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Remoteness Promotes Biological Invasions on Islands Worldwide

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Remoteness Promotes Biological Invasions on Islands Worldwide Remoteness promotes biological invasions on islands worldwide Dietmar Mosera,1, Bernd Lenznera,1,2, Patrick Weigeltb, Wayne Dawsonc, Holger Kreftb, Jan Pergld, Petr Pyšekd,e,f, Mark van Kleuneng,h, Marten Winteri, César Capinhaj,k, Phillip Casseyl, Stefan Dullingera, Evan P. Economom, Pablo García-Díazl,n, Benoit Guénardm,o, Florian Hofhansla,p, Thomas Manga, Hanno Seebensq, and Franz Essla aDivision of Conservation Biology, Vegetation and Landscape Ecology, University of Vienna, 1030 Vienna, Austria; bBiodiversity, Macroecology and Biogeography, University of Goettingen, 37077 Goettingen, Germany; cDepartment of Biosciences, Durham University, DH1 3LE Durham, United Kingdom; dInstitute of Botany, Department of Invasion Ecology, The Czech Academy of Sciences, CZ-252 43 Pruhonice, Czech Republic; eDepartment of Ecology, Faculty of Science, Charles University, CZ-128 44 Prague, Czech Republic; fCentre for Invasion Biology, Department of Botany & Zoology, Stellenbosch University, 7602 Matieland, South Africa; gEcology, University of Konstanz, 78457 Konstanz, Germany; hZhejiang Provincial Key Laboratory of Plant Evolutionary Ecology and Conservation, Taizhou University, 318000 Taizhou, China; iGerman Centre for Integrative Biodiversity Research, Halle-Jena-Leipzig, 04103 Leipzig, Germany; jCentro de Investigação em Biodiversidade e Recursos Genéticos (CIBIO/InBIO), Universidade do Porto, 4485-661 Vairão, Portugal; kZoologisches Forschungsmuseum Alexander Koenig, Museumsmeile Bonn, 53113 Bonn, Germany; lSchool of Biological Sciences and Centre for Conservation Science and Technology, The University of Adelaide, North Terrace Adelaide, SA 5005, Australia; mOkinawa Institute of Science and Technology Graduate University, Onna, 904-0495 Okinawa, Japan; nManaaki Whenua–Landcare Research, 7640 Lincoln, New Zealand; oSchool of Biological Sciences, The University of Hong Kong, Pok Fu Lam, Hong Kong SAR, China; pEcosystem Services and Management Program, International Institute of Applied Systems Analysis, 2361 Laxenburg, Austria; and qSenckenberg Biodiversity and Climate Research Centre, 60325 Frankfurt am Main, Germany Edited by Daniel S. Simberloff, The University of Tennessee, Knoxville, TN, and approved August 2, 2018 (received for review March 9, 2018) One of the best-known general patterns in island biogeography is should be highest on the most remote islands because their the species–isolation relationship (SIR), a decrease in the number impoverished and evolutionarily naive biota provide greater eco- of native species with increasing island isolation that is linked to logical opportunities for introduced species to establish (12–14). lower rates of natural dispersal and colonization on remote oce- Further, alien species establishment might lead to the extinction of anic islands. However, during recent centuries, the anthropogenic native species through enhanced competition or predation, thereby introduction of alien species has increasingly gained importance increasing the establishment odds for additional aliens. These hy- and altered the composition and richness of island species pools. potheses would predict alien species richness on islands to be We analyzed a large dataset for alien and native plants, ants, positively correlated, negatively correlated, or uncorrelated with reptiles, mammals, and birds on 257 (sub) tropical islands, and isolation, depending on the balance between colonization pressure showed that, except for birds, the number of naturalized alien and establishment probabilities. Empirical studies have so far pro- species increases with isolation for all taxa, a pattern that is op- vided ambiguous results, with no correlations[forplants(15,16) posite to the negative SIR of native species. We argue that the and birds (16)] or positive correlations [for birds (17), plants (18), reversal of the SIR for alien species is driven by an increase in and ants (19)] between alien species richness and island isolation. island invasibility due to reduced diversity and increased ecologi- cal naiveté of native biota on the more remote islands. Since these studies vary in methods, predictor variables, and spatial and taxonomic extent, we are so far unable to draw general con- island biogeography | alien species | isolation | island invasibility | clusions regarding the SIR for alien versus native species. naturalization Significance slands harbor a disproportionately high number of evolution- Iarily unique, geographically restricted species, and thus con- Islands are hotspots of alien species invasions, and their dis- tribute significantly to global biodiversity (1). Native species tinct biodiversity is particularly vulnerable to invading species. richness on islands, which arose through colonization events and While isolation has shaped natural colonization of islands for evolution over geological time scales, follows positive species– millions of years, globalization in trade and transport has led to area relationships and negative species–isolation relationships a breakdown of biogeographical barriers and subsequent col- (SIRs), as predicted by the theory of island biogeography (2–5). onization of islands by alien species. Using a large dataset of While the negative SIR for native species is a well-documented 257 subtropical and tropical islands, we show that alien richness pattern in ecology (2, 6, 7), it is less clear whether or how the increases with increasing isolation of islands. This pattern is number of alien species on islands is related to isolation. consistent for plants, ants, mammals, and reptiles, and it cannot On the one hand, globalization in trade and transport has con- simply be explained by island economics and trade alone. Geo- siderably reduced the effective isolation of islands worldwide and graphical isolation does not protect islands from alien species, has led to a breakdown of biogeographical barriers (8). While and island species richness may reach a new dynamic equilibrium natural dispersal to remote islands is extremely rare and has had a at some point, likely at the expense of many endemic species. strong influence on island native species richness and composition, Author contributions: D.M. and B.L. designed research; D.M. and B.L. performed research; human-aided transport increases the frequency of introduction P.W., W.D., H.K., J.P., P.P., M.v.K., M.W., C.C., P.C., S.D., E.P.E., P.G.-D., B.G., H.S., and F.E. events by orders of magnitude; as a result, SIR patterns may de- contributed data for the different taxonomic groups; D.M., B.L., F.H., and T.M. analyzed crease or even vanish (2, 9). Alternately, economic theory predicts data; and D.M., B.L., P.W., W.D., H.K., J.P., P.P., M.v.K., M.W., C.C., P.C., S.D., E.P.E., P.G.-D., that insularity (characterized by smallness and remoteness) has a B.G., F.H., T.M., H.S., and F.E. wrote the paper. strong effect on the socioeconomic structure of an island (10). The authors declare no conflict of interest. Small markets, dependence on sea and air transport, and exclusion This article is a PNAS Direct Submission. from major transport routes, together with higher costs generally, Published under the PNAS license. mean that fewer commodities are transported to more remote is- 1D.M. and B.L. contributed equally to this work. lands (10). Hence, fewer intentional and accidental alien intro- 2To whom correspondence should be addressed. Email: [email protected]. ductions (i.e., lower propagule and colonization pressures), and This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. thus lower colonization rates, might be expected for more remote 1073/pnas.1804179115/-/DCSupplemental. islands (11). Still, another line of reasoning suggests that invasibility Published online August 29, 2018. 9270–9275 | PNAS | September 11, 2018 | vol. 115 | no. 37 www.pnas.org/cgi/doi/10.1073/pnas.1804179115 Downloaded by guest on September 30, 2021 Here, we compiled the most comprehensive datasets of nat- weaker when assessed with combined native and alien richness uralized alien (i.e., those species established outside their native (Figs. 2 and 3 and SI Appendix, Table S1). range and forming self-sustainable populations [sensu Blackburn Effects of the other predictor variables on species richness et al. (20)]) and native species numbers currently available for were as expected: The numbers of both native and naturalized vascular plants, ants, reptiles, mammals, and birds on subtropical alien species increased with island area (Fig. 3 and SI Appendix, and tropical islands (between 30°N and 30°S latitudes) (Fig. 1, Table S1). Socioeconomic development (measured as per capita number of islands: vascular plants = 108, ants = 89, mammals = GDP) did not affect native species richness, but it had a signif- 125, reptiles = 75, and birds = 87; SI Appendix, Table S9) and icant positive effect on alien species richness of all taxonomic assessed the SIR. We restricted the data to subtropical and groups (Fig. 3 and SI Appendix, Table S1A). For plants and tropical islands to reduce the confounding effects of differences mammals, the effect of per capita GDP was still significant when in climatic conditions between islands. Further, remoteness of considering alien and native richness together. Due to the focus islands exhibits a strong latitudinal gradient as the spherical on (sub) tropical islands, climate effects were minor; only the shape of Earth and the distribution of continental land masses richness of native reptile species and alien
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