholar 

  40. 40.

    Silva, L. C. R. et al. Can savannas become forests? A coupled analysis of nutrient stocks and fire thresholds in central Brazil. Plant Soil 373, 829–842 (2013).

    CAS  Article  Google Scholar 

  41. 41.

    Sheil, D., Ladd, B., Silva, L. C., Laffan, S. W. & Van Heist, M. How are soil carbon and tropical biodiversity related? Environ. Conserv. 43, 231–241 (2016).

    Article  Google Scholar 

  42. 42.

    Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach (Springer-Verlag, New York, 2002).

    Google Scholar 

  43. 43

    R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Satistical Computing, Vienna, 2017).

  44. 44.

    Grace, J. B. Structural Equation Models and Natural Systems (Cambridge Univ. Press, Cambridge, 2006).

  45. 45.

    Statistica (Data Analysis Software System), Version 10 (StatSoft, Tulsa, 2001).

Download references

Acknowledgements

We thank the Guyana Environmental Protection Agency and the Ministry of Amerindian Affairs for permission to work in the Rupununi. We thank the National Science Foundation (NSF; Grant BE/CNH 05 08094), the Gordon and Betty Moore Foundation and Stanford University for financial and administrative support. We thank the Iwokrama International Centre for Rainforest Conservation, the North Rupununi District Development Board, and the Deep South Toshaos’ Council for support in Guyana. K. Epps, D. Turner and E. Kurten collaborated with soil sampling and analyses. N. Butts and A. Cummings sampled tree diversity and carbon in trees. Additionally, A. R. Larrinaga, A. Baselga and C. Gómez provided useful suggestions and collaborated with GIS work. We thank H. Mooney, C. Field, E. Garnier, C. Violle, A. Milcu, S. Hattenschwiler, B. Shipley, C. Tucker, M. Grennié, A. M. Cortizas, B. Glaser, A. da Rocha, L. García de Jalón and the Guitián lab for comments on the manuscript. S. García created the illustration. We thank the Makushi, Wapishana and Wai-Wai technicians whose fieldwork and local knowledge made this research possible.

Author information

Affiliations

Authors

Contributions

J.M.V.F., M.S., K.M.S. and L.F.B.O. conceptualized this study. M.S. completed the statistical analyses. J.M.V.F., K.M.S., H.O., L.F.B.O., T.K.R. and other colleagues designed the field study and/or oversaw data collection. M.S. and K.M.S. drafted the manuscript with all authors participating in revisions.

Corresponding author

Correspondence to Mar Sobral.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Supplementary Information

Supplementary tables and figures.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sobral, M., Silvius, K.M., Overman, H. et al. Mammal diversity influences the carbon cycle through trophic interactions in the Amazon. Nat Ecol Evol 1, 1670–1676 (2017). https://doi.org/10.1038/s41559-017-0334-0

Download citation

Further reading