Assessment of biopollution in aquatic ecosystems

Marine Pollution Bulletin 55 (2007) 379–394 www.elsevier.com/locate/marpolbul

Assessment of biopollution in aquatic ecosystems Sergej Olenin a

a,*

, Dan Minchin b, Darius Daunys

a

Coastal Research and Planning Institute, Klaipeda University, H. Manto 84, LT92294, Lithuania b Marine Organism Investigations, 3 Marina Village, Ballina, Killaloe, Co Clare, Ireland

Abstract The introduction of alien species (AS) in marine environments is a factor of disturbance that can be viewed as a pollution agent. Using basic information on abundance and distribution of alien species, we developed an index that classifies AS impacts on native species, communities, habitats and ecosystem functioning. This method can be used to evaluate impact at five different levels of biopollution, fitting within the existing schemes for water quality assessment. Both spatial and temporal comparisons are possible. The assessments may also be used to evaluate management performance where avoidance measures were necessary and assist in preventing further unwanted introductions. Such assessments made for the same areas over time provide opportunities for measuring change in biopollution. We have tested the method using four different well-studied areas within the Baltic Sea (brackish to freshwater environments) for two different times, 20 years apart. Further developments of the scheme may be needed to cover some specific cases and taxonomic groups according to their life history.  2007 Elsevier Ltd. All rights reserved. Keywords: Xenodiversity; Biological pollution; Community; Habitat; Ecosystem; Alien species

1. Introduction The term ‘‘biological pollutants’’ has been used recently to discuss the problems caused by alien aquatic species (AS) (e.g. Boudouresque and Verlaque, 2002). An alien species (synonyms: non-native, non-indigenous, exotic, introduced) was defined as a species intentionally or unintentionally introduced by humans outside its past or present natural range and dispersal potential (based on IUCN, 1999; for recent reviews of alien species terminology see, e.g. Occhipinti-Ambrogi and Galil, 2004; Colautti and MacIsaac, 2004). Natural shifts in distribution range (e.g. due to climatic change or dispersal by ocean currents) do not qualify a species as an alien. An alien species is considered to be invasive if its ‘‘population has undergone an exponential growth stage and is rapidly extending its range’’ (Occhipinti-Ambrogi and Galil, 2004) or its ‘‘intro-

*

Corresponding author. E-mail address: [email protected] (S. Olenin).

0025-326X/$ - see front matter  2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.marpolbul.2007.01.010

duction does or is likely to cause economic or environmental harm or harm to human health (IUCN, 1999)’’. Structural and functional diversity caused by alien species (or xenodiversity, sensu Leppa¨koski and Olenin, 2000) have an effect on various levels of biological organisation: genetic, population, community and habitat/ecosystem (Reise et al., 2006). These ‘‘effects of introduced, invasive species sufficient to disturb an individual (internal biological pollution by parasites or pathogens), a population (by genetic change) or a community (by increasing or decreasing the species complement); including the production of adverse economic consequences’’ were defined as biological pollution (biopollution) (Elliott, 2003). Often the impact of alien species may be interpreted as decline in ecological quality resulting from changes in biological, chemical and physical properties of aquatic ecosystems. These changes include (but are not confined to): elimination or extinction of sensitive and/or rare species; alteration of native communities; algal blooms; modification of substrate conditions and the shore zones; alteration of oxygen and nutrient content, pH and transparency of

380

S. Olenin et al. / Marine Pollution Bulletin 55 (2007) 379–394

water; accumulation of synthetic pollutants, etc. Thus, the definition of biopollution may be widened to include impacts on the structural components (both biotic and abiotic) and functioning of the invaded ecosystems (Text Box 1).

Text Box 1. Definition of biological pollution (modified from Elliott, 2003) The impacts of alien invasive species sufficient to disturb ecological quality by effects on: • an individual (internal biological pollution by parasites or pathogens), • a population (by genetic change, i.e. hybridisation), • a community (by structural shift), • a habitat (by modification of physical–chemical conditions), • an ecosystem (by alteration of energy and organic material flow). The biological and ecological effects of biopollution may also cause adverse economic consequences.

The literature on AS impacts continues to expand world-wide, yet there is currently no method to assess biopollution in different ecosystems affected by xenodiversity. For instance, the concept of ecological quality indicators has been examined in relation to the European Water Framework Directive (WFD Directive, 2000/60/EC) which aims to improve (or maintain good status of) the water quality of rivers, lakes, transitional, coastal waters (e.g. Rolauffs et al., 2004; Borja et al., 2006). Although in WFD there is no explicit mention of AS and their potential impact on quality of surface waters, in the instructive Guidance Document (2003) the introduction of AS is given as an example of biological pressure and impact. The aim of the present study was to elaborate an assessment method enabling comparison of different aquatic ecosystems according to the level of biopollution reflecting the magnitude of impacts of AS. We used numerous published accounts to analyze the distribution and abundance ranges of AS; we related these ranges with impacts of AS on native community structure, habitat traits and ecosystem functioning and constructed the biopollution assessment method based on the relation between the abundance/distribution ranges and the level of impacts. 2. Development of the biopollution assessment method 2.1. Assessment concept According to Carlton (2002) all alien species have impact following their arrival; however, these impacts are

not always possible to measure for practical reasons. The effect of biopollution cannot be deduced simply from alien to native species ratios. Compared to the almost 30,000 listed in the register of European marine species (Costello et al., 2001), the share of aliens is 2%, or 2.5% when taxonomic groups not covered consistently are left out (Reise et al., 2006). Numerically these numbers may seem low, but this comparative assessment does not take into account the contribution of AS to the total community biomass or abundance. For example, in the eastern Gulf of Finland (Baltic Sea), the accumulated plankton and benthic xenodiversity accounts only for 5% of all recorded mesozooplankton and bottom macrofauna species yet this alien component makes up 96% of the total biomass within the community (Orlova et al., 2006). The abundance, distribution range and the magnitude of AS impact can vary over time. We postulate that AS produce measurable effects on a local community and ecosystem only after attaining a particular level of abundance and when occupying a sufficiently large area. It is clear that at the largest level of population expansion an invader has greater impact than close to the time of arrival or subsequent adjustment (sensu Reise et al., 2006). Consequently, the relative abundance of an alien species, the range of its spread and magnitude of impact(s) should be considered when assessing biopollution. Precise measurement and comparison of impacts within and/or between different ecosystems is difficult to achieve when data available from one region may not exist for another. To overcome this difficulty we propose a scale involving five levels of biopollution. These levels correspond to different ranges of abundance and extent of the distribution of AS which are related to the magnitude of their impacts. Thus, the prerequisite for the assessment is the data on the abundance and distribution range of AS. To assess the magnitude of impacts we consider separately the following categories: • Community – the changes caused in native species composition and abundance, including shifts in type-specific communities. • Habitat – the character of habitat modification. • Ecosystem – the impact on ecosystem processes and functioning. The magnitude of the impacts for these three categories is usually interrelated: the higher the level of habitat modification caused by AS the larger is the change to the structure of the native community and the more likely the performance of the ecosystem is altered. Dividing the impacts into three separate groups facilitates an assessment and helps to evaluate a level of biopollution even where there is a limited knowledge of impacts. In each impact category, the scale involves five levels ranging from no impact (no measurable impact) to massive impact (Sections 2.3–2.5). We combined the abundance and distribution ranges of AS with the levels of impact

S. Olenin et al. / Marine Pollution Bulletin 55 (2007) 379–394

on communities, habitats and ecosystems to provide a biopollution index (Section 2.6). 2.2. Ranking abundance and distribution range of alien species The abundance of an AS is ranked in relation to the abundance of the relevant ecological group (i.e. phytoplankton, macroalgae, zoobenthos or fish), to which the AS belongs to. The units of abundance (numbers per area unit, biomass or percentage of coverage) should be the same for the alien and native species. The score ‘‘Low’’ is given for a species that makes up only a small part of the relevant community: for example, when a population of an alien invertebrate forms a minor portion (few %) of the benthic macrofauna community. The score ‘‘Moderate’’ is used if an AS constitutes less than a half of abundance of the native community, and ‘‘High’’ if it exceeds half, i.e. quantitatively dominates in the invaded community. The distribution scale ranges from ‘‘one locality’’ to ‘‘all localities’’. This is evaluated for a given assessment unit, which may be an estuary, bay, port, aquaculture area,

381

coastal zone, or other defined part of a water body, or an entire sea. The distribution scale for AS consists of four scores: ‘‘Local’’ (found only in one place within the assessment unit), ‘‘Several localities’’ (spread beyond one locality but present in less than half of the available localities), ‘‘Many localities’’ (extends to more than a half of the available localities), and ‘‘All localities’’ (all, or nearly all, available habitats are colonised). For example, the invasive ctenophore Mnemiopsis leidyi was first recorded off the Bulgarian coast in 1986 (Kideys, 2002 and references therein), and on the scale of the entire Black Sea its distribution range is scored as ‘‘Local’’. During the height of its invasion it occupied all pelagic parts of the Sea and so the distribution range is scored as ‘‘All localities’’. It is important to note that in making two different assessments at different scales (e.g. one a small inlet and the other a sea that includes this inlet), the same situation will be ranked differently. Should the assessment unit be the small inlet where an AS is confined to and occurs throughout it, the score would be ‘‘all localities’’; but should the assessment unit be the sea, the score would be ‘‘one locality’’ (Fig. 1). This may be illustrated by the case

Fig. 1. Examples of different assessment unit sizes illustrating relative magnitude of the distribution range of a species: (a) ‘‘One locality’’ for a sea; (b) ‘‘Several localities’’ for a coastal zone within a sea; (c) ‘‘Many localities’’ for a lagoon within the coastal zone; and (d) ‘‘All localities’’ for an inlet within the coastal lagoon. Striped area: distribution of an AS.

382

S. Olenin et al. / Marine Pollution Bulletin 55 (2007) 379–394

of the green alga Caulerpa taxifolia (Meinesz, 1999), which once formed a small patch near the Monaco Aquarium (distribution range ‘‘One locality’’) and underwent subsequent stages up to ‘‘Several localities’’ (at the scale of the entire Mediterranean Sea) and ‘‘All localities’’ (at the scale of a particular bay on the coast of Spain, France or Italy). We combined the scale of relative abundance and the scale of distribution range to produce a one-dimensional scale, where 12 possible combinations of the Abundance and Distribution are narrowed down to five Classes (Table 1, Text Box 2). In general, these Classes correspond to different phases of invasion (sensu Karpevich, 1975; Reise et al., 2006): arrival (Class A), establishment (B), expansion (C, D and in extreme cases E) and adjustment. In the later (post-expansion) phase the Abundance and Distribution Class usually would vary between B and D, however, theoretically, a population may become reduced (Class A) or evolves to form a new outbreak (Class E).

for resources (such as food, nutrients, light, space), grazing, predation and parasitism on native species, excretion of toxins by phytoplankton or toxic macroalgae, quantitative changes in community structure and dominance of an AS in the invaded community (Baltic Sea Alien Species Database, 2006 and references therein). We assess the resultant effect by change(s) in species ranking, shift(s) in community dominant species, displacement of native species, loss of type-specific community, and loss of keystone species (Text Box 3).

Text box 3. Classification of alien species impact on native species and communities Code Impact C0

Text box 2. Five classes representing the abundance and distribution range of alien species Code

Description

A

An AS occurs in low numbers in one or several localities An AS occurs in low numbers in many localities or in moderate numbers in one or several localities or in high numbers in one locality An AS occurs in low numbers in all localities, or in moderate numbers in many localities, or in high numbers in several localities An AS occurs in moderate numbers in all localities, or in high numbers in many localities An AS occurs in high numbers in all localities

B

C

D

E

C1

C2

C3

2.3. Assessing impact on native species and communities The impacts of AS on native species and communities may include hybridisation, competition with native species

Table 1 Combination of abundance and distribution ranges into five (A–E) classes, see Text Box 2 Abundance

Low Moderate High

Distribution scale Local

Several localities

Many localities

All localities

A B B

A B C

B C D

C D E

For spatial resolution see Fig. 1 and comments in text.

C4

Description

None

No displacement of native species, although AS may be present. Ranking of native species according to quantitative parameters in the community remains unchanged. Type-specific communities are present Weak Local displacement of native species, but no extinction. Change in ranking of native species, but dominant species remain the same. Type-specific communities are present Moderate Large scale displacement of native species causes decline in abundance and reduction of their distribution range within the assessment unit; and/or type-specific communities are changed noticeably due to shifts in community dominant species Strong Population extinctions within the ecosystem. Former community dominant species still present but their relative abundance is severely reduced; alien species are dominant. Loss of type-specific community within an ecological group Massive Population extinction of native keystone species. Extinction of type-specific communities occurs within more than one ecological group

Changes in a species ranking, according to quantitative parameters (biomass, coverage, abundance, etc.), alters the position of one or more native species within the community but may not necessarily alter the community structure. A shift in community dominant species, however, leads to a reorganisation of the existing quantitative relationships

S. Olenin et al. / Marine Pollution Bulletin 55 (2007) 379–394

between species with a consequent change to the structure of the community. This, in turn, may result in loss of a type-specific community (specific composition and structure of phytoplankton, macroalgae, macrofauna or other ecological group) representative for a given assessment unit. Displacement of a native species is defined here as a change in its spatial distribution that results from direct or indirect effects of AS (competition for resources, predation, transfer of parasite or disease, habitat alteration or loss, etc.). Large scale displacement can lead to the extinction of a native species within an assessment unit. Finally, we grade the loss of a native keystone species (resource providers and ecosystem engineers, sensu Jones et al., 1994; Payton et al., 2002) as the strongest impact at the species/community level. 2.3.1. No impact (C0) According to Williamson (1996), most AS will arrive without any noticeable effect on a native community. For example, the unintentional introduction of the spionid ˚ land polychaete Polydora redeki to the coastal waters of A Archipelago (northern Baltic Sea) did not result in any noticeable change in the benthic macrofauna community (Bonsdorff, 1981). Also AS may occur within an assessment unit occasionally in small quantities, for example being carried in the outflow of brackish water into a sea or from spreading through a marine canal (Cohen, 2006). 2.3.2. Weak impact (C1) Arrival of an AS causing noticeable alterations in the structure of a native community where an AS may became a quantitatively sub-dominant species. AS may displace native species but does not result in their extinction. For example, at the North Sea coast of Germany, the overgrowth and pre-emption of space by the alien barnacle Elminius modestus, diminish other epifaunal species such as the native barnacle Balanus balanoides (Nehring, 2005). Competition for both food and space, due to similarities in feeding mode and sympatric occurrence, can make the native amphipod Monoporeia affinis to avoid areas where the alien polychaete Marenzelleria neglecta (syn.: M. cf. viridis) is present in high numbers (Neideman et al., 2003). There also might be an indirect effect of an alien species resulting in alteration of a native community. For example, the introduction of the alien macrophyte Zostera japonica to the north-east Pacific coast caused increase of the species richness and abundance of native macrofauna in sea grass patches due to organic enrichment of bottom sediments (Posey, 1988). 2.3.3. Moderate impact (C2) This occurs where an AS dominates over native species, yet former native dominant species are still present but as sub-dominants. For example invasion of Sargassum muticum resulted in a significant reduction of native canopy

383

algae (by 75%) and undercanopy (by 50%) that lead to alterations in the predator–prey dynamics in shallows on the west coast of North America (Britton-Simmons, 2004). In the open coastal zone of the Baltic Sea the PontoCaspian water flea Cercopagis pengoi may attain a very high abundance forming a numerically dominant component of the zooplankton, while in the Curonian Lagoon it occurs occasionally in low abundance (Gasiunaite and Didziulis, 2002). Thus, for the coastal zone the situation may be assessed as ‘‘Moderate impact’’, while for the Curonian Lagoon it would be evaluated as ‘‘No impact’’. 2.3.4. Strong impact (C3) Some invasions can lead to non-dominant species losses through competition and displacement. For example, in Lake Banyoles (Iberian Peninsula), 12 alien fish species were introduced during the 20th century and the current fish assemblage is now dominated by invasive species, in particular largemouth bass (Micropterus salmoides) and pumpkinseed (Lepomis gibbosus) in the littoral zone and roach (Rutilus rutilus) in the pelagic zone; two native species were lost (Garcia-Berthou and Moreno-Amich, 2000). However, there are very few examples of species extinctions in the sea because such events are difficult to prove (Carlton et al., 1999). Therefore, other features of the strong impact may be taken into account, such as the complete shift in community dominant species. This occurs where an AS dominates over native species in terms of abundance, yet former native dominant species are still present. For example, due to the proliferation of the slipper limpet Crepidula fornicata in the Gulf of Normandy (northern France) (Quiniou and Blanchard, 1987) it became a community dominant species in the region formerly dominated by the scallop Pecten maximus, which still provides a fishery (Fifas et al., 1990). In pelagic environment, an AS may became dominant for a certain season, like the potentially toxic dinoflagellate Prorocentrum minimum which successfully established itself in the Baltic Sea during the last two decades and has become a coastal summer bloom forming species, although occurring irregularly between years (Hajdu et al., 2000). 2.3.5. Massive impact (C4) Massive impacts from an introduction can result in keystone species and/or type-specific community(s) extinctions in the relatively confined areas found in freshwater bodies, lagoons and saline ponds. For example, in African Lake Victoria, the introduction of the predatory Nile perch Lates niloticus resulted in extinctions of haplochromine cichlid communities and subsequent reorganisation of the lake ecosystem (Gophen et al., 1995). Another example of the massive impact may be the wasting disease of the seagrass which caused serious losses to the expanse of seagrass meadows in different areas of the world. These losses as well as reduced stability of sediments will have had consequences for those associated species that

384

S. Olenin et al. / Marine Pollution Bulletin 55 (2007) 379–394

depend on seagrasses for shelter or substrate (Muehlstein, 1989; Ralph and Short, 2002). The causative organism for the seagrass decline was the slime mould Labyrinthula zosterae (Muehlstein, 1989); several Labyrinthula species were found to be frequent in ships’ ballast tank sediments (Hulsmann and Galil, 2002).

Text box 4. Classification of alien species impact on habitats Code Impact H0 H1

2.4. Assessing impact on habitats A wide range of alien plants, invertebrates and fishes may modify benthic and/or pelagic habitats. These can involve physical–chemical changes to the substrate, sediment transport and water flow, nutrient regime and transparency of water as well as replacement of the keystone habitat forming species (Cuddington and Hastings, 2004; Wallentinus and Nyberg, this volume). A habitat is defined here as an aquatic area of relatively uniform environmental conditions, with a characteristic assemblage of plants and animals. For practical reasons in recent directives, conventions and nature classification systems (e.g. EUNIS, 2006) the term ‘‘habitat’’ is sometimes considered as a synonym for ‘‘biotope’’ (Olenin and Ducrotoy, 2006 and references therein). An example of a habitat (biotope) may be a sublittoral stony bottom with dense colonies of blue mussels; an intertidal sandy beach in an estuary with sea grass meadows; or a coastal water mass with characteristic physical (salinity, temperature, transparency, colour), chemical (nutrients) and biological (plankton composition) features. To assess the degree of habitat modification we use the following criteria: habitat alteration, habitat fragmentation and habitat loss. We define habitat alteration as a change in the quality of a habitat, such as reduction in the density of a sea grass meadow, addition of shell deposits to sandy or muddy bottoms, siltation, or, in general, the decline of existing or addition of a new habitat feature. Conditions in pelagic environments may be changed arising from benthic–pelagic interactions that result in the release of nutrients from sediments by burrowing benthic species, filtering activity of seston-feeding mussels or due to development of alien algae bloom. Habitat fragmentation takes place where a habitat, once continuous, becomes divided into separate parts following an AS invasion. Habitat loss is the reduction of the spatial extent of a habitat. In extreme cases this may lead to the elimination of a habitat within an assessment unit. Finally, we distinguish the key habitats, which are very important for the wider significance of the ecological processes (sensu Hiscock et al., 2003), such as Posidonia meadows, biogenic reefs or spawning grounds. A variety of habitat modification activities of AS may be ranked from no noticeable alterations in benthic or pelagic environment up to massive impacts causing irreversible changes (Text Box 4). 2.4.1. No impact (H0) Although all organisms utilise resources (space, food, nutrients, etc.) and so have at least some impact on their

H2 H3

H4

Description

None Weak

No habitat alteration Alteration of a habitat(s), but no reduction of spatial extent of a habitat(s) Moderate Alteration and reduction of spatial extent of a habitat(s) Strong Alteration of a key habitat, severe reduction of spatial extent of habitat(s); loss of habitat(s) within a small area of the assessment unit Massive Loss of habitats in most or the entire assessment unit, loss of a key habitat

environment, we recognise that many AS will have no measurable impact on the habitats they occupy. For these where no conspicuous changes in physical–chemical structure of a habitat have been noticed we apply the term ‘no impact’. These mainly consist of species for which there are a small number of records, even though they may become more abundant at some future time and have greater impact, as may be expected of the species. 2.4.2. Weak impact (H1) Alteration of physical–chemical structure of a habitat caused by alien species, which may occur, for example due to tube building of the corophiid crustaceans Chelicorophium curvispinum or burrowing activity of the infaunal polychaete M. neglecta (Olenin and Leppa¨koski, 1999; Kotta et al., 2001). A further example is the decline in mean sediment grain size and increase in sediment organic content within patches compared with adjacent unvegetated areas following the introduction of the sea grass Z. japonica (Posey, 1988). Such alterations, however, do not result in fragmentation or loss of the original habitat. 2.4.3. Moderate impact (H2) Moderate changes in the physical–chemical structure of habitats may occur, for example, due to the conversion of a soft sediment surface to a firm substrate from shell deposits (Minchin, 1999; Vallet et al., 2001; Karatayev et al., 2002; Daunys et al., 2006; Reise et al., 2006). Another example is the Chinese mitten crab Eriocheir sinensis, which burrows into river banks leading to erosion and displaced sediment accumulates in navigation channels (Gollasch, 1999 and references therein). Alterations to water flow have been found also for large marine aquatic plants, such as Sargassum muticum (Kumatsu and Murakami, 1994). On rocky shores inside Antofagasta Bay (Northern Chile), the alien ascidian Pyura praeputialis creates broad belts providing

S. Olenin et al. / Marine Pollution Bulletin 55 (2007) 379–394

a novel mid-intertidal habitat which is used by mobile and vagile macro-invertebrates that otherwise would remain excluded from this intertidal level (Castilla et al., 2004). 2.4.4. Strong impact (H3) Large scale changes in the physical–chemical structure of key habitats, i.e. habitats which form significant expanses in a water body; these include spawning grounds, underwater sea grass meadows, and biogenic reefs. For example molluscs can modify habitats in coastal and transitional waters as well as lakes and rivers. In Europe, the American slipper limpet C. fornicata (Vallet et al., 2001), and the Pacific oyster Crassostrea gigas (Reise et al., 2006) alter soft sediments making these firmer from their vacant shells. In Argentina, an alien polychaete Ficopomatus enigmaticus forms extensive colonies that produce reef formations thereby altering the sediment transport and creation of reefs (Schwindt et al., 2001). The introduction of the bryozoan Membranipora membranipora to the subtidal reefs on the north-east coast of America caused the native kelps to atrophy and prematurely break away with a loss of space and shelter for epiphytic species (Grosholz, 2002). 2.4.5. Massive impact (H4) Such events are rare and are more noticeable within small isolated water bodies (ponds, lakes, coastal inlets) rather than in large open systems (transitional waters, coastal zones, seas). For example the invasion of the Louisiana red swamp crayfish Procambarus clarkii to a small shallow lake in Spain reduced plant cover by 99%; the lake became turbid, total phosphorus levels rose 800% and the water chlorophyll content increased by 100% (Rodrıguez et al., 2005). This case may also be used as example of the massive impact on ecosystem functioning (Section 2.5). From time to time changes in the physical–chemical properties of pelagic habitats may be provoked by severe outbreaks of alien planktonic algae and invertebrates altering water colour, oxygen and nutrient content, even over short periods of time, as in the case of blooms of the naked dinoflagellate Karenia mikimotoi (Ottway et al., 1979). Any alien species may have a full range of impacts according to the conditions and situations they have become exposed to. In one region AS may have no noticeable effect and elsewhere they may have strong impact as in the case of the Pacific oyster C. gigas. In Ireland and Britain the species recruits in low numbers (assessed as ‘‘No impact’’ and ‘‘Weak impact’’ respectively) (Minchin pers. ob.; Spencer et al., 1994), whereas along the southern coast of the North Sea they form extensive reefs (‘‘Strong impact’’) (Reise, 1998). The serpulid tubeworm F. enigmaticus in many regions forms intertwining calcareous growths that form small irregular clusters (‘‘Weak impact’’) but in some lagoons can form extensive reefs (‘‘Strong impact’’) (Orensanz et al., 2002).

385

2.5. Assessing impact on ecosystem functioning Bioinvasion may cause shifts in trophic nets and alteration of energy and organic material flow. Such events have been reported from freshwater, estuarine and marine coastal areas for different taxa: mysid shrimps (Ketelaars et al., 1999), crabs (Taylor and Eggleston, 2000), zooplankton crustaceans (Telesh and Ojaveer, 2002), molluscs (Heath et al., 1995; Karatayev et al., 2002), other benthic and pelagic invertebrates and fishes (Baltic Sea Alien Species Database, 2006 and references therein). Some invasions may provoke multiple effects which involve the overall ecosystem functioning (material flow between trophic groups, primary production, relative extent of organic material decomposition, extent of benthic–pelagic coupling). For example, alteration of the linkage between benthic and pelagic environment may evolve with the presence of abundant suspension feeders. The zebra mussels redistribute particulate matter from the water column to bottom sediments, this leads to particle trapping and siltation, decline in chlorophyll concentrations and increase in water transparency (e.g. Haas et al., 2002; Karatayev et al., 2002) and bioaccumulation of heavy metals and other toxic substances (Bruner et al., 1994). Probably, the best way to assess impact on ecosystem functioning would be to quantify the amount of energy channelled through the food web by an AS. However, such detailed studies as yet are very rare, therefore, we rank effects caused by AS using such qualitative categories as a functional group and ecosystem function (Text Box 5). We define a functional group as an assemblage of organisms with similar functional traits (mobility, feeding and reproduction mode, etc.) and an identical position in the ecosystem functional organisation (sensu Pearson, 2001). For example, sessile suspension feeders (mussels, barnacles, sponges, polychaetes, etc.) use suspended material in a near-bottom layer producing a downward energy flux and transferring particulated material from pelagic to benthic environment. Members of the same functional group perform similar functions within an ecosystem but may translocate different amounts of energy: e.g. barnacles, which have lower individual clearance rates, transfer less material when compared with that deposited by mussels. Reduction within a functional group does not usually result in shifts of energy transfer, should there be other species performing the same function. The addition of a new functional group, however, may create a new pathway of energy transfer within the ecosystem. This may take place when an active grazer (e.g. amphipod) arrives and enables transfer of benthic primary production to the next functional group or trophic level (e.g. fishes). Changes of functional groups within different trophic levels may lead to reorganisation of a food web, when existing relationships between group members are lost and new connections become established. Cascading effects known from previous introductions (e.g. Simon and Townsend, 2003; Crooks, 2002) explicitly demonstrate these types of changes in an ecosystem.

386

S. Olenin et al. / Marine Pollution Bulletin 55 (2007) 379–394

Text box 5. Classification of alien species impact on ecosystem functioning Code Impact E0 E1

E2

E3

E4

Description

No Weak

No measurable effect Measurable, but weak changes with no loss or addition of new ecosystem function(s) Moderate Moderate modification of ecosystem performance and/or addition of a new, or reduction of existing, functional group(s) in part of the assessment unit Strong Severe shifts in ecosystem functioning in part of the assessment unit. Reorganisation of the food web as a result of addition or reduction of functional groups within trophic levels Massive Extreme, ecosystem-wide shift in the food web and/or loss of the role of a functional group(s)

2.5.1. No impact (E0) In many cases, the presence of rare and not abundant AS do not noticeably change the ecosystem functioning. Usually these are small organisms, such as the brackish water hydrozoan Clavopsella navis or the filter feeding snail Calyptraea chinensis in some coastal bays of Ireland (Minchin et al., 1987). 2.5.2. Weak impact (E1) Situations when AS causes weak measurable changes to ecosystem functioning, where there is no loss or addition of new ecosystem function, i.e. diversity of functions is not changed. For example, addition of an alien suspension feeder to the ecosystem where the same function was performed by native species, as in the case of the barnacle E. modestus (Nehring, 2005). 2.5.3. Moderate impact (E2) Activities of AS result in an addition of new, or substantial changes to, existing ecosystem functions causing large scale changes in ecosystem processes. This, however, does not result in elimination of native functional groups. For example, an active alien suspension feeder causes clearance of phytoplankton in presence of native suspension feeders e.g. C. fornicata, C. gigas in some coastal areas of the NW Europe (Blanchard, 1996). Due to introduction of alien amphipods, C. curvispinum and Gammarus tigrinus, which became the dominant components of the diet of important benthivorous fish species, the food web was essentially changed in Lower Rhine (Kelleher et al., 1998). The same effect was observed in the pelagic food

web of the Gulf of Finland, where the Baltic herring (Clupea harengus membras) has changed its diet and now targets the alien water flea C. pengoi (Antsulevich and Va¨lipakka, 2000). 2.5.4. Strong impact (E3) Bioinvasion can cause severe shifts in ecosystem functioning, resulting from e.g. removing of functional group(s), cascading effects from introduced diseases, altering the abundance of keystone species, community and ecosystem. Such events may be temporal, occurring at the highest phase of expansion of an invader. For example the bivalve Musculista senhousia forms sufficiently dense cover and anoxic conditions over large expanses that exclude most native biota (Creese et al., 1997). Also, invasions may generate long lasting or even irreversible consequences, like in the case of Bonamia ostreae, a disease of the European native oyster Ostrea edulis, which caused severe decline of the populations and, as a consequence, destruction of native oyster bed ecosystems (Wolff and Reise, 2002). 2.5.5. Massive impact (E4) Invasion causes extreme changes in ecosystem functioning resulting from e.g. ecosystem wide shifts in energy and organic material flow. As it was mentioned above (Section 2.4), such events are rare and are more noticeable within small isolated water bodies rather than in large open systems. In extreme cases, introduction of diseases may cause the large scale extinction of a key ecosystem (e.g. L. zosterae causing loss of the sea grass Zostera marina meadows in many regions of North Atlantic) or total collapse in functioning caused by e.g. deoxygenation at a local scale, and for a short period, from the breakdown of an introduced algal species (Siddom, 2006). The most pronounced shifts in ecosystem functioning at the scale of the entire regional sea have been documented following the recent invasions of the American comb jelly M. leidyi to the Black and Caspian Seas (Volovik, 2000; Ivanov et al., 2000) causing sharp declines in zooplankton abundance and in landings of anchovies and other pelagic fish. Even if such large scale effects might not primarily have been caused by Mnemiopsis, but also due to combinations of overfishing and regime shifts in the plankton community due to eutrophication (Bilio and Niermann, 2004), the rapid expansion of the American comb jelly was clearly one of the causative factors for severe shifts in the ecosystem functioning (Kideys et al., 2005). 2.6. Biopollution level and the assessment support scheme The analysis of the AS impacts (Section 2.3–2.6) shows that they may be ranked according to the scale of the changes produced: from absence of any measurable impacts up to major shifts and even catastrophic perturbations in native community structure, habitat properties and ecosystem functioning. The integrated matrix relates the

S. Olenin et al. / Marine Pollution Bulletin 55 (2007) 379–394

magnitude of AS impacts in the above three categories (community, habitat and ecosystem) with its abundance and distribution range (ADR) (Table 2). Theoretically, the matrix produces 75 combinations, whilst 25 of them are highly unlikely. For instance, if an AS occurs in low numbers in one or several localities

387

(ADR A) it is unlikely that it may cause large scale displacement of native species, reduction of spatial extent of habitats and/or moderate changes in ecosystem functioning, let alone species extinctions, modification of all habitats and/or collapse in ecosystem functioning. In contrast, an AS occurring in high numbers in many or all

Table 2 Assessment of biopollution level (0–4) based on abundance and distribution range (ADR) and impacts of alien species on native species and communities, habitats and ecosystem functioning: ‘‘–’’ highly unlikely situations, explanation in text (for codes, see Text Boxes 1–4) ADR

Impact on Species and communities

A B C D E

Habitats

Ecosystem functioning

C0

C1

C2

C3

C4

H0

H1

H2

H3

H4

E0

E1

E2

E3

E4

0 1 1 – –

1 1 1 2 –

– 2 2 2 3

– – – 3 3

– – – 4 4

0 1 1 – –

1 1 2 2 2

– 2 2 3 3

– 3 3 3 3

– – 4 4 4

0 1 1 – –

1 1 2 2 2

– 2 2 2 3

– – – 3 3

– – – 4 4

ADR Class A. Low numbers in one or several localities

Impact (Code) No (C0, H0, E0) Weak (C1, H1, E1)

B. Low numbers in many localities or moderate numbers in one or several localities or high numbers in one locality

No (C0, H0, E0) or Weak (C1, H1, E1) Moderate (C2, H2, E2) Strong (H3)

C. Low numbers in all localities, or moderate numbers in many localities, or high numbers in several localities

No (C0, H0, E0) or Weak (C1) Weak (H1, E1) or Moderate (C2, H2, E2)

BPL 0 1 1 2 3 1 2 3

Strong impact (H3) Massive impact (H4)

D. Moderate numbers in all localities, or high numbers in many localities

Weak (C1, H1, E1) or Moderate (C2, E2) Moderate (H2) or Strong (C3, H3, E3)

4

2 3 4

Massive (C4, H4, E4)

E. High numbers in all localities

Weak (H1, E1) Moderate (C2, H2, E2) or Strong (C3, H3, E3) Massive (C4, H4, E4)

2 3 4

Fig. 2. The decision support scheme for assessment of biopollution level (BPL). Explanation in text.

388

S. Olenin et al. / Marine Pollution Bulletin 55 (2007) 379–394

localities (ADR D and E) will definitely cause at least some changes in the community structure and/or ecosystem performance, hence, situation of ‘‘No measurable impact’’ is very unlikely. Thus, discrimination of 25 highly unlikely combinations of ADR and impacts leaves 50 possible situations for which biopollution may be assessed. In order to make the assessment system operable we narrowed down these situations to five Biopollution Levels (BPL): 0 – No; 1 – Weak, 2 – Moderate, 3 – Strong and 4 – Massive. These five BPL are distinguished using the case studies described above (Section 2.3–2.6), the literature database created for this study (including papers not referred to here) and the expert evaluation of likelihood and magnitude of impacts of AS at certain ADR classes. Several situations correspond to one and the same biopollution level: there are three situations corresponding to BPL 0, 13 to BPL 1, 15 to BPL 2, 12 to BPL 3 and 7 to BPL 4. If no alien species are present in the ecosystem then a priori the BPL = 0. The generalised decision support system for assessment of BPL is given in Fig. 2. The BPL should be assessed for a defined water body (assessment unit) and for a defined period of time (assessment period). The assessment should be performed for each AS known for the given assessment unit. It is highly unlikely that species, causing more or less serious changes in the invaded system (i.e. BPL > 1) would remain unnoticed. The BPL is determined according to the greatest impact level. For example, if ADR for an AS is defined as ‘‘B’’ (an AS occurs in low numbers in many localities or in moderate numbers in one or several localities or in high numbers in one locality) then the next step is to evaluate the impact. Let us assume that this AS causes local displacement of native species (impact on native species/communities – C1), moderate changes in the physical structure of habitats (impact on habitats – H2) and weak, but measurable changes with no loss or addition of new ecosystem functions (impact on ecosystem functioning – E1). The final assessment for this AS is determined according to the highest impact (in this case, the impact on habitats – H2) and BPL = 2. The overall BPL for the assessment unit is determined according to the greatest impact level for at least one species which was noticed during the evaluation period. For instance, if for a 5-year assessment period, BPL was low (BPL 6 1) for 20 AS, but at least one species once showed BPL = 3, then the BPL for the assessment unit would be 3. 3. Application of the biopollution assessment method 3.1. Data availability and types of assessment To demonstrate the application of the biopollution assessment method we use an example from the comparatively well studied region, the Curonian Lagoon and the open south-eastern coastal zone of the Baltic Sea (Fig. 3). Within this region we consider four areas, which were distinguished according to WFD recommendations for

Fig. 3. Four Lithuanian coastal areas for which the biopollution assessment was made: (a) south-eastern Baltic coastal zone, (b) Klaipeda port area, (c) northern part of the Curonian Lagoon, (d) central part of the Lagoon.

coastal typology based on the analysis of the abiotic conditions, benthic biotope and long-term community data (Olenin and Daunys, 2004, and references therein). The areas have been studied since early 1920s; the comprehensive recent overviews are available on benthic biotopes and communities (Olenin and Daunys, 2004), composition of native biota (Zettler and Daunys, in press) and invasion biology (Olenin and Leppa¨koski, 1999; Olenin, 2005; Daunys and Zettler, 2006; Daunys et al., 2006; Baltic Sea Alien Species Database, 2006, and references therein). The selected areas (assessment units) differ in their environment, composition of native biota and level of anthropogenic impact. The open coast is characterised by comparatively stable salinity (6.0–8.0 psu); extreme wave exposure; sandy, gravel and stony seabed, gently sloping from 0 to 25–30 m. Due to unfavourable salinity conditions (too low for many marine species), the native species richness is lowest here in comparison with other areas. The Klaipeda Port occupies the outlet of the Curonian Lagoon. This area is artificially deepened (14 m) and is characterised by a rapid and irregularly changing salinity (<0.5–8.0 psu), variety of bottom substrates (sand, moraine clay, mud and

S. Olenin et al. / Marine Pollution Bulletin 55 (2007) 379–394

artificial hard surfaces), strong anthropogenic impacts (eutrophication, dredging, industrial and municipal wastes) and has mixture of ‘‘marine’’ (brackish) and freshwater native species. The northern and central parts of the Curonian Lagoon (mean depths 3 m) differ in the salinity regime: there are slight (0.5–3.0 psu) salinity fluctuations in the northern part, while the central area the conditions are limnetic. Both areas accommodate high numbers of native species, however in the central part only limnetic species occur. Using available data we demonstrate the application of the biopollution index for a baseline assessment and a management assessment. The baseline assessment is made for the period before 1985. This year was chosen arbitrarily aiming to summarise all existing information on impacts of AS and evaluate the general level of biopollution in the four selected areas. The second assessment is made for the period from 1986 to 2005 with the aim to reveal changes in BPL from the time when the baseline assessment was made. This is called management assessment because, presumably, some management measures could have been applied to minimise risk of future introductions. In general, such management assessments should help not only to monitor changes but also evaluate the efficacy of the alien species control systems. 3.2. The baseline biopollution assessment There are 29 AS recorded in the Curonian Lagoon and the adjacent coastal zone; 25 of them are established; at least 20 species were introduced prior to 1985 (Baltic Sea Alien Species Database, 2006). Most of AS occur in low numbers in one or several localities and have no measurable impact on native species/communities, habitats or ecosystem functioning, hence their BPL = 0. The AS which cause a noteworthy impact (P1) at least in one of the four assessment units are listed in Table 3. The BPL defined for the same AS in different assessment varies in large extent. For example, the zebra mussel Dreissena polymorpha is not present at the open coast (BPL = 0); it occurs in low numbers in several localities in Klaipeda Port (ADR A) and causes local changes in physical structure of habitats by creating small amount of shell deposits on sites (H1), thus, for the port area – BPL = 1. In the northern part of the Lagoon, D. polymorpha occurs in moderate numbers in many localities and in high numbers on sites (ADR C), it causes moderate changes in type-specific communities of native benthic species, displacing native unionids and changing soft bottom communities (C2); clusters of living zebra mussels and it shell deposits occupy reasonable portions of the former soft bottoms (H2); filtering activity of D. polymorpha moderately effects the budget of total particulated material in this part of the Lagoon (E2) (details in, Daunys et al., 2006), the BPL = 2. Finally, the zebra mussel occurs in high numbers in many localities (ADR D) and its shell deposits and large clusters

389

of living molluscs occupy most of the bottom in the central part of the Lagoon (H3). Hence, for this assessment unit the biopollution level caused by the zebra mussels is defined as strong (BPL = 3). The results of the baseline assessment show that, in overall, the biopollution level is defined as moderate (BPL = 2) for the open coast, Klaipeda Port and the northern part of the Curonian Lagoon, while in the central part it is defined as strong (BPL = 3). However, the number of AS causing measurable effect (BPL P 1) is different in the four assessment units, gradually increasing from the open coast towards the inner part of the Lagoon (Fig. 4). This increase in number of the impacting species corresponds well with results of another recent study showing that habitats of the coastal lagoons, generally, contain much more xenodiversity than the open sea coasts (Zaiko et al., in press). 3.3. The management biopollution assessment For the management assessment all AS are included within each of the four areas and a BPL assessment made. In this case all species recorded up to 1985 were still present in 2005 without having changed their abundance/distribution range or impacts on native communities, habitats or ecosystems. These species were not listed in the Table 3. However, there were five additional species in the twenty year period since 1985 (Table 3). All five recently introduced AS were recorded in the port area and the northern part of the Lagoon. No new AS were recorded in the central part of the Lagoon. The most impacting was the arrival of the spionid polychaete M. neglecta, which appeared in moderate numbers in many localities in the open coast (on sites in high numbers, ADR C) and caused moderate changes in community structure, habitats and ecosystem functioning (C2, H2, E2). In Klaipeda Port and northern part of the Lagoon, this polychaete occurs in moderate numbers in several localities, however, due to its burrowing activity (which is unique for these areas, details in Olenin and Leppa¨koski, 1999; and Daunys, 2001) the large scale changes in the physical structure of habitats were produced, leading to a strong biopollution level of three (BPL = 3). Two plankton species, the water flea C. pengoi and the dinoflagellate P. minimum, on account of their abundance caused outbreaks in 1999 (C. pengoi) and in 1995, 1997 and 2000 (P. minimum) which resulted in changes in type-specific plankton communities and modification of habitats (e.g. changes in water colour at the time of peak abundance). An alien fish, the round goby Neogobius melanostomus appeared in the Klaipeda Port area in 2002 and it was later found in a few localities along the nearby open coastal area and within the Curonian Lagoon. This goby has a low abundance with no known impact, in the port and lagoon areas, and a weak effect on local fish communities along the coast (J. Maksimov, pers. com.). Finally, the North American amphipod G. tigrinus was found in

390

Table 3 Baseline and management assessments of biopollution level (BPL) for alien species in four assessment units of the Baltic Sea South-eastern open coast, Baltic Sea

Curonian Lagoon Klaipeda Port

Baseline assessment to 1985 Balanus improvisus Chaetogammarus warpachowskyi Cordylophora caspia Chelicorophium curvispinum Dreissena polymorpha Limnomysis benedeni Obesogammarus crassus Paramysis lacustris Pontogammarus robustoides

ADR

Impacts

C –

C2 –

H1 –

B –

C1 –

– – – – –

Management assessment 1986–2005 Cercopagis pengoi C Gammarus tigrinus – Marenzelleria neglecta C Neogobius melanostomus A Prorocentrum minimum C

Northern part

BPL

ADR

Impacts

E1 –

2 0

A –

C1 –

H1 –

H2 –

E1 –

2 0

C –

C2 –

– – – – –

– – – – –

– – – – –

0 0 0 0 0

A – B A B

C2 – C2 C1 C2

H2 – H2 H0 H2

E2 – E2 E0 E1

2 0 2 1 2

B B B A A

Central part

BPL

ADR

Impacts

BPL

ADR

Impacts

E0 –

1 0

A B

C1 C1

H1 H1

H2 –

E1 –

2 0

B B

C0 C1

C0 – C1 C0 C1

H1 – H1 H0 H1

E0 – E1 E0 E1

1 0 1 0 1

C B C C B

C2 C1 C1 C0 C0

H1 H1 H3 H0 H0

E1 E1 E2 E0 E0

2 1 3 0 0

B B B A A

E0 E1

1 1

– B

– C2

– H2

– E1

0 2

H1 H1

E0 E1

1 1

– C

– C1

– H2

– E1

0 2

C2 C2 C2 C2 C1

H2 H1 H2 H1 H2

E2 E2 E2 E2 E2

2 2 2 2 2

D B B C B

C2 C2 C2 C2 C1

H3 H1 H2 H1 H2

E2 E2 E2 E2 E2

3 2 2 2 2

C2 C1 C1 C0 C0

H1 H1 H3 H0 H0

E1 E1 E2 E0 E0

2 1 3 0 0

– – – – –

– – – – –

– – – –

– – – – –

0 0 0 0 0

ADR – Abundance and Distribution Range; – species is not present. Impacts on: native species and communities (C), habitats (H) and ecosystem functioning (E). Explanation in text.

BPL

S. Olenin et al. / Marine Pollution Bulletin 55 (2007) 379–394

Alien species

S. Olenin et al. / Marine Pollution Bulletin 55 (2007) 379–394

7

Baseline

391

Management

No. of alien species

6 5 4 3 2 1 0 1

2

Coast

3

1

2

Port

3

1

2

3

1

2

3

Northern Lagoon Central Lagoon

Fig. 4. Number of alien species causing weak (BPL-1), moderate (BPL-2) and strong (BPL-3) biopollution in the four assessment units: open coast of the south-eastern Baltic (Coast), Klaipeda Port area (Port), Northern and Central parts of the Curonian Lagoon revealed in the baseline (up to 1985) and management (1986–2005) assessments.

moderate numbers in several localities in the Klaipeda Port area and in the northern part of the Curonian Lagoon in 2004, causing weak impact on invaded communities and habitats. Thus, according to the results of the management assessment for the period 1986–2005 the biopollution level has increased in the open coast, Klaipeda Port and northern part of the Lagoon (from BPL 2 to BPL 3), while in the central part it remained the same. The total number of AS species causing remarkable effect (BPL > 1) increased in three assessment units and remained the same in the central part of the Lagoon (Fig. 4). 4. Discussion We have developed a method based on abundance and distribution of AS, to group their relative impact, using an index of five classes. The assessment of AS’ impact on a water body is based on the AS effects on native species, their communities, habitats and ecosystems. While using this method, those species with lower levels of impact do not influence the final assessment. This makes an evaluation both practical and rapid to undertake for water bodies but it does require a basic knowledge of the impacting species present within the chosen assessment unit. For those areas where such information is lacking the required data may be gathered rapidly because the most impacting species that is used in the assessment should be easily recognised. In our example, we examined an area of the Baltic Sea on account of the available knowledge, in order to conduct both a spatial and temporal evaluation. Such detailed information may not be available for some regions, although the impacts of the most impacting AS should be known, so making a basic assessment possible.

The initial baseline assessment allowed us to determine the status quo, while the subsequent management assessment has shown how the situation has changed over a 20 year period. Five recently introduced alien species appeared and the overall biopollution levels in two of the four areas have increased from a BPL = 2 to a BPL = 3. All five newcomers primarily have been introduced elsewhere in the Baltic Sea and then spread to the Lithuanian coastal waters of the south-eastern Baltic and the Curonian Lagoon (Baltic Sea Alien Species Database, 2006, and references therein). This secondary spread probably was natural (due to sea currents), but it also could be facilitated by shipping. For example, the round goby was first found at the breakwaters of Klaipeda Port (Olenin, pers. ob.) and only then in the adjacent sea and Lagoon localities. The nearest area, where Neogobius is known from (the Gulf of Gdansk) is separated from Klaipeda Port by a large coastal area along the Curonian Spit still free of this species. However, most probably, these changes in biopollution could not have been prevented because secondary spread of AS was beyond the present control capability. The ability to manage depends on accurate knowledge of the pathways and vectors involved in movement coupled with the lifehistory strategies of species that will determine their rate of spread (ICES, 2005; Minchin, 2006). The ability to manage will also depend on the development of effective rapid assessment surveys, search for target species of consequence and a good knowledge of species occurring in neighbouring regions. There are many circumstances that enable AS to avail of changing situations depending on their life mode and physiological tolerance. Anthropogenic activities, such as chemical and nutrient discharges and dredging, and/or climate change alter the pathways of arrival (ICES, 2005). Such

392

S. Olenin et al. / Marine Pollution Bulletin 55 (2007) 379–394

changes ensure AS will continue to colonise and have impact. Likewise, alterations in climate are expected to result in changes to species ranges as well as to provide new opportunities for AS. We are also aware that AS can alter the biological, chemical and physical parameters, of the water quality elements as appear in the WFD, in rivers, lakes, transitional and coastal waters which in turn may promote changed conditions for further invasion. Ironically in tandem with improvements of water quality under the implementation of the WFD an increase in the arrival of AS may be expected because of reduced challenges for all life-history stages. The five-scale biopollution index needs to be further compared with the five different levels of water quality as they appear in the WFD, ranging from high to bad water quality status. We are presenting here an early stage of a possible biopollution ranking. Whilst assessment of some cases (cryptogenic species, parasites and diseases) still pose difficulties and there might be other situations that are presently not covered by our method, where a review may be necessary. The robustness of the biopollution assessment method presented here should be tested in other regions, and for different species, before its use in management can be routinely accepted. For example, a replacement of a native species by a morphologically and functionally similar species poses difficulties for measurement, as do cryptogenic species and some introduced parasites and diseases. It may be necessary to review this scheme to consider in more details the special circumstances of some major groups such as phytoplankton, zooplankton, macrobenthos and fishes. Nevertheless we consider that the method we have developed may have a useful application for comparing relative impacts and for measuring change for many introduced biota. Acknowledgements We would like to thank Angel Borja of the Department of Oceanography and Marine Ecosystems, Spain for helpful discussion; Adam Petrusek of Charles University, Prague, Czech Republic; Stephan Gollasch of GoConsult, Hamburg, Germany; Petr Pysˇek of the Academy of Sciences of the Czech Republic and two anonymous reviewers for valuable comments on earlier drafts; Irina Ovcharenko of Klaip_eda University for technical assistance in development of the literature database on alien species impacts. This study was supported by the EU Framework 6 Integrated Project 506675 ALARM ‘‘Assessing Large-scale environmental risks with tested methods’’ and project CT 2003-511202 DAISIE ‘‘Delivering Alien Species Inventory for Europe’’. References Antsulevich, A., Va¨lipakka, P., 2000. Cercopagis pengoi – a new important food object of the Baltic herring in the Gulf of Finland. International Revue of Hydrobiology 85 (5–6), 609–619.

Baltic Sea Alien Species Database, 2006. In: Olenin, S., Leppa¨koski, E., Daunys, D. (Eds.), (accessed online 18.02.06). Bilio, M., Niermann, U., 2004. Is the comb jelly really to blame for it all? Mnemiopsis leidyi and the ecological concerns about the Caspian Sea. Marine Ecology Progress Series 269, 173–183. Blanchard, M., 1996. Spread of the slipper limpet Crepidula fornicata (L.) 1758 in Europe. Current state and consequences. Scientia Marina 61, 109–118. Bonsdorff, E., 1981. Notes on the occurrence of Polychaeta (Annelida) in the archipelago of Aland, SW Finland. Memoranda Society Fauna Flora Fennica 57, 141–146. Borja, A., Galparsoro, I., Solaun, O., Muxika, I., Tello, E.T., Uriarte, A., Valencia, V., 2006. The European Water Framework Directive and the DPSIR, a methodological approach to assess the risk of failing to achieve good ecological status. Estuarine Coastal and Shelf Science 66 (1–2), 84–96. Boudouresque, C.F., Verlaque, V.M., 2002. Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Marine Pollution Bulletin 44 (1), 32–38. Britton-Simmons, K.H., 2004. Direct and indirect effects of the introduced alga Sargassum muticum on benthic and subtidal communities of Washington State, USA. Marine Ecology Progress Series 277, 61– 78. Bruner, K.A., Fisher, S.W., Landrum, P.F., 1994. The role of the zebra mussel, Dreissena polymorpha, in contaminant cycling: II. Zebra mussel contaminant accumulation from algae and suspended particles, and transfer to the benthic invertebrate, Gammarus fasciatus. Journal of Great Lakes Research 20, 735–750. Carlton, J., 2002. Bioinvasion ecology: assessing invasion impact and scale. In: Leppa¨koski, E., Gollasch, S., Olenin, S. (Eds.), Invasive Aquatic Species of Europe – Distribution, Impacts and Management. Kluwer Academic Publications, Dordrecht, Boston, London, pp. 7–19. Carlton, J.T., Geller, J.B., Reaka-Kudla, M.L., Norse, E.A., 1999. Historical extinctions in the sea. Annual Review of Ecological Systematics 30, 515–538. Castilla, J.C., Lagos, N.A., Cerda, M., 2004. Marine ecosystem engineering by the alien ascidian Pyura praeputialis on a mid-intertidal rocky shore. Marine Ecology Progress Series 268, 119–130. Cohen, A., 2006. Species introductions and the Panama Canal. In: Gollasch, S., Galil, B., Cohen, A.N. (Eds.), Bridging Divides: Maritime Canals as Invasion Corridors, . In: Monographiae Biologicae, vol. 83. Springer, Dordrecht, pp. 127–206. Colautti, R.I., MacIsaac, H.J., 2004. A neutral terminology to define ‘invasive’ species. Diversity and Distributions 10 (2), 135–141. Costello, M.J., Emblow, C., White, R., 2001. European register of marine species. A check-list of marine species in Europe and a bibliography of guides to their identification. Patrimoines Naturels 50, 1–463. Creese, R., Hooker, S., De Luca, S., Wharton, Y., 1997. Ecology and environmental impact of Musculista senhousia (Mollusca: Bivalvia: Mytilidae) in Tamaki Estuary, Auckland, New Zealand. New Zealand Journal of Marine and Freshwater Research 31, 225–236. Crooks, J.A., 2002. Characterising ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97 (2), 153–166. Cuddington, K., Hastings, A., 2004. Invasive engineers. Ecological Modelling 178, 335–347. Daunys, D., 2001. Patterns of the bottom macrofauna variability and its role in the shallow coastal lagoon. Doctorate dissertation. Klaipeda University, Klaipeda, Lithuania, 115pp. Daunys, D., Zettler, M.L., 2006. Invasion of the North American amphipod (Gammarus tigrinus Sexton, 1939) into the Curonian Lagoon, south-eastern Baltic Sea. Acta Zoologica Lithuanica 16 (1), 20–26. Daunys, D., Zemlys, P., Olenin, S., Zaiko, A., Ferrarin, C., 2006. Impact of the zebra mussel Dreissena polymorpha invasion on the budget of suspended material in a shallow lagoon ecosystem. Helgoland Marine Research 60 (2), 113–120.

S. Olenin et al. / Marine Pollution Bulletin 55 (2007) 379–394 Elliott, M., 2003. Biological pollutants and biological pollution – an increasing cause for concern. Marine Pollution Bulletin 46, 275–280. EUNIS. 2006. European Nature Information System. EEA, European Environment Agency. . Fifas, S., Dao, J-C., Boucher, J., 1990. Un mode`le empirique de recruitment por le stock de coquilles Saint_Jacques, Pecten maximus (L.) en baie de Saint Brieuc (Manche, France). Aquatic Living Resources 3 (1), 13–28. Garcia-Berthou, E., Moreno-Amich, R., 2000. Introduction of exotic fish into a Mediterranean lake over a 90-year period. Archiv fuer Hydrobiologie 149 (2), 271–284. Gasiunaite, Z.R., Didziulis, V., 2002. Ponto-Caspian Invader Cercopagis pengoi (Ostroumov, 1891) in the Lithuanian Coastal Waters. Sea and Environment 2, 97–101. Gollasch, S., 1999. Eriocheir sinensis. In: Gollasch, S., Minchin, D., Rosenthal, H., Voigt, M. (Eds.), Exotics Across the Ocean. Case Histories on Introduced Species: Their General Biology, Distribution, Range Expansion and Impact. Logos Verlag, Berlin, pp. 55–60. Gophen, M., Ochumba, P.B.O., Kaufman, L.S., 1995. Some aspects of perturbation in the structure and biodiversity of the ecosystem of Lake Victoria (East Africa). Aquatic Living Resources 8 (1), 27–41. Grosholz, E., 2002. Ecological and evolutionary consequences of coastal invasions. Trends in Ecology and Evolution 17 (1), 22–27. Guidance document, 2003. Common implementation strategy for the Water Framework Directive (2000/60/EC). Transitional and Coastal Waters – Typology, Reference Conditions and Classification Systems. Produced by WG 2.4. – COAST. Guidance document No 5. Luxemburg: Office for Official Publications of the European Communities, 107pp. Haas, G., Brunke, M., Streit, B., 2002. Fast turnover in dominance of exotic species in the Rhine River determines biodiversity and ecosystem function: an affair between amphipods and mussels. In: Leppa¨koski, E., Gollasch, S., Olenin, S. (Eds.), Invasive Aquatic Species of Europe – Distribution, Impacts and Management. Kluwer Academic Publications, Dordrecht, Boston, London, pp. 426–432. Hajdu, S., Edler, L., Olenina, I., Witek, B., 2000. Spreading and establishment of the potential toxic dinoflagellate Prorocentrum minimum in the Baltic Sea. International Review of Hydrobiology 85, 561–575. Heath, R.T., Fahnenstiel, G.L., Gardner, W.S., Cavaletto, J.F., Hwang, S.-J., 1995. Ecosystem-level effects of zebra mussel (Dreissena polymorpha): an enclosure experiment in Saginaw Bay, Lake Huron. Journal of Great Lakes Research 21 (4), 501–516. Hiscock, K., Elliott, M., Laffoley, D., Rogers, S., 2003. Data use and information creation: challenges for marine scientists and for managers. Marine Pollution Bulletin 46 (5), 534–541. Hulsmann, N., Galil, B.S., 2002. Protists – a dominant component of the ballast-transported biota. In: Leppa¨koski, E., Gollasch, S., Olenin, S. (Eds.), Invasive Aquatic Species of Europe – Distribution, Impacts and Management. Kluwer Academic Publications, Dordrecht, Boston, London, pp. 20–26. ICES, 2005. Vector pathways and the spread of exotic species in the sea. International Council for Exploration of the Seas. ICES Co-operative Report No. 271, 25pp. IUCN, 1999. IUCN guidelines for the prevention of biodiversity loss due to biological invasions. Newsletter of the Species Survival Commission IUCN – The World Conservation Union 31, pp. 28–42. Ivanov, V.P., Kamakin, A.M., Ushivtzev, V.B., Shiganova, T., Zhukova, O., Aladin, N., Wilson, S.I., Harbison, G.R., Dumont, H.J., 2000. Invasion of the Caspian Sea by the comb jellyfish Mnemiopsis leidyi (Ctenophora). Biological Invasions 2, 255–258. Jones, C.G., Lawton, J.H., Shachak, M., 1994. Organisms as ecosystem engineers. Oikos 69 (3), 373–386. Karatayev, A.Y., Burlakova, L.E., Padilla, D.K., 2002. Impacts of zebra mussels on aquatic communities and their role as ecosystem engineers. In: Leppa¨koski, E., Gollasch, S., Olenin, S. (Eds.), Invasive Aquatic Species of Europe – Distribution, Impacts and Management. Kluwer Academic Publications, Dordrecht, Boston, London, pp. 433–446.

393

Karpevich, A.F., 1975. Theory and Practice of Acclimatization of Aquatic Organisms. Pischevaya Promishlennost Press, Moscow, 431pp (in Russian). Kelleher, B., Bergers, P.J.M., van den Brink, F.W.B., Giller, P.S., van der Velde, G., de Vaate, A.B., 1998. Effects of exotic amphipod invasions on fish diet in the Lower Rhine. Archiv fuer Hydrobiologie 143 (3), 363–382. Ketelaars, H.A.M., Lambregts-van de Clundert, F.E., Carpentier, C.J., Wagenvoort, A.J., Hoogenboezem, W., 1999. Ecological effects of the mass occurrence of the Ponto-Caspian invader, Hemimysis anomala G.O. Sars, 1907 (Crustacea: Mysidacea), in a freshwater storage reservoir in the Netherlands, with notes on its autecology and new records. Hydrobiologia 394, 233–248. Kideys, A.E., 2002. The comb jelly Mnemiopsis leidyi in the Black Sea. In: Leppa¨koski, E., Gollasch, S., Olenin, S. (Eds.), Invasive Aquatic Species of Europe – Distribution, Impacts and Management. Kluwer Academic Publications, Dordrecht, Boston, London, pp. 56–61. Kideys, A.E., Roohi, A., Bagheri, S., Finenko, G., Kamburska, L., 2005. Impacts of invasive ctenophores on the fisheries of the Black Sea and Caspian Sea. Oceanography 18 (2), 76–85. Kotta, J., Orav, H., Sandberg-Kilpi, E., 2001. Ecological consequence of the introduction of the polychaete Marenzelleria cf. viridis into a shallow-water biotope of the northern Baltic Sea. Journal of Sea Research 46, 273–280. Kumatsu, T., Murakami, S.-I., 1994. Influence of a Sargassum forest on the spatial distribution of water flow. Fisheries Oceanography 3, 256–266. Leppa¨koski, E., Olenin, S., 2000. Xenodiversity of the European brackish water seas: the North American contribution. In: J. Pederson Marine Bioinvasions: Proc. First National Conference, Massachusetts Institute of Technology, January 24–27, pp. 107–119. Meinesz, A., 1999. Killer Algae. University of Chicago Press, Chicago, 359pp. Minchin, D., 1999. Crepidula fornicata (Linnaeus, 1758), Calyptraeidae, Gastropoda. In: Gollasch, S., Minchin, D., Rosenthal, H., Voigt, M. (Eds.), Exotics Across the Ocean. Case Histories on Introduced Species. Logos Verlag, Berlin, Germany, p. 74. Minchin, D., 2006. The transport and spread of living aquatic species. In: Davenport, J., Davenport, J.L. (Eds.), The Ecology of Transportation: Managing Mobility for the Environment. Springer, Dordrecht, pp. 77– 97. Minchin, D., Duggan, C.B., McGrath, D., 1987. Calyptraea chinensis (Mollusca: Gastropoda) on the west coast of Ireland: a case of accidental introduction. Journal of Conchology 32 (5), 297–302. Muehlstein, L.K., 1989. Perspectives in the wasting disease of eelgrass Zostera marina. Diseases of Aquatic Organisms 7, 211–221. Nehring, S., 2005. International shipping – a risk for aquatic biodiversity in Germany. In: Nentwig, W. (Ed.), Biological Invasions – From Ecology to Control. Neobiota 6, pp. 125–144. ´ lafsson, E., 2003. Competition between the Neideman, R., Wenngren, J., O introduced polychaete Marenzelleria sp. and the native amphipod Monoporeia affinis in Baltic soft bottoms. Marine Ecology Progress Series 264, 49–55. Occhipinti-Ambrogi, A., Galil, B.S., 2004. A uniform terminology on bioinvasions: a chimera or an operative tool? Marine Pollution Bulletin 49, 688–694. Olenin, S., 2005. Invasive Aquatic Species in the Baltic States Monograph. E. Leppa¨koski & D. Minchin (reviewers). Klaip_eda University Press, Klaipeda, 42p. Olenin, S., Daunys, D., 2004. Coastal typology based on benthic biotope and community data: the Lithuanian case study. In: Schernwski, G., Wielgat, M., (Eds.), Baltic Sea Typology. Coastline Reports 4, pp. 65–83. . Olenin, S., Ducrotoy, J.-P., 2006. The concept of biotope in marine ecology and coastal management. Marine Pollution Bulletin 53, 20–29. Olenin, S., Leppa¨koski, E., 1999. Non-native animals in the Baltic Sea: alteration of benthic habitats in coastal inlets and lagoons. Hydrobiologia 393, 233–243.

394

S. Olenin et al. / Marine Pollution Bulletin 55 (2007) 379–394

Orensanz, J.M., Schwindt, E., Pastorino, G., Bortolus, A., Casas, G., Darrigan, G., Elı´as, R., Lo´pez Gappa, J.J., Obernat, S., Pascual, M., Penchaszadeh, P., Piriz, M.L., Scarabino, F., Spivak, E.D., Vallarino, E.A., 2002. No longer the pristine confines of the world ocean: a survey of exotic marine species in the southwestern Atlantic. Biological Invasions 4 (1–2), 115–143. Orlova, M., Telesh, I., Berezina, N., Antsulevich, A., Maximov, A., Litvinchuk, L., 2006. Effects of nonindigenous species on diversity and community functioning in the eastern Gulf of Finland (Baltic Sea). Helgoland Marine Research 60 (2), 98–105. Ottway, B., Parker, M., McGrath, D., Crowley, M., 1979. Observations on a bloom of Gyrodinium aureolum Hulbert on the south coast of Ireland, summer 1976, associated with mortalities of littoral and sublittoral organisms. Irish Fisheries Investigations Series B (18), 9. Payton, I.J., Fennel, M., Lee, W.G., 2002. Keystone species: the concept and its relevance for conservation management in New Zealand. Science for Conservation, 203. Department of Conservation, Wellington, New Zealand, 29pp. . Pearson, T.H., 2001. Functional group ecology in soft-sediment marine benthos: the role of bioturbation. Oceanography and Marine Biology. An Annual Review 39, 233–267. Posey, M.H., 1988. Community changes associated with the spread of an introduced seagrass, Zostera japonica. Ecology 69 (4), 974–983. Quiniou, F., Blanchard, M., 1987. Etat de la proliferation de la crepidule (Crepidula fornicata L.) dans le secteur de Granville (Golfe NormanoBreton, 1985). Haliotus 16, 513–525. Ralph, P.J., Short, F.T., 2002. Impact of wasting disease pathogen, Labyrinthula zosterae, on the photobiology of eelgrass Zostera marina. Marine Ecology Progress Series 226, 265–271. Reise, K., 1998. Pacific oysters invade mussel beds in the European Wadden Sea. Senckenbergiana Maritima 28, 167–175. Reise, K., Olenin, S., Thieltges, D.W., 2006. Are aliens threatening European aquatic coastal ecosystems? Helgoland Marine Research 60 (2), 106–112. Rodrıguez, C.F., Becares, E., Fernandez-Alaez, M., Fernandez-Alaez, C., 2005. Loss of diversity and degradation of wetlands as a result of introducing exotic crayfish. Biological Invasions 7, 75–85. Rolauffs, P., Stubauer, I., Zahra´dkova´, S., Brabec, K., Moog, O., 2004. Integration of the saprobic system into the European Union Water Framework Directive – Case studies in Austria, Germany and Czech Republic. Hydrobiologia 516 (1–3), 285–298. Schwindt, E., Bortolus, A., Iribarne, O.O., 2001. Invasion of a reef-builder polychaete: direct and indirect impacts on the native benthic community structure. Biological Invasions 3, 137–149.

Siddom, J., 2006. Harmful algae: a review of HAB species in northern European waters with emphasis on the possible development of a fuzzy logic expert system. NCOF, Technical report 3, 21pp. (accessed 22.11.06). Simon, K.S., Townsend, C.R., 2003. Impacts of freshwater invaders at different levels of ecological organisation, with emphasis on salmonids and ecosystem consequences. Freshwater Biology 48 (6), 982–995. Spencer, B.E., Edwards, D.B., Kaiser, M.J., 1994. Spatfalls of the nonnative Pacific oyster, Crassostrea gigas in British waters. Aquatic Conservation: Marine and Freshwater Ecosystems 4, 203–217. Taylor, D.L., Eggleston, D.B., 2000. Effects of hypoxia on an estuarine predatorprey interaction: foraging behavior and mutual interference in the blue crab Callinectes sapidus and the infaunal clam prey Mya arenaria. Marine Ecology Progress Series 196, 221–237. Telesh, I.R., Ojaveer, H., 2002. The predatory water flea Cercopagis pengoi in the Baltic Sea: invasion history, distribution and implications to ecosystem dynamics. In: Leppa¨koski, E., Gollasch, S., Olenin, S. (Eds.), Invasive Aquatic Species of Europe – Distribution, Impacts and Management. Kluwer Academic Publications, Dordrecht, Boston, London, pp. 62–65. Vallet, C., Dauvin, J.C., Hamon, D., Dupuy, C., 2001. Effect of the introduced common slipper shell on the suprabenthic biodiversity of the subtidal communities in the Bay of Saint-Brieuc. Conservation Biology 15 (6), 16–86. Volovik, S.P., 2000. Ctenophore Mnemiopsis leidyi (A. Agassiz) in the Azov and Black Seas: Its Biology and Consequences of Its Intrusion. State Fisheries Commission of Russian Federation, Rostov-on-Don, 497pp (in Russian). Wallentinus, I., Nyberg, C.D., this volume. Introduced marine organisms as habitat modifiers. Marine Pollution Bulletin. Williamson, M., 1996. Biological Invasions. Chapman & Hall, London, 244pp. Wolff, W.J., Reise, K., 2002. Oyster imports as a vector for the introduction of alien species into northern and western European coastal waters. In: Leppa¨koski, E., Gollasch, S., Olenin, S. (Eds.), Invasive Aquatic Species of Europe – Distribution Impacts and Management. Kluwer Academic Publications, Dordrecht, Boston, London, pp. 193–205. Zaiko, A., Olenin, S., Daunys, D., Nalepa, T., in press. Vulnerability of benthic habitats to the aquatic invasive species. Biological Invasions, doi:10.1007/s10530-006-9070-0. Zettler, M.L., Daunys, D., in press. Long-term macrozoobenthos changes in a shallow boreal lagoon: comparison of a recent biodiversity inventory with historical data. Limnologica.