a the invasive red alga gracilaria vermiculophylla in the baltic … · weinberger et al.:...
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AQUATIC BIOLOGYAquat Biol
Vol. 3: 251–264, 2008doi: 10.3354/ab00083
Printed September 2008 Published online September 2, 2008
INTRODUCTION
The native distribution area of the red macroalgaGracilaria vermiculophylla (Ohmi) Papenfuss is theNorthwest Pacific (Tseng & Xia 1999, Terada & Yama-moto 2002). During the last 15 yr it has been detectedat the North American eastern coast (Freshwater et al.2006, Thomsen et al. 2006) and western coast (Bellorinet al. 2004), as well as in Europe (Rueness 2005). At theNE Atlantic coast the known distribution area of G.vermiculophylla extends in latitude from Morocco (C.Destombe pers. comm.) to SW Sweden (57.7° N; Ny-
berg 2007). In 2005 the species was detected for thefirst time east of the Danish Belt at Kiel (Germany,54.3° N; Schories & Selig 2006).
The invasive success and ecological impact of a spe-cies in a new environment cannot be predicted withcertainty (Boudouresque & Verlaque 2002). Nonethe-less, certain traits exist that are typical for successfulinvasive macroalgae (Maggs & Stegenga 1999, Bou-douresque & Verlaque 2002, Nyberg & Wallentinus2005). Nyberg & Wallentinus (2005) proposed the useof 13 different traits to estimate potential macroalgaldispersal, settlement and ecological impact. Based on
© Inter-Research 2008 · www.int-res.com*Email: [email protected]
The invasive red alga Gracilaria vermiculophyllain the Baltic Sea: adaptation to brackish water
may compensate for light limitation
Florian Weinberger1,*, Björn Buchholz1, Rolf Karez2, Martin Wahl1
1Leibniz-Institut für Meereswissenschaften (IFM-GEOMAR), Düsternbrooker Weg 20, 24105 Kiel, Germany2Landesamt für Natur und Umwelt des Landes Schleswig-Holstein, Hamburger Chaussee 25, 24220 Flintbek, Germany
ABSTRACT: The recent introduction of Gracilaria vermiculophylla (Rhodophyta) to the Kiel Fjordarea was a reason for concern, since this red macroalga perfoms best under mesohaline conditionsand thus appears well adapted to thrive and spread in the Baltic Sea environment. A systematic sur-vey on a coastal range of 500 km in 2006 and 2007 indicated considerable multiplication and spread-ing of G. vermiculophylla within Kiel Fjord, but provided little evidence of long-distance transport.Nonetheless, flow-through growth experiments conducted at a range of salinities under ambient lightshowed that G. vermiculophylla should be able to grow in most of the Baltic Sea. Growth declinedonly below a salinity of 5.5. High water temperatures in summer seem to reduce resistance againstlow salinity. Growth of G. vermiculophylla in the SW Baltic is limited by light and is only possible dur-ing summer and above a depth of 3 m. Drifting fragments are dispersed by currents. Either they sinkto deeper waters, where they degrade, or they accumulate in shallow and sheltered waters, wherethey form perennial mats. These overgrow not only soft bottom sediments, but also stones, which arean important habitat to Fucus vesiculosus, the main native perennial alga in the Baltic Sea. As com-pared to F. vesiculosus, G. vermiculophylla seems to represent a preferred refuge for mesograzersand other invertebrates, particularly in winter. Nonetheless, feeding trials showed that potentialgrazers avoided G. vermiculophylla relative to F. vesiculosus. Daily biomass uptake by grazers asso-ciated with G. vermiculophylla in nature did not exceed 2 g kg–1 and is
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this method, they placed Gracilaria vermiculophyllaamong the 4 most potent invaders out of 114 non-indigenous macroalgal species in Europe (Nyberg2007). Specific traits of G. vermiculophylla that havebeen considered as indicative of its considerable inva-sive potential are: a remarkable ability to recruit fromspores and grow from fragments (Rueness 2005,Nyberg 2007, Thomsen et al. 2007) and a high toler-ance to environmental stress (Yokoya et al. 1999, Rue-ness 2005, Nyberg 2007). In particular, G. vermiculo-phylla is highly resistant to low salinities (Yokoya et al.1999, Raikar et al. 2001, Rueness 2005, Nyberg 2007,Thomsen et al. 2007), and mainly grows in estuariesand brackish water lagoons (Terada & Yamamoto2002, Rueness 2005, Freshwater et al. 2006, Thomsenet al. 2007). Resistance to low salinity is an importantpreadaptation for successful invasion into brackishwater seas (Paavola et al. 2005). A strong performanceof G. vermiculophylla in the Baltic Sea has thereforebeen prognosticated (Schories & Selig 2006, Nyberg2007, Thomsen et al. 2007).
The Baltic Sea east of the Danish straits is the world’slargest brackish water sea without significant tides,but with prolonged periods of high or low water mainlycaused by atmospheric fluctuations. The present salin-ity decreases over a gradient from about 20 at the Dan-ish straits to 12°, from 53° 40’to 65° 50’ N. Resulting from this extension, day lengthin the northern and southern Baltic Sea differs consid-erably: the longest day of the year lasts nearly 24 h at65° 50’ N, but only 17 h at 53° 40’ N. On the other hand,solar radiation is stronger in the southern than in thenorthern Baltic Sea, resulting in similar total input ofsun light in summer, but higher input in the southernBaltic Sea in winter (Chandler et al. 2004).
Here, we report on the recent distribution andspreading velocity of Gracilaria vermiculophylla alongthe German Baltic coast and on its growing capacity
and loss to grazers in this region. We also estimate itspotential for further spread, taking into considerationthe specific conditions of the inner Baltic. We presentresults of growth experiments, suggesting that G. ver-miculophylla may cope with the light regime and salin-ity conditions in large parts of the Baltic, profit fromlack of grazers and spread to more northward latitudesthan in its natural distribution range or in fully marineconditions. We also present first evidence that G. ver-miculophylla has the capacity to accelerate the declineof Fucus vesiculosus — previously the main habitat-forming macroalga in the Baltic Sea (Rönnbäck et al.2007) — in sheltered coastal regions. On the other hand,we also show that G. vermiculophylla provides a newhabitat — comparably or more attractive than F. vesicu-losus — to various seaweed-associated animals.
MATERIALS AND METHODS
Distribution of Gracilaria vermiculophylla. In orderto identify preferred habitats and to quantify thespreading velocity of G. vermiculophylla, its distribu-tion was monitored in 2 consecutive years (2006 and2007). For this purpose, approximately 1 km long beachsections that were located in distances of approxi-mately 10 km were browsed on a coastal range of ap-proximately 500 km between Glücksburg (54° 50’ N,9° 31’ E) and Warnemünde (54° 10’ N, 12° 03’ E). Areaswhere G. vermiculophylla was detected on the beachwere investigated further by boat, using an aquascopein shallow water and a video system in selected deepwater areas. The taxonomy of Gracilaria and relatedgenera is notoriously difficult, but material from theKiel area has been identified as G. vermiculophyllabased upon DNA sequencing (Schories & Selig 2006),and from the Baltic Sea east of the Belt no otherGracilariaceae have been reported (Nielsen et al.1995). Morphologically similar native Gracilariaceae(Gracilaria gracilis or Gracilariopsis longissima) fromthe North Sea do not tolerate the salinity conditions inKiel Fjord (authors’ unpubl. obs.).
Growth capacity in the sea. A growth experimentwith Gracilaria vermiculophylla was conducted fromthe end of May 2006 to the end of June 2007 in the seain order to investigate water depth and seasonaleffects upon growth. G. vermiculophylla was collectedin Kiel-Wik (54° 21’ 11’’ N, 10° 08’ 29’’ E). Incubation inthe sea was conducted in standardized net bags ofpolypropylene with a mesh size that allowed meso-grazers to enter the bags (Novanet Kunststoff, maxi-mum length: 20 cm, maximum width: 10 cm, meshwidth: 9 mm). For exposure in the sea, the net bagswere attached at a distance of 3 km from the collectionsite to 6 vertical ropes at 0.25, 0.5, 1, 2, 3, 4 and 5 m
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below mean sea surface level, representing the fulldepth range in which G. vermiculophylla may bedetected in the Kiel Fjord. The bags were initially filledwith 10 g fresh weight (FW) of G. vermiculophylla, andgrowth was quantified by biweekly weight measure-ments (FW1, FW2). Growth was calculated as (FW2 –FW1) × FW1–1 × incubation time–1. After each measure-ment, the algal fresh weight was readjusted to 10 g. Onthese occasions, the net bags were replaced when theywere covered by fouling organisms, in order to preventshading. Linear correlations of G. vermiculophyllagrowth during biweekly time intervals with the pre-vailing water temperature, photosynthetically activeradiation (PAR) and solar radiation (SR) were calcu-lated, while iterative adaptation of a logistic dose–response function using the Prism 4 software package(GraphPad Software) allowed the identification of SRdoses that were required to support growth directlybelow the water surface.
In addition to the biweekly growth measurements,the photosynthetic capacity of Gracilaria vermiculo-phylla adapted to different water depths was mea-sured in 3 mo intervals by pulse-amplitude-modulatedfluorometry, in order to estimate the algal capacity toadapt to sudden changes in light exposure, using aDiving-PAM (Walz) underwater fluorometer. Upon theapplication of a saturating flash (21 000 µmol m–2 s–1 for1 s), the rise in tissue fluorescence from the base value(Fo) to the maximum value (Fm) was quantified. Lightsaturation fully reduces the first electron acceptor ofphotosystem II (PSII) and the quantum efficiency ofPSII primary photochemistry is therefore given byFv/Fm = (Fm – Fo)/Fm, where Fv is maximum variablefluorescence. Adaptation to darkness for 10 min priorto the measurement allowed for quantification of themaximal quantum yield, while measurement duringsunlight exposure allowed for quantification of the realquantum yield in steady state.
Abiotic data. Results obtained during the growthexperiment were examined for correlation with hydro-graphic and meteorological parameters of the innerKiel Fjord. Data for sea surface level, water tempera-ture and SR (300 to 2800 nm) were kindly provided bythe Marine Meteorology Department of IFM-GEO-MAR in intervals of 8 min for the whole period of theexperiment. PAR (400 to 700 nm) was measured usinga LI192 quantum sensor connected to a LI1400 datalogger (Li-Cor). Simultaneous measurement of PARand SR during 2 time periods in June 2005 and Novem-ber 2005 allowed the development of a mathematicalmodel that extrapolates PAR from SR with sufficientaccuracy (Fig. 1). Long-term input of PAR above thesea surface could in this way be estimated from long-term input of SR. Depth profiles of PAR attenuation inthe water column were measured in biweekly to
monthly time intervals and used to estimate the long-term input of PAR below the sea surface at differentwater depths.
Growth capacity at low salinities. The capacity ofGracilaria vermiculophylla to grow at different salini-ties — usually in batch cultures and under laboratoryconditions — has repeatedly been investigated (Yokoyaet al. 1999, Raikar et al. 2001, Rueness 2005, Nyberg2007, Thomsen et al. 2007), and it was the purpose ofour experiments to simulate more natural conditions,including continuous water exchange, oscillatingsalinities and grazing. For this purpose, aquaria con-taining 25 l of water with a depth of 0.1 m were usedand exposed to ambient light in 3 successive experi-ments that were conducted in spring, summer andautumn 2007. The flow-through rate was 2 l min–1. Inorder to obtain different salinities seawater from the in-ner Kiel Fjord was mixed with non-chlorinated tap wa-ter in different ratios, so that the final salinity was ap-proximately 80, 60, 40, 20 and 5% of the Kiel Fjordsalinity (13 to 17). Each salinity was tested in 2 aquaria,each of which contained 6 net bags with G. vermi-culophylla. Algal origin and the methodology of growthmeasurement were as in the experiment conducted inthe sea. Salinities were monitored regularly with a con-ductometer (Cond 315i, WTW GmbH), and water tem-peratures were continuously logged (Pendant Temp/Light, HOBO). In order to guarantee sufficient nutrientsupply at all salinities, fertilizer (Hakaphos Gartenfre-und, Compo) was added every 15 min from a stock so-lution (1% in H2O) to the incoming sea- and tapwater,using a dosing pump (Dupla Alpha, Dohse AquaristikKG). In this way, average medium concentrations of1.8 µM NO32–, 8.2 µM NH4+, 1 µM PO43– and 9 nMFe2+/3+ were maintained. Grazers originating from theKiel Fjord were added to G. vermiculophylla at the be-
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Fig. 1. Correlation of photosynthetically active radiation(PAR, 400 to 700 nm) measured and PAR extrapolated fromsolar radiation (SR, 300 to 2800 nm) measured. Line repre-sents the best fitting linear function (r2 = 0.992, p < 0.0001),
dotted lines indicate the 95% prediction interval
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ginning of each experiment at the densities that wereassociated with the alga in nature (5 to 15 Idotea balth-ica Pallas, 2 to 4 Littorina sp., 3 to 19 Gammarus sp.).Densities of associated organisms were determined asdescribed below. Prior to each experiment, G. vermicu-lophylla and grazers were adapted stepwise over 1 wkto reduced salinities. Growth observed at differentsalinities in a given time period was tested for signifi-cant differences (p = 0.05) using Kruskal-WallisANOVA and the Nemenyi post hoc test.
Growth capacity at different light intensity/daylength combinations. Overall light input in summer issimilar in the northern and southern Baltic, while lightintensity and day length regime vary considerably. Anexperiment was therefore conducted in order to inves-tigate possible effects of different combinations of daylength and light intensity upon Gracilaria vermiculo-phylla growth. Aquaria were incubated in a constanttemperature room of 15°C and continuously providedwith filtered seawater (2 l min–1). They were protectedfrom unwanted light with black plastic foil and eithermaintained in darkness or exposed to artificial light for6, 8, 12, or 24 h d–1. Light was provided by 4, 3, 2 and 1fluorescent lamps (Triplus 450 mm 15W, Interpet),respectively, and each lamp provided approximately110 µmol m–2 s–1. In this way, G. vermiculophylla wasexposed to similar daily doses of PAR in all light treat-ments (9.5 mol m–2 d–1). Algal origin and the methodol-ogy of growth measurement were as in the experimentconducted in the sea, with 6 net bags aquarium–1.Growth observed at different salinities in a given timeperiod was tested for significant differences (p = 0.05)using Kruskal-Wallis ANOVA and the Nemenyi posthoc test.
Quantification of associated animals. For the quan-tification of animals that were associated with Graci-laria vermiculophylla and Fucus vesiculosus, 5 algalindividuals (between 50 and 150 g fresh weight) werecollected at Kiel-Wik (54° 21’ 11’’ N, 10° 08’ 29’’ E) inshallow water in a net (mesh size: 0.1 mm) and fixed inseawater containing formaldehyde (4%). The algaewere then systematically browsed and associated ani-mals were identified according to Bick & Gosselck(1985), Jagnow & Gosselck (1987) and Köhn & Gos-selck (1989) and counted. Feeding habits of all taxawere drawn from the same literature. Complete quan-tifications were conducted in February 2006, June2006 and February 2007, in order to cover aspects dur-ing a normal winter, during summer and during anextremely mild winter, respectively. A nonparametric2-way ANOVA according to Sheirer-Ray-Hare (Dyt-ham 2005) was conducted in order to detect significanteffects of season and alga upon the diversity and den-sity of associated organisms. Additional quantificationsof potential main mesograzers on G. vermiculophylla
were conducted prior to growth experiments atreduced salinities (see above).
Feeding experiments. The susceptibility of Graci-laria vermiculophylla and Fucus vesiculosus to se-lected herbivores and omnivores was investigated infeeding trials. Both algae and grazers were collected inKiel-Wik (54°21’11’’N, 10° 08’ 29’’ E). These experi-ments were conducted in small aquaria (2.6 l) thatwere continuously provided with filtered seawater.They were maintained at 15°C in a constant tempera-ture room and exposed to a PAR of 75 µM m–2 s–1 for12 h d–1 (Master ECO TL-D cool white, Philips). Analgal fresh weight of 3 g — either G. vermiculophylla orF. vesiculosus or both species in equal amounts — wasincubated under such conditions with and withoutpotential grazers (6 Idotea balthica, 10 Littorina sp., or32 Gammarus sp.). After 1 wk the algal weight wasquantified by weighing, and the difference betweengrowth controls and treatments indicated the amountof biomass that had been consumed by grazers. TheMann-Whitney U-test and the Wilcoxon test were usedin order to test the consumption rates of grazers in no-choice and 2-way-choice experiments, respectively, forsignificant differences (p = 0.05).
RESULTS
Distribution of Gracilaria vermiculophylla
Between Flensburg and Warnemünde, populationsconsisting of >3 separate fragments of G. vermiculo-phylla were only detected in the Kiel Fjord. Fragmentscast ashore were occasionally found on a coastal rangeextending 75 km east of Kiel. Three largely decom-posed fragments suspected to be G. vermiculophyllawere once detected in Boltenhagen (53° 59’ N,11° 13’ E), approximately 250 km east of Kiel (Fig. 2A).Their identity could not be confirmed, due to their poorcondition. In the Kiel Fjord, G. vermiculophylla wasparticularly abundant in shallow and sheltered waters.Between 2006 and 2007 ground coverage in the KielFjord increased in most observation areas — on aver-age by a factor of approximately 3 (data not shown)—and 2 of 7 areas were newly invaded. A particularlylarge population was present on the west shore ofinner Kiel Fjord (Fig. 2B). The most dense part of thispopulation—covering 50 to 100% of the ground —increased in size from 0.3 ha in 2005 to 1 ha in 2006.In 2007, it covered approximately 2.7 ha, which wasmost of the available sea ground shallower than 2 m inthis area. Ground coverage at the periphery of thispopulation decreased with increasing depth, and onlya few small individuals were detected in water depthsof 5 m or more.
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Fig. 2. Gracilaria vermiculophylla. (A) Distribution between Flensburg and Warnemünde until 2007. (B) Distribution and density in2007 in Kiel Fjord. (C) Mat overgrown in part by Chaetomorpha linum (26 October 2006). (D) Detail of mat in (C), layer of C. linum
has been locally removed. (E) Individuals of Fucus vesiculosus overgrown by G. vermiculophylla
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Sporogenic Gracilaria vermiculophylla or individu-als attached to stones — and thus grown up fromspores — were occasionally detected in the outer KielFjord. In the inner Kiel Fjord G. vermiculophyllalargely grows unattached, lying on the sea floor irre-spective of the substrate type. Even the most densepopulations were only loosely attached to the ground.They consisted of up to 45 cm thick mats of entangledindividuals that covered up to several hundred squaremeters of ground. The basis of such mats was oftendecaying, at the same time the upper layer of the matscontinued to grow. From time to time G. vermiculo-phylla mats were overgrown by ephemeral filamen-tous algae such as Chaetomorpha linum (O.F. Müller)Kützing, which persisted for several weeks, indicatinga relatively stable structure of the mats (Fig. 2C,D). Insome locations the bladder wrack Fucus vesiculosuswas overgrown by G. vermiculophylla mats (Fig. 2E).
Growth in the sea
In a growth experiment conducted in the inner KielFjord, Gracilaria vermiculophylla grew primarily insummer. Between June 2006 and June 2007, growthwas mainly observed before mid-September andafter mid-April, when average rates of SR exceeded3 kWh m–2 d–1 (Fig. 3). Maximal growth rates of 4 to7% d–1 were observed in June and July and directlybelow the water surface. Extreme low tides, exposingG. vermiculophylla to air for extended time periods,usually resulted in losses of biomass. However, suchdying of G. vermiculophylla was not observed innature. For example, an extremely low tide in the KielFjord on 26 to 27 October 2006 exposed substrates andorganisms at water depths of 0.25 and 0.5 m below themean sea surface level for 26 and 16 h to air, respec-tively (Fig. 2C). This event nearly completely killedisolated individuals of G. vermiculophylla that wereexperimentally exposed in net bags at both waterdepths (Fig. 3). In contrast, natural G. vermiculophyllamats at the same depth (Fig. 2C) largely survived thisair exposure event, as could be observed duringrepeated visits to the site.
Growth rates of Gracilaria vermiculophylla at differ-ent water depths and at different times of the year werepositively correlated with PAR at these depths and atthese times (Fig. 4A) (r = 0.71, p < 0.0001). Directly be-low the water surface (0.25 m below the mean sea sur-face), growth was better correlated with SR above thewater surface (r = 0.71, p < 0001; Fig. 4B) than withmean water temperature (r = 0.45, p < 0.0001; Fig. 4C).No or little growth was observed at this water depthwhen SR above the surface was
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m–2 s–1. Increasing water depth resulted, not only in de-creasing growth, but also in decreasing correlations oflight availability and growth. At 5 m below the meansea surface level, growth was negatively correlatedwith water temperature (r = –0.276, p = 0.0003; Fig. 4D).
Gracilaria vermiculophylla that had previously beenincubated for at least 14 d at different water depths didnot differ significantly in the maximum yield of photo-synthesis after adaptation to darkness (Kruskal-WallisANOVA, p = 0.05; Fig. 5). Similarly, the photosyntheticyield in steady state during exposure to sunlight con-taining 210 to 390 µmol m–2 s–1 PAR was not signifi-cantly different in algae that had been adapted for 2wk to a maximum PAR of 30 µmol m–2 s–1 at a waterdepth of 5 m below the mean sea level and algae thathad been adapted to a maximum PAR of 650 µmol m–2
s–1 at a water depth of 0.25 m.
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Fig. 4. Gracilaria vermiculophylla. Effects of sunlight and water temperature in the Kiel Fjord on growth. (A) the ratio betweengrowth at all water depths between 0.25 and 5 m below mean sea level and photosynthetically active radiation (PAR) at thesewater depths, (B,C) the ratios between growth at 0.25 m water depth and solar radiation (SR; B) and water temperature (C),and (D) the ratio between growth at 5 m water depth and water temperature. Lines indicate best fitting logistic (B) and linear
(A,C,D) functions with 95% prediction intervals
0 1 2 3 4 50.0
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Fig. 5. Gracilaria vermiculophylla. Yield of photosynthesisFv/Fm in material from different water depths. Maximumyields were measured after 10 min of darkness adaptation,while real yields were measured in steady state during expo-sure to ambient light (directly below water surface); data are
mean ± 95% CI, n = 6
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Effect of day length and salinity upon growth
Under laboratory conditions, growth of Gracilariavermiculophylla was slightly affected by day lengthwhen equal doses of PAR were applied: growth ratesduring permanent exposure to relatively low lightwere significantly lower than during exposure for 8 or6 h d–1 to stronger light (Fig. 6).
During 3 growth experiments at different salinitiesconducted in spring, summer and autumn with continu-ous water exchange, the average salinity of the incomingseawater was 14.9. However, a higher average salinitywas observed in autumn (16.2) than in spring and sum-mer (14.2), which, accordingly, resulted in differentsalinities, when seawater was mixed with tap water.Additional salinity fluctuations were also observed dur-ing each of the 3 experiments (on average approximately±1). During all 3 experiments, growth of Gracilariavermiculophylla in aquaria supplied with 100% seawa-ter was similar to growth in the sea, while diluted seawa-ter sometimes caused significant growth reductions(Fig. 7). Particularly pronounced effects were observedin summer. For example, a seawater content of 5%caused the death of all algal biomass within 2 wk in sum-mer (mid-May to the end of June; average salinity: 1.0),while such death was neither observed during the 6 wkin spring (mid-March to the end of April; 0.6) nor duringthe 4 wk in autumn (mid-September to mid-October; 1.5)(Fig. 7). In summer, significantly more growth of G. ver-miculophylla was observed during the 6 wk in 100%seawater (salinity: 14.2) than in 80% seawater (10.2)or less (Kruskal-Wallis ANOVA and Nemenyi test,α = 0.05), and this difference was particularly pro-nounced after 4 and 6 wk of incubation (Fig. 7). Inaddition, growth in 20% seawater (4.7) was, after 4 and6 wk, significantly lower than in 40%seawater (5.4) or more (Fig. 7). In contrastto summer, growth rates were not sig-nificantly different among salinitiesranging from 20% (4.3) to 100% (14.2)seawater during 6 wk in spring (salinityrange: 4.3 to 14.2) and 4 wk in autumn(salinity range: 4.3 to 16.2). Of the inver-tebrates that were incubated togetherwith G. vermiculophylla, Littorina spp.and Idotea balthica did not survive in40% seawater or less in spring, summer,or autumn, while Gammarus spp. diedin 20% seawater or less in all 3 experi-ments.
Not surprisingly, the average watertemperature was lower in the spring ex-periment (7.4 to 12.4°C) than in autumn(13.7 to 15.3°C) and summer (13.8 to17.9°C), and the highest water tempera-
tures (15.8 and 17.9°C) were observed in the last 4 wkof the summer experiment, when Gracilaria vermiculo-phylla responded particularly sensitively to low salini-ties. SR was lower in autumn (2.0 to 2.5 kWh m–2 d–1)than in spring (3.0 to 4.7 kWh m–2 d–1) and summer (3.8to 5.3 kWh m–2 d–1).
Associated animals and feeding antagonists
The diversity of most of the functional and taxonomicgroups of animals (all except omnivores, Isopoda andfishes) associated with Gracilaria vermiculophylla mats
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Fig. 6. Gracilaria vermiculophylla. Growth response when ex-posed over 1 wk to no light or to similar daily doses of photo-synthetically active radiation (PAR, 9.3 to 9.7 mol m–2 d–1), butdifferent combinations of light intensity and exposure time;data are mean ± 95% CI, n = 5. Data marked with differentletters were significantly different (Kruskal-Wallis ANOVA
and Nemenyi test, α = 0.05)
Fig. 7. Gracilaria vermiculophylla. Effect of different salinities on growth in 3successive experiments conducted in spring, summer and autumn 2007. Theaverage salinity of 100% seawater was 14.2 in spring and summer and 16.2 inautumn. Results obtained during the same time periods in the sea at a waterdepth of 0.25 m are included for comparison (*); data are mean ± 95% CI,
n = 2 × 6 = 12 (*: n =6)
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and with Fucus vesiculosus individuals growing withinthese mats was affected by the sampling time, in mostcases with significantly less taxa in the relatively coldwinter of 2005/2006 (surface water temperature rangein the 2 mo preceding sampling: –1.1 to 4.6°C) than inthe relatively warm winter of 2006/2007 (surface watertemperature range in the 2 mo preceding sampling:2.8 to 7.6°C) or in the summer of 2006 (Table 1). Totalanimals, omnivores, Bivalvia, Isopoda and Amphipodawere overall more diverse on G. vermiculophylla thanon F. vesiculosus (Table 1). This difference was strongeror only present in winter (February 2006 and/or Febru-ary 2007) and the diversity was therefore subject to sig-nificant interactive effects of season and associatedalga (Table 1).
Seasonal differences were also observed in the den-sity of most functional groups and taxa that were asso-ciated with the 2 algae (all except Gammarus salinus,omnivores and Idotea balthica; Table 2), with particu-larly low densities in February 2006. G. salinus wasnearly exclusively detected on Gracilaria vermiculo-phylla. Overall, higher densities of Gammarus spp.,I. balthica, omnivores and various mussels were alsodetected on G. vermiculophylla (Table 2). Similar tothe diversity, the density of associated animals oftendiffered among the 2 algal species in winter, but notin summer, and was subject to significant interactiveeffects of season and alga (Table 2). For example, I.balthica was, in winter, exclusively present on G. ver-miculophylla, while Pomatoschistus pictus was onlydetected in summer and with G. vermiculophylla. Lar-vae of filter feeders such as Mya arenaria and Cerasto-derma lamarckii settled preferentially on G. vermicu-lophylla, but did not persist on this alga until summer.
Of the animals associated with Gracilaria vermiculo-phylla and known as consumers of macroalgae, onlyLittorina spp., Idotea balthica and Gam-marus spp. were relatively abundantand therefore considered to be poten-tially important grazers. No-choice-feeding trials revealed that all 3 havethe capacity to feed on G. vermiculo-phylla (Fig. 8). Both in summer and win-ter, the largest amounts were ingestedby I. balthica. However, I. balthica con-sumed more Fucus vesiculosus in no-choice assays, and this preference wasconfirmed when G. vermiculophyllaand F. vesiculosus were offered togetherin 2-way-choice assays. A clear prefer-ence for F. vesiculosus was also ob-served in a 2-way-choice assay with Lit-torina spp. in winter, but not in summer.Gammarus spp. only consumed signifi-cant amounts of G. vermiculophylla.
DISCUSSION
Within 1 yr of survey, Gracilaria vermiculophyllaclearly increased on a local scale within the KielFjord. In contrast with this — and also in contrast withthe marked spreading of G. vermiculophylla over acoastal range of 150 km around Göteborg (Sweden)within 2 yr (Nyberg 2007), little confirmed spreadingwas observed along the German Baltic coast. Frag-ments suspected to be G. vermiculophylla were, onone occasion, detected at a distance of 250 km east ofKiel, and it is not impossible that the alga was pre-sent at densities below the detection limit at othersites. However, it is also possible that the potential ofG. vermiculophylla of being transported is not quiteas high in the inner Baltic Sea as in environmentswith regular tidal currents. The alga predominantlylies loose, drifts and is capable of propagating byfragmentation, but it has no great buoyancy, whichlimits the distance that can be overcome by drifting.The global spreading of G. vermiculophylla has beensuspected to result from its association with oysters(Rueness 2005, Thomsen et al. 2007), but cultivationof mollusks has little economic importance in theBaltic Sea. G. vermiculophylla does not usually growon ship hulls (which would increase the risk ofanthropogenic dispersal). Moreover, attachment of G.vermiculophylla to hard substrates largely dependson the formation of spores, which so far happens rela-tively rarely in the Kiel Fjord. The future long-dis-tance spreading of G. vermiculophylla into the BalticSea may, therefore, rely on entanglement with boatpropellers or anchors, fishing gear, etc., or on trans-port with ballast water and could result in a patchyrather than a closed distribution area during the nextdecades.
259
Fig. 8. Gracilaria vermiculophylla and Fucus vesiculosus. Consumption in: (A)summer and (B) winter by 3 different grazers. The algae were offered either sep-arately (no-choice assay) or together (2-way-choice assay). Significantly differentconsumption rates of G. vermiculophylla and F. vesiculosus in the same seasonby the same grazer are marked by asterisks (no-choice assays, Mann-WhitneyU-test, α = 0.05) and crosses (2-way choice assays, Wilcoxon test, α = 0.05);
data are mean ± 95% CI, n = 8. nd = no data
-
Aquat Biol 3: 251–264, 2008260
AS
A ×
SF
eb 2
006
Jun
200
6F
eb 2
007
F. v
esic
ulo
sus
G. v
erm
icu
l.F.
ves
icu
losu
sG
. ver
mic
ul.
F. v
esic
ulo
sus
G. v
erm
icu
l.M
edia
n25
%M
edia
n25
%M
edia
n25
%M
edia
n25
%M
edia
n25
%M
edia
n25
%
To
tal
anim
als
++
–1
(1–1
)4
(3–
5)7
(7–
9)7
(6–
9)5
(5–
6)13
(12
–16)
Her
biv
ores
–+
–0
(0–
0)1
(0–2
)2
(2–2
)2
(2–2
)2
(2–2
)4
(3–
5)O
mn
ivor
es+
–+
0(0
–0)
1(1
–1)
1(1
–2)
0(0
–1)
0(0
–1)
3(2
–3)
Car
niv
ores
–+
–0
(0–
0)0
(0–
0)1
(1–2
)2
(2–2
)1
(0–1
)2
(2–2
)D
etri
tivo
res
–+
–0
(0–
0)1
(1–1
)1
(0–2
)1
(1–1
)1
(1–1
)2
(1–2
)F
ilte
r fe
eder
s–
+–
1(1
–1)
1(1
–1)
1(1
–2)
1(1
–1)
1(1
–2)
3(3
–3)
Gas
trop
oda
–+
–0
(0–
0)1
(1–2
)2
(1–2
)1
(1–1
)3
(3–
3)3
(3–
3)B
ival
via
++
+1
(1–1
)1
(1–1
)1
(0–1
)1
(1–1
)1
(1–1
)3
(3–
3)Is
opod
a+
–+
0(0
–0)
1(1
–1)
1(1
–1)
0(0
–1)
0(0
–1)
2(2
–3)
Am
ph
ipod
a+
+–
0(0
–0)
1(0
–1)
2(2
–2)
2(2
–2)
0(0
–0)
3(3
–4)
Dec
apod
a–
+–
0(0
–0)
0(0
–0)
1(1
–1)
1(1
–1)
1(0
–1)
2(1
–2)
Pis
ces
––
–0
(0–
0)0
(0–
0)0
(0–
0)1
(0–1
)0
(0–
0)0
(0–1
)
Tab
le 1
. D
iver
sity
(ta
xa k
g–
1 ) o
f an
imal
s as
soci
ated
wit
h G
raci
lari
a ve
rmic
ulo
ph
ylla
and
Fu
cus
vesi
culo
sus
at 3
dif
fere
nt
sam
pli
ng
s. M
edia
n o
f n
= 5
(25
% q
uar
tile
s in
bra
cket
s). S
ign
ific
ant
(non
par
amet
ric
2-w
ay A
NO
VA
acc
ord
ing
to
Ste
irer
-Ray
-Har
e, p
= 0
.05)
eff
ects
of
alg
a (A
) or
sam
pli
ng
tim
e (S
), a
s w
ell
as s
ign
ific
ant
inte
ract
ion
s (A
×S
) ar
e in
dic
ated
by
a p
lus
sig
n, n
on-s
ign
ific
ance
is in
dic
ated
by
a m
inu
s si
gn
AS
A ×
SF
eb 2
006
Jun
200
6F
eb 2
007
F. v
esic
ulo
sus
G. v
erm
icu
l.F.
ves
icu
losu
sG
. ver
mic
ul.
F. v
esic
ulo
sus
G. v
erm
icu
l.M
edia
n25
%M
edia
n25
%M
edia
n25
%M
edia
n25
%M
edia
n25
%M
edia
n25
%
To
tal
anim
als
–+
–14
(14
–14)
268
(213
–295
)25
15(3
85–
3836
)59
0(1
92–
790)
798
(674
–87
1)29
67(2
175
–34
52)
Her
biv
ore
s–
+–
0(0
–0)
6(0
–9)
233
(78
–254
)98
(38
–33
3)31
7(1
75–
340)
109
(109
–155
)L
itto
rin
a li
ttor
eaL
.–
+–
0(0
–0)
0(0
–3)
12(0
–29)
0(0
–0)
129
(98
–159
)29
(27
–50
)L
itto
rin
a sa
xati
lis
–+
–0
(0–
0)0
(0–
0)0
(0–1
0)0
(0–
0)15
9(7
7–2
01)
27(2
4–
44)
Oli
viG
amm
aru
ssp
p.
++
–0
(0–
0)3
(0–
9)78
(20
–233
)98
(38
–33
3)0
(0–
0)48
(36
–54
)G
. sal
inu
sS
poo
ner
+–
–0
(0–
0)3
(0–
9)0
(0–
0)15
(0–1
04)
0(0
–0)
10(5
–36
)O
mn
ivo
res
+–
+0
(0–
0)64
(61
–72
)19
(12
–233
)0
(0–
49)
0(0
–2)
286
(168
–39
7)Id
otea
bal
thic
a+
–+
0(0
–0)
64(6
1–
72)
19(1
2–2
33)
0(0
–49
)0
(0–
0)26
2(1
39–
347)
Pal
las
Car
niv
ore
s–
+–
0(0
–0)
0(0
–0)
39(3
7–
39)
98(4
5–
98)
6(0
–11)
30(2
4–
38)
Pal
aem
on e
leg
ans
L.
–+
–0
(0–
0)0
(0–
0)26
(0–
39)
49(3
0–
78)
6(0
–7)
0(0
–0)
Pal
aem
on s
qu
illa
–+
+0
(0–
0)0
(0–
0)0
(0–1
2)0
(0–
0)0
(0–
0)20
(12
–27)
Rat
hk
eP
omat
osch
istu
s –
++
0(0
–0)
0(0
–0)
0(0
–0)
15(0
–21)
0(0
–0)
0(0
–0)
pic
tus
Mal
mD
etri
tivo
res
–+
–0
(0–
0)4
(3–
4)13
(0–1
47)
19(1
5–
39)
130
(109
–175
)78
1(7
50–1
200)
Hyd
rob
iasp
.–
+–
0(0
–0)
4(3
–4)
13(0
–19)
0(0
–0)
130
(109
–175
)75
0(6
79–
942)
Fil
ter
feed
ers
–+
+14
(14
–14)
196
(147
–226
)18
56(5
8–
3209
)78
(21
–96
)22
2(1
89–
503)
1080
(107
3–1
567)
Myt
ilu
s ed
uli
sL
.+
+–
14(1
4–1
4)19
2.5
±50
.724
(0–
58)
96.1
±10
3.7
175
(142
–222
)98
5(9
64–1
538)
Mya
are
nar
iaL
.+
++
0(0
–0)
0(0
–0)
0(0
–0)
0(0
–0)
0(0
–0)
12(1
0–2
1)C
eras
tod
erm
a +
++
0(0
–0)
0(0
–0)
0(0
–0)
0(0
–0)
0(0
–0)
20(1
1–
44)
lam
arck
ii R
eeve
Tab
le 2
. D
ensi
ties
(in
d.
kg
–1 )
of
anim
als
asso
ciat
ed w
ith
Gra
cila
ria
verm
icu
lop
hyl
laan
d F
ucu
s ve
sicu
losu
sat
3 d
iffe
ren
t sa
mp
lin
gs.
Med
ian
of
n =
5 (
25%
qu
arti
les
inb
rack
ets)
. Sig
nif
ican
t (n
onp
aram
etri
c 2-
way
AN
OV
A a
ccor
din
g t
o S
teir
er-R
ay-H
are,
p =
0.0
5) e
ffec
ts o
f al
ga
(A)
or s
amp
lin
g t
ime
(S),
as
wel
l as
sig
nif
ican
t in
tera
ctio
ns
(A ×
S)
are
ind
icat
ed b
y a
plu
s si
gn
, non
-sig
nif
ican
ce is
ind
icat
ed b
y a
min
us
sig
n
-
Weinberger et al.: Gracilaria invasion in the Baltic Sea
In the Kiel Fjord, with a maximum depth of 17 m, sin-gle drifting individuals of Gracilaria vermiculophyllawere detected in most locations, but large populationswere only present in relatively sheltered and shallowareas. This may be a result of the drifting life history ofthe alga. However, multiplication of the yields andlosses of biomass observed in 2006/2007 during exper-imental exposure of G. vermiculophylla in the seashows that net growth is impossible long term at waterdepths of 3 m or more below the mean sea surface level(Table 3). In contrast, the annual average of dailygrowth at the first 2 m below the mean sea surfacelevel was 18.45 mg g–1 and nearly 80-fold biomass in-creases per year are possible in shallow water as longas G. vermiculophylla survives extremely low tides,which was usually the case in 2006/2007 (Table 3).The peak growth rates obtained at a water depth of0.25 m reach approximately 30% of the maximalgrowth rates observed with G. vermiculophylla underoptimized laboratory conditions (Raikar et al. 2001). At5 m below the mean sea surface level, 84% of theG. vermiculophylla biomass exposed degraded within1 yr (Table 3). Single individuals were occasionally de-tected in deeper water, but they probably drifted tothese regions after they had grown up in shallower wa-ter. Thalli of G. vermiculophylla that are kept in insuf-ficient light conditions may survive for long periods oftime (Rueness 2005, Nyberg 2007, Thomsen et al.2007). The loss of algal biomass at water depths below3 m that was observed in our experiments indicatesthat G. vermiculophylla will nonetheless eventually bedegraded in nature. At a depth of 5 m, the loss of bio-mass increased with increasing water temperature,suggesting that it was due to biological processes suchas grazing or respiration, rather than to mechanicaldamage. The order of magnitude of biomass drifting todepths below the light compensation point is difficultto estimate, but it may be considerable: G. vermiculo-
phylla, experimentally exposed in situ, on average pro-duced an 18.5-fold increase of biomass in the first 2 mbelow mean sea surface level, while the size of naturalpopulations in the Kiel Fjord was only estimated to in-crease by a factor of 3. Increases in weight and inground coverage are obviously difficult to compare,but the discrepancy must at least in part be due to lossof biomass to deeper waters.
Our study indicates that only a few potential con-sumer species are associated with Gracilaria vermicu-lophylla in the Kiel Fjord at numbers high enough tocause significant biomass loss. Multiplication of thenumbers of individuals that were detected on the algawith the amounts of algal biomass that were consumedper individual and day in feeding trials allows an esti-mation of biomass consumption in nature. Accordingto this calculation of each gram of G. vermiculophyllain June 2006 approximately 2 mg d–1 were consumed.At the same time growth rates in the sea reached up to60 mg g–1 d–1, indicating that an efficient control bygrazers did not take place. In February 2006 — after arelatively cold winter — consumption was considerablyless (approximately 0.4 mg g–1 d–1) than in June 2006,while it was nearly as high as in June after a mild win-ter in February 2007 (approximately 1.6 mg g–1 d–1).In situ growth rates of G. vermiculophylla during 2successive time intervals of 2 wk in February 2007, at awater depth of 0.25 m, were determined as 1.5 mg g–1
d–1 (95% CI: 1.9) and 2.1 mg g–1 d–1 (95% CI: 1.9),indicating that growth in nature was, at that time,approximately in the same order of magnitude as con-sumption. In conclusion, grazing may prevent G.vermiculophylla biomass in the Kiel Fjord fromincreasing in winter, but not in summer. In our experi-ments, grazers from the Kiel Fjord did not survive atsalinities of approximately 5.5 or less and the effect ofgrazing upon G. vermiculophylla in areas with salini-ties
-
Aquat Biol 3: 251–264, 2008
also suggest that the growth inhibition in winter is notdue to a day length effect: G. vermiculophylla grewslightly better under short-day than under long-dayconditions, when it was provided with the same totalamount of PAR.
In the sea and at a water depth of 0.25 m below themean surface level, Gracilaria vermiculophylla wascapable of growing, when SR above the water surfaceexceeded an average level of approximately 3.5 kWhm–2 d–1. According to the Surface Meteorology andSolar Energy (SSE)-Model of NASA (Chandler et al.2004) such conditions are below the long-term aver-age given for all parts of the Baltic Sea from May toAugust and for all parts except the northern BothnianSea also in April. Our results indicate that G. vermicu-lophylla grows somewhat less when it is exposed forlong time periods to low light than when it is exposedfor short periods to high light. A growth reduction ofup to 15% due to less intense SR may, therefore, beexpected in the northern part of the Baltic Sea.Nonetheless, sufficient amounts of SR should be avail-able in all parts of the Baltic Sea to sustain growth ofG. vermiculophylla.
Marked effects of salinity on survival and growthperformance were observed in our experiments, sug-gesting that this factor rather than insolation may limitthe future spread of Gracilaria vermiculophylla in theBaltic Sea. The growth optimum of G. vermiculophyllahas been determined in different studies to lie be-tween salinities of 10 and 35 (Yokoya et al. 1999), be-tween 10 and 20 (Rueness 2005) and at 15 (Raikar et al.2001). Following this information the salinity in KielFjord (13 to 17) and adjacent waters is optimal for thegrowth of G. vermiculophylla and further spreadinginto the Baltic Sea should confront it with successivelyless favorable salinities.
Yokoya et al. (1999) and Nyberg (2007) reportedthat Gracilaria vermiculophylla is capable of growingat salinities of 5 and 2, respectively. In our study, sur-vival and even slow growth were possible at salinitiesas low as 0.5 and 1.6, although only in spring andautumn. Interestingly, G. vermiculophylla was moreresponsive to different salinities in summer than inspring or autumn, with reduced growth at 10.2, veryreduced growth at 4.7 and incapacity to survive at 1.The ultimate cause for this seasonally variable sus-ceptibility remains unclear. However, it is reminiscentof the increasing sensitivity of G. vermiculophyllatoward high salinities during a water temperatureincrease from 11.5 to 20°C (Rueness 2005). A similareffect of temperature on the sensitivity of G. vermicu-lophylla to low salinities may explain our observa-tions: particularly high sensitivity toward low salinitywas detected in periods when the water temperatureexceeded 15.3°C.
Under present salinity conditions, Gracilaria ver-miculophylla should find optimal conditions with max-imum growth rates in summer in the Belt Sea. Goodgrowth with reduced peak rates in summer should alsobe possible in most parts of the inner Baltic, wheresalinities do not usually fall below 5.5. The perfor-mance of G. vermiculophylla in the Bothnian Gulf andthe inner Gulf of Finland will probably be severelyreduced, since water temperatures in summer must beexpected to increase the algal sensitivity toward theprevailing low salinities.
Our observations suggest that Gracilaria vermiculo-phylla has the potential to modify certain habitats inthe Baltic Sea, for example, as a competitor of othermacrophytes. In the Kiel Fjord and adjacent waterssheltered shallow environments are until now typicallyinhabited by Fucus vesiculosus and other Fucus spe-cies, when hard bottom substrate is available. How-ever, as in other regions of the Baltic Sea, Fucus spp.generally perform better in wave-exposed areas,which has been attributed to reduced recruitment suc-cess on substrates that are covered by silt or filamen-tous algae (Berger et al. 2003, Isaeus 2004). Coverageof hard substrate by drifting or attached G. vermiculo-phylla may, however, interfere with the settlement ofFucus spp. Moreover, our preliminary evidence indi-cates that G. vermiculophylla has the capacity to over-grow and probably shade F. vesiculosus.
Gracilaria vermiculophylla is not restricted to hardbottom substrates. Therefore, it also has a potential tomodify soft-bottom communities, which dominate inthe Kiel Fjord and adjacent waters. Seagrass (Zosterasp.) beds typically develop in water depths between1 and 5 m below sea surface level in the westernBaltic (authors’ per. obs.). Therefore, they may overlapwith the lower distribution range of G. vermiculo-phylla. A first settlement of G. vermiculophylla individ-uals in seagrass beds in the Kiel Fjord was observed in2006. During the first year, we could not observe obvi-ous effects on the seagrass (M. Wahl pers. obs.), whichmay be due to the relatively low density of the invader.It has been shown that intermediate amounts of ben-thic drift algae may add resources and increase thehabitat complexity of otherwise bare soft bottom (Raf-faelli et al. 1998, Norkko et al. 2000), causing the diver-sity and density of infauna and epifauna to increase(Bolam et al. 2000, Rossi & Underwood 2002). In con-trast, extended closed macroalgal mats may cause oxy-gen deficiency and subsequent changes of infauna(Norkko & Bonsdorff 1996a,b). Such effects may poten-tially also be caused by G. vermiculophylla. During thesummer of 2007, the sediments under extended G. ver-miculophylla mats in Kiel Fjord often appearedhypoxic. These oxygen depletion events were pro-bably due to excessive input of decomposing organic
262
-
Weinberger et al.: Gracilaria invasion in the Baltic Sea
matter. However, it is unknown whether they hadoccurred before G. vermiculophylla arrived.
Seagrass beds and Fucus spp. belts in the Baltic Seaare known to be essential nursery grounds for inverte-brates and fish (Anders & Möller 1988, Beck et al. 2001,Worm & Karez 2002, Moore & Short 2006, Rönnbäck etal. 2007). However, in our experiments, the diversityand density of such organisms in Gracilaria vermicu-lophylla mats were similar or higher than on Fucusvesiculosus. Apparently, G. vermiculophylla has thecapacity to deliver some ecological services that areprovided by Fucus spp. Interestingly, the main meso-grazer of F. vesiculosus in the Kiel Fjord (Idotea balth-ica) also uses G. vermiculophylla as a refuge in winter.This choice is not due to feeding preferences, since I.balthica in all seasons preferentially fed on F. vesiculo-sus rather than on G. vermiculophylla. If the presenceof G. vermiculophylla increases the abundance of iso-pods by providing suitable shelter, then individuals ofF. vesiculosus in the close vicinity of G. vermiculo-phylla mats may experience increased consumptionby I. balthica. Preferential grazing by I. balthica mayresult in the decline of F. vesiculosus relative to otherseaweeds (Schaffelke et al. 1995, Engkvist et al. 2004).Mesograzers could, thus, modulate the competitionbetween G. vermiculophylla and other seaweeds.
In conclusion, the performance of Gracilaria vermicu-lophylla in different parts of the Baltic depends on thehighly complex, interactive effects of salinity, light, tem-perature, competitors and consumers. It is difficult topredict exactly how fast and far G. vermiculophylla willspread, and how it will fare in the new locations, but thespecific conditions in the Baltic appear particularly favor-able. Based on our results, a future spread of G. vermicu-lophylla to the Åland archipelago (60° N) and beyondinto the southern Bothnian Gulf appears as probable andas possible, respectively. The alga may, therefore, beable to reach latitudes that are located 10° or more fur-ther north than the northern edge of its natural distribu-tion range (Island of Sacchalin, approximately 52° N, asG. verrucosa; Skriptsova et al. 2001) and 2° or more fur-ther north than the northern edge of its distributionrange on the European Atlantic coast. As to the impact ofsuch a potential invasion upon native communities, theeffects may be not only be negative (e.g. loss of habitatfor Fucus vesiculosus), but also positive (e.g. functionalreplacement of F. vesiculosus and gain of habitat for sea-weed-associated organisms on soft-bottom substrates),which for other reasons has been receding for decades.
Acknowledgements. We thank the department for MarineMeteorology at IFM-GEOMAR for data on shortwave solarradiation, water temperature and tide gauge in Kiel Fjord. Wealso thank Mareike Hammann, Ammelie Heimholt and KaiLohbeck for help with experiments.
LITERATURE CITED
Anders K, Möller H (1988) Seasonal fluctuations in macroben-thic fauna of the Fucus belt in Kiel Fjord (western BalticSea). Mar Ecol Prog Ser 103:141–150
Beck MW, Heck KL, Able KW, Childers DL and others (2001)The identification, conservation, and management of estu-arine and marine nurseries for fish and invertebrates. Bio-Science 51:633–641
Bellorin AM, Oliveira MC, Oliveira EC (2004) Gracilaria ver-miculophylla: a western Pacific species of Gracilariaceae(Rhodophyta) first recorded from the eastern Pacific.Phycol Res 52:69–79
Berger R, Henriksson E, Kautsky L, Malm T (2003) Effects offilamentous algae and deposited matter on the survival ofFucus vesiculosus L. germlings in the Baltic Sea. AquatEcol 37:1–11
Bick A, Gosselck F (1985) Arbeitsschlüssel zur Bestimmung derPolychaeten der Ostsee. Mitt Zool Mus Berlin 61:171–272
Bolam SG, Fernandes TF, Read P, Raffaelli D (2000) Effects ofmacroalgal mats on intertidal sandflats: an experimentalstudy. J Exp Mar Biol Ecol 249:123–137
Boudouresque CF, Verlaque M (2002) Biological pollution inthe Mediterranean Sea: invasive versus introducedmacrophytes. Mar Pollut Bull 44:32–38
Chandler WS, Whitlock CH, Stackhouse PW Jr (2004) NASAclimatological data for renewable energy assessment. JSol Energy Eng 126:945–949
Dytham C (2005) Choosing and using statistics: a biologist’sguide, 2nd edn. Blackwell Publishing, Oxford
Engkvist R, Malm T, Nilsson J (2004) Interaction between iso-pod grazing and wave action: a structuring force in macro-algal communities in the southern Baltic Sea. Aquat Ecol38:403–413
Freshwater DW, Montgomery F, Greene JK, Hamner RM,Williams M, Whitfield PE (2006) Distribution and identifi-cation of an invasive Gracilaria species that is hamperingcommercial fishing operations in southeastern North Car-olina, USA. Biol Invasiom 8:631–637
Jagnow B, Gosselck F (1987) Bestimmungschlüssel für dieGehäuseschnecken und Muscheln der Ostsee. Mitt ZoolMus Berlin 63:191–268
Isæus M, Malm T, Persson S, Svensson A (2004) Effects of fila-mentous algae and sediment on recruitment and survivalof Fucus serratus (Phaephyceae) juveniles in the eutrophicBaltic Sea. Eur J Phycol 39:301–307
Köhn J, Gosselck F (1989) Bestimmungsschlüssel der Malako-straken der Ostsee. Mitt Zool Mus Berlin 65:3–114
Maggs CA, Stegenga H (1999) Red algal exotics on North Seacoasts. Helgol Meersunters 52:243–258
Meier HEM (2006) Baltic Sea climate in the late twenty-firstcentury: a dynamical downscaling approach using twoglobal models and two emission scenarios. Clim Dyn 27:39–68
Moore KA, Short FT (2006) Zostera: biology, ecology, andmanagement. In: Larkum AWD, Orth RJ, Duarte CM (eds)Seagrasses: biology, ecology and conservation. Springer,Dordrecht, p 361–386
Nielsen R, Kristiansen A, Mathiesen L, Mathiesen H (1995)Distributional index of the benthic macroalgae of theBaltic Sea area. Acta Bot Fenn 155:1–55
Norkko A, Bonsdorff E (1996a) Altered benthic prey-avail-ability due to episodic oxygen deficiency caused by drift-ing algal mats. PSZNI: Mar Ecol 17:355–372
Norkko A, Bonsdorff E (1996b) Population responses ofcoastal zoobenthos to stress induced by drifting algalmats. Mar Ecol Prog Ser 140:141–151
263
-
Aquat Biol 3: 251–264, 2008
Norkko J, Bonsdorff E, Norkko A (2000) Drifting algal mats asan alternative habitat for benthic invertebrates: speciesspecific responses to a transient resource. J Exp Mar BiolEcol 248:79–104
Nyberg C (2007) Introduced marine macroalgae and habitatmodifiers—their ecological role and significant attributes.PhD thesis, Göteborg University, Göteborg
Nyberg CD, Wallentinus I (2005) Can species traits be used topredict marine macroalgal introductions? Biol Invest 7:265–279
Paavola M, Olenin S, Leppäkoski E (2005) Are invasive spe-cies most successful in habitats of low native species rich-ness across European brackish water seas? Estuar CoastShelf Sci 64:738–750
Raffaelli DG, Raven JA, Poole LJ (1998) Ecological impact ofgreen macroalgal blooms. Oceanogr Mar Biol Ann Rev 36:97–126
Raikar SV, Ima M, Fujita Y (2001) Effects of temperature,salinity and light intensity on the growth of Gracilaria spp.(Gracilariales, Rhodophyta) from Japan, Malaysia andIndia. Indian J Mar Sci 30:98–104
Rönnbäck P, Kautsky N, Pihl L, Troell M, Söderqvist T,Wennhage H (2007) Ecosystem goods and services fromSwedish coastal habitats—identification, valuation, andimplications of ecosystem shifts. Ambio 36:534–544
Rossi F, Underwood AJ (2002) Small-scale disturbance andincreased nutrients as influences on intertidal macroben-thic assemblages: experimental burial of wrack in differ-ent intertidal environments. Mar Ecol Prog Ser 241:29–39
Rueness J (2005) Life history and molecular sequences ofGracilaria vermiculophylla (Gracilariales, Rhodophyta),a new introduction to European waters. Phycologia 44:120–128
Schaffelke B, Evers D, Walhorn A (1995) Selective grazing ofthe isopod Idotea baltica between Fucus evanescens and
F. vesiculosus from Kiel Fjord (western Baltic). Mar Biol124:215–218
Schories D, Selig U (2006) How to deal with alien specieswithin the EU Water Framework Directive? RostockMeeresbiol Beitr 15:147–158
Skriptsova AV, Titlyanova TV, Titlyanov EA (2001) Red algaeof the genus Gracilaria in the south of the Russian far east.Russ J Mar Biol 27:538–542
Terada R, Yamamoto H (2002) Review of Gracilaria vermicu-lophylla and other species in Japan and Asia. In: Abbott IA(ed) Taxonomy of economic seaweeds, Vol 8. CaliforniaSea Grant College Program, University of California, LaJolla, CA, p 215–224
Thomsen MS, Gurgel CFD, Fredericq S, McGlathery KJ(2006) Gracilaria vermiculophylla (Rhodophyta, Gracilari-ales) in Hog Island Bay, Virginia: a cryptic alien and inva-sive macroalga and taxonomic correction. J Phycol 42:139–141
Thomsen MS, Staehr PA, Nyberg CD, Schwaerter S, Krause-Jensen D, Silliman BR (2007) Gracilaria vermiculophylla(Ohmi) Papenfuss, 1967 (Rhodophyta, Gracilariaceae) innorthern Europe, with emphasis on Danish conditions,and what to expect in the future. Aquatic Invasions 2:83–94
Tseng CK, Xia BM (1999) On the Gracilaria in the westernPacific and the southeastern Asia region. Bot Mar 42:209–217
Worm B, Karez R (2002) Competition, coexistence and diver-sity on rocky shores. In: Sommer U, Worm B (eds) Com-petiton and coexistence. Ecological Studies 161. Springer-Verlag, Heidelberg, p 133–164
Yokoya NS, Kakita H, Obika H, Kitamura T (1999) Effects ofenvironmental factors and plant growth regulators ongrowth of the red alga Gracilaria vermiculophyllafrom Shikoku Island, Japan. Hydrobiologia 398/399:339–347
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Editorial responsibility: Erik Bonsdorf, Åbo, Finland andKarsten Reise, Sylt, Germany
Submitted: November 2, 2007; Accepted: July 11, 2008Proofs received from author(s): August 26, 2008
cite3: cite4: cite5: cite6: cite7: cite8: cite9: cite10: cite11: cite12: cite13: cite15: cite16: cite17: cite18: cite19: cite20: cite21: cite22: cite23: cite25: cite26: cite1: cite2: cite14: