Introduced marine organisms as habitat modifiers

Marine Pollution Bulletin 55 (2007) 323–332 www.elsevier.com/locate/marpolbul

Introduced marine organisms as habitat modifiers Inger Wallentinus *, Cecilia D. Nyberg Department of Marine Ecology, Marine Botany, Go¨teborg University, P.O. Box 461, SE 405 30 Go¨teborg, Sweden

Abstract Introductions of non-indigenous species (NIS) are mostly discussed through their impact on biodiversity. However, NIS can also act as ecosystem engineers, influencing the habitat itself, positively or negatively, directly or indirectly, which should be included when making risk assessments. Special concern should be given to changes in ecological services provided by the ecosystem. Physically, NIS may affect the substrate itself, or alter habitat architecture, indirectly influencing water movements, sediment accumulation, and light conditions. Chemical changes brought upon by NIS occur both on small and large scales, some having positive effects on ecosystem services, others can perturb epibionts. Furthermore, NIS may negatively affect natural resources, aquaculture or create fouling communities, all resulting in a negative impact on economics. However, if removed, already established NIS can be used as bioremediators, having a positive effect on different ecosystems. Using NIS for habitat management may be economically profitable, but could affect the habitat adversely. Ó 2006 Elsevier Ltd. All rights reserved. Keywords: Aliens; Ecosystem engineers; Foundation species; Habitat architecture; Ecosystem services; Management

1. Introduction 1.1. General background Non-indigenous species (NIS), once having become established, have caused much concern, since they are almost impossible to eradicate, especially when occurring submersed, and even worse when present as only small, viable algal fragments or microscopic stages (e.g. Ceccherelli and Piazzi, 2005; Conklin and Smith, 2005; Glasby et al., 2005; Hewitt et al., 2005; Nyberg and Wallentinus, 2006). The reason for concern is the ability of NIS to change adversely the ecosystem they arrive in. The consequences often are due to ecological interactions through e.g. competition for resources, including place to settle and spawning grounds, grazing or predation, trophic cascading effects, or filling up empty niches. However, many NIS can also have a severe impact by changing the habitat itself, physically or

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0025-326X/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.marpolbul.2006.11.010

chemically, directly or indirectly. In such cases, it is even more difficult for the native inhabitants to survive and flourish, especially if NIS will more or less monopolize the area. Many marine plants and macroalgae, but also several sessile invertebrates, have a profound architectural importance for the ecosystem structure. Hence, unintentional or intentional introductions of such species may play a fundamental role, especially when they establish in high abundances. In fact, they may also have a positive impact, by providing places for shelter in previously barren areas or increasing habitat diversity and spatial heterogeneity. In this review, we will give examples of different scenarios, where marine and brackish introduced organisms have been involved in habitat modifications. The speed, with which a habitat is changed, is also coupled to the stability and resilience of the ecosystem, and the impact can also be on different scales in space and time. It should also be remembered that an ecosystem may have more than one phase of equilibrium (Holling et al., 1995; Folke et al., 2004), and if reaching a new phase (either brought upon by a NIS or by other processes), return to the former state may be almost impossible. In this paper we will also incor-

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porate scenarios, when organisms, through habitat modifications, could directly influence economics, mostly negatively, while effects of intentional introductions for aquaculture and fisheries will not be discussed (as assumed by definition economically positive). 1.2. Biodiversity aspects and ecosystem engineers The impact of NIS on biodiversity has been recognized since long. Although, at a first glance, one could argue that NIS establishment would increase species richness, the opposite effect is mostly the case, resulting in what can be called biological pollution. That is because many NIS tend to become invasive, in the sense of having negative ecological and/or economical impact (e.g. Boudouresque and Verlaque, 2002). In the wider definition of biodiversity (i.e. including the relative abundances of different species), this would mean decreased diversity and evenness of the system. Such impact, for which there are copious amounts of references, is often reached by being a superior competitor for resources, or by being an efficient predator/grazer, resulting in decreased populations of prey species. However, also influences on the habitat itself, either directly or indirectly, could in a longer perspective drastically decrease the biodiversity. Such species, termed ecosystem engineers, have been considered keystone species for the ecosystem (e.g. Jones et al., 1994, 1997; Crooks, 2002; Cuddington and Hastings, 2004; Wright and Jones, 2006). This has mainly been discussed when such species, which also have the ability to create more complex ecosystems, decrease drastically, e.g. by over-fishing (Coleman and Williams, 2002). However, the establishment of a NIS, acting as an ecosystem engineer, could imply a significant impact on the ecosystem. Thus, habitat modifications, and the processes driving them, also must be considered in management and control efforts. Bruno et al. (2003) used ‘‘foundation species’’ for organisms that change the habitat by facilitating establishment of other species, and pointed to their importance in restoration, with Spartina alterniflora Loisel. as an example, which elsewhere is an invasive species. 1.3. Ecosystem services Many recent studies in ecosystem ecology have focused on the importance of the ecological services and goods provided by the ecosystems studied (e.g. Folke et al., 1996, 2004; de Groot et al., 2002; Chee, 2004; Eamus et al., 2005). The terms are used mainly for the benefit they provide to humans, and thus these aspects also need to be considered, when managing a coastal area. Many attempts have been made to evaluate those processes in monetary terms (e.g. Costanza et al., 1997; Farber et al., 2002). However, Chee (2004) in a review paper criticized the methods used in economics to achieve those values, since the complexity and dynamics of the ecosystems were not taken into account, nor were the couplings between ecosystems. He

especially emphasized the difficulty in evaluating resilience of ecosystems, incorporating irreversibility and uncertainties, and techniques other than those commonly applied were presented, the discussion of these, however, are outside the scope of this paper. Goods provided by an ecosystem largely depend on which species are present, and although NIS may affect those, both positively (e.g. harvestable NIS replace nonharvestable, native species) or negatively (e.g. non-harvestable NIS replace harvestable, native species), this may or may not be coupled to habitat modifications. Ruesink et al. (2006) described how a ‘‘pristine’’ area, after being invaded by four important NIS, increased primary productivity (>50%) (through the introductions of Zostera japonica Aschers. and Graebn. and S. alterniflora) as well as secondary productivity (250%) (through the introductions of Crassostrea gigas (Thunberg 1793) and Ruditapes (= Venerupis = Tapes) philippinarum (Adams and Reeve, 1850)), in comparison to when native mussels were harvested. Furthermore, also water filtration, detritus passways and biogenic structure were changed and the ecological character of this estuary was reshaped. Thus changes in the ecological services could be connected to induced habitat changes, since the NIS partly occupied areas with no similar native species. Of course, also many other processes such as eutrophication, overexploitation of natural resources, biotope fragmentations could lead to altered ecosystem services. Examples of changeable ecosystem services are given in Table 1, and some modifications caused by NIS are highlighted below. 1.4. Aims of the paper The aims of this review were not to give a complete account for all NIS causing habitat modifications. We wanted to elucidate these processes as such, which are less often discussed in invasion literature (but see e.g. Crooks, 2002; Cuddington and Hastings, 2004), by describing whether the impact has been positive or negative, mainly from an ecosystem perspective. Not included are effects on man-made structures caused by NIS, such as fouling on artificial surfaces by algae and sessile invertebrates (e.g. the main ship-fouling organism in the Baltic Sea is the introduced barnacle Balanus improvisus (Darwin, 1854), nor organisms boring in wooden structures such as the introduced ship-worms of several genera and, the isopods Sphaeroma and Limnoria. Many of the examples quoted below have come from direct field observations, while others are results from experimental work or from modelling. For instance, Cuddington and Hastings (2004) developed a model quantifying the effects of an invasive species, using the saltmarsh grass S. alterniflora as model organism, which has been shown to increase sedimentation rates and reduce water movements, resulting in elevated bottoms and marshlands, replacing previous mudflats. Their main conclusions from the simulations were that invasive species, which modify their envi-

I. Wallentinus, C.D. Nyberg / Marine Pollution Bulletin 55 (2007) 323–332 Table 1 Examples of ecological services provided by different ecosystems, which can be affected by non-indigenous species O2 production/absorption CO2 absorption/production N2 fixation Storage of nutrients, etc. Regeneration of nutrients, etc. Denitrification (shunt for eutrophication) Possibilities of bioremediation Trapping of sediment Protection of shoreline against erosion, flooding, etc. Filter for land runoff Clear water by filtering capacity Shelter for many organisms incl. temporary commercial species Nursery ground for juveniles from other systems (mobile links) Provide organic material, nutrients and food to other systems Records of pollutants (can be used in monitoring) Scientific and educational information Recreational values Aesthetic and artistic values

ronment, perform better in areas sub-optimal regarding their reproductive optima than non-modifying species, or than modifying species colonizing areas of their reproductive optima. Furthermore, they considered the largest risks of invasions to come from species combining tolerance of sub-optimal conditions with intermediate rates of habitat modification. 2. Habitat changes – examples 2.1. Physical changes of natural environments 2.1.1. Active changes of the physical condition of the substrate The most obvious modifications are animals digging into the sediments. In several areas, many native species such as crabs, polychaetes, mussels, etc. are digging out burrows. However, in other environments such activities do not occur frequently, and the sediment structure may be more vulnerable, should burrows and holes be created. Quite large negative disturbances of riverbanks have been reported for the migrating, catadromous Chinese mitten crab, Eriocheir sinensis H. Milne Edwards, 1854, where the vegetation on these banks may break down, or in the worst case disappear, due to the collapse of soft banks. Also the European green crab, Carcinus maenas (Linnaeus, 1758), in several introduced areas has been seen digging into shore banks causing erosion. It is well known that many polychaetes can dig quite deeply into the sediment, and that bioturbation has an environmentally positive effect, through increased denitrification rates. For areas, where there are few species representing that group, e.g. in the brackish Baltic Sea, during the 1980s, introduced species of the North-American polychaete genus Marenzelleria have been found to dig much deeper holes than the native polychaete, Nereis diversicolor (O.F. Mu¨ller, 1776), (Olenin and Leppa¨koski, 1999). This

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means that more oxygen can enter deeper into the otherwise anoxic seabed, creating steep gradients between oxic and anoxic conditions, which enhance oxidation of ammonium to nitrate and hence denitrification, an important ecosystem service. A different type of physical interaction is when the introduced Asian crab Hemigrapsus sanguineus (de Haan, 1835) has been seen taking over burrows built by native fiddler crabs in Connecticut, USA. There, the sediment disturbance is a natural one, which a NIS is taking advantage of (Brousseau et al., 2003). Since the two types of crabs were never seen together, this is more competition for resources (i.e. spaces to hide), than a modifying effect of a NIS. 2.1.2. Changes of habitat architecture Seaweeds, phanerogams and sessile invertebrates of moderate to large sizes are organisms that largely influence the architecture on both rocky and sediment bottoms. There are many examples of when NIS have changed this structure, and only a few will be highlighted here. When previously non-colonized shallow areas are occupied by introduced large sessile organisms, water movements may change drastically, which in turn can affect the substrate conditions both physically and chemically, see also Section 2.1.3. There are many papers on how introduced seaweeds have drastically changed the habitat by growing on previously unvegetated areas, either on grazed or otherwise perturbed rocks, or on small stones, shells, etc. on sediments, and even in the sediments (e.g. the green algae Caulerpa taxifolia (M. Vahl) C. Agardh 1817, C. racemosa var. cylindracea (Sonder) Verlaque, Huisman and Boudouresque 2003, Codium fragile ssp. tomentosoides (van Goor) P.C. Silva 1955, the brown algae Sargassum muticum (Yendo) Fensholt 1955, Undaria pinnatifida (Harvey) Suringar 1873 and the red algae Acrothamnion preissii (Sonder) E.M.Wollaston 1968, Gracilaria vermiculophylla (Ohmi) Papenfuss 1967, Grateloupia turuturu Yamada 1941, Womersleyella setacea (Hollenberg) R.E. Norris 1992, for references see e.g. Boudouresque, 2002; Wallentinus, 2002, 2006a,b and references therein). Several of these invasive algae can form mats or uniform meadows, which also may change the existing architectural structure from a complex three-dimensional system, formed by large seaweeds and phanerogams, into an almost two-dimensional one, with implications for other species in the community and their contributions to ecosystem services. Reef-building animals in general, including molluscs, are also obvious examples. The introduced polychaete Ficopomatus enigmaticus (Fauvel, 1923) behaves as a true ecosystem engineer in many brackish waters, and Schwindt et al. (2004) described how their tubes drastically had changed most of the seabed in an Argentinean lagoon, by building large platforms during 24 years. Those reefs in turn altered both water flow and sedimentation. Gutie´rrez et al. (2003) argued that the role of molluscs in general,

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as ecosystem engineers, was worth protection, by their production of shells, since shells were highly important as substrates for epibionts and as shelter. They also emphasized the trapping of particles and influence on water speed by reefs of oysters. Their mollusc species listed were nearly all native, but there are several examples of introduced bivalves (e.g. C. gigas) having shown large impact on the habitat. For the effects of colonization of zebra mussels, Dreissena polymorpha (Pallas, 1771), providing substrate for macroalgae, see Section 2.1.5. Also ascidians can act as habitat modifiers. Species of the colonial genus Didemnum have created nuisance, especially in US and New Zealand waters, on fishing grounds as well at aquaculture sites, and have also been found in Canadian and European waters (USGS, 2006). On the other hand, positive impact on biodiversity has been found for the in northern Chile introduced Australian ascidian Pyura praeputialis (Heller, 1878). Castilla et al. (2004) described it as an engineering species, creating dense three-dimensional matrices in broad belts, which modify the intertidal habitat structure. They found that 55% of the total 145 species recorded in the mid-intertidal habitat were found only in these matrices, which was especially apparent for macroinvertebrates. Habitat modifications also occur on smaller scales. The bulldozing of the periwinkle, Littorina littorea (Linnaeus, 1758), introduced in eastern North America, has implications for the intertidal rocks, removing sediments, which accumulate in the absence of the snails, turning hard substrate into sediment habitats (Bertness, 1984). 2.1.3. Indirect changes of the physical condition of the substrate Whereas mobile animals can directly influence the substrate, sessile organisms only have indirect influence on the seabed. Several mat-forming introduced macroalgae can act as a trap for suspended and depositing particles. The invasive red algae A. preissii and W. setacea, introduced in the Mediterranean, have been found to accumulate sediments in the mats (e.g. Piazzi and Cinelli, 2000). Due to their asexual reproduction by fragmentation, an essential part of the invasive strategy for many macroalgae, such mats can develop rather quickly, and the trapping of sediment could also reduce the possibilities for the infauna beneath to collect deposited particles. Such changes could also occur indirectly, by their shift of the balance between other algal components. When dense beds of Caulerpa species, such as the introduced C. taxifolia and C. racemosa var. cylindracea, grow in soft sediments, the risk of accumulating deposits from land-runoff is quite large. The invasive C. racemosa variety has been found to accumulate allochthonous sediments, and by that causes a depression of erect and prostrate algae, but not of turf species (e.g. Piazzi et al., 2005). According to that study, synergistic interactions between increased deposition of sediments and the invasion success seem to occur. Furthermore, Glasby et al. (2005) described

that C. taxifolia could survive total burial for 17 days and could recover, after becoming free of sediments, albeit with reduced growth rates. Partially buried fragments survived up to three months, which might give a competitive advantage. The phenomenon of trapping depositing particles has been more extensively studied for saltmarsh species. Especially species of the genus Spartina have been documented to accumulate much sediment, such as the dense stands of S. alterniflora, introduced on the American Pacific coast, Europe and China (e.g. Bruno, 2000; Bruno and Kennedy, 2000; Chen et al., 2004; Cuddington and Hastings, 2004 and references therein). A negative impact is the transformation of beaches to marshes, while a positive effect is that more rooted plants can grow there and seedlings of other species can emerge and survive due to Spartina’s reduction of physical disturbances. For S. anglica C.E. Hubbard, introduced on several continents, sediments accumulate among the large underground parts and, since long established population often show a die-back, particles have then been redistributed to surrounding shipping canals (Gray et al., 1991; Hacker et al., 2001 and references therein). Posey (1988) reported that Z. japonica stabilizes sediments with their roots, giving protection from infrequent wave disturbance, compared to adjacent unvegetated areas, and he also saw differences in sediment structure. According to Bando (2006) this ecosystem engineer is increasing on the American west coast, reacting positively to disturbance, while the native eelgrass Z. marina Linnaeus decreases. He also stated that all Zostera species are protected in the State of Washington, favouring the invasive intruder. 2.1.4. Effects on foraging Dense cover of algal NIS on previously more or less barren substrates, or in areas where vegetation easily permitted access to the sediments, can negatively affect the foraging of many animals. For example, Levi and Francour (2004) described how dense coverage of the invasive green alga C. taxifolia, especially its network of stolons, created a physical barrier causing a change of behaviour of the foraging of red mullets, Mullus surmuletus Linnaeus. These fishes avoided the dense beds and mainly searched for food on bare sand patches in less dense algal cover. However, the authors pointed out that the same behaviour could also be seen in dense beds of the native seagrass Posidonia oceanica (Linnaeus) Delile, where fish was not even seen resting, as it was above C. taxifolia. Further increase in Caulerpa colonization could result in insufficient surface of clearings among densely covered substrate, constituting a threat to the maintenance of this fish, especially to young ones, which are less likely to migrate deeper, where C. taxifolia is not predominant. Dense belts or mats of NIS on the seabed may also, in general, reduce the amount of suspended particles from reaching the seabed, which could imply less food for ben-

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thic suspension- and deposit-feeders (e.g. Gribsholt and Kristensen, 2002; see also Section 2.1.3). 2.1.5. Changes in light climate The large filtering capacity of introduced mussels have resulted in positive environmental effects by clearing water masses that were very turbid before they established. The Ponto-Caspian bivalve D. polymorpha, introduced in many fresh and slightly brackish water in both Europe (19th and 20th century) and North America (1980s), has in many studies been proposed as an ecosystem engineer (e.g. Cuddington and Hastings, 2004; Hecky et al., 2004) and is often given as example on a striking impact, due to its high biomasses coupled to very efficient filtering capacity (see also modelling results by Caraco et al., 1997). The high filtration rate of Dreissena, in comparison to the modest rates of native benthic suspension-feeders in the Great Lakes, has increased light penetration and the depth of the euphotic zone, resulting also in increased abundances of benthic macroalgae such as Cladophora (e.g. Hecky et al., 2004). Besides creating better light climate, the shells of these mussels also provide a better substrate for benthic algal attachment. For chemical changes due to the mussel activity, see Section 2.2.1. It is also as obvious that dense belts or mats of introduced algae may imply a shading effect on other algae, including benthic microalgae, which might decrease their production rates. For example, the large canopies and often high densities of the introduced brown alga S. muticum have been implicated in having a negative effect on native species by reducing the light conditions for them, especially in the subtidal and lower intertidal zones (e.g. Britton-Simmons, 2004; Sa´nchez et al., 2005). 2.2. Chemical changes of natural environments 2.2.1. Nutrient concentrations in the water column Hecky et al. (2004) tried to elucidate how D. polymorpha could influence the nutrient dynamics of the lakes colonized. They proposed a conceptual model, the nearshore phosphorus (P) shunt, which could describe the fundamental redirection of nutrient and energy flow after zebra mussel establishment. The mussels’ removal of particles from the water created aggregated, more larger-sized material. This had long-term implications for the nearshore benthic community, while offshore P-concentrations remained low. Their model explained some problems such as reemergence of the nuisant green alga Cladophora in coastal areas caused by increased P-concentrations, emanating from the remineralisation by the mussels. To understand the role of dreissenids in the lakes, they also emphasized that the sources of particulate nutrient inputs to dreissenids, and the fate of materials exported from the benthic community, are critical. Furthermore, they pointed out that the benthic algae have an advantage over phytoplankton by their closeness to nutrients regenerated by the bival-

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ves and to nutrients regenerated, when faecal materials are degenerated. Furthermore, regeneration of carbon dioxide from these sources may also increase the benthic algal productivity. According to them, the proposed nearshore phosphorus shunt would require even more stringent Pmanagement for lakes strongly influenced by zebra mussels, to maintain neashore water quality. For the innermost, eastern part of the brackish Baltic Sea, Orlova et al. (2004) discussed if D. polymorpha could be regarded also as a source of pollution, by the large amount of organic material in the deposited faeces and pseudofaeces – and not just a biofilter. Experiments with sediments inhabited by the introduced Manila clam, Tapes philippinarum, in the Adriatic Sea showed that, in comparisons to controls, the mussels as a mean increased the outflux of ammonium from the sediment 18 times, phosphorus 15 times, and silicate and carbon dioxide 9 times, while the oxygen demand increased 5 times, partly because of the large production of faeces and pseudofaeces, favouring bacterial growth (Bartoli et al., 2001). That not only the introduced species themselves, but also the harvesting techniques used had a huge impact, by resuspending sediments into the overlaying water, and resulting in a oxygen depletion there, has been shown in several studies (e.g. Bartoli et al., 2001; Sfriso et al., 2005). If long-lived introduced large seaweeds establish, they may decrease nutrient availability for other primary producer by storing nutrients and trace elements for longer periods. On the other hand, algal NIS with large surface:volume ratios can influence nutrient availability by their rapid uptake (see also Section 2.4.2). 2.2.2. Changes in sediments and biodeposition The introduced suspension-feeding gastropod Crepidula fornicata (Linnaeus, 1758), native on the northwestern Atlantic coast, has a very high food intake. In several areas it has been considered a serious competitor to other suspension-feeders such as oysters, scallops, etc. Recently, Ragueneau et al. (2005) showed that C. fornicata also considerably influences the biogeochemical cycle, through depositing biogenic silicate via faeces and pseudofaeces. In many coastal areas, decreased concentrations of silicate, in relation to nitrogen and phosphorus, have lead to lower abundance of diatoms, favouring other microalgal groups, including those causing harmful algal blooms (HABs). Studies in the Bay of Brest, NW France (Ragueneau et al., 2005), have shown that not only do the slipper limpets contribute to substantial amounts of organic material being accumulated on the sediment, but also that the enrichment of silicate is proportionally even greater with a factor 2–3. This, in turn, may favour a higher abundance of diatoms in summer, which could also be expected, where other suspension-feeding molluscs have been introduced. Chauvaud et al. (2000) proposed the following mechanisms to occur in this ecosystem: (1) there is a decrease of chlorophyll biomass during the first spring bloom resulting from

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limitation of silicic acid and increased suspension-feeder activity, (2) benthic filtration and biodeposition activities enhance biogenic silica retention at the sediment-water interface, and (3) recycling of trapped biogenic silica maintains diatom populations by providing silicic acid in summer and reduces primary production seasonality. These hypotheses suggest that benthic organisms control the export rate of biogenic silica, and hence the species composition of secondary phytoplankton blooms in the Bay. Later tests confirmed these hypotheses (Ragueneau et al., 2002), proposing that, although less abundances of C. fornicata would be desirable from a scallop fishery perspective, the slipper limpets helped the bay to cope with excessive loads of nitrogen by not enhancing HABs. For T. philippinarum in the Adriatic Sea, Bartoli et al. (2001) pointed out that the nutrients released into the water, from the sediment and the clams themselves, could promote new phytoplankton blooms, being positive for the clams, and also could favour macroalgae during summer, when nutrient levels are low, while the dieback of these macroalgal mats caused dystrophy, being negative for the clams. Due to the large area farmed there (35– 40% of the total lagoon), clam farming did not control eutrophication in the area, since totally ammonium release increased around 7 times and phosphorus release around 5 times. Studies on Z. japonica have shown, compared to the native eelgrass, that an altered decomposition community can accelerate decomposition rates, and change nutrient fluxes between sediments and water column, the latter could lead to less nutrient availability (Hahn, 2003; Larned, 2003). The presence of rooted plants also increases the oxidizing capacity of sediments and enhanced total microbial mineralization in comparison to unvegetated areas, as shown by Gribsholt and Kristensen (2002) for S. alterniflora.

capacity for thallus regeneration. In Asia, many areas are covered and very few seaweeds can recolonize this substratum, which changes the ecosystem from three-dimensional, providing much shelter, to a very simple, strictly twodimensional one, which can have adverse, indirect influences on fishery. Should such whitening areas develop also in European coastal areas, where L. yessoense has been introduced, similar negative ecosystem effects may result. Later, it has been shown (Kim et al., 2004) that it also has several allelopathic substances, which inhibit settlement and germination of various other Asiatic red, brown and green seaweeds. Among those tested were also species having been introduced in Europe, such as the red algae G. turuturu and Lomentaria hakodatensis Yendo, 1920, the brown alga U. pinnatifida and the green alga Ulva pertusa Kjellman 1897 (Verlaque, 2001; Wallentinus, 2002 and references therein). Several higher plants such as Myriophyllum spicatum Linnaeus and Elodea canadensis Michx. have been proposed to release allelopathic substances affecting several phyto- and zooplankton species, although these substances may not be quantitatively important for whole communities (e.g. van Donk and van de Bund, 2002; Gross, 2003). Many macroalgal NIS have substances deterring settling of epibionts. The red alga G. turuturu, introduced in many areas, contains floridoside, which inhibits settling of cyprid larvae of the Balanus amphitrite Darwin, also introduced in several areas (Hellio et al., 2004). Wikstro¨m and Pavia (2004) showed that the introduced Fucus evanescens C. Agardh 1820 had lower amounts of settled B. improvisus than the native bladder-wrack, which was due to an antifouling mechanism acting on post-settlement stages, while the native fucoid was more efficient in deterring settling.

2.3. Effects on cultured habitats 2.2.3. Allelopathy and toxic compounds Small scale changes in surface structure or chemical composition may change settling of epibionts, if native organisms are replaced by introduced ones. One of the most well-known introduced alga, C. taxifolia, does not only change the habitat by competing with canopy species (see Section 2.1.2), but has toxic secondary metabolites (e.g. Guerriero et al., 1992), which have been seen to directly affect the Posidonia leaves, by causing chlorosis and necrosis (de Ville`lle and Verlaque, 1995). A later study, however, showed that, in fact, lower levels of caulerpenyne was found in individuals experiencing the highest level of competition with P. oceanica, and those individuals also had the longest fronds (Dumay et al., 2002). The introduced calcareous red algal crust, Lithophyllum yessoense Foslie 1909, was first recorded in the Thau lagoon, southern France, in 1994, probably being brought by Japanese oysters (Verlaque, 2001). In Japan, this species dominates and outcompetes others by its grazer-resistance and strategy to peel off the epithallus, as well as by having a high

The concern on impact by NIS on aquaculture (not including farmed NIS) largely has dealt with spread of diseases, trophic interactions such as filtering of introduced toxic phytoplankton, and predation by e.g. introduced crabs. However, there are also NIS creating nuisance by their high abundances, not only on cages and lines, but also overgrowing mollusc beds and oyster reefs, directly affecting the economic gain. Examples of such NIS are both seaweeds, such as the green C. fragile, the brown U. pinnatifida and the red alga Heterosiphonia japonica Yendo 1920, and animals, such as the ascidians Didemnum spp., Styela clava Herdman, 1882, and bryozoans. Some seaweeds such as the brown algae Colpomenia peregrina Sauvageau 1927 and S. muticum, as well as the green alga C. fragile may also literally float away with oysters and mussels. Cultivated NIS may in turn act as vectors for species being habitat modifiers, especially flagrant for oysters having brought germlings of large or mat-forming seaweeds (e.g. Verlaque, 2001; Wallentinus, 2002).

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2.4. Management perspectives 2.4.1. Protection against erosion The plants most widely used to protect coastal areas from erosion have been species of the saltmarsh grasses Spartina (see Sections 2.1.3 and 2.2.2). Less often cited examples on plantations against erosion are mangroves, which in tropical intertidal areas comprise a community that provide a vast number of goods and ecosystem services, including coastal protection, improved water quality, nursery and foraging areas for a huge number of organisms (e.g. Ro¨nnba¨ck, 1999). Before 1902, there were no mangroves on Hawaii, but Rhizophora mangle Linnaeus was planted on Molokai to stabilize mudflats and later spread and built almost monospecific stands (Allen, 1998). Also the species Bruguiera gymnorhiza (Linnaeus) Lamk. and Conocarpus erectus Linnaeus became established, but had limited dispersal. Allen (1998) described how the establishment of mangrove communities have had striking effects on the shores, where no trees grow naturally, changing also ecosystem functions and services, and the tall plants have changed the architecture of the shores. However, the mangroves also partly have replaced other, previously introduced species. Although some positive effects were seen, such as more clear water outside the mangroves, which act as a sink for sediment and particles; in narrow canals with slow-flowing waters mangroves have caused stagnation by trapping debris among the stilt roots. Furthermore, habitats of historic and cultural values such as old fish-ponds have been devastated. Allen (1998) quoted costs of 108,000–377,000 USD ha 1 for controlling mangroves on Hawaii, depending on if machines could be used or not. 2.4.2. Bioremediation and biofilters The accumulation of different chemical substances by NIS, as well as by native organisms, can be used to remove pollutants and nutrients from the ecosystem, if and when the species are later harvested or removed from the sea. This has an indirect impact, mainly positive, on more or less degraded ecosystems. However, in the Italian lagoon Sacca di Goro, Bartoli et al. (2001) concluded that the nutrient amounts removed, when T. philippinarum was harvested, was only a small fraction in comparison to the amount of nutrients regenerated from the sediments in the densely farmed lagoon. Equally positive effects, reducing the risk of increased eutrophication of coastal waters, can also be achieved, if waste water discharges, e.g. from farming plants are passed through biofilters. Using bioremediators and biofilters is especially attractive if the organisms used, or products they produce, also have commercial values; but if accumulating toxic pollutants there are generally strong restrictions on using these organisms, especially bivalves, as food. Several NIS have been tested for such a purpose, as well as of course many native species. Schuenhoff et al. (2006) tested the efficiency of the tetrasporophyte of the intro-

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duced red alga Asparagopsis armata Harvey 1855, established since a long time in southern Portugal, which produces biologically active secondary metabolites (used in cosmetics and medicine), as biofilters growing in tanks for a commercial farm of the gilthead seabream, Sparus aurata Linnaeus, 1758. They showed that the nutrient uptake of this thin, filamentous alga was more than twice that of the native, sheet-formed green alga of the genus Ulva. Using Asparagopsis could turn this procedure to something favourable for the environments, also being economically sustainable. Species of the red algal family Gracilariaceae, used for agar production, have often been used as an integrated part of fish-cultures in several countries, but they are also grown together with molluscs (e.g. Troell et al., 1997, 1999; Yang et al., 2005; Herna´ndez et al., 2006; Zhou et al., 2006). In many cases local species were used, but in the Chinese studies, the species Gracilariopsis lemaneiformis (Bory de SaintVincent) E.Y. Dawson, Acleto and Foldvik 1964 had been selectively bred in the laboratory to achieve higher growth rates and then moved to southern China, later being retransferred to northern China. In all studies the seaweeds were growing well and the polycultures considered as an economic benefit with high potential in both reducing nutrients and giving commercial products. Such enterprises will probably increase much in the future, when pressure on aquaculture to reduce effluents certainly will increase. With the quite rapid spread of the Asian G. vermiculophylla in Europe and elsewhere (e.g. Rueness, 2005; Nyberg, 2006; Thomsen et al., 2006 and references therein), there might be another potential Gracilaria candidate for bioremediation, if harvest could be economically feasible. However, the risk of further dispersing this introduced species by fragments should not be neglected. Also species of the red algal genus Porphyra, including the introduced Asian P. yezoensis Ueda 1932 used as nori in Japan, have been tested as potential bioremediators for fish-farms (Carmona et al., 2006 and references therein). They concluded that Porphyra spp. in general were quite efficient nutrient scrubbers for moderately eutrophic effluents, with high growth rates for the native P. amplissima (Kjellman) Setchell and Hus ex Hus 1900 and the Asian P. yezoensis, all species being better in removing nitrogen than phosphorus. Although the majority of species discussed as bioremediators are algae and plants, also filter-feeding bivalves are suitable candidates (e.g. Lindahl et al., 2005). Around 20 years ago tests were performed to see if zebra mussels, D. polymorpha, on nets could be used as biofilters to reduce the pollutants in freshwater systems in the Netherlands (Reeders and Bij de Vaate, 1990, 1992). They calculated that mussels from Lake IJsselmeer exposed for seven months would bioaccumulate toxicants, especially organic pollutants and Polycyclic Aromatic Hydrocarbons (up to 10-fold accumulation), and that a milliard zebra mussels were needed in the biological filter to treat the waterflow (14 m3 s 1) entering Lake Volkerak-Zoommeer. However,

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as pointed out by Pires et al. (2005), the risk of further dispersal of this invasive species must be carefully considered, before any operation of this kind is undertaken. For tropical waters, pearl mussel farms have been suggested as a profitable environmental remediation (Gifford et al., 2004), and in many areas local species can be used. The very high filtration rate of these mussels, resulting in absorption of nutrients, heavy metals and presumably also bacteria, as well as yielding non-consumable products with commercial values, makes these mussels promising applicants for such purposes also in degraded waters. However, such mussels should definitely not be intentionally introduced into new areas. 3. Conclusions Ecosystem engineers (sensu Jones et al., 1994, 1997) are to be considered as keystone species for the ecosystem. Thus NIS acting as habitat modifiers (invasive NIS) could have a pronounced ecosystem impact, not only working by metabolic and trophic interactions (bottom-up, top-down, trophic cascades) or competition, but also affecting physical and chemical processes in the system as well as biological ones (e.g. reproductive behaviour, life cycle). This should be paid more attention to in risk analyses, especially for intentional species introductions and management. In principle, those NIS could also negatively affect native ecosystem engineers, resulting in an even greater ecosystem impact. By their modifications of the habitat also many ecosystem services can be altered. In conclusion, when a NIS is an attested or supposed ecosystem engineer, the environmental risks associated with an intentional introduction are too high and such a project must be banned. Acknowledgement This review was compiled as part of the research programme AquAliens, financed by the Swedish Environmental Protection Agency (Contract #I-89-02). We would also like to greatly acknowledge all authors of the many interesting papers used for this review, and the valuable comments by two referees. References Allen, J.A., 1998. Mangroves as alien species: the case of Hawaii. Global Ecology and Biogeography Letters 7 (1), 61–71. Bando, K.J., 2006. The roles of competition and disturbance in a marine invasion. Biological Invasions 8 (4), 755–763. Bartoli, M., Nizzoli, D., Viaroli, P., Turolla, E., Castaldelli, G., Fano, E.A., Rossi, R., 2001. Impact of Tapes philippinarum farming on nutrient dynamics and benthic respiration in the Sacca di Goro. Hydrobiologia 455, 203–212. Bertness, M.D., 1984. Habitat and community modification by an introduced herbivorous snail. Ecology 65 (2), 370–381. Boudouresque, C.-F., 2002. The spread of a non-native marine species, Caulerpa taxifolia. Impact on the Mediterranean biodiversity and possible economic consequences. In: di Castri, F., Balaji, V. (Eds.),

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