Introducing desirable patches to initiate ecosystem transitions and accelerate ecosystem restoration.

ecological modeling ecosystem restoration nucleation theory patch introduction plant community dynamics restoration strategy spatial dynamics

Journal

Ecological applications : a publication of the Ecological Society of America
ISSN: 1051-0761
Titre abrégé: Ecol Appl
Pays: United States
ID NLM: 9889808

Informations de publication

Date de publication:
Dec 2023
Historique:
revised: 30 05 2023
received: 18 08 2022
accepted: 17 07 2023
medline: 4 12 2023
pubmed: 21 8 2023
entrez: 21 8 2023
Statut: ppublish

Résumé

Meeting restoration targets may require active strategies to accelerate natural regeneration rates or overcome the resilience associated with degraded ecosystem states. Introducing desired ecosystem patches in degraded landscapes constitutes a promising active restoration strategy, with various mechanisms potentially causing these patches to become foci from which desired species can re-establish throughout the landscape. This study considers three mechanisms previously identified as potential drivers of introduced patch dynamics: autocatalytic nucleation, directed dispersal, and resource concentration. These mechanisms reflect qualitatively different positive feedbacks. We developed an ecological model framework that compared how the occurrence of each mechanism was reflected in spatio-temporal patch dynamics. We then analyzed the implications of these relationships for optimal restoration design. We found that patch expansion accelerated over time when driven by the autocatalytic nucleation mechanism, while patch expansion driven by the directed dispersal or resource concentration mechanisms decelerated over time. Additionally, when driven by autocatalytic nucleation, patch expansion was independent of patch position in the landscape. However, the proximity of other patches affected patch expansion either positively or negatively when driven by directed dispersal or resource concentration. For autocatalytic nucleation, introducing many small patches was a favorable strategy, provided that each individual patch exceeded a critical patch size. Introducing a single patch or a few large patches was the most effective restoration strategy to initiate the directed dispersal mechanism. Introducing many small patches was the most effective strategy for reaching restored ecosystem states driven by a resource concentration mechanism. Our model results suggest that introducing desirable patches can substantially accelerate ecosystem restoration, or even induce a critical transition from an otherwise stable degraded state toward a desired ecosystem state. However, the potential of this type of restoration strategy for a particular ecosystem may strongly depend on the mechanism driving patch dynamics. In turn, which mechanism drives patch dynamics may affect the optimal spatial design of an active restoration strategy. Each of the three mechanisms considered reflects distinct spatio-temporal patch dynamics, providing novel opportunities for empirically identifying key mechanisms, and restoration designs that introduce desired patches in degraded landscapes according to these patch dynamics.

Identifiants

pubmed: 37602903
doi: 10.1002/eap.2910
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2910

Subventions

Organisme : NSF
ID : DEB-1556664
Organisme : NSF
ID : DEB-1738041
Organisme : NSF
ID : OIA-1656006
Organisme : University of Zurich
Organisme : University Research Priority Program

Informations de copyright

© 2023 The Authors. Ecological Applications published by Wiley Periodicals LLC on behalf of The Ecological Society of America.

Références

Aide, T. M., J. K. Zimmerman, L. Herrera, M. Rosario, and M. Serrano. 1995. “Forest Recovery in Abandoned Tropical Pastures in Puerto Rico.” Forest Ecology and Management 77: 77-86.
Allstadt, A., T. Caraco, and G. Korniss. 2007. “Ecological Invasion: Spatial Clustering and the Critical Radius.” Evolutionary Ecology Research 9: 375-394.
Angelini, C., and B. R. Silliman. 2012. “Patch Size-Dependent Community Recovery After Massive Disturbance.” Ecology 93: 101-110.
Angelini, C., J. N. Griffin, J. van de Koppel, L. P. M. Lamers, A. J. P. Smolders, M. Derksen-Hooijberg, T. van der Heide, and B. R. Silliman. 2016. “A Keystone Mutualism Underpins Resilience of a Coastal Ecosystem to Drought.” Nature Communications 7: 12473.
Aronson, J., N. Goodwin, L. Orlando, C. Eisenberg, and A. T. Cross. 2020. “A World of Possibilities: Six Restoration Strategies to Support the United Nation's Decade on Ecosystem Restoration.” Restoration Ecology 28: 730-736.
Averill, C., C. Fortunel, D. S. Maynard, J. van den Hoogen, M. C. Dietze, J. M. Bhatnagar, and T. W. Crowther. 2022. “Alternative Stable States of the Forest Microbiome are Maintained Through Positive Feedbacks.” Nature Ecology & Evolution 6: 375-382.
Bastiaansen, R., O. Jaibi, V. Deblauwe, M. B. Eppinga, K. Siteur, E. Siero, S. Mermoz, A. Bouvet, A. Doelman, and M. Rietkerk. 2018. “Multistability of Model and Real Dryland Ecosystems Through Spatial Self-Organization.” Proceedings of the National Academy of Sciences USA 115: 11256-11261.
Bauer, J. T., K. M. L. Mack, and J. D. Bever. 2015. “Plant-Soil Feedbacks as Drivers of Succession: Evidence from Remnant and Restored Tallgrass Prairies.” Ecosphere 6: 1-12.
Bechara, F. C., B. E. Trentin, V. L. Engel, D. A. Estevan, and T. Ticktin. 2021. “Performance and Cost of Applied Nucleation Versus High-Diversity Plantations for Tropical Forest Restoration.” Forest Ecology and Management 491: 119088.
Bechara, F. C., S. J. Dickens, E. C. Farrer, L. Larios, E. N. Spotswood, P. Mariotte, and K. N. Suding. 2016. “Neotropical Rainforest Restoration: Comparing Passive, Plantation and Nucleation Approaches.” Biodiversity and Conservation 25: 2021-2034.
Bera, B. K., O. Tzuk, J. J. R. Bennett, and E. Meron. 2021. “Linking Spatial Self-Organization to Community Assembly and Biodiversity.” eLife 10: e73819.
Bernik, B. M., M. B. Eppinga, A. S. Kolker, and M. J. Blum. 2018. “Clonal Vegetation Patterns Mediate Shoreline Erosion.” Geophysical Research Letters 45: 6476-6484.
Bowman, D. M. J. S., G. L. W. Perry, and J. B. Marston. 2015. “Feedbacks and Landscape-Level Vegetation Dynamics.” Trends in Ecology & Evolution 30: 255-260.
Bromley, J., J. Brouwer, A. P. Barker, S. R. Gaze, and C. Valentine. 1997. “The Role of Surface Water Redistribution in an Area of Patterned Vegetation in a Semi-Arid Environment, South-West Niger.” Journal of Hydrology 198: 1-29.
Burrill, H. M., G. Wang, and J. D. Bever. 2023. “Rapid Differentiation of Soil and Root Microbiomes in Response to Plant Composition and Biodiversity in the Field.” ISME Communications 3: 31.
Byers, J. E., K. Cuddington, C. G. Jones, T. S. Talley, A. Hastings, J. G. Lambrinos, J. A. Crooks, and W. G. Wilson. 2006. “Using Ecosystem Engineers to Restore Ecological Systems.” Trends in Ecology & Evolution 21: 493-500.
Carlo, T. A., and J. J. Tewksbury. 2014. “Directness and Tempo of Avian Seed Dispersal Increases Emergence of Wild Chiltepins in Desert Grasslands.” Journal of Ecology 102: 248-255.
Caughlin, T. T., S. Elliott, and J. W. Lichstein. 2016. “When Does Seed Limitation Matter for Scaling up Reforestation from Patches to Landscapes?” Ecological Applications 26: 2439-2450.
Cheeke, T. E., C. Zheng, L. Koziol, C. R. Gurholt, and J. D. Bever. 2019. “Sensitivity to AMF Species Is Greater in Late-Successional than Early-Successional Native or Nonnative Grassland Plants.” Ecology 100: e02855.
Cole, R. J., K. D. Holl, and R. A. Zahawi. 2010. “Seed Rain under Tree Islands Planted to Restore Degraded Lands in a Tropical Agricultural Landscape.” Ecological Applications 20: 1255-1269.
Cole, R. J., P. Selmants, S. Khan, and R. Chazdon. 2020. “Litter Dynamics Recover Faster than Arthropod Biodiversity during Tropical Forest Succession.” Biotropica 52: 22-33.
Collins, S. L. 1990. “Patterns of Community Structure during Succession in Tallgrass Prairie.” Bulletin of the Torrey Botanical Club 117: 397-408.
Conway, J. H. 1976. On Numbers and Games. London: Academic Press.
Corbin, J. D., and K. D. Holl. 2012. “Applied Nucleation as a Forest Restoration Strategy.” Forest Ecology and Management 265: 37-46.
Crouzeilles, R., M. S. Ferreira, R. L. Chazdon, D. B. Lindenmayer, J. B. B. Sansevoro, L. Monteiro, A. Irribarrem, A. A. Latawiec, and B. B. N. Strassburg. 2017. “Ecological Restoration Success Is Higher for Natural Regeneration than for Active Restoration in Tropical Forests.” Science Advances 3: 1701345.
De la Peña-Domene, M., E. S. Minor, and H. F. Howe. 2016. “Restored Connectivity Facilitates Recruitment by an Endemic Large-Seeded Tree in a Fragmented Tropical Landscape.” Ecology 97: 2511-2517.
Deblauwe, V., N. Barbier, P. Couteron, O. Lejeune, and J. Bogaert. 2008. “The Global Biogeography of Semi-Arid Periodic Vegetation Patterns.” Global Ecology and Biogeography 17: 715-723.
Ellison, A. M., M. S. Bank, B. D. Clinton, E. A. Colburn, K. Elliott, C. R. Ford, D. R. Foster, et al. 2005. “Loss of Foundation Species: Consequences for the Structure and Dynamics of Forested Systems.” Frontiers in Ecology and the Environment 3: 479-486.
Eppinga, M. 2023. “Model_Script_Eppinga_et_al_1708.m.” Figshare. Software. https://doi.org/10.6084/m9.figshare.20509749.v1.
Eppinga, M. B., C. A. Pucko, M. Baudena, B. Beckage, and J. Molofsky. 2013. “A New Method to Infer Vegetation Boundary Movement from ‘Snapshot’ Data.” Ecography 36: 622-635.
Eppinga, M. B., M. Baudena, E. A. Haber, M. Rietkerk, M. J. Wassen, and M. J. Santos. 2021. “Spatially Explicit Removal Strategies Increase the Efficiency of Invasive Plant Species Control.” Ecological Applications 31: e02257.
Eppinga, M. B., M. Rietkerk, M. J. Wassen, and P. C. De Ruiter. 2009. “Linking Habitat Modification to Catastrophic Shifts and Vegetation Patterns in Bogs.” Plant Ecology 200: 53-68.
Eppinga, M. B., M. Rietkerk, S. C. Dekker, P. C. de Ruiter, and W. H. van der Putten. 2006. “Accumulation of Local Pathogens: A New Hypothesis to Explain Exotic Plant Invasion.” Oikos 114: 167-176.
Eppinga, M. B., P. C. de Ruiter, M. J. Wassen, and M. Rietkerk. 2009. “Nutrients and Hydrology Indicate the Driving Mechanisms of Peatland Surface Patterning.” The American Naturalist 173: 803-818.
Eppinga, M. B., W. H. Van der Putten, and J. D. Bever. 2022. “Plant-Soil Feedback as a Driver of Spatial Structure in Ecosystems.” Physics of Life Reviews 40: 6-14.
Eppstein, M. J., J. D. Bever, and J. Molofsky. 2006. “Spatio-Temporal Community Dynamics Induced by Frequency Dependent Interactions.” Ecological Modelling 197: 133-147.
Fink, R. D., C. A. Lindell, E. B. Morrison, R. A. Zahawi, and K. D. Holl. 2009. “Patch Size and Tree Species Influence the Number and Duration of Bird Visits in Forest Restoration Plots in Southern Costa Rica.” Restoration Ecology 17: 479-486.
Fischer, J., M. Riechers, J. Loos, B. Martin-Lopez, and V. M. Temperton. 2020. “Making the UN Decade on Ecosystem Restoration a Social-Ecological Endeavour.” Trends in Ecology & Evolution 36: 20-28.
Frenzel, B. 1983. “Mires-Repositories of Climatic Information or Self-Perpetuating Ecosystems.” In Mires: Swamp, Bog, Fen, and Moor. Ecosystems of the World 4, edited by A. J. P. Gore, 35-67. New York: Elsevier.
Fujita, T. 2016. “Relative Importance of Perch and Facilitative Effects on Nucleation in Tropical Woodland in Malawi.” Acta Oecologica 70: 45-52.
Herrera, J. M., and D. García. 2009. “The Role of Remnant Trees in Seed Dispersal through the Matrix: Being Alone Is Not Always So Sad.” Biological Conservation 142: 149-158.
Holl, K. D. 1998. “Do Bird Perching Structures Elevate Seed Rain and Seedling Establishment in Abandoned Tropical Pasture?” Restoration Ecology 6: 253-261.
Holl, K. D. 2017. “Research Directions in Tropical Forest Restoration.” Annals of the Missouri Botanical Garden 102: 237-250.
Holl, K. D., J. Leighton, J. M. Chaves-Fallas, F. Oviedo-Brenes, and R. A. Zahawi. 2017. “Local Tropical Forest Restoration Strategies Affect Tree Recruitment more Strongly than Does Landscape Forest Cover.” Journal of Applied Ecology 54: 1091-1099.
Holl, K. D., J. L. Reid, R. J. Cole, F. Oviedo-Brenes, J. A. Rosales, and R. A. Zahawi. 2020. “Applied Nucleation Facilitates Tropical Forest Recovery: Lessons Learned from a 15-Year Study.” Journal of Applied Ecology 57: 2316-2328.
Holl, K. D., and R. A. Zahawi. 2014. “Factors Explaining Variability in Woody above-Ground Biomass Accumulation in Restored Tropical Forest.” Forest Ecology and Management 319: 36-43.
Holmgren, M., and M. Scheffer. 2001. “El Niño as a Window of Opportunity for the Restoration of Degraded Arid Ecosystems.” Ecosystems 4: 151-159.
Hu, Z., J. Van Belzen, D. Van Der Wal, T. Balke, Z. B. Wang, M. Stive, and T. J. Bouma. 2015. “Windows of Opportunity for Salt Marsh Vegetation Establishment on Bare Tidal Flats: The Importance of Temporal and Spatial Variability in Hydrodynamic Forcing.” Journal of Geophysical Research: Biogeosciences 120: 1450-1469.
Hulvey, K. B., E. A. Leger, L. M. Porensky, L. M. Roche, K. E. Veblen, A. Fund, J. Shaw, and E. S. Gornish. 2017. “Restoration Islands: A Tool for Efficiently Restoring Dryland Ecosystems?” Restoration Ecology 25: S124-S134.
Hulvey, K. B., and E. S. Zavaleta. 2012. “Abundance Declines of a Native Forb Have Nonlinear Impacts on Grassland Invasion Resistance.” Ecology 93: 378-388.
Inderjit, Callaway, R. M., and E. Meron. 2021. “Belowground Feedbacks as Drivers of Spatial Self-Organization and Community Assembly.” Physics of Life Reviews 38: 1-24.
Jones, C. G., J. H. Lawton, and M. Shachak. 1994. “Organisms as Ecosystem Engineers.” Oikos 69: 373-386.
Koziol, L., and J. D. Bever. 2015. “Mycorrhizal Response Trades off with Plant Growth Rate and Increases with Plant Successional Status.” Ecology 96: 1768-1774.
Koziol, L., and J. D. Bever. 2019. “Mycorrhizal Feedbacks Generate Positive Frequency Dependence Accelerating Grassland Succession.” Journal of Ecology 107: 622-632.
Larsen, L. G., C. Thomas, M. B. Eppinga, and T. Coulthard. 2014. “Exploratory Modelling: Extracting Causality from Complexity.” Eos 95: 285-286.
Larsen, L. G., M. B. Eppinga, P. Passalacqua, W. M. Getz, K. A. Rose, and M. Liang. 2016. “Appropriate Complexity Landscape Modelling.” Earth-Science Reviews 160: 111-130.
Mack, K. M. L., and J. D. Bever. 2014. “Coexistence and Relative Abundance in Plant Communities Are Determined by Feedbacks When the Scale of Feedback and Dispersal Is Local.” Journal of Ecology 102: 1195-1201.
Matzek, V., E. S. Gornish, and K. B. Hulvey. 2017. “Emerging Approach to Successful Ecological Restoration: Five Imperatives to Guide Innovation.” Restoration Ecology 25: S110-S113.
Meli, P., K. D. Holl, J. M. Rey Benayas, H. P. Jones, P. C. Jones, D. Montoya, and D. Moreno Mateos. 2017. “A Global Review of Past Land Use, Climate, and Active vs. Passive Restoration Effects on Forest Recovery.” PLoS One 12: 0171368.
Meron, E. 2016. “Pattern Formation - A Missing Link in the Study of Ecosystem Response to Environmental Changes.” Mathematical Biosciences 271: 1-18.
Michaels, T. K., M. B. Eppinga, C. Angelini, K. D. Holl, and J. D. Bever. 2022. “Can Nucleation Bridge to Desirable Alternative Stable States? Theory and Applications.” Bulletin of the Ecological Society of America 103: e01953.
Michaels, T. K., M. B. Eppinga, and J. D. Bever. 2020. “A Nucleation Framework for Transition between Alternate States: Short-Circuiting Barriers to Ecosystem Recovery.” Ecology 101: e03099.
Molofsky, J., and J. D. Bever. 2002. “A Novel Theory to Explain Species Diversity in Landscapes: Positive Frequency Dependence and Habitat Suitability.” Proceedings of the Royal Society of London B 269: 2389-2393.
Moody, M., and R. N. Mack. 1988. “Controlling the Spread of Plant Invasions: The Importance of Nascent Foci.” Journal of Applied Ecology 25: 1009-1021.
Pausas, J. G., A. Bonet, F. T. Maestre, and A. Climent. 2006. “The Role of the Perch Effect on the Nucleation Process in Mediterranean Semi-Arid Old Fields.” Acta Oecologica 29: 346-352.
Piaia, B. B., A. P. M. Rovedder, D. Procknow, B. Camargo, M. D. Gazzola, J. P. Croda, and M. de Moraes Stefanello. 2020. “Natural Regeneration as an Indicator of Ecological Restoration by Applied Nucleation and Passive Restoration.” Ecological Engineering 157: 105991.
Rietkerk, M., S. C. Dekker, P. C. de Ruiter, and J. van de Koppel. 2004. “Self-Organized Patchiness and Catastrophic Shifts in Ecosystems.” Science 305: 1926-1929.
Rietkerk, M., and J. Van de Koppel. 2008. “Regular Pattern Formation in Real Ecosystems.” Trends in Ecology & Evolution 23: 169-175.
Robroek, B. J. M., J. Limpens, A. Breeuwer, J. van Ruijven, and M. G. C. Schouten. 2007. “Precipitation Determines the Persistence of Hollow Sphagnum Species on Hummocks.” Wetlands 27: 979-986.
Shaw, J. A., L. M. Roche, and E. S. Gornish. 2020. “The Use of Spatially Patterned Methods for Vegetation Restoration and Management across Systems.” Restoration Ecology 28: 766-775.
Simioni, G. F., A. L. Schmitt Filho, F. Joner, J. Farley, A. C. Fantini, and A. P. Moreira. 2022. “Response of Birds to High Biodiversity Silvopastoral Systems: Integrating Food Production and Biodiversity Conservation through Applied Nucleation in Southern Brazil.” Agriculture, Ecosystems & Environment 324: 107709.
Strassburg, B. B., A. Iribarrem, H. L. Beyer, C. L. Cordeiro, R. Crouzeilles, C. C. Jakovac, A. Braga Junqueira, et al. 2020. “Global Priority Areas for Ecosystem Restoration.” Nature 586: 724-729.
Suding, K. N., K. L. Gross, and G. R. Houseman. 2004. “Alternative States and Positive Feedbacks in Restoration Ecology.” Trends in Ecology & Evolution 19: 46-53.
Thiéry, J. M., J.-M. d'Herbès, and C. Valentin. 1995. “A Model Simulating the Genesis of Banded Vegetation Patterns in Niger.” Journal of Ecology 83: 497-507.
Toh, I., M. Gillespie, and D. Lamb. 1999. “The Role of Isolated Trees in Facilitating Tree Seedling Recruitment at a Degraded Sub-Tropical Rainforest Site.” Restoration Ecology 7: 288-297.
Van Belzen, J., J. van de Koppel, M. L. Kirwan, D. van der Wal, P. M. J. Herman, V. Dakos, S. Kéfi, M. Scheffer, G. R. Guntenspergen, and T. J. Bouma. 2017. “Vegetation Recovery in Tidal Marshes Reveals Critical Slowing Down under Increased Inundation.” Nature Communications 8: 15811.
van Belzen, J., G. S. Fivash, Z. Hu, T. J. Bouma, and P. M. J. Herman. 2022. “A Probabilistic Framework for Windows of Opportunity: The Role of Temporal Variability in Critical Transitions.” Journal of the Royal Society Interface 19: 20220041.
Verdu, M., and P. Garcia-Fayos. 1996. “Nucleation Processes in a Mediterranean Bird-Dispersed Plant.” Functional Ecology 10: 275-280.
Vogel, H. F., J. B. Campos, K. S. Sheldon, and F. C. Bechara. 2017. “Comparative Analysis of Birdlife in Different Ecological Restoration Methods with Emphasis on the Role of Artificial Perches.” Revista de Biologia Neotropical 14: 111-134.
von Hardenberg, J., E. Meron, M. Shachak, and Y. Zarmi. 2001. “Diversity of Vegetation Patterns and Desertification.” Physical Review Letters 87: 198101.
Wang, G., L. Koziol, B. L. Foster, and J. D. Bever. 2022. “Microbial Mediators of Plant Community Response to Long-Term N and P Fertilization: Evidence of a Role of Plant Responsiveness to Mycorrhizal Fungi.” Global Change Biology 28: 2721-2735.
Weidlich, E. W., C. R. Nelson, J. L. Maron, R. M. Callaway, B. M. Delory, and V. M. Temperton. 2021. “Priority Effects and Ecological Restoration.” Restoration Ecology 29: e13317.
Wilson, J. B., and A. D. Q. Agnew. 1992. “Positive-Feedback Switches in Plant Communities.” Advances in Ecological Research 23: 263-336.
Zahawi, R. A., K. D. Holl, R. J. Cole, and J. L. Reid. 2013. “Testing Applied Nucleation as a Strategy to Facilitate Tropical Forest Recovery.” Journal of Applied Ecology 50: 88-96.
Zahawi, R. A., and C. K. Augspurger. 2006. “Tropical Forest Restoration: Tree Islands as Recruitment Foci in Degraded Lands of Honduras.” Ecological Applications 16: 464-478.

Auteurs

Maarten B Eppinga (MB)

Department of Geography, University of Zurich, Zurich, Switzerland.

Theo K Michaels (TK)

Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, Kansas, USA.
Kansas Biological Survey, University of Kansas, Lawrence, Kansas, USA.

Maria J Santos (MJ)

Department of Geography, University of Zurich, Zurich, Switzerland.

James D Bever (JD)

Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, Kansas, USA.
Kansas Biological Survey, University of Kansas, Lawrence, Kansas, USA.

Articles similaires

Vancomycin Polyesters Anti-Bacterial Agents Models, Theoretical Drug Liberation
Lakes Salinity Archaea Bacteria Microbiota
Rivers Turkey Biodiversity Environmental Monitoring Animals
1.00
Iran Environmental Monitoring Seasons Ecosystem Forests

Classifications MeSH