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The long-term restoration of ecosystem complexity

Abstract

Multiple large-scale restoration strategies are emerging globally to counteract ecosystem degradation and biodiversity loss. However, restoration often remains insufficient to offset that loss. To address this challenge, we propose to focus restoration science on the long-term (centuries to millennia) re-assembly of degraded ecosystem complexity integrating interaction network and evolutionary potential approaches. This approach provides insights into eco-evolutionary feedbacks determining the structure, functioning and stability of recovering ecosystems. Eco-evolutionary feedbacks may help to understand changes in the adaptive potential after disturbance of metacommunity hub species with core structural and functional roles for their use in restoration. Those changes can be studied combining a restoration genomics approach based on whole-genome sequencing with replicated space-for-time substitutions linking changes in genetic variation to functions or traits relevant to the establishment of evolutionarily resilient communities. This approach may set the knowledge basis for future tools to accelerate the restoration of ecosystems able to adapt to ongoing global changes.

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Fig. 1: Global restoration initiatives.

European Union, 1995–2020 (European Commission logo) under a Creative Commons CC BY 4.0 licence; New York Declaration on Forests Global Platform, United Nations Development Programme (New York Declaration on Forests Global Platform symbol); Convention on Biological Diversity (Convention on Biological Diversity symbol and Aichi Biodiversity Target symbols); United Nations (UN/SDG; SDG symbol)

Fig. 2: Meta-analyses on restoration performance.

The Integration and Application Network, University of Maryland Center for Environmental Science (background landscape elements; ian.umces.edu/symbols/)

Fig. 3: Measures of recovery through time.
Fig. 4: Approaches to analyse genomic variation.
Fig. 5: Future steps to improve restoration science and derived management actions.

The Integration and Application Network, University of Maryland Center for Environmental Science (background landscapes elements, tree and insect images; ian.umces.edu/symbols/)

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References

  1. Haddad, N. M. et al. Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci. Adv. 1, e1500052 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  2. Miraldo, A. et al. An Anthropocene map of genetic diversity. Science 353, 1532–1535 (2016).

    Article  CAS  PubMed  Google Scholar 

  3. Newbold, T. et al. Global effects of land use on local terrestrial biodiversity. Nature 520, 45–50 (2015).

    Article  CAS  PubMed  Google Scholar 

  4. Gann, G. D. et al. International principles and standards for the practice of ecological restoration. Second edition. Restor. Ecol. 27, S1–S46 (2019).

    Article  Google Scholar 

  5. United Nations Environment Program. New UN Decade on Ecosystem Restoration offers unparalleled opportunity for job creation, food security and addressing climate change. United Nations Environment Program Press Release (01 March 2019); https://go.nature.com/2wMjUZt

  6. Progress on the New York Declaration on Forests - Achieving Collective Forest Goals. Updates on Goals 1-10 (Climate Focus, 2016).

  7. COP 11 Decision X1/16. Ecosystem Restoration (Convention on Biological Diversity, 2012).

  8. Our Life Insurance, Our Natural Capital: an EU Biodiversity Strategy to 2020 2011/2307(INI) (European Parliament, 2012).

  9. Zedler, J. B. & Callaway, J. C. Tracking wetland restoration: do mitigation sites follow desired trajectories? Restor. Ecol. 7, 69–73 (1999).

    Article  Google Scholar 

  10. Zedler, J. B. Progress in wetland restoration ecology. Trends Ecol. Evol. 15, 402–407 (2000).

    Article  CAS  PubMed  Google Scholar 

  11. Moreno-Mateos, D. et al. Anthropogenic ecosystem disturbance and the recovery debt. Nat. Commun. 8, 14163 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Cardinale, B., Duffy, J. & Gonzalez, A. Biodiversity loss and its impact on humanity. Nature 486, 59–67 (2012).

    Article  CAS  PubMed  Google Scholar 

  13. Tittensor, D. P. et al. A mid-term analysis of progress toward international biodiversity targets. Science 346, 241–244 (2014).

    Article  CAS  PubMed  Google Scholar 

  14. Jones, H. P. et al. Restoration and repair of Earth’s damaged ecosystems. Proc. R. Soc. B Biol. Sci. 285, 20172577 (2018).

    Article  Google Scholar 

  15. Forup, M. L., Henson, K. S. E., Craze, P. G. & Memmott, J. The restoration of ecological interactions: plant-pollinator networks on ancient and restored heathlands. J. Appl. Ecol. 45, 742–752 (2008).

    Article  Google Scholar 

  16. Kaiser-Bunbury, C. N. et al. Ecosystem restoration strengthens pollination network resilience and function. Nature 542, 223–227 (2017).

    Article  CAS  PubMed  Google Scholar 

  17. Ribeiro da Silva, F. et al. The restoration of tropical seed dispersal networks. Restor. Ecol. 23, 852–860 (2015).

    Article  Google Scholar 

  18. Society for Ecological Restoration International, Science and Policy Working Group The SER Primer on Ecological Restoration (Society for Ecological Restoration, 2004).

  19. Keenleyside, K., Dudley, N., Cairns, S., Hall, C. & Stolton, S. Ecological Restoration for Protected Areas: Principles, Guidelines and Best Practices (IUCN, 2012).

  20. Hastings, A. Timescales and the management of ecological systems. Proc. Natl Acad. Sci. USA 113, 14568–14573 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Cole, L. E. S., Bhagwat, S. A. & Willis, K. J. Recovery and resilience of tropical forests after disturbance. Nat. Commun. 5, 3906 (2014).

    Article  CAS  PubMed  Google Scholar 

  22. Tylianakis, J. M., Tscharntke, T. & Lewis, O. T. Habitat modification alters the structure of tropical host-parasitoid food webs. Nature 445, 202–205 (2007).

    Article  CAS  PubMed  Google Scholar 

  23. Albrecht, M., Duelli, P., Schmid, B. & Müller, C. B. Interaction diversity within quantified insect food webs in restored and adjacent intensively managed meadows. J. Anim. Ecol. 76, 1015–1025 (2007).

    Article  PubMed  Google Scholar 

  24. Wardle, D. A., Bardgett, R. D., Callaway, R. M. & van der Putten, W. H. Terrestrial ecosystem responses to species gains and losses. Science 332, 1273–1278 (2011).

    Article  CAS  PubMed  Google Scholar 

  25. Aizen, M. A., Sabatino, M. & Tylianakis, J. M. Specialization and rarity predict nonrandom loss of interactions from mutualist networks. Science 335, 1486–1489 (2012).

    Article  CAS  PubMed  Google Scholar 

  26. Valiente-Banuet, A. et al. Beyond species loss: the extinction of ecological interactions in a changing world. Funct. Ecol. 29, 299–307 (2015).

    Article  Google Scholar 

  27. Morriën, E. et al. Soil networks become more connected and take up more carbon as nature restoration progresses. Nat. Commun. 8, 14349 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Petanidou, T., Kallimanis, A. S., Tzanopoulos, J., Sgardelis, S. P. & Pantis, J. D. Long-term observation of a pollination network: fluctuation in species and interactions, relative invariance of network structure and implications for estimates of specialization. Ecol. Lett. 11, 564–575 (2008).

    Article  PubMed  Google Scholar 

  29. Hackett, T. D. et al. Reshaping our understanding of species’ roles in landscape-scale networks. Ecol. Lett. 22, 1367–1377 (2019).

    Article  PubMed  Google Scholar 

  30. CaraDonna, P. J. et al. Interaction rewiring and the rapid turnover of plant–pollinator networks. Ecol. Lett. 20, 385–394 (2017).

    Article  PubMed  Google Scholar 

  31. Poisot, T., Stouffer, D. B. & Gravel, D. Beyond species: why ecological interaction networks vary through space and time. Oikos 124, 243–251 (2015).

    Article  Google Scholar 

  32. Beckett, J. S. & Hywel, T. P. Williams. Coevolutionary diversification creates nested-modular structure in phage–bacteria interaction networks. Interface Focus 3, 20130033 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  33. Rohr, R. P. & Bascompte, J. Components of phylogenetic signal in antagonistic and mutualistic networks. Am. Nat. 184, 556–564 (2014).

    Article  PubMed  Google Scholar 

  34. Gross, T. & Blasius, B. Adaptive coevolutionary networks: a review. J. R. Soc. Interface 5, 259–271 (2008).

    Article  PubMed  Google Scholar 

  35. Raimundo, R. L. G., Guimarães, P. R. & Evans, D. M. Adaptive networks for restoration ecology. Trends Ecol. Evol. 33, 664–675 (2018).

    Article  PubMed  Google Scholar 

  36. Morales-Castilla, I., Matias, M. G., Gravel, D. & Araújo, M. B. Inferring biotic interactions from proxies. Trends Ecol. Evol. 30, 347–356 (2015).

    Article  PubMed  Google Scholar 

  37. Toju, H. et al. Species-rich networks and eco-evolutionary synthesis at the metacommunity level. Nat. Ecol. Evol. 1, 0024 (2017).

    Article  Google Scholar 

  38. Rooney, N., McCann, K., Gellner, G. & Moore, J. C. Structural asymmetry and the stability of diverse food webs. Nature 442, 265–269 (2006).

    Article  CAS  PubMed  Google Scholar 

  39. Schleuning, M., Fründ, J. & García, D. Predicting ecosystem functions from biodiversity and mutualistic networks: an extension of trait-based concepts to plant-animal interactions. Ecography 38, 380–392 (2015).

    Article  Google Scholar 

  40. Pocock, M. J. O., Evans, D. M. & Memmott, J. The robustness and restoration of a network of ecological networks. Science 335, 973–977 (2012).

    Article  CAS  PubMed  Google Scholar 

  41. Perez-Mendez, N., Jordano, P., Garcia, C. & Valido, A. The signatures of Anthropocene defaunation: cascading effects of the seed dispersal collapse. Sci. Rep. 6, 24820 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Pilosof, S., Porter, M. A., Pascual, M. & Kéfi, S. The multilayer nature of ecological networks. Nat. Ecol. Evol. 1, 0101 (2017).

    Article  Google Scholar 

  44. Montoya, D., Yallop, M. L. & Memmott, J. Functional group diversity increases with modularity in complex food webs. Nat. Commun. 6, 7379 (2015).

    Article  CAS  PubMed  Google Scholar 

  45. Allan, E. et al. Land use intensification alters ecosystem multifunctionality via loss of biodiversity and changes to functional composition. Ecol. Lett. 18, 834–843 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  46. Montoya, D. et al. Trade-offs in provisioning and stability of multiple ecosystem services in agroecosystems. Ecol. Appl. 29, e01853 (2018).

    Google Scholar 

  47. Donohue, I. et al. On the dimensionality of ecological stability. Ecol. Lett. 16, 421–429 (2013).

    Article  PubMed  Google Scholar 

  48. Hillebrand, H. et al. Decomposing multiple dimensions of stability in global change experiments. Ecol. Lett. 21, 21–30 (2018).

    Article  PubMed  Google Scholar 

  49. Tilman, D., Reich, P. B. & Knops, J. M. H. Biodiversity and ecosystem stability in a decade-long grassland experiment. Nature 441, 629–632 (2006).

    Article  CAS  PubMed  Google Scholar 

  50. Hector, A. et al. General stabilizing effects of plant diversity on grassland productivity through population asynchrony and overyielding. Ecology 91, 2213–2220 (2010).

    Article  CAS  PubMed  Google Scholar 

  51. Lyons, S. K. et al. Holocene shifts in the assembly of plant and animal communities implicate human impacts. Nature 529, 80–83 (2016).

    Article  PubMed  CAS  Google Scholar 

  52. Sarrazin, F. & Lecomte, J. Evolution in the Anthropocene. Science 351, 922–923 (2016).

    Article  CAS  PubMed  Google Scholar 

  53. Eizaguirre, C. & Baltazar-Soares, M. Evolutionary conservation—evaluating the adaptive potential of species. Evol. Appl. 7, 963–967 (2014).

    Article  PubMed Central  Google Scholar 

  54. Hoffmann, A. A., Sgrò, C. M. & Kristensen, T. N. Revisiting adaptive potential, population size, and conservation. Trends Ecol. Evol. 32, 506–517 (2017).

    Article  PubMed  Google Scholar 

  55. Sgrò, C. M., Lowe, A. J. & Hoffmann, A. A. Building evolutionary resilience for conserving biodiversity under climate change. Evol. Appl. 4, 326–337 (2011).

    Article  PubMed  Google Scholar 

  56. Harrisson, K. A., Pavlova, A., Telonis-Scott, M. & Sunnucks, P. Using genomics to characterize evolutionary potential for conservation of wild populations. Evol. Appl. 7, 1008–1025 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  57. Fraser, H. B. et al. Systematic detection of polygenic cis-regulatory evolution. PLoS Genet. 7, e1002023 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Rockman, M. V. The QTN program and the alleles that matter for evolution: all that’s gold does not glitter. Evolution 66, 1–17 (2012).

    Article  PubMed  Google Scholar 

  59. De Kort, H. & Honnay, O. in Evolutionary Biology: Self/Nonself Evolution, Species and Complex Traits Evolution, Methods and Concepts (ed. Pontarotti, P.) 313–327 (Springer, 2017).

  60. Fuentes-Pardo, A. P. & Ruzzante, D. E. Whole-genome sequencing approaches for conservation biology: advantages, limitations and practical recommendations. Mol. Ecol. 26, 5369–5406 (2017).

    Article  CAS  PubMed  Google Scholar 

  61. Chandler, C. H., Chari, S. & Dworkin, I. Does your gene need a background check? How genetic background impacts the analysis of muta- tions, genes, and evolution. Trends Genet. 29, 358–366 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Le Rouzic, A. & Carlborg, Ö. Evolutionary potential of hidden genetic variation. Trends Ecol. Evol. 23, 33–37 (2008).

    Article  PubMed  Google Scholar 

  63. Goodwin, S., McPherson, J. D. & McCombie, W. R. Coming of age: ten years of next-generation sequencing technologies. Nat. Rev. Genet. 17, 333–351 (2016).

    Article  CAS  PubMed  Google Scholar 

  64. Ekblom, R. & Wolf, J. B. W. A field guide to whole-genome sequencing, assembly and annotation. Evol. Appl. 7, 1026–1042 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  65. Lin, M. F. et al. Locating protein-coding sequences under selection for additional, overlapping functions in 29 mammalian genomes. Genome Res. 6, 1916–1928 (2011).

    Article  CAS  Google Scholar 

  66. Grossman, S. R. et al. Identifying recent adaptations in large-scale genomic data. Cell 152, 703–713 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Wagner, A. Genotype networks shed light on evolutionary constraints. Trends Ecol. Evol. 26, 577–584 (2011).

    Article  PubMed  Google Scholar 

  68. Rey, O., Danchin, E., Mirouze, M., Loot, C. & Blanchet, S. Adaptation to global change: a transposable element-epigenetics perspective. Trends Ecol. Evol. 31, 514–526 (2016).

    Article  PubMed  Google Scholar 

  69. Alberdi, A., Aizpurua, O., Bohmann, K., Zepeda-Mendoza, M. L. & Gilbert, M. T. P. Do vertebrate gut metagenomes confer rapid ecological adaptation? Trends Ecol. Evol. 31, 689–699 (2016).

    Article  PubMed  Google Scholar 

  70. Balaguer, L., Escudero, A., Martín-Duque, J. F., Mola, I. & Aronson, J. The historical reference in restoration ecology: re-defining a cornerstone concept. Biol. Conserv. 176, 12–20 (2014).

    Article  Google Scholar 

  71. Damgaard, C. A critique of the space-for-time substitution practice in community ecology. Trends Ecol. Evol. 34, 416–421 (2019).

    Article  PubMed  Google Scholar 

  72. Walker, L. R., Wardle, D. A., Bardgett, R. D. & Clarkson, B. D. The use of chronosequences in studies of ecological succession and soil development. J. Ecol. 98, 725–736 (2010).

    Article  Google Scholar 

  73. Hendry, A. P. et al. Evolutionary principles and their practical application. Evol. Appl. 4, 159–183 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  74. Hendry, A. P. Key questions in the genetics and genomics of eco-evolutionary dynamics. Heredity 111, 456–466 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Bascompte, J., Jordano, P., Melián, C. J. & Olesen, J. M. The nested assembly of plant-animal mutualistic networks. Proc. Natl Acad. Sci. USA 100, 9383–9387 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Bascompte, J. & Jordano, P. Mutualistic Networks (Princeton Univ. Press, 2014).

  77. Memmott, J., Waser, N. M. & Price, M. V. Tolerance of pollination networks to species extinctions. Proc. R. Soc. B Biol. Sci. 271, 2605–2611 (2004).

    Article  Google Scholar 

  78. Pellissier, L. et al. Comparing species interaction networks along environmental gradients. Biol. Rev. 93, 785–800 (2018).

    Article  PubMed  Google Scholar 

  79. Brose, U., Ostling, A., Harrison, K. & Martinez, N. D. Unified spatial scaling of species and their trophic interactions. Nature 428, 167–171 (2004).

    Article  CAS  PubMed  Google Scholar 

  80. Arrizabalaga-Escudero, A. et al. Trophic requirements beyond foraging habitats: the importance of prey source habitats in bat conservation. Biol. Conserv. 191, 512–519 (2015).

    Article  Google Scholar 

  81. Moreno-Mateos, D., Power, M. E., Comín, F. A. & Yockteng, R. Structural and functional loss in restored wetland ecosystems. PLoS Biol. 10, e1001247 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Mccrackin, M. L., Jones, H. P., Jones, P. C. & Moreno-Mateos, D. Recovery of lakes and coastal marine ecosystems from eutrophication: a global meta-analysis. Limnol. Oceanogr. 62, 507–518 (2017).

    Article  CAS  Google Scholar 

  83. Meli, P. et al. A global review of past land use, climate, and active vs. passive restoration effects on forest recovery. PLoS ONE 12, e0171368 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  84. Cover, T. M. & Thomas, J. A. Elements of Information Theory (John Wiley & Sons, Inc., 2006).

  85. Walker, B., Holling, C. S., Carpenter, S. R. & Kinzig, A. Resilience, adaptability and transformability in social–ecological systems. Ecol. Soc. 9, 5 (2004).

    Article  Google Scholar 

  86. Pimm, S. The complexity and stability of ecosystems. Nature 307, 321–326 (1984).

    Article  Google Scholar 

  87. van der Heijden, M. G. A., Martin, F. M., Selosse, M.-A. & Sanders, I. R. Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol. 205, 1406–1423 (2015).

    Article  PubMed  CAS  Google Scholar 

  88. Gange, A. C., Stagg, P. G. & Ward, L. K. Arbuscular mycorrhizal fungi affect phytophagous insect specialism. Ecol. Lett. 5, 11–15 (2002).

    Article  Google Scholar 

  89. Ngosong, C., Gabriel, E. & Ruess, L. Collembola grazing on arbuscular mycorrhiza fungi modulates nutrient allocation in plants. Pedobiologia 57, 171–179 (2014).

    Article  Google Scholar 

  90. Bardgett, R. D. & van der Putten, W. H. Belowground biodiversity and ecosystem functioning. Nature 515, 505–511 (2014).

    Article  CAS  PubMed  Google Scholar 

  91. Macfadyen, S., Craze, P. G., Polaszek, A., van Achterberg, K. & Memmott, J. Parasitoid diversity reduces the variability in pest control services across time on farms. Proc. R. Soc. B Biol. Sci. 278, 3387–3394 (2011).

    Article  Google Scholar 

  92. Smith, S. & Read, D. Mycorrhizal Symbiosis (Academic Press, 2008).

  93. Low, W. Y. et al. Chromosome-level assembly of the water buffalo genome surpasses human and goat genomes in sequence contiguity. Nat. Commun. 10, 260 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  94. Jones, M. R. & Good, J. M. Targeted capture in evolutionary and ecological genomics. Mol. Ecol. 25, 185–202 (2016).

    Article  PubMed  Google Scholar 

  95. Clement, C. R., de Cristo-Araújo, M., d’Eeckenbrugge, G. C., Pereira, A. A. & Picanço-Rodrigues, D. Origin and domestication of native Amazonian crops. Diversity 2, 72–106 (2010).

    Article  Google Scholar 

  96. Levis, C. et al. Persistent effects of pre-Columbian plant domestication on Amazonian forest composition. Science 355, 925–931 (2017).

    Article  CAS  PubMed  Google Scholar 

  97. Ross, N. J. Modern tree species composition reflects ancient Maya ‘forest gardens’ in northwest Belize. Ecol. Appl. 21, 75–84 (2011).

    Article  PubMed  Google Scholar 

  98. Roberts, P., Hunt, C., Arroyo-Kalin, M., Evans, D. & Boivin, N. The deep human prehistory of global tropical forests and its relevance for modern conservation. Nat. Plants 3, 17093 (2017).

    Article  PubMed  Google Scholar 

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Acknowledgements

D.M.-M. has been funded for this research by the Spanish Ministry of Economy and Competiveness through Societal Challenge Program (grant no. CGL2015-70452-R) and María de Maeztu excellence accreditation MDM-2017-0714. A.A. was funded by Lundbeckfonden (grant no. R250-2017-1351). E.M. is supported through a NWO-Veni grant (863.15.021). A.R.-U. was funded by an Environmental Fellowship Program from Fundación “Tatiana Pérez de Guzmán el Bueno” in 2016. D.M. was funded by the French ANR through LabEx TULIP (ANR-10-LABX-41; ANR-11-IDEX-002-02) and by the European Research Council (FRAGCLIM Consolidator Grant no. 726176).

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D.M.-M. and A.A. conceived the idea and wrote the manuscript. D.M., E.M., A.R.-U. and W.H.v.d.P. wrote the manuscript.

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Correspondence to David Moreno-Mateos.

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Moreno-Mateos, D., Alberdi, A., Morriën, E. et al. The long-term restoration of ecosystem complexity. Nat Ecol Evol 4, 676–685 (2020). https://doi.org/10.1038/s41559-020-1154-1

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