Predicting the spread of marine species introduced by global shipping

Significance Predicting the arrival of alien species remains a big challenge, which is assumed to be a consequence of the complexity of the invasion process. Here, we demonstrate that spreading of alien marine species can be predicted by a simple model using only global shipping intensities, environmental variables, and species occurrence data. We provide species lists of the next potentially invading species in a local habitat or species causing harmful algal blooms with their associated probability of invasion. This will help to improve mitigation strategies to reduce the further introduction of alien species. Although this study focuses on marine algae, the model approach can be easily adopted to other taxonomic groups and their respective drivers of invasion. The human-mediated translocation of species poses a distinct threat to nature, human health, and economy. Although existing models calculate the invasion probability of any species, frameworks for species-specific forecasts are still missing. Here, we developed a model approach using global ship movements and environmental conditions to simulate the successive global spread of marine alien species that allows predicting the identity of those species likely to arrive next in a given habitat. In a first step, we simulated the historical stepping-stone spreading dynamics of 40 marine alien species and compared predicted and observed alien species ranges. With an accuracy of 77%, the model correctly predicted the presence/absence of an alien species in an ecoregion. Spreading dynamics followed a common pattern with an initial invasion of most suitable habitats worldwide and a subsequent spread into neighboring habitats. In a second step, we used the reported distribution of 97 marine algal species with a known invasion history, and six species causing harmful algal blooms, to determine the ecoregions most likely to be invaded next under climate warming. Cluster analysis revealed that species can be classified according to three characteristic spreading profiles: emerging species, high-risk species, and widespread species. For the North Sea, the model predictions could be confirmed because two of the predicted high-risk species have recently invaded the North Sea. This study highlights that even simple models considering only shipping intensities and habitat matches are able to correctly predict the identity of the next invading marine species.

[1]  Dalia Rosenfeld Invasions , 2016 .

[2]  H. Seebens,et al.  Global trade will accelerate plant invasions in emerging economies under climate change , 2015, Global change biology.

[3]  Michael T. Gastner,et al.  The risk of marine bioinvasion caused by global shipping. , 2013, Ecology letters.

[4]  Yuehua Wu,et al.  An inventory of invasive alien species in China , 2012 .

[5]  D. Yemshanov,et al.  Modelling the Arrival of Invasive Organisms via the International Marine Shipping Network: A Khapra Beetle Study , 2012, PloS one.

[6]  Jan Pergl,et al.  A global assessment of invasive plant impacts on resident species, communities and ecosystems: the interaction of impact measures, invading species' traits and environment , 2012, Global Change Biology.

[7]  D. Lodge,et al.  Linking environmental conditions and ship movements to estimate invasive species transport across the global shipping network , 2011 .

[8]  Petr Pyšek,et al.  Invasive Species, Environmental Change and Management, and Health , 2010 .

[9]  Shan-Huah Wu,et al.  Insights of the Latest Naturalized Flora of Taiwan: Change in the Past Eight Years , 2010 .

[10]  J. Lamarque,et al.  Global Biodiversity: Indicators of Recent Declines , 2010, Science.

[11]  Wilfried Thuiller,et al.  Predicting potential distributions of invasive species: where to go from here? , 2010 .

[12]  S. Butchart,et al.  Global indicators of biological invasion: species numbers, biodiversity impact and policy responses , 2010 .

[13]  Jennifer L. Molnar,et al.  Assessing the global threat of invasive species to marine biodiversity , 2008 .

[14]  Jean-Pascal van Ypersele de Strihou,et al.  Towards New Scenarios for Analysis of Emissions, Climate Change, Impacts, and Response Strategies , 2008 .

[15]  Wolfgang Nentwig,et al.  Grasping at the routes of biological invasions: a framework for integrating pathways into policy , 2008 .

[16]  Dazhi Wang,et al.  Neurotoxins from Marine Dinoflagellates: A Brief Review , 2008, Marine drugs.

[17]  Susan L. Williams,et al.  A Global Review of the Distribution, Taxonomy, and Impacts of Introduced Seaweeds , 2007 .

[18]  Susan L. Williams Introduced species in seagrass ecosystems: Status and concerns , 2007 .

[19]  Jennifer L. Molnar,et al.  Marine Ecoregions of the World: A Bioregionalization of Coastal and Shelf Areas , 2007 .

[20]  Christopher L Jerde,et al.  Waiting for Invasions: A Framework for the Arrival of Nonindigenous Species , 2007, The American Naturalist.

[21]  L. Herborg,et al.  Predicting invasion risk using measures of introduction effort and environmental niche models. , 2007, Ecological applications : a publication of the Ecological Society of America.

[22]  A. Kerswell Global biodiversity patterns of benthic marine algae. , 2006, Ecology.

[23]  M. Çınar,et al.  Alien species on the coasts of Turkey , 2005 .

[24]  D. Post,et al.  Studying invasion: have we missed the boat? , 2005 .

[25]  M. Hoppenrath A revised checklist of planktonic diatoms and dinoflagellates from Helgoland (North Sea, German Bight) , 2004, Helgoland Marine Research.

[26]  D. Lodge,et al.  Global hot spots of biological invasions: evaluating options for ballast–water management , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[27]  Jonathan M. Levine,et al.  Forecasting Biological Invasions with Increasing International Trade , 2003 .

[28]  C. Kolar,et al.  Ecological Predictions and Risk Assessment for Alien Fishes in North America , 2002, Science.

[29]  Van Dolah Fm Marine algal toxins: origins, health effects, and their increased occurrence. , 2000, Environmental health perspectives.

[30]  MacIsaac,et al.  Recent mass invasion of the North American Great Lakes by Ponto-Caspian species. , 2000, Trends in ecology & evolution.

[31]  J. Carlton,et al.  Historical and recent introductions of non-indigenous marine species into Pearl Harbor, Oahu, Hawaiian Islands , 1999 .

[32]  C. Maggs,et al.  Red algal exotics on North Sea coasts , 1998, Helgoländer Meeresuntersuchungen.

[33]  G. Hallegraeff A review of harmful algal blooms and their apparent global increase , 1993 .

[34]  R. Levins Some Demographic and Genetic Consequences of Environmental Heterogeneity for Biological Control , 1969 .

[35]  J. H. Ward Hierarchical Grouping to Optimize an Objective Function , 1963 .

[36]  Jan Freiwald,et al.  Range expansion of a non-native, invasive macroalga Sargassum horneri (Turner) C. Agardh, 1820 in the eastern Pacific. , 2015 .

[37]  J. Aronson,et al.  Impacts of biological invasions: what's what and the way forward. , 2013, Trends in ecology & evolution.

[38]  K. Walker,et al.  Non-Native Species in Great Britain: establishment, detection and reporting to inform effective decision making , 2012 .

[39]  B. Leung,et al.  Is invasion history a useful tool for predicting the impacts of the world's worst aquatic invasive species? , 2011, Ecological applications : a publication of the Ecological Society of America.

[40]  Daisie,et al.  Handbook of alien species in Europe , 2009 .

[41]  Inger Wallentinus,et al.  Introduced marine organisms as habitat modifiers. , 2007, Marine pollution bulletin.

[42]  F. V. Van Dolah,et al.  Marine Algal Toxins : Origins , Health Effects , and Their Increased Occurrence , 2006 .

[43]  Naeem,et al.  Ecosystems and Human Well-Being: Biodiversity Synthesis , 2005 .

[44]  Michael J. Keough,et al.  Introduced and cryptogenic species in Port Phillip Bay, Victoria, Australia , 2004 .

[45]  J. Bolton Global Seaweed Diversity: Patterns and Anomalies , 1994 .