Unwelcome exchange: International trade as a direct and indirect driver of biological invasions worldwide

Abstract

Biological invasions are synonymous with international trade. The direct effects of trade have largely been quantified using relationships between imports and the number of alien species in a region or patterns in the global spread of species linked to shipping and air traffic networks. But trade also has an indirect role on biological invasions by transforming the environments and societies of exporting and importing nations. Here, both the direct and indirect roles of trade on biological invasions, as well as their interaction, are examined for the first time. Future trends in international trade, including e-commerce, new trade routes, and major infrastructure developments, will lead to the pressure on national borders soon outstripping the resources available for intervention. The current legislative and scientific tools targeting biological invasions are insufficient to deal with this growing threat and require a new mindset that focuses on curbing the pandemic risk posed by alien species. Biological invasions are synonymous with international trade. The direct effects of trade have largely been quantified using relationships between imports and the number of alien species in a region or patterns in the global spread of species linked to shipping and air traffic networks. But trade also has an indirect role on biological invasions by transforming the environments and societies of exporting and importing nations. Here, both the direct and indirect roles of trade on biological invasions, as well as their interaction, are examined for the first time. Future trends in international trade, including e-commerce, new trade routes, and major infrastructure developments, will lead to the pressure on national borders soon outstripping the resources available for intervention. The current legislative and scientific tools targeting biological invasions are insufficient to deal with this growing threat and require a new mindset that focuses on curbing the pandemic risk posed by alien species. Alien species are defined as those taxa whose presence in a region is attributable to human transport, whether deliberate or accidental, that has enabled them to overcome fundamental biogeographical barriers to their geographic distribution.1Richardson D.M. Pyšek P. Carlton J.T. A compendium of essential concepts and terminology in invasion ecology.in: Richardson D.M. Fifty Years of Invasion Ecology: The Legacy of Charles Elton. Wiley, 2011: 409-420Google Scholar,2Essl F. Bacher S. Genovesi P. Hulme P.E. Jeschke J.M. Katsanevakis S. Kowarik I. Kühn I. 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Ecol. 2015; 52: 1418-1424Google Scholar Yet, despite the importance of human travel and migration to the introduction and establishment of alien species in new regions, international trade is widely regarded as the primary driver of biological invasions in both terrestrial and aquatic ecosystems.5Essl F. Bacher S. Blackburn T.M. Booy O. Brundu G. Brunel S. Cardoso A.C. Eschen R. Gallardo B. Galil B. et al.Crossing frontiers in tackling pathways of biological invasions.Bioscience. 2015; 65: 769-782Google Scholar, 6Hulme P.E. Trade, transport and trouble: managing invasive species pathways in an era of globalization.J. Appl. Ecol. 2009; 46: 10-18Google Scholar, 7Jenkins P.T. Free trade and exotic species introductions.Conserv. Biol. 1996; 10: 300-302Google Scholar, 8Perrings C. Dehnen-Schmutz K. Touza J. Williamson M. How to manage biological invasions under globalization.Trends Ecol. Evol. 2005; 20: 212-215Google Scholar International trade occurs as a result of geographical specialization, whether in terms of the availability of natural resources (e.g., Brazil nuts, minerals, marine fisheries) or in the production of goods (e.g., kiwi fruit, iPads, vaccines), and consequently buyers and sellers reside in different countries. In some cases, the commodity traded may itself be an alien species (e.g., ornamental fish or plants) but often alien species are introduced unintentionally as a contaminant of traded commodities (e.g., weed seeds in grain, parasites in livestock) or as a stowaway on transport vessels or other means of conveyance (e.g., hull fouling biota on ships, soil on the exterior of cargo containers).9Saul W.C. Roy H.E. Booy O. Carnevali L. Chen H.J. Genovesi P. Harrower C.A. Hulme P.E. Pagad S. Pergl J. et al.Assessing patterns in introduction pathways of alien species by linking major invasion data bases.J. Appl. Ecol. 2017; 54: 657-669Google Scholar Given the robust evidence that many invasive alien species have major negative impacts on human health, food security, ecosystem services, and biodiversity, understanding the role international trade plays in biological invasions is crucial to secure sustainable economic outcomes.10Pyšek P. Hulme P.E. Simberloff D. Bacher S. Blackburn T.M. Carlton J.T. Dawson W. Essl F. Foxcroft L.C. Genovesi P. et al.Scientists' warning on invasive alien species.Biol. Rev. 2020; 95: 1511-1534Google Scholar Although international trade has been a feature of human society for thousands of years,11Parker P. History of World Trade in Maps. HarperCollins Publishers Limited, 2021Google Scholar since the beginning of the 19th century the share of the world Gross Domestic Product (GDP) accounted for by merchandise imports has more than tripled (Figure 1). The growth in volumes handled by international transportation, particularly by container shipping, has been especially marked since the 1990s due to the surge in global exports in the wake of rapid industrialization in developing economies and the massive offshoring of manufacturing, particularly in China.12Rodrigue J.P. The Geography of Transport Systems. Routledge, 2020Google Scholar The number of new occurrences of alien species recorded each year worldwide has outpaced the growth of international trade, increasing almost 20-fold since the start of the 19th century (Figure 1). The positive association between the first records of alien species and the percentage contribution international imports make to GDP is clearly evident, but is much stronger in recent decades (for 1950 to 2000, Pearson correlation r = 0.92, df 49, p < 0.00001) than before 1950 (for 1827 to 1949, Pearson correlation r = 0.31, df 121, p < 0.00053). Bilateral trade has grown dramatically since the 1950s with the numbers of reported countries and trading partners increasing over time from 76 countries and 5,700 country–country bilateral trade pairs in 1948 to 186 countries and 34,410 pairs in 2000.13Seebens H. Essl F. Dawson W. Fuentes N. Moser D. Pergl J. Pyšek P. van Kleunen M. Weber E. Winter M. et al.Global trade will accelerate plant invasions in emerging economies under climate change.Glob. Change Biol. 2015; 21: 4128-4140Google Scholar Governments engaged in international trade have a long history of implementing controls on the import and export of merchandise commodities, and national legislation has become increasingly shaped by international trade rules.14Poon J.P.H. Rigby D.L. International Trade: The Basics. Taylor & Francis Group, 2017Google Scholar This trend is clearly illustrated in the growth of regional trade agreements that have come into force since 1950 and encourage the free movement of goods across the borders of signatories (Figure 2). A significant factor in the development of national and international regulations has been the need to reduce the risk of introducing alien pests and diseases of agricultural significance through trade.15Hulme P.E. An introduction to plant biosecurity: past, present and future.in: Gordh G. McKirdy S. The Handbook of Plant Biosecurity. Springer, 2014: 1-25Google Scholar It would be expected that with the growth in international trade so the likelihood of alien species being introduced as commodities, contaminants, or stowaways will also increase. Not surprisingly, trends in international trade have often been used as the basis for projecting future risks of invasive alien species.13Seebens H. Essl F. Dawson W. Fuentes N. Moser D. Pergl J. Pyšek P. van Kleunen M. Weber E. Winter M. et al.Global trade will accelerate plant invasions in emerging economies under climate change.Glob. Change Biol. 2015; 21: 4128-4140Google Scholar,16Bradley B.A. Blumenthal D.M. Early R. Grosholz E.D. Lawler J.J. Miller L.P. Sorte C.J. D'Antonio C.M. Diez J.M. Dukes J.S. et al.Global change, global trade, and the next wave of plant invasions.Front. Ecol. Environ. 2012; 10: 20-28Google Scholar, 17Liebhold A.M. Brockerhoff E.G. Kimberley M. Depletion of heterogeneous source species pools predicts future invasion rates.J. Appl. Ecol. 2017; 54: 1968-1977Google Scholar, 18Levine J.M. D'Antonio C.M. Forecasting biological invasions with increasing international trade.Conserv. Biol. 2003; 17: 322-326Google ScholarFigure 2Cumulative number of regional trade agreements in force since 1950Show full captionThe growth of bilateral and multilateral trade as depicted by the cumulative number of regional trade agreements in relation to the year in which the agreement came into force (http://rtais.wto.org/).View Large Image Figure ViewerDownload Hi-res image Download (PPT) The growth of bilateral and multilateral trade as depicted by the cumulative number of regional trade agreements in relation to the year in which the agreement came into force (http://rtais.wto.org/). However, to date the interpretation of international trade as a driver of biological invasions has often been too simplistic. It is essential to consider the multidimensional nature of trade that not only includes the direct effects of changes in the trade network and volume of commodities transported but also the indirect effects through other social and physical drivers that may be equally, if not more, important. Both this complexity as well as significant emerging issues are explored in this review by examining the evidence of international trade as not only a direct driver, especially as a result of technological change that has accelerated rates of biological invasions, but also as an indirect driver stemming from the role international trade is playing in resource extraction, pollution, urbanization, and climate change that in themselves also facilitate invasions. The marked interactions between the direct and indirect roles of international trade on biological invasions are examined and shown to be highly dynamic such that past trends are not necessarily a sound basis to predict future prospects. One clear message is that more effective regulation of international trade is urgently needed to limit the risks of future biological invasions. Despite invasive alien species being viewed as one of the most important contemporary drivers of biodiversity change worldwide,10Pyšek P. Hulme P.E. Simberloff D. Bacher S. Blackburn T.M. Carlton J.T. Dawson W. Essl F. Foxcroft L.C. Genovesi P. et al.Scientists' warning on invasive alien species.Biol. Rev. 2020; 95: 1511-1534Google Scholar humans have moved species through trade across biogeographical barriers for millennia. For example, a substantial influx of alien plant species to the UK occurred in the Late Bronze Age (1000–700 BC), possibly reflecting changes in agriculture and the increasing trade and transport at that time.21Preston C.D. Pearman D.A. Hall A.R. Archaeophytes in Britain.Bot. J. Linn. Soc. 2004; 145: 257-294Google Scholar Yet the role played in the spread of alien species by the extensive trade networks that criss-crossed Mesopotamia in the Early Bronze Age (3000 BC) and linked Europe, North Africa, the Middle East, and South Asia22Parker P. The Great Trade Routes: A History of Cargoes and Commerce over Land and Sea. Naval Institute Press, 2012Google Scholar can only be conjectured. Undoubtedly, the movement of people, crops, and livestock prior to detailed floristic and faunistic records has blurred the distinction between the native and introduced ranges of many species. Although there is clear evidence that ancient introductions have been severely underestimated, there is no arguing with the evidence that the past two centuries have witnessed a dramatic increase in the number of alien species recorded worldwide.20Seebens H. Blackburn T.M. Dyer E.E. Genovesi P. Hulme P.E. Jeschke J.M. Pagad S. Pyšek P. Winter M. Arianoutsou M. et al.No saturation in the accumulation of alien species worldwide.Nat. Commun. 2017; 8: 14435Google Scholar International trade has been identified as one of the primary reasons for this increasing trend since the acceleration of global commerce coincides with the escalation in alien species numbers.23Seebens H. Blackburn T.M. Dyer E.E. Genovesi P. Hulme P.E. Jeschke J.M. Pagad S. Pyšek P. van Kleunen M. Winter M. et al.Global rise in emerging alien species results from increased accessibility of new source pools.Proc. Natl. Acad. Sci. U S A. 2018; 115: E2264-E2273Google Scholar Reviews of the history of trade have shown that the dramatic gear shift in international trade since the 1800s was the product of technological change, infrastructure improvements, and a less protectionist global economy.14Poon J.P.H. Rigby D.L. International Trade: The Basics. Taylor & Francis Group, 2017Google Scholar,24O'Rourke K.H. Williamson J.G. Globalization and History: The Evolution of a Nineteenth-Century Atlantic Economy. MIT Press, 2001Google Scholar However, how these major technological and infrastructural developments have accelerated the opportunities for introducing alien species around the world has not been elaborated in detail. In this section, seven major technological developments that accelerated trade are shown to also be major drivers of alien species invasions: the increased speed of transport by sea, new trade routes, changes to ballast, the use of refrigeration, containerization, air transport, and the development of global communication technologies. The introduction of the ocean-going steamship in the 1840s sharply reduced transport costs and ocean freight rates fell 70% between 1840 and 1910 because of technological change and improved navigation techniques.25Levinson M. The Box: How the Shipping Container Made the World Smaller and the World Economy Bigger. Princeton University Press, 2008Google Scholar Ship size increased from the largest tonnage of 3,800 gross registered tons (revenue-making cargo space) in 1871 to 47,000 tons in 1914.12Rodrigue J.P. The Geography of Transport Systems. Routledge, 2020Google Scholar Steamships took approximately half the time to cross the Atlantic as vessels that relied solely on sails and this meant that alien species were more likely to survive the journey and avoid detection. The introduction of the potato late blight fungus (Phytophthora infestans) from Mexico to Ireland in 1845 likely occurred because the shorter journey time on steamships meant that disease symptoms were less evident on the imported tubers and thus they were imported into the country, whereas previously the longer incubation times under sail would have resulted in infected consignments having rotted on board and thus being rejected.26Shah S. Pandemic: Tracking Contagions, from Cholera to Ebola and beyond. Farrar, Straus and Giroux, 2016Google Scholar Today, the shorter travel times that link-up the world mean that surviving transport is much less of a barrier to the introduction of alien species than it was in the past. Sailing ships still dominated the longer journey to Asia but this changed when the Suez Canal opened in 1869, halving the distance between London and Bombay and allowing steamships to carry more cargo and less fuel, effectively ending the commercial reign of sail.24O'Rourke K.H. Williamson J.G. Globalization and History: The Evolution of a Nineteenth-Century Atlantic Economy. MIT Press, 2001Google Scholar Unfortunately, several hundred marine species in the western Indian Ocean and Red Sea have been subsequently able to traverse the Suez Canal and establish alien populations in the Mediterranean Sea with considerable negative consequences for native species.27Galil B.S. Mienis H.K. Hoffman R. Goren M. Non-indigenous species along the Israeli Mediterranean coast: tally, policy, outlook.Hydrobiologia. 2020; 19: 1-9Google Scholar In contrast, while the opening of the Panama Canal in 1914 also substantially decreased steamship journey times between the Atlantic and Pacific Oceans, it resulted in a much less dramatic redistribution of species.28Ros M. Ashton G.V. Lacerda M.B. Carlton J.T. Vázquez-Luis M. Guerra-García J.M. Ruiz G.M. The Panama canal and the transoceanic dispersal of marine invertebrates: Evaluation of the introduced amphipod Paracaprella pusilla Mayer, 1890 in the Pacific Ocean.Mar. Environ. Res. 2014; 99: 204-211Google Scholar Both canals represent significant bottlenecks to international trade; however, recently engineered expansions of both the Suez (2015) and Panama (2016) Canals to increase the flow of shipping have accelerated the introduction of alien marine fishes and other organisms between their adjacent waters.29Castellanos-Galindo G.A. Robertson D.R. Torchin M.E. A new wave of marine fish invasions through the Panama and Suez canals.Nat. Ecol. Evol. 2020; 4: 1444-1446Google Scholar The end of sail and the transition of maritime cargo transport to steel hulled steamships with watertight bulkheads not only led to faster travel by larger vessels and thus increased rates of global trade, but concomitantly introduced an effective means of alien species introductions through ballast water. Solid ballast (e.g., soil, rocks, gravel) had long been used to increase the stability of ocean-going vessels when cargo holds were empty, with the ballast unceremoniously dumped on the quayside at the port of arrival. Many alien plant and invertebrate species were introduced to new regions through solid ballast, but with few exceptions, they rarely spread beyond the port environment.30Mack R.N. Global plant dispersal, naturalization, and invasion: pathways, modes, and circumstances.in: Ruiz G. Carlton J. Invasive Species: Vectors and Management Strategies. Island Press, 2003: 3-30Google Scholar By 1880, the development of watertight bulkheads allowed the widespread use of ballast water tanks that were filled at the port of departure with marine, brackish, or freshwater as ballast and subsequently discharged at the port of arrival.31Carlton J.T. Ballast.in: Simberloff D. Rejmanek M. Encyclopedia of Biological Invasions. University of California Press, 2011: 43-49Google Scholar However, many microorganisms, marine invertebrates, and fish picked up in ballast water were also discharged, leading to the introduction of large numbers of alien species to coastal seas, estuaries, and freshwaters to the extent that the global movement of ballast water is now widely recognized as a leading cause of aquatic invasions worldwide.32Carlton J.T. Ruiz G.M. The magnitude and consequences of bioinvasions in marine ecosystems.in: Norse E.A. Crowder L.B. Marine Conservation Biology. Island Press, 2005: 123-148Google Scholar Currently, it is estimated that worldwide more than 7,000 marine species travel in the more than 3 million tonnes of ballast water that are transported every day by world shipping.33World Health Organization Guide to Ship Sanitation. World Health Organization, 2011Google Scholar Another technological innovation with major trade implications was the equipping of vessels with refrigeration, which began in earnest in the 1880s primarily for the transport of frozen meat but increasingly used to prolong the freshness of more delicate commodities, such as fruit.24O'Rourke K.H. Williamson J.G. Globalization and History: The Evolution of a Nineteenth-Century Atlantic Economy. MIT Press, 2001Google Scholar For example, cool storage onboard vessels helped the international trade in bananas from Central America to the United States and Europe to grow dramatically from 1900 onward.34Lennerfors T.T. Birch P. Snow in the Tropics: A History of the Independent Reefer Operators. Brill, 2019Google Scholar Bananas are now grown commercially in more than 150 countries since refrigeration allows the product to reach distant markets, but shipments are notorious for concealing spiders and several species have become established as aliens in new regions following transport in bananas.35Vetter R.S. Crawford R.L. Buckle D.J. Spiders (Araneae) found in bananas and other international cargo submitted to North American arachnologists for identification.J. Med. Entomol. 2014; 51: 1136-1143Google Scholar The growth in the movement of fresh produce facilitated by improved cool storage has provided opportunities for many pests and diseases to be shipped around the world. Indeed, many insect larvae can survive for several months at 4°C and thus international shipments of cold-stored fruit have facilitated the spread of alien pest insects.36Mangan R.L. Hallman G.J. Temperature Treatments for Quarantine Security: New Approaches for Fresh Commodities. Westview Press, Inc., 1998Google Scholar Consequently, refrigerated cargo is often responsible for most alien species interceptions at international borders.37Work T.T. McCullough D.G. Cavey J.F. Komsa R. Arrival rate of nonindigenous insect species into the United States through foreign trade.Biol. Invasions. 2005; 7: 323-332Google Scholar The freight container is arguably one of the most important developments in international trade that has revolutionized the design of shipping vessels and ports helping integrate land and sea transport networks and so reduce shipping costs of a vast range of commodities.25Levinson M. The Box: How the Shipping Container Made the World Smaller and the World Economy Bigger. Princeton University Press, 2008Google Scholar The development of intermodalism, where the same container, with the same cargo, can be transported seamlessly between ships, trucks, and trains from an initial place of receipt to a final delivery point many kilometers away, has vastly increased the efficiency of trade. Transit times of containers at ports of arrival are markedly reduced, which facilitates higher survival rates and more rapid distribution of alien species away from ports, increasing propagule supply and invasion opportunity. Since the widespread adoption of standardized container designs in the 1960s, the growth in containerized transport has been spectacular (Figure 3). Today, the cargo handled by seaports is largely reflective of the economic complexity of their hinterlands with simple economies associated with bulk cargoes, while complex economies generate more containerized flows.12Rodrigue J.P. The Geography of Transport Systems. Routledge, 2020Google Scholar Containers have facilitated the trade in many commodities that would be difficult to transport otherwise, and these have changed the likelihood of introducing alien species. Once such commodity is used tires, awkward, bulky items that are costly to handle at the dockside. Containers made the trade in tires more cost-effective and opened up new sources in Asia for the growing market in Europe and the United States.38Reiter P. Sprenger D. The used tire trade - a mechanism for the worldwide dispersal of container breeding mosquitos.J. Am. Mosq. Contr. Assoc. 1987; 3: 494-501Google Scholar The Asian tiger mosquito (Aedes albopictus) can breed in residual water left inside used tires, and the conditions within a container are conducive to allow survival of desiccation-resistant eggs. As a consequence, this vector of several human diseases has become established in multiple new areas due to containerized international trade in used tires.39Hawley W.A. Reiter P. Copeland R.S. Pumpuni C.B. Craig G.B. Aedes albopictus in North America - probable introduction in used tires from northern Asia.Science. 1987; 236: 1114-1116Google Scholar A further distinction with containerized trade, is that the container itself can be a vector for the introduction of alien pests, weeds, and pathogens. Containers have their own international travel itineraries, being loaded and unloaded at multiple ports since one container will be used multiple times to ship different products (Figure 4). Over time, cargo containers accumulate debris both internally and externally that facilitate the international transport of invertebrate adults, larvae and eggs, plant seeds, and pathogen spores that have the potential to lead to the establishment of economically important alien species in new regions.40Stanaway M.A. Zalucki M.P. Gillespie P.S. Rodriguez C.M. Maynard G.V. Pest risk assessment of insects in sea cargo containers.Aust. J. Entomol. 2001; 40: 180-192Google Scholar During its lifetime, a single container will circumnavigate the globe multiple times such that the risk it might introduce an alien species into a new country rarely reflects only its most recent origin.Figure 4The itinerary of a single shipping containerShow full captionApproximate global route (originating and ending at the port of Southampton, UK) of a single 40-foot shipping container monitored by the BBC for 421 days over which it covered 75,762 km by container ship, 5,197 km by train, and 2,171 km by road (www.bbc.co.uk/thebox). Countries are shaded in relation to the total value of merchandise imports in 2019 (https://data.wto.org/).View Large Image Figure ViewerDownload Hi-res image Download (PPT) Approximate global route (originating and ending at the port of Southampton, UK) of a single 40-foot shipping container monitored by the BBC for 421 days over which it covered 75,762 km by container ship, 5,197 km by train, and 2,171 km by road (www.bbc.co.uk/thebox). Countries are shaded in relation to the total value of merchandise imports in 2019 (https://data.wto.org/). Commercial jet aviation began in the 1950s and initiated the global transport of freight by air. However, in terms of tonnage, air transportation carries an insignificant amount of freight (0.2% of total tonnage) compared with maritime transportation that handles about 90% of global trade.12Rodrigue J.P. The Geography of Transport Systems. Routledge, 2020Google Scholar Nevertheless, it remains one of the faster-growing sectors in international trade (Figure 3). In contrast to the important role in the introduction of pests, weeds, and pathogens into new regions that is played by the baggage carried by airline passengers,41McCullough D.G. Work T.T. Cavey J.F. Liebhold A.M. Marshall D. Interceptions of nonindigenous plant pests at US ports of entry and border crossings over a 17-year period.Biol. Invasions. 2006; 8: 611-630Google Scholar air cargo plays a proportionally minor role in trade-related transport of alien species. Nevertheless, air cargo has assisted in the development of new trade in high-value products that need to be shipped relatively quickly across the world. The increased speed of transport provides greater opportunity for the survival of alien species in air cargo, international airports provide quite different entry points to a new region compared with maritime ports, and the high-value products shipped by air represent different risks to commodities shipped in maritime trade. A wide range of potentially economically important alien insects have been intercepted on airline cargo, especially associated with plant products.42Caton B.P. Dobbs T.T. Brodel C.F. Arrivals of hitchhiking insect pests on international cargo aircraft at Miami international airport.Biol. Invasions. 2006; 8: 765-785Google Scholar The speed of airline cargo has led to a rapid increase in the international trade in fresh-cut flowers since this commodity needs to be transported rapidly from the areas of production in tropical countries to consumers around the world (Figure 5A). However, fresh-cut flowers often also host many unwanted invertebrate species that may potentially establish as alien species in the importing country.43Areal F.J. Touza J. MacLeod A. Dehnen-Schmutz K. Perrings C. Palmieri M.G. Spence N.J. Integrating drivers influencing the detection of plant pests carried in the international cut flower trade.J. Environ. Manage. 2008; 89: 300-307Google Scholar From the 1850s onward, the telegraph has had a direct impact on the integration of global trade, and by the end of the 19th century, cables were established that not only linked Europe and the United States, but also the Far East and Australia.44Standage T. The Victorian Internet: The Remarkable Story of the Telegraph and the Nineteenth Century's On-Line Pioneers. Bloomsbury Publishing, 2018Google Scholar The telegraph had an enormous impact on global trade market integration, resulting in increased convergence in the pr