Are invasives worse in freshwater than terrestrial ecosystems?

Opinion Are invasives worse in freshwater than terrestrial ecosystems? Tom P. Moorhouse∗ and David W. Macdonald Several lines of evidence suggest that the effects of invasive species may be greater in aquatic freshwaters than in terrestrial ecosystems. We argue that freshwaters are significantly more invasible—from a number of poorly regulated sources—and also more susceptible to negative biodiversity, physical ecosystem, and socioeconomic impacts when invaded, than their terrestrial counterparts. Moreover, the nature of freshwaters appears to result in impacts that are wide ranging and severe while being indirect, diffuse, and difficult to both detect and predict. For these reasons, we conclude that freshwater invasive species represent a special case, when compared with terrestrial invasives, in which the likelihood of negative impacts, and their effects, is disproportionately severe. We suggest that future approaches to research in this area should aim to audit the full array of impacts of a number of representative invasive species, with a view to building an evidence base to support the global implementation of a precautionary approach to the release of aquatic freshwater non-native species. © 2014 Wiley Periodicals, Inc. How to cite this article: WIREs Water 2015, 2:1–8. doi: 10.1002/wat2.1059 INTRODUCTION I nvasive species are a signiicant component of human-caused global environmental change.1 Practically, every biome, however remote, has been affected by invasive species to some extent.1,2 Most countries have recorded several hundred established non-native species—including invertebrates, vertebrates, plants, bacteria, and fungi—and even Antarctica has nearly 200 of them.2 Invasive species are a major driving force behind species extinctions,3,4 have detrimental effects on the biodiversity5 and genetic diversity6 of native species, and can alter the food web structure7 and the physical or abiotic properties8,9 of invaded ecosystems. Established non-native species can certainly have positive effects (e.g., the creation of isheries; see below) but also have substantial negative impacts, both on ecosystem services and human well-being10 and on economies.11 For instance, in the USA alone, excluding microbes ∗ Correspondence to: [email protected] Wildlife Conservation Research Unit, Department of Zoology, University of Oxford, The Recanati-Kaplan Centre, Tubney House, Abingdon Road, Tubney, UK Conlict of interest: The authors have declared no conlicts of interest for this article. Volume 2, January/February 2015 and diseases of humans and livestock, there are 30,000 non-native species, and the small fraction of these considered ‘harmful’ is responsible for associated economic damages totaling more than $72.9 billion per annum.11 The impacts of invasive species are globally ubiquitous, but some biomes and ecosystems are more invasible by, and prone to adverse impacts from, non-native species than others.2,12–14 For example, a model of biodiversity scenarios for the year 2100 for a range of biomes concluded that biotic exchange (i.e., ecosystem changes resulting from the introduction of non-native species) was likely to be the fourth largest driver of biodiversity change overall, but was relatively more important for freshwater than terrestrial ecosystems.12 The intention of this opinion piece is to propose, and present the initial arguments supporting, the hypothesis that the negative impacts of invasive species are typically more severe, and more dificult to discern and manage, in freshwater ecosystems than in terrestrial ones. We compare a number of properties of those habitats found on land masses (therefore excluding marine environments), and outline the ways in which the intrinsic nature of aquatic freshwater ecosystems, and the human demands and uses © 2014 Wiley Periodicals, Inc. 1 wires.wiley.com/water Opinion thereof, supports our proposition: that in terms of negative ecological and socioeconomic impacts, aquatic freshwater ecosystems are disproportionately at risk from, and affected by, invasion by non-native species than their terrestrial counterparts. INVASIBILITY The invasibility of a particular geographical location is a function of a number of factors, but principal determinants are the number of introduced species (‘colonization pressure’,15 which operates at the community level) and the number of individuals of those species (‘propagule pressure’, operating at the population level), and how well those individuals survive in the new location—which in turn is a function of a species’ intrinsic nature and the environment into which it is introduced.2 As a general rule, all else being equal, the more species introduced, the more that become established in that area.2,15 It is the comparative ease with which not only single species (commonly from aquarium releases in which large, healthy specimens are released16 ) but also relatively intact communities—containing 100s to 10,000s of individuals of 10s to 1000s of pelagic and benthic aquatic species (e.g., from boat wells)—are transported, and the lack of comparable vectors for terrestrial communities, which make freshwater ecosystems disproportionately at risk of invasion.17 Vectors for the introduction of non-native species into these ecosystems include: ballast water; ish bait buckets; boats, including their live wells, boat trailers, and hulls; shipments of ishes, invertebrates, and macrophytes for aquarium hobbyists, aquaculturists, and water gardens.17 Such vectors can be crudely divided into those that introduce non-native species into a new geographic location from a long distance (particularly ballast water—on any given day several thousand of species are moved around the planet in ballast tanks18 —and aquarium or ornamental trades, which are largely unregulated16 ), and those that allow the secondary spread of organisms between lakes and throughout river networks. Once introduced, secondary spread, or dispersal of invasives from the introduction point, is facilitated by the comparative lack of dispersal barriers in freshwater ecosystems,17 or vectored by a number of agents.19,20 Species can spread from the invasion point through direct water connections20 and the low of rivers can aid colonization, in much the same way that the effects of an intravenous injection can spread quickly throughout a body: average dispersal rates of six invasive species in the Rhine have been shown to be between 44 and 112 km year−1 , with substantially 2 shorter time lags in colonization for species that arrived in upstream sections compared with species initially arriving in downstream areas.21 Alternately species may be vectored by larger animals (e.g., water birds, livestock, or deer moving between river catchments or ponds20 ) or by human activities. In the latter case, boats are heavily implicated in increasing both the rate and spatial scale of secondary spread, both trailered—when transported overland between water bodies—and through in-water transport. One study predicted 170 dispersal events of zebra mussels (Dreissena polymorpha) from boats from one primary public launch location on Lake St. Clair in Michigan, USA, over a summer season,19 and another found a total of 321 individuals comprising at least 15 different species of zooplankton in the standing water in vessels traveling into Lake Simcoe, Canada.22 In addition to the above accidental routes of release, many species have been deliberately introduced. A total of 582 non-native spawning ish and lamprey species are known to have extant populations across 17 countries, and of these 375 were deliberately introduced.23 In Britain the American signal crayish (Pacifastacus leniusculus) was deliberately introduced in 1976 to serve as a ishery and had colonized more than 250 British waters by 1988.24 (As an aside, despite the colossal numbers of signal crayish now present in British waters, the vast majority of crayish consumed in the UK are imported from China.25 ) Given the wealth of sources for unintentional and intentional release of non-native species into freshwater ecosystems, the facility with which these invasives may be secondarily spread, and the lack of comparable whole-community vectors for terrestrial ecosystems, we suggest that aquatic habitats are plausibly disproportionately invasible by, and therefore susceptible to, impacts from non-native species.12 BIODIVERSITY Aquatic freshwaters are substantially more biodiverse than would be expected from the area that they occupy. Surface freshwater habitats contain only around 0.01% of the world’s water and cover 0.8% of the Earth’s surface,26 but approximately 6% of every species currently described by scientists, 9.5% of all known animal species, and a third of the world’s vertebrates (including approximately 40% of global ish diversity), are conined to freshwater.27,28 Moreover, freshwater habitats tend to be insular (in that given basins may be hydrologically, and so biotically separate from others), which has led to the evolution of biotas with high endemism and high species turnover between basins,29 and this in turn may make them © 2014 Wiley Periodicals, Inc. Volume 2, January/February 2015 WIREs Water Freshwater and terrestrial invasive species susceptible to invasive species.12 Studies making direct comparisons between extinction rates of terrestrial and freshwater ecosystems are few, but one attempt to construct a model predicting the recent and future extinction rates for a variety of North American terrestrial and aquatic faunal groups showed that the projected mean future extinction rate for freshwater fauna was approximately ive times greater than for terrestrial fauna, and three times the rate for coastal marine mammals.30 The authors noted that at least 123 North American freshwater ishes, mollusks, crayishes, and amphibians have already gone extinct since the beginning of the 20th century, and that this estimate was undoubtedly conservative owing to the extinction of species before their discovery. The threats to global freshwater biodiversity underpinning these rates fall into ive categories: overexploitation; water pollution; low modiication; destruction or degradation of habitat; and invasion by exotic species.27,30 While invasive species constitute only one of a suite of threats to freshwater biodiversity, the wider point remains that freshwaters are uniquely biodiverse per unit area, relative to their terrestrial surroundings. To quote one author, ‘Not surprisingly, considering their landscape position and value as a natural resource, freshwaters are experiencing declines in biodiversity far greater than those in the most affected terrestrial ecosystems’,27 and the impact of invasive species is one primary cause of these uniquely rapid declines. ECOSYSTEM CHANGES Invasive species not only have impacts on individual plants and animals but can also transform entire ecosystems by altering resource availability, disturbance regimes, or habitat structure. Examples from terrestrial habitats are many, e.g., a nitrogen-ixing tree, Myrica faya, in Hawaii has a dominant inluence on the soil chemistry and productivity through its ability to enrich soil at a rate 90 times greater than native plants, and promotes populations of non-native earthworms owing to its shading and leaf litter.2 We suggest that freshwater ecosystems, however, may be more susceptible to such broad environmental alterations simply because they represent the interface between multiple diverse abiotic and biotic components. A perhaps useful concept is that freshwaters represent ‘ecotonal’ habitats, zones of transition between adjacent ecological systems, in this case operating at the terrestrial or aquatic interface, with key roles in regulating the low of water and materials across the landscape.31 From a biological perspective, freshwater ecotones form sharp transitions and linkages from terrestrial habitats to riparian and aquatic habitats, Volume 2, January/February 2015 and between their relevant physical substrates and environments (e.g., from river banks and riverbed to water), and typically occur across a relatively small (often tens of meters or less) distance, while longitudinally (i.e., upstream–downstream) they form continuous features that ramify through the landscape.31 The ecotonal nature of these ecosystems means that freshwater invasive species are particularly likely to have not only direct effects on other species but also effects on the physical environment that can indirectly affect a broad suite of other aquatic species.32,33 For example, invasive signal crayish (transported from North America to Britain) have well-studied direct negative effects on a large array of native lora and fauna,34 and also appear to inluence yields of suspended sediment in invaded water courses.9 Signal crayish can be extraordinarily numerous in invaded habitats (see Hidden Problems below), and a wide range of their activities, including feeding, walking, ighting, and burrowing, can mobilize sediments35–37 (see Figure 1). Laboratory experiments have demonstrated direct inluence of signal crayish on mobilization of pulses of ine sediment through burrowing into banks and ine bed material, particularly around the mid-point of the nocturnal period (when crayish are most active), and similar patterns of pulsed ine sediment mobilization, leading to an increase in ambient turbidity levels with a clear nocturnal trend, have been shown under ield conditions.9 Signal crayish are just one example of a growing number of invasive species known to alter the aquatic environment.32 Zebra mussels, for example, can have the converse effect of substantially increasing water transparency in North American and European lakes, in turn stimulating the growth of benthic algae and macrophytes and altering physical habitat for invertebrates and ishes.8 Any such widespread alteration in turbidity or clarity may have significant potential to affect the aquatic environment: aggradation of ine sediments can degrade aquatic habitats, reduce survival rates of ish and aquatic invertebrates,38,39 alter community structure,40 and hamper river restoration efforts41 as well as reduce low conveyance, with the potential to increase lood risks.42 In addition, ine sediments play a signiicant role in the transport of both nutrients and pollutants within luvial environments,43–45 with implications for water quality. SOCIOECONOMIC IMPACTS The socioeconomic impacts from freshwater aquatic invasive species are vast. By one estimate, the percentage of the accessible global supply of renewable © 2014 Wiley Periodicals, Inc. 3 wires.wiley.com/water Opinion Impacts of signal crayfish on fluvial sediments and morphology Behavior Non feeding activities Decreasing scientific evidence base Feeding Impacts on local environment and biota Impacts on subreach scale flow and sediment dynamics Potential reach-tocatchment scale impacts Management issues Reduction in aquatic macrophytes Reduction/ Shredding of CPOM change in and production of composition of FPOM/DOM macroinvertebrates Flow resistance and hydrodynamics Bed material composition, size distribution,and structural arrangement Movement Burrowing Bed microtopography Bank erosion Impacts on: sediment stability, sediment yields, sediment connectivity, channel and bank morphology, turbidity, nutrients and contaminated sediments, hydraulics, flow conveyance Physical habitat Water quality Sediment-related flood risks Within the context of changes in land use/land management and climate change FIGURE 1 | A conceptual model of the impacts of American signal crayfish on the physical structure of river systems, from the microscale to the catchment scale, demonstrating how the behavior of individuals might influence the local environment, which in turn may lead to impacts on sediments at the reach and catchment scale. CPOM and FPOM stand for coarse and fine organic particulate matter, respectively. (Reprinted with permission from Ref 37. Copyright Sage Publications 2011) freshwater that is appropriated for human use approximates 30% (24,980 km3 of 82,100 km3 ), and this percentage is likely to increase.46 Human uses for freshwaters include drinking and irrigation, waste disposal, transportation, power production, harvest of plants, ish, game, and minerals, and sites for homes, farms, and industries,29 in addition to a number of amenity, recreation, and sporting uses. Aside from the huge direct economic value of humans’ water use, the ecosystem services provided by freshwater ecosystems have been estimated at US $6.5 trillion per year, 20% of the value provided by all of the Earth’s ecosystems.47 All of these uses are made of a resource that, as we state above, covers only 0.8% of the Earth’s surface,26 therefore providing signiicant potential for freshwater invasive species to have wide-ranging negative effects, on almost any use and ecosystem service, while invading a comparatively small area. These impacts range from those with fundamental implications for human survival (e.g., those affecting availability of water for drinking and irrigation) to those that are indirect and dificult to foresee, but which nonetheless may have substantial socioeconomic costs. An example in the irst category is the ‘draw down’ of water reserves by water hyacinth 4 (Eichhornia crassipes), which has an exceptional rate of evapotranspiration, in the Nile region, resulting in one tenth of the average available water (7 billion m3 of water per year) being lost from the river before control efforts were implemented.48 As an example of an indirect, unforeseen cost, Eurasian watermilfoil (Myriophyllum spicatum) invasions of lakes in Wisconsin have been shown to decrease average land values for lakefront properties by 13% on average, in effect meaning that lakefront property owners are willing to pay more than $28,000 for a property on a lake free of milfoil, all else being equal.49 A given invasive species can have impacts that affect a broad spectrum of human enterprises. Possibly, the most (in)famous example of a freshwater invasive with wide-ranging negative effect is the zebra mussel in the Northern USA Great Lakes. Among other effects, it affects supplies of freshwater by clogging intake pipes, causing $69,070,780 of management expenses over a 6-year period to 1995; it affects water puriication through ilter feeding activities that impart odor in drinking water, with a cost of $323,000 per year to remove the taste and smell; it affects food sources by changing light conditions and competing with ish for zooplankton, causing $32.3 million © 2014 Wiley Periodicals, Inc. Volume 2, January/February 2015 WIREs Water Freshwater and terrestrial invasive species per year in net costs to aquaculture; and it threatens tourism and recreation (an industry worth $4 billon per annum) through covering beaches, boats, docks, and piers, causing cyanobacterial blooms, and increasing organochlorine and heavy metal concentrations in some recreational ishes and the ducks that prey on them.10 Similarly, in the UK, loating pennywort (Hydrocotyle ranunculoides), introduced in the 1980s from the aquatic plant trade, forms dense vegetative mats that outcompete most native aquatic plants in slow-moving channels, resulting in water courses becoming non-navigable and useless for ishing, and total annual costs to tourism and for management are estimated as £25,467,000; current annual estimated costs to the British economy of signal crayish (which do not include any potential costs resulting from their sediment-mobilization ability, which are not suficiently quantiied but which potentially include costs from biodiversity loss, pollutant mobilization, and lood risk9 ) are estimated as £2,689,000.50 HIDDEN PROBLEMS We propose that one key distinction between freshwater aquatic invasive species and terrestrial invasive species is that the former often have impacts that while certainly substantially damaging and widespread, are particularly dificult to detect. This dificulty may stem from a combination of the nature of the impacts, which are often diffuse in nature, and the observation that events occurring below the water’s surface are simply more dificult to detect. As an example of diffuse impacts, Figure 1 shows a schematic of how local increases in sediment yield resulting from the behavior of individual American signal crayish might be expected to have extensive impacts, with considerable management implications, when multiplied across whole catchments. As an example that to the majority of the human population, many freshwater invasives themselves are simply not as detectable as their terrestrial counterparts, invasive American signal crayish (Pacifastacus leniusculus) populations can reach estimated densities of 0.9–20 individuals per square meter,51–53 and a recent capture-mark-recapture study of four 100-m lengths of lowland UK rivers made 27,354 captures of 15,793 individual adult crayish over 64 days of ieldwork (with uncountable juvenile individuals remaining uncaptured).54 If these densities were to occur in a given terrestrial UK habitat it appears likely, in our opinion and to paraphrase one colleague, that ‘People would be out destroying crayish by any means possible’. And it appears equally likely that considerably greater legislative and management resources would currently be Volume 2, January/February 2015 targeted at preventing their introduction and facilitating their removal. While invasive crayish are certainly the focus of control efforts,55 the UK public remains largely ignorant of their presence, and current legislation is far from optimized to prevent further invasions.56 These observations appear to be part of a wider trend with respect to freshwater communities. Data on the population status or extinction rates of freshwater biota are biased in terms of geography, habitat types, and taxonomy, and most populations and habitats in some regions have not been monitored at all.27 A comprehensive global analysis of freshwater biodiversity, comparable to those available for terrestrial systems, is lacking, and indeed, for reasons related to the dificulty of studying and quantifying freshwater species, it is not possible to accurately estimate or project extinction rates of the majority of freshwater biodiversity using the approaches applied to terrestrial biota.27 Similarly, global awareness of the need to conserve freshwater biodiversity appears limited to the extent where a study showed that between 1997 and 2001, only 7% of papers in Conservation Biology were concerned with freshwater species or habitats.57 To quote the author of that study, ‘Some specialized journals … feature articles on freshwater biodiversity and conservation … but the paucity of freshwater research in Conservation Biology suggests that the mainstream conservation community has not given this critical issue the attention it requires’.57 CONCLUSION The intention of this opinion piece was to construct a hypothesis that aquatic freshwater ecosystems are disproportionately likely to suffer negative impacts from invasive species than are terrestrial ecosystems. We approached this by providing initial arguments supporting our hypothesis, but without intending to provide a deinitive test of it. Overall, our argument is necessarily one of degree rather than kind. All ecosystems to some extent to suffer biodiversity impacts12 and socioeconomic impacts11,50 from invasive species, and many terrestrial ecosystems have been physically altered by invasive species, with knock-on consequences for their co-occurring biota.1 We argue, however, that freshwater ecosystems are inherently more invasible, more biodiverse, and more at risk of ecosystem-wide changes (owing to their ecotonal nature) than their terrestrial counterparts, and, given the vast array of human pressures on, and uses of, freshwater habitats, and their constituent biodiversity, the potential for socioeconomic impacts—including those that threaten lives and © 2014 Wiley Periodicals, Inc. 5 wires.wiley.com/water Opinion livelihoods—resulting from disruption by invasive species is concomitantly vast. Within this context there is an apparent disconnect between, on one hand, the highly biodiverse nature of freshwaters and the severity of the impacts of freshwater invasive species, and on the other a comparative lack of global research on freshwater biodiversity27,57 and a seemingly passive global attitude toward the prevention of invasions or the implementation of early-stage postinvasion responses by resource managers.16,58,56 For example, a principal source of invasions, the ornamental aquarium trade, remains largely unregulated—and notorious invaders such as water hyacinth remain freely available for purchase online, although banned in many countries and states16 —and there remain ‘ … considerable policy questions as to what constitutes a ‘suficiently protective’ ballast water discharge standard … ’ with respect to reducing the likelihood of future invasions.59 This disconnect is perhaps symptomatic of the inal property of freshwater invasive species we identify above: the often hidden and diffuse nature of their presence and impacts. In short, our hypothesis is that a number of factors intrinsic to freshwater ecosystems predispose them to disproportionately severe, and disproportionately dificult to detect, impacts from invasive species (as well as from numerous other anthropogenic sources). A suitable response to this situation might comprise a threefold approach, incorporating: (1) a renewed research focus, aimed at auditing the full range of all impacts of a selection of freshwater invasive species, to catalog and understand the full ecological and socioeconomic costs of their presence; (2) using the evidence thus obtained to derive steps for mitigation and solution of the issues identiied (where this is possible, many aquatic invasive species are notably resistant to mitigation efforts); and (3) again using the scientiic evidence as a basis, an appeal to the precautionary principal, which here might dictate substantial legislative curbs to the currently ubiquitous sources of introduction for freshwater invasive species, with a view to drastically reducing the rate at which global freshwaters are being invaded. REFERENCES 1. Vitousek PM, D’Antonio CM, Loope LL, Westbrooks R. Biological invasions as global environmental change. Am Sci 1996, 84:468–478. 2. Ricciardi A. 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