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Dynamic Species Distribution Modeling Reveals the Pivotal Role of Human-Mediated Long-Distance Dispersal in Plant Invasion

SIMPLE SUMMARY: Understanding biological invasion mechanisms is crucial to design effective management strategies preventing their impacts on ecosystems. If the role of long-distance dispersal and age-dependent fecundity in plant invasion speed has been characterized in theory, empirical support is...

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Autores principales: Botella, Christophe, Bonnet, Pierre, Hui, Cang, Joly, Alexis, Richardson, David M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9495778/
https://www.ncbi.nlm.nih.gov/pubmed/36138772
http://dx.doi.org/10.3390/biology11091293
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author Botella, Christophe
Bonnet, Pierre
Hui, Cang
Joly, Alexis
Richardson, David M.
author_facet Botella, Christophe
Bonnet, Pierre
Hui, Cang
Joly, Alexis
Richardson, David M.
author_sort Botella, Christophe
collection PubMed
description SIMPLE SUMMARY: Understanding biological invasion mechanisms is crucial to design effective management strategies preventing their impacts on ecosystems. If the role of long-distance dispersal and age-dependent fecundity in plant invasion speed has been characterized in theory, empirical support is still rare given the difficulty to jointly fit demographic and spread parameters of dynamic models to available data. We proposed a statistical model to fit such parameters to heterogeneous observations collected across space and time. We can directly test hypotheses on the importance of various mechanisms in a past invasion. We demonstrated the potential of this method by determining the roles of human-mediated long-distance dispersal and age-dependent fecundity in the invasion of the shrub Plectranthus barbatus in South Africa. Our model revealed a massive wave of spread driven by human-mediated long-distance dispersal and originating from the cities of first introduction. The species completed its invasion of all favorable areas a few years after, in the mid-1990s. Without human-mediated long-distance dispersal, the maximum population would have been obly 30% of the current population. The delayed reproductive maturity explained the invasion lag phase. It highlights the importance of early eradication of weedy horticultural alien plants around urban areas to hamper the invasive spread. ABSTRACT: Plant invasions generate massive ecological and economic costs worldwide. Predicting their spatial dynamics is crucial to the design of effective management strategies and the prevention of invasions. Earlier studies highlighted the crucial role of long-distance dispersal in explaining the speed of many invasions. In addition, invasion speed depends highly on the duration of its lag phase, which may depend on the scaling of fecundity with age, especially for woody plants, even though empirical proof is still rare. Bayesian dynamic species distribution models enable the fitting of process-based models to partial and heterogeneous observations using a state-space modeling approach, thus offering a tool to test such hypotheses on past invasions over large spatial scales. We use such a model to explore the roles of long-distance dispersal and age-structured fecundity in the transient invasion dynamics of Plectranthus barbatus, a woody plant invader in South Africa. Our lattice-based model accounts for both short and human-mediated long-distance dispersal, as well as age-structured fecundity. We fitted our model on opportunistic occurrences, accounting for the spatio-temporal variations of the sampling effort and the variable detection rates across datasets. The Bayesian framework enables us to integrate a priori knowledge on demographic parameters and control identifiability issues. The model revealed a massive wave of spatial spread driven by human-mediated long-distance dispersal during the first decade and a subsequent drastic population growth, leading to a global equilibrium in the mid-1990s. Without long-distance dispersal, the maximum population would have been equivalent to 30% of the current equilibrium population. We further identified the reproductive maturity at three years old, which contributed to the lag phase before the final wave of population growth. Our results highlighted the importance of the early eradication of weedy horticultural alien plants around urban areas to hamper and delay the invasive spread.
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spelling pubmed-94957782022-09-23 Dynamic Species Distribution Modeling Reveals the Pivotal Role of Human-Mediated Long-Distance Dispersal in Plant Invasion Botella, Christophe Bonnet, Pierre Hui, Cang Joly, Alexis Richardson, David M. Biology (Basel) Article SIMPLE SUMMARY: Understanding biological invasion mechanisms is crucial to design effective management strategies preventing their impacts on ecosystems. If the role of long-distance dispersal and age-dependent fecundity in plant invasion speed has been characterized in theory, empirical support is still rare given the difficulty to jointly fit demographic and spread parameters of dynamic models to available data. We proposed a statistical model to fit such parameters to heterogeneous observations collected across space and time. We can directly test hypotheses on the importance of various mechanisms in a past invasion. We demonstrated the potential of this method by determining the roles of human-mediated long-distance dispersal and age-dependent fecundity in the invasion of the shrub Plectranthus barbatus in South Africa. Our model revealed a massive wave of spread driven by human-mediated long-distance dispersal and originating from the cities of first introduction. The species completed its invasion of all favorable areas a few years after, in the mid-1990s. Without human-mediated long-distance dispersal, the maximum population would have been obly 30% of the current population. The delayed reproductive maturity explained the invasion lag phase. It highlights the importance of early eradication of weedy horticultural alien plants around urban areas to hamper the invasive spread. ABSTRACT: Plant invasions generate massive ecological and economic costs worldwide. Predicting their spatial dynamics is crucial to the design of effective management strategies and the prevention of invasions. Earlier studies highlighted the crucial role of long-distance dispersal in explaining the speed of many invasions. In addition, invasion speed depends highly on the duration of its lag phase, which may depend on the scaling of fecundity with age, especially for woody plants, even though empirical proof is still rare. Bayesian dynamic species distribution models enable the fitting of process-based models to partial and heterogeneous observations using a state-space modeling approach, thus offering a tool to test such hypotheses on past invasions over large spatial scales. We use such a model to explore the roles of long-distance dispersal and age-structured fecundity in the transient invasion dynamics of Plectranthus barbatus, a woody plant invader in South Africa. Our lattice-based model accounts for both short and human-mediated long-distance dispersal, as well as age-structured fecundity. We fitted our model on opportunistic occurrences, accounting for the spatio-temporal variations of the sampling effort and the variable detection rates across datasets. The Bayesian framework enables us to integrate a priori knowledge on demographic parameters and control identifiability issues. The model revealed a massive wave of spatial spread driven by human-mediated long-distance dispersal during the first decade and a subsequent drastic population growth, leading to a global equilibrium in the mid-1990s. Without long-distance dispersal, the maximum population would have been equivalent to 30% of the current equilibrium population. We further identified the reproductive maturity at three years old, which contributed to the lag phase before the final wave of population growth. Our results highlighted the importance of the early eradication of weedy horticultural alien plants around urban areas to hamper and delay the invasive spread. MDPI 2022-08-30 /pmc/articles/PMC9495778/ /pubmed/36138772 http://dx.doi.org/10.3390/biology11091293 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Botella, Christophe
Bonnet, Pierre
Hui, Cang
Joly, Alexis
Richardson, David M.
Dynamic Species Distribution Modeling Reveals the Pivotal Role of Human-Mediated Long-Distance Dispersal in Plant Invasion
title Dynamic Species Distribution Modeling Reveals the Pivotal Role of Human-Mediated Long-Distance Dispersal in Plant Invasion
title_full Dynamic Species Distribution Modeling Reveals the Pivotal Role of Human-Mediated Long-Distance Dispersal in Plant Invasion
title_fullStr Dynamic Species Distribution Modeling Reveals the Pivotal Role of Human-Mediated Long-Distance Dispersal in Plant Invasion
title_full_unstemmed Dynamic Species Distribution Modeling Reveals the Pivotal Role of Human-Mediated Long-Distance Dispersal in Plant Invasion
title_short Dynamic Species Distribution Modeling Reveals the Pivotal Role of Human-Mediated Long-Distance Dispersal in Plant Invasion
title_sort dynamic species distribution modeling reveals the pivotal role of human-mediated long-distance dispersal in plant invasion
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9495778/
https://www.ncbi.nlm.nih.gov/pubmed/36138772
http://dx.doi.org/10.3390/biology11091293
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