Alien species in a brackish water temperate ecosystem: Annual-scale dynamics in response to environmental variability

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Alien species in a brackish water temperate ecosystem: Annual-scale dynamics in response to environmental variability ~ ~ ¨ b, Maria Pollup Henn Ojaveer a,n, Jonne Kotta b, Arno Pollum ae u¨ u¨ b, Andres Jaanus b, Markus Vetemaa c a

Estonian Marine Institute, University of Tartu, Lootsi 2a, 80012 P¨ arnu, Estonia Estonian Marine Institute, University of Tartu, M¨ aealuse 14, 12618 Tallinn, Estonia c Estonian Marine Institute, University of Tartu, Vanemuise 46a, 51014 Tartu, Estonia b

a r t i c l e i n f o


Article history: Received 14 October 2010 Received in revised form 26 February 2011 Accepted 3 March 2011 Available online 26 March 2011

Alien species contribute to global change in all marine ecosystems. Environmental variability can affect species distribution and population sizes, and is therefore expected to influence alien species. In this study, we have investigated temporal variability of 11 alien species representing different trophic levels and ecological functions in two gulfs of the brackish Baltic Sea in relation to environmental change. Independent of the invasion time, organism group or the life-history stage, abundance and/or biomass of the investigated alien species was either stable or displayed abrupt increases over time. Timing in population shifts was species-specific and exhibited no generic patterns, indicating that the observed large shifts in environmental parameters have no uniform consequences to the alien biota. In general, the inter-annual dynamics of alien and native species was not largely different, though native species tended to exhibit more diverse variability patterns compared to the alien species. There were no key environmental factors that affected most of the alien species, instead, the effects varied among the studied gulfs and species. Non-indigenous species have caused prominent structural changes in invaded communities as a result of exponential increase in the most recent invasions, as well as increased densities of the already established alien species. & 2011 Elsevier Inc. All rights reserved.

Keywords: Baltic Sea Non-indigenous species Different trophic levels Abundance/biomass Spatio-temporal dynamics

1. Introduction Marine ecosystems are facing strong natural and multiple human-induced pressures worldwide (Costello et al., 2010). Impacts and consequences of climate variability, resource extraction and eutrophication on the structure and function of populations and ecosystems are relatively widely documented (Jennings and Kaiser, 1998; Pauly et al., 1998, Drinkwater et al., 2009; Smith and Schindler, 2009; Valdes et al., 2009). Recently, more effort has been invested on studies on the separate and combined impacts of these drivers. These studies identified, amongst other prominent consequences, abrupt changes in population density as well as ecosystem states (also called a regime shifts; Oguz and Gilbert, ¨ sterblom et al., 2007; McQuatters-Gollop et al., 2008; 2007; O ¨ Mollmann et al., 2009; Conversi et al., 2010) and alteration of ecosystem biodiversity and carrying capacity (Beaugrand et al., 2008). In addition, increased sensitivity and therefore reduction in resilience of populations and ecosystems to future climate variability and change due to human activities has also been suggested (Perry et al., 2010; Planque et al., 2010).


Corresponding author. Fax: þ372 6718 900. E-mail address: [email protected] (H. Ojaveer).

0013-9351/$ - see front matter & 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.envres.2011.03.002

Evidences of historical invasions (Carlton, 1999; Strasser, 1999) suggest that the human-mediated invasion of alien species should be considered at the same historical time scale as several other important anthropogenic factors (e.g., Lotze and Worm, 2009). Despite, this field of research has only relatively recently received elevated and systematic attention from both scientific and a wider human community (Shirley and Kark, 2006), meaning a comparatively weak incorporation into systematic marine ecosystem studies. However, there are evidences that the effects caused by alien species invasions in marine environments are very substantial, ranging from impacts on biodiversity (e.g., Bax et al., 2003; Leprieur et al., 2008) to the structure and function of populations, communities and ecosystems (e.g., Oguz et al., 2008; Wallentinus and Nyberg, 2007; Roohi et al., 2010). These are, in general, at comparable levels than those induced by climate variability and other anthropogenic activities. Environmental changes, induced by both climate and a variety of man-made habitat alterations, are known to affect ecological properties of marine ecosystems and, therefore, are influencing biological invasions (e.g., Bax et al., 2003; Walther et al., 2009). Due to the complexity of interactions between abiotic changes and biological responses in the marine environment, such fields deserve a great deal of research in order to understand current patterns and predict future changes (Hoegh-Guldberg and Bruno,

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2010). Earlier studies have indicated that abrupt changes in abiotic conditions may directly alter survival and growth of individuals but, likewise, biotic interactions may indirectly affect the patterns of distribution (Occhipinti-Ambrogi, 2007). However, due to the size and complexity of the ocean, deeper insight is needed to relate environmental variables, timing of introductions and population expanse of already established species. Unfortunately, the related knowledge on alien species is relatively limited as yet. This is, at least, partly driven because of lack or limitation of appropriate monitoring data with sufficient spatio-temporal coverage and pre-invasion observations needed to carry out such analyses (e.g., Stachowicz et al., 2002). Because of multiple strong human pressures, the Baltic Sea is one of the most severely impacted seas globally (Costello et al., 2010). Human-mediated biological introductions have resulted in 117 alien species being recorded in the Baltic Sea (incl. Kattegat), about 70 of which are known to have established self-reproducing populations (Ojaveer et al., 2010). In the northeastern Baltic Sea, strong natural disturbances due to low salinity, temperature extremes and ice scrape have resulted in impoverished benthic and pelagic communities, with many native and alien species inhabiting the area living at the edge of their tolerance limits. Recent warming of such high-latitude environment can potentially increase the chances of species transported from lower latitudes to be able to establish and spread. On the other hand, such conditions may pose a growing risk on the native biota by increasing their mortalities when certain thresholds are exceeded. Due to the large uncertainties about the interplay between the shift in abiotic environment and community interactions, it is difficult to predict, without proper data analysis, whether the role of invasive species will increase or decrease in the changing climate conditions. Moreover, even nowadays the functional diversity of the alien species in the northeastern Baltic Sea is high and they represent virtually all trophic levels and a multitude of functions. Several of them have already caused strong impacts (Kotta et al., 2006; Hulme et al., 2009; Kotta et al., 2010) and, therefore, have a potential to overwhelm key species and ecosystems. By utilizing the national monitoring database (with data availability for some taxa dating back to the late 1950s), we have studied the annual-scale variability of abundance and/or biomass of the key alien species in coastal areas of the northeastern Baltic Sea (Gulf of Riga, Gulf of Finland and northern Baltic Proper), with the aim of identifying the existence and timing of population regime shifts in relation to shifts in the abiotic environment. In addition, we have investigated annual-scale similarities and differences in performance amongst selected alien species populations as well as between alien and native species with identifying environmental factors responsible for the observed variability patterns. The obtained results should improve our general understanding of the magnitude and direction marine population, community and foodweb modifications as a result of the interactive effect between environmental variability and alien species invasions in the changing marine ecosystems.

2. Material and methods 2.1. Sampling and sample analysis The current paper considers all alien species (11 in total) for which reliable and annually comparable data were available. Data on the studied alien species (zooplankton, macrozoobenthos and fish; see Table 1) originated from several localities in the coastal area of two sub-systems of the Baltic Sea: Gulf of Finland and Gulf of Riga. For zooplankton, we used the continuous time-series from the shallow northeastern part of the Gulf of Riga during the period of 1957–2009 (Fig. 1). The samples were collected at weekly basis from May to September. In the

Gulf of Finland, zooplankton samples were available from three stations from a biweekly sampling design conducted since 1963 and with seasonal coverage from May to September (Fig. 1). Annual continuous data were available since 1974. Zooplankton sampling was performed by doing vertical tows with a Juday net (mouth opening of 0.1 m2; mesh size 90–160 mm). The samples were preserved in 4% formalin, sub-sampled with a Stempel pipette and individuals of the different species have been counted under a binocular microscope. The samples were further analyzed according to the guidelines set out by the Baltic Marine Environment Protection Commission (HELCOM) since the 1970s.1 The benthic invertebrate samples were collected with a van Veen type bottom grab (grab area of 0.1 m2) from altogether six localities in the Gulf of Riga and two localities in the Gulf of Finland (Fig. 1). The sampling was conducted annually during May–June from 1993 to 2009. One locality was represented by 1–3 stations. Depending on the range of natural variability of habitat, one to three replicate samples were collected at each station annually. Grab samples were sieved in the field on 0.25 mm mesh screens. The residuals were stored at  20 1C and subsequent sorting, counting and determination of invertebrate species were performed in the laboratory using a stereomicroscope. All species were determined to species level except for oligochaetes, insect larvae and juvenile gammarid amphipods. The dry weight of species was obtained after the individuals had been desiccated at 60 1C for 2 weeks. Chinese mitten crab Eriocheir sinensis was sampled by gillnet fishing (net height of 1.5–1.8 m, mesh size of 40–55 mm) in one station in the Gulf of Finland (Fig. 1), multiple times per month since spring 1991 during the ice-free season. For each fishing operation that resulted in a catch of E. sinensis, the catch-per-uniteffort (CPUE, number of crabs caught per hour and length of nets, in meters, employed) was calculated according to: CPUE ¼NL  1D  1, where CPUE is the catch-per-unit-effort, N is the number of crabs in a catch, L is the length of nets (in meters) and D is the duration of catch (in hours). Each year sampling was undertaken from March to December with relatively similar sampling intensity, in terms of both number of days fished and number of nets employed. The annual P catch index was calculated according to CIa ¼ 103CPUEi; where CIa is the annual catch index and CPUEi is monthly total catch-per-unit-effort. To investigate the occurrence and quantify the amounts of alien fish species, experimental fishing by applying two different methodologies was carried out in several coastal areas. Gibel carp Carassius gibelio was monitored in the Gulf of Riga according to the guidelines of the coastal fish monitoring (Thoresson, 1996). The available data allowed to study the fish in three nearby localities since 1993 and in one locality since 2005 (Fig. 1). In the three nearby stations, the sampling took place by means of bottom gillnets (height of 1.8 m, length of 30 m) with six mesh sizes (17, 21.5, 25, 30, 33 and 38 mm, here and further, from knot to knot) from late July to early August. Annual catch-per-unit-effort (CPUE, weight units) for a sampling station was calculated according to: CPUE¼ WFi  1; where W is the weight of fish in a catch and Fi is the number of experimental fishing operations performed, and expressed as an average over the three sampling stations. At the separate station, gillnets with the following mesh sizes were additionally used: 42, 45, 50, 55 and 60 mm. The round goby Neogobius melanostomus was sampled by gillnet fishing (height of 3.0 m, length of 60 m, mesh size of 18 and 22 mm) in one station in the Gulf of Finland (Fig. 1) since 2005. Surveys were carried out during April–December 1–5 times per month. Annual catch-per-unit-effort (CPUE, weight units) was calculated as for the gibel carp (see above).

2.2. Statistical analyses In the data analysis, the alien copepod Acartia tonsa was combined with the native Acartia spp., as the two species were not routinely identified to a species level. Similarly, the alien Evadne anonyx was not determined and all Evadne individuals were considered as the native Evadne nordmani in the Gulf of Riga. For the same reason, larvae of the alien Marenzelleria neglecta were combined with other polychate larvae and the combined unit was not grouped among aliens. The category ‘others’ predominantly contained relatively rarely occurring native zooplankton taxa. In the models relating to the dynamics of environment and biota altogether, 13 abiotic variables were used for the Gulf of Riga and 11 for the Gulf of Finland, respectively (for details, see Table 2). Multivariate data analyses on the abiotic environment and the studied species were performed by the statistical program ‘‘PRIMER’’ version 6.1.5 (Clarke and Gorley, 2006). Environmental variables were normalized prior to analyses and similarities between years were calculated using Euclidian index. Then non-metric multidimensional scaling analysis (MDS) on the environmental variables was used to visualize the dissimilarities in inter-annual dynamics and to demonstrate the occurrence of shifts in the abiotic environment. To test the regime shift hypothesis as a step change in the mean level of the studied alien species, we used a parametric method based on sequential t-test analysis of regime shifts STARS (Rodionov, 2004; Rodionov and Overland, 2005). The method consists of calculating a Regime Shift Index (RSI), which represents a

1 See: annex7/#3

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Table 1 Overview of the alien species considered within the current study. Species name

Common name

Organism group

Native to

First record in study area

Ecological function

Balanus improvisus Carassius gibelio Cercopagis pengoi Dreissena polymorpha Eriocheir sinensis Evadne anonyx Gammarus tigrinus Marenzelleria neglecta Mya arenaria Neogobius melanostomus Potamopyrgus antipodarum

Crriped Gibel carp Fish-hook waterflea Zebra mussel Chinese mitten crab Cladoceran Gammarid amphipod Polychaete Soft-shell clam Round goby New Zealand mud snail

Zoobenthos Fish Zooplankton Zoobenthos Zoobenthos Zooplankton Zoobenthos Zoobenthos Zoobenthos Fish Zoobenthos

North America South-East Asia Ponto-Caspia Ponto-Caspia Far East Ponto-Caspia North America North America North America Ponto-Caspia New Zealand

¨ ¨ 19th century (Jarvek ulg, 1979) 1985 (Vetemaa et al., 2005) 1992 (Ojaveer and Lumberg, 1995) 19th century (Schrenk, 1848) 1930s Ojaveer et al., 2007) ~ 1999 (Pollup u¨ u¨ et al., 2008) ¨ et al., 2006) 2003 (Herkul 1991 (Kotta and Kotta, 1998) ¨ 11–12th century (Leppakoski et al., 2002) Early 2000s (Ojaveer, Spilev, 2003) ¨ ¨ 19th century (Jarvek ulg, 1979)

Suspension feeding Omnivory Predation Suspension feeding Omnivory, burrowing, Predation Grazing, predation Deposit feeding, burrowing Suspension feeding Predation Grazing

Fig. 1. Map of the sampling locations in the Gulf of Finland and the Gulf of Riga. Legend: open triangles—mesozooplankton, filled triangles—macrozoobenthos, filled circles—gibel carp Carassius gibelio, asterisk—Chinese mitten crab Eriocheir sinensis and round goby Neogobius melanostomus. One sampling locality of macrozoobenthos represents 1–3 stations. cumulative sum of normalized anomalies relative to a critical value. In this work we used the cut-off length of 10 years, and a probability level equal to 0.05. Similarities between species abundances and biomasses among stations and years were calculated using a zero-adjusted Bray–Curtis coefficient. The coefficient is known to outperform most other similarity measures and enables samples containing no organisms at all to be included (Clarke et al., 2006). Non-metric multidimensional scaling analysis (MDS) on the species biomasses was used to visualize the dissimilarities in the inter-annual dynamics of the studied species. Statistical differences in the trends were assessed by the ANOSIM permutation test (Clarke, 1993). BEST analysis (BIOENV procedure) was used to relate the patterns of environmental variables to the biomasses of each studied species. The analysis showed which environmental variables best predicted the observed biotic patterns. A Spearman rank correlation (r) was computed between the similarity matrices of environmental data (abiotic variables; Euclidean distance) and different invertebrate species (a zero-adjusted Bray–Curtis distance). A global BEST match permutation test was run to examine the statistical significance of observed relationships between environmental variables and biotic patterns.

3. Results The MDS analysis on abiotic environmental variables suggested a clear shift in environmental conditions in 1995/1996,

both in the Gulf of Riga and in the Gulf of Finland (Fig. 2). Such changes were mainly attributed to an increase in mean sea surface temperature and a decrease in North Atlantic Oscillation (NAO) index. Altogether 35 zooplankton, 38 benthic invertebrate and 25 fish taxa were identified in the study area. While several species were abundantly present within the zooplankton community, Macoma balthica, Hediste diversicolor and Oligochaeta were the most frequently detected benthic taxa, and perch Perca fluviatilis and white bream Blicca bjoerkna dominated amongst fish. The total biomass of benthic and pelagic invertebrates in samples ranged from 0 to 90 g dry weight m  2 and from 3 to 3100 mg wet weight m  2, respectively. Fish catch (CPUE) in experimental gillnet fishing ranged between 0.2 and 45.6 kg. Regardless of the invasion timing, organism group or the lifehistory stage (larvae or adults), the abundance and/or biomass of the studied alien species did not decrease in the studied basins. Some species, however, significantly increased their abundances/ biomasses during the course of study. Timing in population shifts was species-specific and exhibited no generic patterns. Several

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Table 2 Details on the environmental variables used in the Gulf of Riga and the Gulf of Finland. No.

Description (with data source in brackets)


Gulf of Riga 1 2 3 4 5 6 7 8 9 10 11 12 13

Maximum ice coverage in the Baltic Sea, km2 (Finnish Institute of Marine Research) North Atlantic Oscillation winter index (December–March) (National Center of Atmospheric Research, USA) Sea surface temperature anomaly, second week of May, 1C (National Center of Environmental Predictions, USA) Sea surface temperature anomaly, second week of August, 1C (National Center of Environmental Predictions, USA) Mean sea surface temperature anomaly, May–August, 1C (National Center of Environmental Predictions, USA) Air temperature, mean for May–August, 1C (Estonian Meteorological and Hydrological Institute) Number of days with mean wind speed 410 m/s, May–August (Estonian Meteorological and Hydrological Institute) ¨ Surface salinity in Parnu Bay, mean for May–August, PSU (Estonian Marine Institute) Chlorophyll a concentration (aggregate for 1–10 m), mean for May–August, mg m  3 (Estonian Marine Institute) Water transparency, mean for May–July, m (Estonian Marine Institute) Duration of icecover, days (Estonian Meteorological and Hydrological Institute) Date of ice melt, Julian Day (Estonian Meteorological and Hydrological Institute) Mean sea level, May–August, m (Estonian Meteorological and Hydrological Institute)

MaxIce NAOdecmar SSTAMay STAAugust SSTAMay–August AirTemperature Storms Salinity Chl a Secchi Icedays Icemelting Sealevel

Gulf of Finland 1 Maximum ice coverage in the Baltic Sea, km2 (Finnish Institute of Marine Research) 2 North Atlantic Oscillation winter index (December–March) (National Center of Atmospheric Research, USA) 3 Sea surface temperature anomaly, second week of May, 1C (National Center of Environmental Predictions, USA) 4 Sea surface temperature anomaly, second week of August, 1C (National Center of Environmental Predictions, USA) 5 Mean sea surface temperature anomaly, May–August, 1C (National Center of Environmental Predictions, USA) 6 Air temperature, mean for May–August, 1C (Estonian Meteorological and Hydrological Institute) 7 Number of days with mean wind speed 410 m s  1, May–August (Estonian Meteorological and Hydrological Institute) 8 Salinity (aggregate for 0–40 m), mean for May–August, PSU (Estonian Marine Institute) 9 Chlorophyll a concentration (aggregate for 1–10 m), mean for May–August, mg m  3 (Estonian Marine Institute) 10 Water transparency, mean for May–August, m (Estonian Marine Institute) 11 Water temperature (aggregate for 0–40 m), mean for May–August, 1C (Estonian Marine Institute)

Fig. 2. Non-metric multidimensional scaling ordination in the inter-annual dynamics of environmental variables in the Gulf of Riga (A) and Gulf of Finland (B).

alien invertebrates that were established in the Baltic Sea more than one century ago increased in the late 1990s/early 2000s (Balanus improvisus larvae) and in the mid-late 2000s

MaxIce NAOdecmar SSTAMay STAAugust SSTAMay-August AirTemperature Storms Salinity Chl a Secchi WaterTemperature

(Dreissena polymorpha, adult B. improvisus, Mya arenaria). The Chinese mitten crab, which has no reproduction capabilities in the low-saline Baltic Sea (Ojaveer et al., 2007), has exhibited significant population increase in the Gulf of Finland since 2002, similar to that of the locally reproducing gibel carp C. gibelio in the Gulf of Riga (Figs. 4 and 5). Similarly, species that invaded the region more recently (in the early 1990s, Cercopagis pengoi, M. neglecta) have exhibited abrupt population increases since then (Fig. 3). The most recent invaders in the study area, the amphipod Gammarus tigrinus and the round goby N. melanostomus, both have exponentially increased their densities after the invasion (Fig. 6). Generally, the inter-annual dynamics of non-indigenous and native species were not largely different; though, native species tended to exhibit more diverse variability patterns compared to the non-indigenous species (Fig. 7). The comparisons between individual species indicated significant differences in the case of pelagic invertebrates (ANOSIM tests, po0.05), whereas benthic species were more similar in that respect in the Gulf of Riga but not in the Gulf of Finland. While the inter-annual variability of the pelagic B. improvisus nauplii, C. pengoi and E. anonyx significantly differed from many native pelagic invertebrate species, the dynamics of the benthic B. improvisus, D. polymorpha, Potamopyrgus antipodarum, G. tigrinus and M. arenaria in the Gulf of Riga differed from a handful of native invertebrate species only, often involving, e.g., the native clam M. balthica and Oligochaeta. Similar to the pelagic species, the dynamics of the non-indigenous benthic species significantly differed from the majority of native benthic species in the Gulf of Finland. Generally, correlations between the studied abiotic environmental variables and biota were moderate in the Gulf of Riga (BEST permutation test, Rhoo0.4, p o0.05), except for pelagic species (C. pengoi and B. improvisus nauplii) and fish (C. gibelio) that showed high match with environmental variability (Rho around 0.5, po0.05). In the Gulf of Finland, pelagic species (E. anonyx and B. improvisus nauplii) also tended to display better links with environmental variability (BEST permutation test, Rho40.4, p o0.05) than benthic alien invertebrates. The analyses

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also suggested that there were no key environmental variables that affected most of the non-indigenous species (Table 3). Instead, the effects varied among the studied gulfs and species. While both benthic and pelagic invertebrates were affected by a combination of temperature, salinity, wind and ice conditions, and water chlorophyll level, alien fish dynamics were best related to water temperature in spring. In addition, environmental variables that described the variability of an alien species were different in the Gulf of Riga and the Gulf of Finland (Table 3). Decadal-scale dynamics of the percent contribution of pelagic alien species in local zooplankton communities evidenced substantial increase in both sub-basins (i.e., Gulf of Finland and Gulf of Riga) since the early 1990s onwards, with the peak annual value of 25% (Fig. 8). This was due to both an invasion of new alien species (e.g., C. pengoi) as well as a significant increase in population size of the already existing B. improvisus (Fig. 3). While

Fig. 3. Long-term abundance dynamics of three alien zooplankton species in the Gulf of Riga (filled diamonds) and the Gulf of Finland (open diamonds). The lines indicate abundance regimes.

Fig. 5. Catch-per-unit-effort (CPUE, kg) with regime shift line of the alien gibel carp Carassius gibelio in the Gulf of Riga during 1993–2009.

Fig. 4. Long-term biomass dynamics of six alien zoobenthos species in the Gulf of Riga and the Gulf of Finland. For legend, see Fig. 3.

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4. Discussion

Fig. 6. Population dynamics of the two most recently invaded alien species: the amphipod Gammarus tigrinus (A) in the Gulf of Riga since 2003 and the round goby Neogobius melanostomus (B) in the Gulf of Finland since 2005.

the native zooplankton biomass did not exhibit any long-term trends in the Gulf of Riga, it has gradually increased in the Gulf of Finland since the first half of the 1990s. The share of alien species within benthic invertebrate communities was high but, both, spatially and temporally variable. Although benthic alien species were on average more important in the Gulf of Finland than in the Gulf of Riga, they contributed to more than 35% of benthic biomasses in both Gulfs in the mid-2000s. Even more, within 7 years of its invasion history, the recent crustacean immigrant G. tigrinus constituted the majority of benthic biomass and had replaced the native gammarid amphipods at some stations in the Gulf of Riga. Biomass of the native benthic invertebrate communities did not reveal any long-term trends in none of the two subbasins studied, with annual-scale variability of native species biomass being very different from that of the percentage contribution of alien species in benthic communities. In contrast to benthic invertebrates, the share of pelagic aliens was higher in the Gulf of Riga compared to that in the Gulf of Finland (Fig. 8). Thus, the patterns and consequences of alien invertebrate invasions have large spatial variability (i.e., among Gulfs, benthos and plankton) and might result both in increased biomass of invaded communities and in reduction of biomass of some native taxa. Importance of the gibel carp was remarkably higher in the experimental catches in the separate station (19.2% on average for 2005–2009) compared to that in the three adjacent stations of the Gulf of Riga (1.5% on average for 2002–2009). Proportion of the round goby in the coastal fish community cannot be estimated in sufficient detail as the species has very recently invaded the system and is in the phase of exponential population growth. However, as the biomass-based proportion of this species has increased from 0.2% to 42.8% during the first 5 years of invasion (from 2005 to 2009), this species probably plays, besides the amphipod G. tigrinus, the strongest role in structuring native communities in the invaded system.

Analyses of temporal dynamics of the abundance and biomass of alien species representing different trophic levels and ecological functions in the coastal Baltic Sea provided two major evidences. Firstly, no abrupt population decreases amongst the studied alien species were detected, but some species significantly increased their abundances and biomasses during the course of study. Secondly, timing of such shifts in alien population abundance and biomass was clearly species-specific. Other recent studies have evidenced pronounced changes (including regime shifts) in several sub-systems of the Baltic Sea and also elsewhere and timing of these events matched across the ecosystems, ¨ especially in the North Atlantic (Diekmann and Mollmann, 2010 and references therein). In contrast, our study clearly demonstrated that large shifts in environmental parameters had no uniform consequences to the alien biota in the coastal areas of the Baltic Sea. Instead, these effects were species-specific and due to significant interactions of large-scale environmental variables with local environment, the inter-annual dynamics of alien species also varied among the studied gulfs. This supports earlier view that alterations in the structure of ecosystems are likely driven by changes between the complex interrelationships of environmental forcing and ecosystem elements (Hughes, 2000; Stenseth et al., 2002). Seemingly, large-scale environmental variables and local forcing (e.g., nutrient loading, biotic interactions) interfere with the communities at similar intensities, show strong interactive effects (Kotta et al., 2009) and occur over different spatial and temporal scales (Wu et al., 2000; Hewitt and Thrush, 2009). The consistency of effects of environmental shifts likely depends on the degree of the small-scale heterogeneity of communities. As compared to alien benthic herbivores and deposit feeders, alien benthic suspension feeders inhabiting the Gulf of Riga responded more strongly to large-scale environmental variables (e.g., temperature, salinity, large storms) than local variables (e.g., ice). Similarly, the developmental characteristics of alien species determined the types of response, i.e., pelagic species or benthic species with larval development were more likely influenced by large-scale forcing (e.g., NAO), compared to benthic species that had direct development. Our study clearly demonstrated abrupt increases in populations range and density of existing alien species in the Baltic Sea in recent decades and such shifts may be attributed to milder winters and warmer summers in the region (e.g., virtually all invertebrate models included temperature). This supports the current view that recent accelerated warming of high-latitude environments has increased the chances of species transported from lower latitudes to be able to establish and spread (Stachowicz et al., 2002). Recent observations elsewhere indicate that not only changed climate conditions, but also local hydrodynamics might have important consequences on population abundance of alien invertebrates, which have been present in the invaded system for more than 50 years (Rigal et al., 2010; Witte et al., 2010). In addition to generic temperature effects, all models of benthic alien invertebrates included the salinity term. In the Baltic Sea area, milder winters are known to be associated with stronger fresh water inflows from rivers which directly affect coastal salinities. This all suggests large difficulties to predict the interplay between environmental setting, spread of invasive species and the potential for large-scale synergisms of these processes in the Baltic Sea area. In European seas, alien species are dominated by benthic invertebrates (Gollasch, 2006). This is also confirmed by the current study where 7 out of the 11 frequently occurring species were benthic invertebrates. The observed strong differences in the long-term dynamics of the studied alien benthic species in the

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Fig. 7. Non-metric multidimensional scaling ordination in the dynamics of environmental variables, benthic and pelagic invertebrate and fish species in the Gulf of Riga (A) and Gulf of Finland (B). Category ‘others’ predominantly contain relatively rarely occurring native zooplankton taxa. For explanation of abbreviated environmental parameters, see Table 2.

Gulf of Finland may be due to more intense competition among benthic invertebrates in the Gulf of Finland than in the Gulf of Riga. This is likely reflecting better feeding conditions in the Gulf of Riga that release benthic species from food competition. It has been demonstrated that elevated eutrophication results in ´ lafsson and blooms of opportunistic micro- and macroalgae (O Elmgren, 1997; Pasternack and Brush, 2001; Berglund et al., 2003; Kotta et al., 2004a). These algae provide a habitat and food for benthic invertebrates (Kotta et al., 2004b, 2008; Orav-Kotta and Kotta, 2004). Although the spring detrital pulse used to explain a large part of the annual offshore benthic production, coastal macroinvertebrates nowadays clearly take advantage of the greater biomasses of drifting macroalgae as an important source

of nutrients all the year round. Therefore, the dynamics of native and alien species in the Gulf of Riga is affected by weather conditions and nutrient loading rather than biotic interactions ¨ et al., 2006). On the other hand, biotic interactions seem (Herkul to be plausible mechanisms to explain the dissimilarities in the population dynamics of different benthic species in the Gulf of Finland area. Macroalgae are known to outcompete benthic suspension feeders at shallow depths (Janke, 1990). Moderate mechanical disturbance, either due to ice or waves, may partly remove the algal carpet and, thus, release benthic suspension feeders from such interspecific competition (Kotta and Witman, 2009). A mechanical disturbance so great, however, also removes most

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Table 3 Results of BEST permutation (Rho, BIOENV) analysis showing the environmental variables that contribute significantly to the variability in the dominance structure of alien invertebrate and fish species. Significant effects are shown in bold. For variable identification and description, see Table 2. Gulf of Riga Species Evadne anonyx Cercopagis pengoi Balanus improvisus nauplii Marenzelleria neglecta larvae B. improvisus M. neglecta Mya arenaria Potamopyrgus antipodarum Dreissena polymorpha Gammarus tigrinus Eriocheir sinensis Neogobius melanostomus Carassius gibelio

Gulf of Finland




0.479 0.544 0.348 0.280 0.424 0.255 0.286 0.215 0.214

0.015 0.010 0.225 0.430 0.100 0.600 0.630 0.770 0.885

2,5,6,7,13 9 2,13 3,6,7,8,13 4,9,10,12,13 6,7,8,9 4,8,9,12 1,6,8,10,12 6,8,13



Fig. 8. Decadal-scale dynamics of the biomass-based percent contribution of alien species in mesozooplankton (A) and macrozoobenthos (B) communities in the Gulf of Riga (empty columns) and Gulf of Finland (filled columns).

suspension feeders. Such abiotic factor mediating biotic interactions may also explain similarities in the temporal population dynamics of the alien suspension feeding species B. improvisus and D. polymorpha. This may also explain why alien suspension feeders benefited from moderate mechanical disturbances, and why their densities were low when the duration of ice cover was either very short or very long and when the number of storms was moderate. Another alien suspension feeding invertebrate M. arenaria inhabits soft bottoms and it is expected that elevated flow velocity and phytoplankton biomass interactively increase their food supply as evidenced from the BIOENV models. The models




0.415 0.135 0.462

0.055 0.850 0.020

3 9 2,3,6,10

0.180 0.408 0.272 0.167

0.720 0.100 0.425 0.870

10,11 1,4,6,8 4,10 6,10

0.399 0.393

0.076 0.980

3,7,9 3,7


also acknowledge that the response of suspension feeders to environmental forcing is complex (Lauringson et al., 2009). Suspension feeders are simultaneously affected by basin-wide effects on phytoplankton and by local factors such as the availability of resuspended microphytobenthic cells or detritus. Basinwide and local effects can to some extent even counteract each other; for instance, frequent storms can promote phytoplankton blooms via upwelling events but carry away detrital material locally, and stormy weather or large-scale phytoplankton blooms can in turn result in reduced light conditions, which may locally suppress the development of benthic microalgae. However, the significance of phytoplankton biomass in the models suggested that M. arenaria is often depleted of suspended particulate matter; increasing phytoplankton biomasses can reverse this food limitation (Lauringson et al., 2007). The Chinese mitten crab E. sinensis is unable to reproduce in the Baltic Sea because of low salinity. Therefore, it has been suggested that the present distribution and abundance of this species in the Baltic reflect its immigration from the nearest reproduction area in the North Sea (Ojaveer et al., 2007). However, the current study showed that this species displayed a significant increase in abundance in the early 2000s, with the timing corresponding well to the observed regime shift in the ¨ Baltic Sea (Diekmann and Mollmann, 2010). Further, our analysis showed that the species is significantly influenced by local climatic conditions as well as by marine productivity. Thus, besides external factors, local conditions in the destination area of immigration likely influence abundance of the Chinese mitten crab in the Baltic Sea. Our analysis demonstrated that pelagic alien invertebrates were a less stable component of an ecosystem compared to benthic alien invertebrates. It is likely that, owing to a large natural instability of the system, the benthic invertebrates inhabiting the Baltic Sea are highly adaptive and very resistant to any ¨ and Rosenberg, physical and biological disturbances (Jernelov ¨ et al., 2006). It is expected that while impacts of 1976; Herkul benthic alien invertebrates on native biota might be essentially confined to certain specific habitats—e.g., in deep sea where food or shelter is highly limited (M. neglecta vs. Monoporeia affinis and ´ lafsson, 2003) and H. diversicolor) (Kotta et al., 2001; Kotta and O macrophyte habitats (e.g., G. tigrinus vs. other native amphipods) (Orav-Kotta et al., 2009; Kotta et al., 2010)—that of alien pelagic invertebrates (e.g., C. pengoi vs. native zooplankton and pelagic fish) are wider and encompasse both coastal and offshore areas ~ ¨ 2010). (e.g., Lankov et al., 2010; Pollup u¨ u, The impacts of alien species have large spatial variability. Our study indicated that pelagic invertebrate communities were more

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influenced by alien species in shallow areas of the Gulf of Riga than in the Gulf of Finland, while the opposite was valid for benthic invertebrate communities. However, the structuring role of alien fish might be more substantial at local scales than that of alien invertebrates. Percentage contribution of the very aggressive round goby N. melanostomus in the local fish community in the Gulf of Finland (Muuga Bay), which is the only locality in the studied Gulfs where this species is established, has reached to about 40% during the first 5 years of invasion since 2005. Even more, there is evidence to expect that the abundance of the round goby will continue to increase during the coming years (VelezEspino et al., 2010). The other studied alien fish species – the gibel carp C. gibelio – which was found first in the Estonian coastal sea around 20 years ago (Vetemaa et al., 2005) made substantial contribution (19.2%) in experimental catches in the Gulf of Riga during the same time-period (i.e., 2005–2009). In addition, this fish may dominate in commercial catches in some specific localities in the Gulf of Riga during the warm summer months. Thus, although the studied alien invertebrates impact the invaded ecosystem at large spatial extent, alien fish likely have more substantial influence at local scales. More comprehensive analysis on the long-term development of non-indigenous species in this area and identification of the responsible environmental variables are limited, mainly for the following three aspects. Firstly, data availability during earlier decades, which poses serious restrictions essentially for zoobenthos. Secondly, precision of taxonomic identification that limits tracking of the performance of the alien zooplankton taxa. And thirdly, spatial coverage, which should be considered problematic for all alien invertebrates as we lack long-term data in offshore and deeper areas. However, and despite the shortcomings listed above, we were able to track the annual-scale performance of several alien species populations, representing different trophic levels and ecological functions, over a decade and a half and to identify the environmental factors responsible for the observed variability. In addition, to continue the already started monitoring activities and to expand them to more open areas, steps should be undertaken to eliminate the critical deficiency in taxonomic identification of some pelagic alien invertebrates.

5. Conclusions The effects of environmental factors on the annual-scale variability of alien species representing different trophic levels and ecological functions appeared to be species and area specific, with no clearly identifiable key environmental factors responsible for their population dynamics. However, temperature seems to be a common significant forcing factor for the population dynamics of most of the species. Both, recently introduced as well as historically established alien species displayed one or more abrupt increases in abundance and/or biomass during the past two decades. Timing of these shifts was independent from that in the abiotic environment and pointed to the importance of biotic interactions in modifying local communities as a result of bioinvasions. Compared to the native species, alien species tended to exhibit less diverse annual-scale variability patterns and acted, therefore, as a stable and important structural and functional compartment of the invaded ecosystems.

Acknowledgments The authors thank Mart Simm for making zooplankton data available for the current study. They also thank two reviewers and


the special volume co-editor Gemma Quilez-Badia for the comments and suggestions made on the manuscript. Funding sources: This work was partially financed by the Estonian Ministry of Education and Research (Grant nos. SF0180013s08 and SF0180005s10), EU FP 7 project VECTORS (Grant no. 266445) and Estonian Science Foundation (Grant nos. 8254 and 8281). The funding sources had no involvement in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; and in the decision to submit the paper for publication.

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