Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Trophic rewilding revives biotic resistance to shrub invasion

Nature Ecology & Evolution volume 4, pages 712–724 (2020)Cite this article

Subjects

Abstract

Trophic rewilding seeks to rehabilitate degraded ecosystems by repopulating them with large animals, thereby re-establishing strong top-down interactions. Yet there are very few tests of whether such initiatives can restore ecosystem structure and functions, and on what timescales. Here we show that war-induced collapse of large-mammal populations in Mozambique’s Gorongosa National Park exacerbated woody encroachment by the invasive shrub Mimosa pigra—considered one of the world’s 100 worst invasive species—and that one decade of concerted trophic rewilding restored this invasion to pre-war baseline levels. Mimosa occurrence increased between 1972 and 2015, a period encompassing the near extirpation of large herbivores during the Mozambican Civil War. From 2015 to 2019, mimosa abundance declined as ungulate biomass recovered. DNA metabarcoding revealed that ruminant herbivores fed heavily on mimosa, and experimental exclosures confirmed the causal role of mammalian herbivory in containing shrub encroachment. Our results provide mechanistic evidence that trophic rewilding has rapidly revived a key ecosystem function (biotic resistance to a notorious woody invader), underscoring the potential for restoring ecological health in degraded protected areas.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Study system, experimental design, and hypotheses.
Fig. 2: Trends in ungulate biomass, M. pigra abundance, and rainfall.
Fig. 3: Consumption of M. pigra by LMH in the Urema floodplain.
Fig. 4: Large herbivores suppressed vital rates of M. pigra.
Fig. 5: Large herbivores regulate the density and biomass of M. pigra.

Data availability

The field data are provided in Supplementary Data 1–8. The field data along with raw dietary sequence data and metadata from 2013, 2015, 2017, and 2018 are available via Dryad (https://doi.org/10.5061/dryad.sxksn02zc). Dietary sequence data and metadata from 2016, along with the local plant reference database, are available via Dryad (https://doi.org/10.5061/dryad.63tj806).

References

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  3. Malhi, Y. et al. Megafauna and ecosystem function from the Pleistocene to the Anthropocene. Proc. Natl Acad. Sci. USA 113, 838–846 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  5. Smith, F. A., Elliott Smith, R. E., Lyons, S. K. & Payne, J. L. Body size downgrading of mammals over the Late Quaternary. Science 360, 310–313 (2018).

    Article  CAS  PubMed  Google Scholar 

  6. Barnosky, A. D. Assessing the causes of late Pleistocene extinctions on the continents. Science 306, 70–75 (2004).

    Article  CAS  PubMed  Google Scholar 

  7. Ceballos, G. et al. Accelerated modern human–induced species losses: entering the sixth mass extinction. Sci. Adv. 1, e1400253 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  8. Daskin, J. H. & Pringle, R. M. Warfare and wildlife declines in Africa’s protected areas. Nature 553, 328–332 (2018).

    Article  CAS  PubMed  Google Scholar 

  9. 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, 43–54 (2011).

    Article  Google Scholar 

  10. Johnson, B. E. & Cushman, J. H. Influence of a large herbivore reintroduction on plant invasions and community composition in a California grassland. Conserv. Biol. 21, 515–526 (2007).

    Article  PubMed  Google Scholar 

  11. 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).

    Article  Google Scholar 

  12. Cromsigt, J. P. G. M., Kemp, Y. J. M., Rodriguez, E. & Kivit, H. Rewilding Europe’s large grazer community: how functionally diverse are the diets of European bison, cattle, and horses? Restor. Ecol. 26, 891–899 (2018).

    Article  Google Scholar 

  13. Zamboni, T., Di Martino, S. & Jiménez-Pérez, I. A review of a multispecies reintroduction to restore a large ecosystem: the Iberá Rewilding Program (Argentina). Perspect. Ecol. Conserv. 15, 248–256 (2017).

    Google Scholar 

  14. Svenning, J.-C. et al. Science for a wilder Anthropocene: synthesis and future directions for trophic rewilding research. Proc. Natl Acad. Sci. USA 113, 898–906 (2016).

    Article  CAS  PubMed  Google Scholar 

  15. Bakker, E. S. & Svenning, J.-C. Trophic rewilding: impact on ecosystems under global change. Phil. Trans. R. Soc. Lond. B 373, 20170432 (2018).

    Article  Google Scholar 

  16. Pettorelli, N., Durant, S. M. & du Toit, J. (eds) Rewilding (Cambridge Univ. Press, 2019).

  17. Svenning, J.-C., Munk, M. & Schweiger, A. in Rewilding (eds Pettorelli, N. et al.) 73–98 (Cambridge Univ. Press, 2019).

  18. Sinclair, A. R. E. et al. Predicting and assessing progress in the restoration of ecosystems. Conserv. Lett. 11, e12390 (2017).

    Article  Google Scholar 

  19. Schweiger, A. H., Boulangeat, I., Conradi, T., Davis, M. & Svenning, J.-C. The importance of ecological memory for trophic rewilding as an ecosystem restoration approach. Biol. Rev. 41, 571 (2018).

    Google Scholar 

  20. Torres, A. et al. Measuring rewilding progress. Phil. Trans. R. Soc. Lond. B 373, 20170433 (2018).

    Article  Google Scholar 

  21. Fuhlendorf, S. D., Davis, C. A., Elmore, R. D., Goodman, L. E. & Hamilton, R. G. Perspectives on grassland conservation efforts: should we rewild to the past or conserve for the future? Phil. Trans. R. Soc. Lond. B 373, 20170438 (2018).

    Article  Google Scholar 

  22. Stevens, N., Lehmann, C. E. R., Murphy, B. P. & Durigan, G. Savanna woody encroachment is widespread across three continents. Glob. Change Biol. 23, 235–244 (2016).

    Article  Google Scholar 

  23. Ratajczak, Z., Nippert, J. B. & Collins, S. L. Woody encroachment decreases diversity across North American grasslands and savannas. Ecology 93, 697–703 (2012).

    Article  PubMed  Google Scholar 

  24. Honda, E. A. & Durigan, G. Woody encroachment and its consequences on hydrological processes in the savannah. Phil. Trans. R. Soc. Lond. B 371, 20150313 (2016).

    Article  CAS  Google Scholar 

  25. Stevens, N., Erasmus, B. F. N., Archibald, S. & Bond, W. J. Woody encroachment over 70 years in South African savannahs: overgrazing, global change or extinction aftershock? Phil. Trans. R. Soc. Lond. B 371, 20150437 (2016).

    Article  Google Scholar 

  26. Hempson, G. P., Archibald, S. & Bond, W. J. The consequences of replacing wildlife with livestock in Africa. Sci. Rep. 7, 17196 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Archer, S. R. et al. in Rangeland Systems (ed. Briske, D. D.) 25–84 (Springer, 2017).

  28. Zavaleta, E. The economic value of controlling an invasive shrub. Ambio 29, 462–467 (2000).

    Article  Google Scholar 

  29. Lowe, S., Browne, M., Boudjelas, S. & De Poorter M. 100 of the World’s Worst Invasive Alien Species: A Selection from the Global Invasive Species Database (Invasive Species Specialist Group of the Species Survival Commission of the World Conservation Union, 2004).

  30. Ratajczak, Z., Nippert, J. B., Hartman, J. C. & Ocheltree, T. W. Positive feedbacks amplify rates of woody encroachment in mesic tallgrass prairie. Ecosphere 2, 121 (2011).

    Article  Google Scholar 

  31. Olofsson, J. & Post, E. Effects of large herbivores on tundra vegetation in a changing climate, and implications for rewilding. Phil. Trans. R. Soc. Lond. B 373, 20170437 (2018).

    Article  Google Scholar 

  32. Derham, T. T., Duncan, R. P., Johnson, C. N. & Jones, M. E. Hope and caution: rewilding to mitigate the impacts of biological invasions. Phil. Trans. R. Soc. Lond. B 373, 20180127 (2018).

    Article  Google Scholar 

  33. Vavra, M., Parks, C. G. & Wisdom, M. J. Biodiversity, exotic plant species, and herbivory: the good, the bad, and the ungulate. For. Ecol. Manage. 246, 66–72 (2007).

    Article  Google Scholar 

  34. Maron, J. L. & Vilà, M. When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95, 361–373 (2001).

    Article  Google Scholar 

  35. Stalmans, M. E., Massad, T. J., Peel, M. J. S., Tarnita, C. E. & Pringle, R. M. War-induced collapse and asymmetric recovery of large-mammal populations in Gorongosa National Park, Mozambique. PLoS ONE 14, e0212864 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Pringle, R. M. Upgrading protected areas to conserve wild biodiversity. Nature 546, 91–99 (2017).

    Article  CAS  PubMed  Google Scholar 

  37. Bouley, P., Poulos, M., Branco, R. & Carter, N. H. Post-war recovery of the African lion in response to large-scale ecosystem restoration. Biol. Conserv. 227, 233–242 (2018).

    Article  Google Scholar 

  38. Tinley, K. L. Framework of the Gorongosa Ecosystem, Mozambique. PhD thesis, Univ. Pretoria (1977).

  39. Beilfuss, R. Adaptive Management of the Invasive Shrub Mimosa pigra at Gorongosa National Park (Gorongosa National Park Department of Scientific Services, 2007).

  40. Lonsdale, W. M. in A Guide to the Management of Mimosa pigra (ed. Harley, K. L. S.) 8–32 (CSIRO, 1992).

  41. Janzen, D. H. in Costa Rican Natural History (ed. Janzen, D. H.) 277–278 (Univ. Chicago Press, 1983).

  42. Keane, R. M. & Crawley, M. J. Exotic plant invasions and the enemy release hypothesis. Trends Ecol. Evol. 17, 164–170 (2002).

    Article  Google Scholar 

  43. Levine, J. M., Adler, P. B. & Yelenik, S. G. A meta-analysis of biotic resistance to exotic plant invasions. Ecol. Lett. 7, 975–989 (2004).

    Article  Google Scholar 

  44. Parker, J. D., Burkepile, D. E. & Hay, M. E. Opposing effects of native and exotic herbivores on plant invasions. Science 311, 1459–1461 (2006).

    Article  CAS  PubMed  Google Scholar 

  45. Cerling, T. E., Harris, J. M. & Passey, B. H. Diets of East African Bovidae based on stable isotope analysis. J. Mammal. 84, 456–470 (2003).

    Article  Google Scholar 

  46. Daskin, J. H., Stalmans, M. & Pringle, R. M. Ecological legacies of civil war: 35-year increase in savanna tree cover following wholesale large-mammal declines. J. Ecol. 104, 79–89 (2016).

    Article  Google Scholar 

  47. Attard, E., Chopping, C., Austin, P., Williams, J. & Pople, T. Minimising the Risk of Spread of Mimosa pigra from Peter Faust Dam, Proserpine (State of Queensland Department of Natural Resources and Water, 2006).

  48. Lonsdale, W. M., Harley, K. & Gillett, J. D. Seed bank dynamics in Mimosa pigra, an invasive tropical shrub. J. Appl. Ecol. 25, 963–976 (1988).

    Article  Google Scholar 

  49. Braithwaite, R. W., Lonsdale, W. M. & Estbergs, J. A. Alien vegetation and native biota in tropical Australia: the impact of Mimosa pigra. Biol. Conserv. 48, 189–210 (1989).

    Article  Google Scholar 

  50. Cook, G. D., Setterfield, S. A. & Maddison, J. P. Shrub invasion of a tropical wetland: implications for weed management. Ecol. Appl. 6, 531–537 (1996).

    Article  Google Scholar 

  51. Perino, A. et al. Rewilding complex ecosystems. Science 364, eaav5570 (2019).

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  53. Hirota, M., Holmgren, M., van Nes, E. H. & Scheffer, M. Global resilience of tropical forest and savanna to critical transitions. Science 334, 232–235 (2011).

    Article  CAS  PubMed  Google Scholar 

  54. Staver, A. C., Archibald, S. & Levin, S. A. The global extent and determinants of savanna and forest as alternative biome states. Science 334, 230–232 (2011).

    Article  CAS  PubMed  Google Scholar 

  55. Pekel, J.-F., Cottam, A., Gorelick, N. & Belward, A. S. High-resolution mapping of global surface water and its long-term changes. Nature 540, 418–422 (2016).

    Article  CAS  PubMed  Google Scholar 

  56. Mumba, M. & Thompson, J. R. Hydrological and ecological impacts of dams on the Kafue Flats floodplain system, southern Zambia. Phys. Chem. Earth 30, 442–447 (2005).

    Article  Google Scholar 

  57. Codron, D. et al. Diets of savanna ungulates from stable carbon isotope composition of faeces. J. Zool. 273, 21–29 (2007).

    Article  Google Scholar 

  58. Pansu, J. et al. Trophic ecology of large herbivores in a reassembling African ecosystem. J. Ecol. 107, 1355–1376 (2019).

    Article  Google Scholar 

  59. Deagle, B. E. et al. Counting with DNA in metabarcoding studies: how should we convert sequence reads to dietary data? Mol. Ecol. 28, 391–406 (2019).

    Article  PubMed  Google Scholar 

  60. Craine, J. M., Towne, E. G., Miller, M. & Fierer, N. Climatic warming and the future of bison as grazers. Sci. Rep. 5, 16738 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Lonsdale, W. M. Rates of spread of an invading species—Mimosa pigra in northern Australia. J. Ecol. 81, 513–521 (1993).

    Article  Google Scholar 

  64. Freeland, W. J. & Janzen, D. H. Strategies in herbivory by mammals: the role of plant secondary compounds. Am. Nat. 108, 269–289 (1974).

    Article  CAS  Google Scholar 

  65. Dearing, M. D., Foley, W. J. & McLean, S. The influence of plant secondary metabolites on the nutritional ecology of herbivorous terrestrial vertebrates. Annu. Rev. Ecol. Evol. Syst. 36, 169–189 (2005).

    Article  Google Scholar 

  66. Thaiyah, A. G. et al. Acute, sub-chronic and chronic toxicity of Solanum incanum L in sheep in Kenya. Kenya Vet. 35, 1–8 (2011).

    Google Scholar 

  67. Pringle, R. M. et al. Low functional redundancy among mammalian browsers in regulating an encroaching shrub (Solanum campylacanthum) in African savannah. Proc. R. Soc. B 281, 20140390 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  68. Seastedt, T. R., Hobbs, R. J. & Suding, K. N. Management of novel ecosystems: are novel approaches required? Front. Ecol. Environ. 6, 547–553 (2008).

    Article  Google Scholar 

  69. Bakker, E. S. et al. Combining paleo-data and modern exclosure experiments to assess the impact of megafauna extinctions on woody vegetation. Proc. Natl Acad. Sci. USA 113, 847–855 (2016).

    Article  CAS  PubMed  Google Scholar 

  70. Branco, P. S. et al. Determinants of elephant foraging behavior in a coupled human-natural system: is brown the new green? J. Anim. Ecol. 88, 780–792 (2019).

    Article  PubMed  Google Scholar 

  71. Goheen, J. R. et al. Piecewise disassembly of a large-herbivore community across a rainfall gradient: the UHURU experiment. PLoS ONE 8, e55192 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Pringle, R. M., Prior, K. M., Palmer, T. M., Young, T. P. & Goheen, J. R. Large herbivores promote habitat specialization and beta diversity of African savanna trees. Ecology 97, 2640–2657 (2016).

    Article  PubMed  Google Scholar 

  73. Coverdale, T. C. et al. Elephants in the understory: opposing direct and indirect effects of consumption and ecosystem engineering by megaherbivores. Ecology 97, 3219–3230 (2016).

    Article  PubMed  Google Scholar 

  74. Goheen, J. R. et al. Conservation lessons from large-mammal manipulations in East African savannas: the KLEE, UHURU, and GLADE experiments. Ann. N.Y. Acad. Sci. 1429, 31–49 (2018).

    Article  PubMed  Google Scholar 

  75. Carter, N. H. et al. Climate change, disease range shifts, and the future of the Africa lion. Conserv. Biol. 32, 1207–1210 (2018).

    Article  PubMed  Google Scholar 

  76. Sinclair, A. R. E., Mduma, S. & Brashares, J. S. Patterns of predation in a diverse predator-prey system. Nature 425, 288–290 (2003).

    Article  CAS  PubMed  Google Scholar 

  77. Atkins, J. L. et al. Cascading impacts of large-carnivore extirpation in an African ecosystem. Science 364, 173–177 (2019).

    CAS  PubMed  Google Scholar 

  78. Miller, I. L. & Lonsdale, W. M. Early records of Mimosa pigra in the Northern Territory. Plant Prot. Q. 2, 140–142 (1987).

    Google Scholar 

  79. Zedler, J. B. & Kercher, S. Causes and consequences of invasive plants in wetlands: opportunities, opportunists, and outcomes. Crit. Rev. Plant Sci. 23, 431–452 (2004).

    Article  Google Scholar 

  80. Seburanga, J. L., Kaplin, B. A., Bizuru, E. & Mwavu, E. N. The folk biology of South American–native shrub, Mimosa pigra L. [Leguminosae] and its invasive success in Rwanda. Int. J. Biodiv. Conserv. 5, 486–497 (2013).

    Google Scholar 

  81. CABI Mimosa pigra (giant sensitive plant) [original text by Rojas-Sandoval, J. & Acevedo-Rodríguez, P.] in Invasive Species Compendium (CAB International, 2019); https://www.cabi.org/isc

  82. Shanungu, G. K. Management of the invasive Mimosa pigra L. in Lochinvar National Park, Zambia. Biodiversity 10, 56–60 (2009).

    Article  Google Scholar 

  83. Rijal, S. & Cochard, R. Invasion of Mimosa pigra on the cultivated Mekong River floodplains near Kratie, Cambodia: farmers’ coping strategies, perceptions, and outlooks. Reg. Environ. Change 16, 681–693 (2015).

    Article  Google Scholar 

  84. Paynter, Q. Evaluating the impact of biological control against Mimosa pigra in Australia: comparing litterfall before and after the introduction of biological control agents. Biol. Control 38, 166–173 (2006).

    Article  Google Scholar 

  85. Paynter, Q. & Flanagan, G. J. Integrating herbicide and mechanical control treatments with fire and biological control to manage an invasive wetland shrub, Mimosa pigra. J. Appl. Ecol. 41, 615–629 (2004).

    Article  Google Scholar 

  86. Ostermeyer, N. & Grace, B. S. Establishment, distribution and abundance of Mimosa pigra biological control agents in northern Australia: implications for biological control. BioControl 52, 703–720 (2007).

    Article  CAS  Google Scholar 

  87. Lonsdale, W. M. & Miller, I. L. Fire as a management tool for a tropical woody weed: Mimosa pigra in northern Australia. J. Environ. Manage. 39, 77–87 (1993).

    Article  Google Scholar 

  88. Adams, V. M., Setterfield, S. A., Douglas, M. M., Kennard, M. J. & Ferdinands, K. Measuring benefits of protected area management: trends across realms and research gaps for freshwater systems. Phil. Trans. R. Soc. Lond. B 370, 20140274 (2015).

    Article  Google Scholar 

  89. Heard, T. A. & Paynter, Q. in Biological Control of Tropical Weeds Using Arthropods (eds Muniappan, R. et al.) 256–273 (Cambridge Univ. Press, 2009).

  90. Cook, D. C., Sheppard, A., Liu, S. & Lonsdale, W. M. in Pest Risk Modelling and Mapping for Invasive Alien Species (ed. Venette, R. C.) 145–161 (CABI, 2015).

  91. Böhme, B., Steinbruch, F., Gloaguen, R., Heilmeier, H. & Merkel, B. Geomorphology, hydrology, and ecology of Lake Urema, central Mozambique, with focus on lake extent changes. Phys. Chem. Earth 31, 745–752 (2006).

    Article  Google Scholar 

  92. Steinbruch, F. & Weise, S. M. Analysis of water stable isotopes fingerprinting to inform conservation management: Lake Urema wetland system, Mozambique. Phys. Chem. Earth 72-75, 13–23 (2014).

    Article  Google Scholar 

  93. Stalmans, M. & Beilfuss, R. Landscapes of the Gorongosa National Park (Gorongosa National Park Department of Scientific Services, 2008).

  94. Convery, I. & Morley, R. in Displaced Heritage: Responses to Disaster, Trauma, and Loss (eds Convery, I. et al.) 129–142 (Boydell, 2014).

  95. Taberlet, P. et al. Power and limitations of the chloroplast trnL (UAA) intron for plant DNA barcoding. Nucl. Acids Res. 35, e14 (2007).

    Article  PubMed  CAS  Google Scholar 

  96. Valentini, A. et al. New perspectives in diet analysis based on DNA barcoding and parallel pyrosequencing: the trnL approach. Mol. Ecol. Res. 9, 51–60 (2009).

    Article  CAS  Google Scholar 

  97. Pansu, J. et al. Reconstructing long-term human impacts on plant communities: an ecological approach based on lake sediment DNA. Mol. Ecol. 24, 1485–1498 (2015).

    Article  PubMed  Google Scholar 

  98. Taberlet, P., Bonin, A., Zinger, L. & Coissac, E. Environmental DNA for Biodiversity Research and Monitoring (Oxford Univ. Press, 2018).

  99. Boyer, F. et al. obitools: a Unix-inspired software package for DNA metabarcoding. Mol. Ecol. Res. 16, 176–182 (2016).

    Article  CAS  Google Scholar 

  100. Binladen, J. et al. The use of coded PCR primers enables high-throughput sequencing of multiple homolog amplification products by 454 parallel sequencing. PLoS ONE 2, e197 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  101. Ficetola, G. F. et al. Replication levels, false presences and the estimation of the presence/absence from eDNA metabarcoding data. Mol. Ecol. Res. 15, 543–556 (2014).

    Article  CAS  Google Scholar 

  102. Ficetola, G. F. et al. An in silico approach for the evaluation of DNA barcodes. BMC Genomics 11, 434 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  103. R Development Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2016).

  104. Csárdi, G. & Nepusz, T. The igraph software package for complex network research. InterJournal Complex Systems, 1695 (2006).

  105. Zinger, L. et al. Extracellular DNA extraction is a fast, cheap and reliable alternative for multi-taxa surveys based on soil DNA. Soil Biol. Biochem. 96, 16–19 (2016).

    Article  CAS  Google Scholar 

  106. Carlsen, T. et al. Don’t make a mista(g)ke: is tag switching an overlooked source of error in amplicon pyrosequencing studies? Fungal Ecol. 5, 747–749 (2012).

    Article  Google Scholar 

  107. Schnell, I. B., Bohmann, K. & Gilbert, M. T. P. Tag jumps illuminated—reducing sequence-to-sample misidentifications in metabarcoding studies. Mol. Ecol. Res. 15, 1289–1303 (2015).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Parque Nacional da Gorongosa and the government of Mozambique for permission to conduct this research. We thank the Gorongosa Project for facilitating scientific research, with special thanks to M. Marchington, F. Moniz, A. Dos Santos, T. Massad, and G. Carr. The Gorongosa Project had no role in the conceptualization, design, data collection, data analysis, manuscript preparation, or decision to publish. We are indebted to K. Tinley for his pioneering research38 on Gorongosa’s pre-war ecology. Supplementary Video 1 was produced in collaboration with National Geographic Labs Crittercam. Funding was provided by National Geographic Young Explorers Grant no. 9459-14; the US National Science Foundation (grant no. IOS-1656527 and the Graduate Research Fellowship Program); the Princeton Environmental Institute’s Grand Challenges programme; the Randall and Mary Hack ’69 Award for Water and the Environment; Princeton University’s Institutes for African Studies and International and Regional Studies; the Greg Carr Foundation; the Cameron Schrier Foundation; the Sherwood Foundation; and Princeton’s Innovation Fund for New Ideas in the Natural Sciences.

Author information

Authors and Affiliations

  1. Department of Ecology & Evolutionary Biology, Princeton University, Princeton, NJ, USA

    Jennifer A. Guyton, Johan Pansu, Matthew C. Hutchinson, Tyler R. Kartzinel, Arjun B. Potter, Tyler C. Coverdale, Joshua H. Daskin & Robert M. Pringle

  2. Station Biologique de Roscoff, UMR 7144 CNRS-Sorbonne Université, Roscoff, France

    Johan Pansu

  3. CSIRO Ocean & Atmosphere, Lucas Heights, New South Wales, Australia

    Johan Pansu

  4. Department of Ecology & Evolutionary Biology, Brown University, Providence, RI, USA

    Tyler R. Kartzinel

  5. Department of Ecology & Evolutionary Biology, Cornell University, Ithaca, NY, USA

    Tyler C. Coverdale

  6. Department of Ecology & Evolutionary Biology, Yale University, New Haven, CT, USA

    Joshua H. Daskin

  7. Department of Scientific Services, Parque Nacional da Gorongosa, Sofala, Mozambique

    Ana Gledis da Conceição, Marc E. Stalmans & Robert M. Pringle

  8. ARC-Animal Production Institute, Rangeland Ecology Group, Nelspruit, South Africa

    Mike J. S. Peel

Authors
  1. Jennifer A. Guyton
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Johan Pansu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Matthew C. Hutchinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tyler R. Kartzinel
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Arjun B. Potter
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tyler C. Coverdale
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Joshua H. Daskin
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ana Gledis da Conceição
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Mike J. S. Peel
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Marc E. Stalmans
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Robert M. Pringle
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

J.A.G. and R.M.P. conceived and designed the research. J.A.G. conducted the primary plant surveys and the exclosure experiment, and collected specimens for the plant reference database. J.P., M.C.H., and T.R.K. conducted the DNA metabarcoding analyses. J.P. analysed the dietary data. A.B.P. contributed the forage-quality data. M.J.S.P. contributed additional plant-survey data. M.E.S. contributed the wildlife-count data. J.A.G., J.P., M.C.H., T.R.K., T.C.C., J.H.D., A.G.C., and R.M.P. collected samples and field data. J.A.G. and R.M.P. analysed the field data. J.A.G., J.P., and R.M.P. wrote the manuscript. All authors made revisions and approved the final draft.

Corresponding author

Correspondence to Robert M. Pringle.

Ethics declarations

Competing interests

A.G.C. and M.E.S. were employed by the Gorongosa Project, a non-profit organization that co-manages conservation and restoration in Gorongosa National Park in partnership with the government of Mozambique. M.J.S.P. was contracted by the Gorongosa Project to conduct vegetation surveys. R.M.P. was an unpaid member on the board of directors of the Gorongosa Project. All other authors have no competing interests.

Additional information

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

Extended data

Extended Data Fig. 1 Top food plants for six dominant ungulates in the Urema floodplain between 2013 and 2018.

Bars show the mean relative read abundance of each plant taxon across all fecal samples in each year for each species. Sample sizes for each species in each year are shown in Fig. 3a. The best possible taxonomic identification for each plant (see Methods) is provided beneath each bar, and the corresponding plant life-form (grass, shrub, tree, or forb) is listed above each bar. Stars within bars denote Mimosa pigra (the first or second most abundant food for all ruminant species in all years).

Extended Data Fig. 2 Mimosa consumption in early (June–August) versus late (October–November) dry season of 2017 (below-average rainfall year) and 2018 (above-average rainfall year).

Bars show the mean (±1 s.e.m.) relative read abundance of Mimosa pigra across all fecal samples in each season for each species. Sample sizes for each species in each season are shown above bars. As for Fig. 3, quantitative comparisons between years (and between seasons for 2018) should be interpreted cautiously (see Methods). Although sample sizes are limited for some species in some seasons, the data show that antelope species consumed mimosa in appreciable quantities throughout the dry season.

Extended Data Fig. 3 Suppression of Mimosa pigra reproduction by large herbivores.

Here, the results in Fig. 4c, d are broken down to show independent trends in immature floral buds (a) and mature flowers (b), along with immature green fruits (c) and mature brown seed pods (d) in the experimental exclosure and control plots. Points show the mean (±1 s.e.m.) number of reproductive structures per plant in each treatment over three years. As in Fig. 4a–d, measurements at the level of individual plants were averaged at the plot level before the analysis (from left to right in each panel, n = 12, 6, 12, 9, 10, and 9 plots per survey). These data show that large herbivores have essentially eliminated reproductive output by mimosa in Gorongosa: few reproductive structures at any stage of development were recorded in the control plots as of 2017, and none at all were found in 2018.

Extended Data Fig. 4 Estimation of aboveground dry biomass from field measurements of plant volume.

Plant volume was calculated using measurements of height and canopy dimensions for each of 34 Mimosa pigra individuals, assuming an ellipsoidal shrub shape, and regressed against the dry aboveground biomass measured for each of the same plants (see Methods). The regression equation shown was used to estimate the aboveground biomass of standing plants in each experimental exclosure and control plot in 2018 (see Fig. 5b).

Extended Data Fig. 5 Rapid recruitment and growth of Mimosa pigra inside, but not outside, experimental herbivore exclosures.

All photos are from the same exclosure-control pair (in long-term monitoring plot 16). a, Panoramic photograph of the control plot in 2018, showing floodplain dominated by grasses (mostly Cynodon dactylon) and forbs (mostly Heliotropium spp.); a total of 13 mimosa plants were recorded in this 260-m2 plot in 2018, none taller than 43 cm. The exclosure plot is visible at top center. b, Forb-dominated understory in the exclosure plot in September 2017, when a total of 57 small mimosa plants were recorded, none taller than 31 cm (up from just one individual recorded in September 2016). c–e, Three views of the same exclosure plot in August 2018, when 661 mimosa plants of at least 15-cm stem length were recorded, including individuals up to 158-cm tall.

Supplementary information

Reporting Summary

Supplementary Data 1–8

Field data.

Supplementary Video 1

Waterbuck foraging on Mimosa pigra in the Urema floodplain (8 August 2015). This footage was obtained from a National Geographic Labs Crittercam fitted around the animal’s neck. Note that this individual is foraging within one of the many mudflats that occur at the edges of Lake Urema and adjoining ponds and drainage channels (specific location 18°52’43.82”S, 34°27’26.55”E); these mudflats typically have sparse, forb-dominated plant communities. The limited grass cover evident in the video should not be interpreted as evidence that grass or other forages were limited in the floodplain at large.

Supplementary Video 2

Oribi foraging on Mimosa pigra in the Urema floodplain (23 July 2019).

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guyton, J.A., Pansu, J., Hutchinson, M.C. et al. Trophic rewilding revives biotic resistance to shrub invasion. Nat Ecol Evol 4, 712–724 (2020). https://doi.org/10.1038/s41559-019-1068-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-019-1068-y

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing