Marine Turf of an Invasive Alga Ousts Lugworms From Lower Shore

Bare sandy ats at and below low tide level were observed in 2020 to have been invaded by an introduced grass-like alga, Vaucheria cf. velutina (Xanthophyceae). A dense algal turf accumulated and stabilized mud where resident seniors of the lugworm Arenicola marina had reworked rippled sand. Algae and worms were incompatible. Initially, rising patches with algal turf alternated with bare pits where lugworms crowded. Their bioturbation inhibited young algae, while the felt of established algal rhizoids clogged feeding funnels of worm burrows. Eventually, the mosaic pattern of competitors gave way to a coherent algal turf without lugworms. Concomitantly, a rich small-sized benthic fauna took advantage of the novel algal turf. This exotic Vaucheria has the potential for taking over at the lower shore of the Wadden Sea (eastern North Sea, European Atlantic).


Introduction
In an increasingly interconnected human world, invasive alien species transform ecological webs, particularly on island and coastal ecosystems (Anton et al. 2019;Pyšek et al. 2020). In marine and estuarine sediments, effects may escalate when alien sediment stabilizers rival with resident destabilizers for bio-engineering dominance (Crooks 2002;Sousa et al. 2009;Guy-Haim et al. 2017). We here present the story of a regime shift from marine sandy bottom reworked by resident lugworms Arenicola marina towards a muddy turf of an invading alga with an extensive rhizoid felt in the sediment. This is a striking example for ecological change in the wake of biological globalization. In the Wadden Sea, resident lugworms recycle the upper layer of sediment 10-20 times per year through their guts (Cadée 1976) and keep the sand permeable with their reworking and irrigating activities (Volkenborn et al. 2007). The seniors of lugworms dwell at modest density on sand bars of the lower shore (Beukema and de Vlas 1979;Lackschewitz and Reise 1998;Reise et al. 2001). There, loose sand and strong hydrodynamics keep this habitat free from macroalgal growth. A nascent invasion of an exotic member of the genus Vaucheria (Xanthophyceae) is about to change this.
Based on plastid encoding rbcL-gene sequences and psbA/rbcL spacer region, the Vaucheria at the lower shore is distinct from that at upper shore salt marshes, although morphology suggests it belongs to the cosmopolitan V. velutina C. Agardh 1824 (Rybalka et al., submitted). We suspect a complex of hidden species, and refer to the population of the lower shore as V. cf. velutina until taxonomic revision. Green unicellular laments, up to 8 cm long and with a mean density of 1.5 mm − 2 , are anchored with felted rhyzoids down to 5 cm in the sediment. In only three years, this Vaucheria spread over an area of 180 ha at the lee side of the island of Sylt in the northern Wadden Sea, generating bumpy mud with hummocks up to 20 cm higher than ambient sand ats (Reise et al., submitted).
Lugworms are sedentary but keep the upper sediment layer in motion by feeding funnels with downward sliding surface sediment and by mounds of fecal strings with ejections about every half hour (Riisgård and Banta 1998;Wendelboe et al. 2013). This sediment reworking activity seems incompatible with sediment stabilizing Vaucheria. Interference competition is to be expected between such antagonistic benthic bioengineers. What are the mechanisms at work and how does the competitive contest proceed?
How is this cascading into associated benthos? We here present observations on the initial phase of an invasion by an alien species which may have far-reaching and lasting effects on benthic processes in the Wadden Sea and beyond.

Area And Methods
In the northern Wadden Sea, the List tidal basin at the Danish-German boundary comprises 400 km² with vast intertidal and shallow subtidal sandy ats, intersected by deep channels (Gätje and Reise 1998). Tides are semi-diurnal with a range of almost 2 m. Salinity ranges from 26 to 32, and mean water temperatures from 0 to 20°C with a recent warming of 1°C since the 1980s (Rick et al. 2021). Muddy beds of Vaucheria cf. velutina were rst discovered in June 2020 from + 0.2 m to -0.5 m relative to mean low tide level at shoals in Blidsel Bay, east of northern Sylt (54°97' N, 08°38' E; Rybalka et al., submitted; Reise et al., submitted). All investigations reported here were carried out at that site.
As a proxy of lugworm abundance on ambient sand ats, fecal mounds of Arenicola marina were counted per unit area (10 m² at very low to 0.25 m² at high density) during low tide exposure. As a proxy of body size, diameters of fecal strings were estimated to the nearest millimeter. Sixteen individuals were dug out, cleaned and put on blotting paper, and then into calibrated cylinders with seawater for measuring individual volume to the nearest 0.1 cm³. Length of relaxed worms was estimated to nearest centimeter.
To measure Vaucheria, tubes of 10 cm² cross section and sharpened lower edge, were gently screwed through the algal turf to a depth of 5 cm. Obtained sediment cores were washed through a 125-µm mesh and algal tufts were picked up with forceps. These were further washed to remove adhering sand grains.
Entangled tubes of spionid worms were individually pulled out and other algae (mainly Rhizoclonium and Ectocarpus) were removed when present. Vaucheria was then put on blotting paper for 6 h in sunlight to dry. Weight to nearest mg was used as a proxy for the phytomass of Vaucheria. This was done with 3 replicate samples taken along a 150-m transect with intervals every 25 m, reaching from bare ambient sand at through a belt of young growth and into the interior of an established bed of Vaucheria on June 23 in 2020. Concomitantly, algal cover was categorized from 0 with no green laments above sediment surface, 1 with few laments, 2 with modest density and 3 with complete cover at 10-cm² areas, replicated 20 times at each interval. Along the same transect the abundance of lugworm fecal mounds was counted per 0.25 m², also replicated 20 times at each interval.
Abundance of live associated benthic fauna was estimated from sieved sediment cores for three size categories: (1) obligatory and temporary meiofauna retained by a 63-µm mesh by decanting of seawater from a beaker with 1 cm³ (1 cm² core to 1 cm depth) of surface sediment. Decanting was repeated until no more animals were retained, and residual sand in the beaker was also inspected. Individuals were pipetted from petri dishes under a stereo microscope, identi ed to major taxon and counted. Four replicates were taken from ambient bare sand 50 m outside the Vaucheria-bed and from muddy hummocks inside the bed on June 17 in 2020. (2) Mesofauna (small-sized macrofauna) retained by a 250-µm mesh, washing 10-cm² sediment cores (depth from surface to 5 cm) in seawater. Individuals were picked up with forceps, identi ed under stereo microscope and counted. Six replicates were taken from ambient bare sand and from the Vaucheria-bed (see above) on June 12 in 2020. Additional replicates were taken July 03 at the young Vaucheria-belt with a mosaic of patches with dense growth alternating with pits of bare sand. To assess small benthic fauna speci cally associated with above-ground green siphons of Vaucheria, these were clipped at the sediment-water interface on 6 areas of 50 cm² and then washed over a 125-µm mesh. (3) To retain also larger macrofauna, cores of 50 cm² (depth from surface to 20 cm) were sieved through a 1-mm mesh. Ten replicates were taken from bare sand 50 to 100 m outside the Vaucheria-bed, and from inside the bed at muddy hummocks and at sandy troughs from July 13 to 22 in 2020. Differences in abundance were tested with the non-parametric U-test from Wilcoxon, Mann and Whitney.

Lugworm population
Arenicola marina constitutes a major component of the benthic fauna in terms of bioturbation and biomass. Mean worm size increases and abundance decreases from upper to lower shore. In Blidsel Bay, worms at an upper site (400 m from shoreline at about mid-tide level) were smaller but more abundant than worms at the lower site (2 km from shoreline at spring low tide level) where Vaucheria was spreading. Young lugworms occurred at the upper shore and were notably absent from lower shore. There, individuals dug up from their deep (> 20 cm) burrows were on average 3-times bigger and 2-times longer than lugworms at the upper shore site in June 2020 (Table 1). This difference in size was also apparent from diameters of defecated strings of sand. On the other hand, abundance of fecal mounds was 4-times lower at the lower shore compared to upper shore. Total biovolume of lugworms per unit area was 27 % higher at the upper compared to lower site (156 and 114 cm³ m -2 ). This spatial lugworm pattern was still apparent in August but differences between upper and lower shore were less striking. Fecal string diameter had decreased at the lower shore and increased at upper shore: 3.2 ± 1.0 (n=30) and 4.0 ± 0.3 mm (n=30) (compare with Table 1). Also, abundance of fecal mounds per 0.25 m² had increased at lower and decreased at upper shore: 4.6 ± 1.5 (n=60) and 8.8 ± 2.2 (n=30).
These tendencies suggest that some lugworms may have migrated from upper to lower shore during summer.
Mosaic pattern of lugworms and Vaucheria-turf Vaucheria cf. velutina had invaded sand ats occupied by very large lugworms dwelling at relatively low abundance in a patchy manner. Variance of fecal mound abundance (SD/mean) at 0.25-m² scale was 59 % at lower shore compared to 22 % at upper shore (see Table 1). Hardly recognizable, parallel sand waves at m-scale were less frequented by lugworms than the shallow pits between at the exposed lower shore. Since early June in 2020, new growth of Vaucheria had advanced from an existing bed in northern and western direction in a wide belt, preferentially colonizing the slightly elevated sand waves (Reise et al., submitted). A mosaic pattern emerged (Fig. 1). The overall abundance of lugworm fecal mounds in the young mosaic-belt remained similar to that at bare ambient sand further north. However, fecal mounds concentrated at bare pits with 3.9 ± 0.9 [3-5] (n=10) 0.25 m -2 , while at 1 to 4 cm higher plateaus with a dense algal turf these were almost absent (0.1 ± 0.3 [0-1] (n=10) 0.25 m -2 ) (p < 0.01, U-test). This was counted June 17 and suggests that lugworms moved their burrows away from establishing turfs and aggregated in pits ( Fig. 1). In the innermost part of the established Vaucheria-bed, lugworms were almost gone (fecal mound abundance of 5.8 ± 3.4 per 10 m² [n=6], corresponding to 0.15 per 0.25 m²).
The mechanism of competition between Arenicola and Vaucheria could be observed directly ( Fig. 1 and 2). While fecal mounds produced by lugworms bury green algal laments, their feeding funnels are clogged by tufts of algae with their felt of rhizoids. These resisted the downward sliding of loose sand.
An inverse relation between lugworms and algal turf was apparent along a transect, running from bare sand at across patches of young Vaucheria-growth alternating with lugworms, and from there further into old Vaucheria-growth with hummocks and troughs, established since 2019 and partly already 2018 (Fig. 3). Note that in Fig. 3, data are scaled up to m² from counting areas of 0.25 m² for lugworm fecal mounds and 10 cm² for measuring cover and dry weight of Vaucheria. This exaggerates variance because patchiness decreased from small to larger scale. This is caused by subtle sand waves at the bare sand at, by a mosaic of plateaus with dense turf and pits with lugworms where Vaucheria commenced growing since June, and in the old bed by alternating hummocks and troughs. Some lugworms persisted in troughs but none on hummocks.
In August 2020, the mosaic pattern in the young growth became blurred and overall abundance of fecal mounds had decreased by 59 % from 8.0 ± 8.4 (n=20) in June to 3.3 ± 1.9 (n=60) fecal mounds per m² in August (p < 0.05, U-test). This shows the gradual displacement of lugworms by Vaucheria.

Associated benthos
While large burrowing lugworms became displaced by a turf of Vaucheria, this does not hold true for meiofauna (Table 2). Abundance was entirely dominated by nematodes (83 and 76 % in bare sand and in algal turf, respectively). At the level of major meiofaunal taxa differences between habitats were minor.
Only juvenile macrofauna of meiofaunal size showed a clear preference for algal turf (p < 0.05, U-test).
Most of them were juvenile mud snails crawling on green laments.
Small macrofauna retained by a 250-μm mesh was 4-times more numerous and 3-times more diverse in species within algal turf than on bare sand at (Table 3). This difference is mainly caused by young mollusks and small annelid worms, although most of the young P. ulvae were too small to be retained. Only amphipods were more numerous at the sand at habitat but not signi cantly because of strong patchiness (U-test). When in early July a similar set of samples was taken at the young belt of Vaucheria which had emerged since the beginning of June 2020, no signi cant differences had yet developed between pits with lugworms and plateaus with algal turf. All individuals found below 10 cm² were 2.67 ± 2.80 at pits and 3.17 ± 1.94 at algal turf. However, the species composition at the young algal turf already resembled that of the old turf shown in Table 3 with a dominance of spionid polychaetes.  Table 3 Mesofauna (small macrofauna) 10 cm -2 (0 to 5 cm depth) retained by 250-μm mesh at bare sand at and at algal turf on muddy hummocks (n = 6 + 6). Blidsel Bay, June 12 in 2020 Given are means ± standard deviation; * signi cantly (p < 0.05) higher (U-test) Table 4 Macrofauna 50 cm -2 (0 to 20 cm depth) retained by a 1-mm mesh (n=10) at bare sand at, at algal turf on muddy hummocks and at troughs in between, Blidsel Bay in July 2020 Given are means ± standard deviation and range [ ]; * signi cantly (p < 0.05) higher values at hummocks than at sand at (U-test) Macrofauna retained by a 1-mm mesh from bare sand was rather poor in abundance and species richness, compared to troughs and hummocks in the old Vaucheria-bed (Table 4). At hummocks with a dense turf and absence of lugworms, abundance was 20 times higher than in bare sand. Troughs with a moderate or very patchy turf were intermediate. Differences in species richness were modest. As shown in Table 4 by standard deviations and wide ranges of data, macrofauna was highly patchy at the 50-cm² scale, most conspicuous at troughs in the Vaucheria-bed. Only amphipods, mainly Urothoe poseidonis associated with lugworm burrows, were more abundant in bare sand and there comprised 76 % of all individuals. Troughs and hummocks in the Vaucheria-bed were entirely dominated by annelids (94 %). Among the tube-dwelling spionid worms, Pygospio elegans occurred at all three habitats but was most abundant in dense algal turf, together with Streblospio benedicti and Polydora cornuta, while the more agile Spio martinensis was most abundant at troughs. Of these tube-dwellers, relatively small individuals were retained by the 1-mm mesh because tubes were entangled in tufts of Vaucheria. Although crabs (Carcinus maenas, Hemigrapsus takanoi and Pagurus bernhardus) and periwinkles (Littorina littorea) were abundant on adjacent beds of oysters and mussels, Magallana (Crassostrea) gigas and Mytilus edulis, these remained rare in Vaucheria-beds.
Exposed sand ats at and below low tide level were usually devoid of macroalgae, while Vaucheria-beds intermittently accumulated drift algae between July and September. Of these, Rhizoclonium riparium and Ectocarpus spp. were the most persistent (Fig. 4). The latter grew massively as epiphytes in adjacent kelp beds on Sargassum muticum, and probably drifted from there to the Vaucheria-bed. Other species were more ephemeral but frequent at times: Cladophora albida, Ulva spp., Gracilaria vermiculophylla, Dasya bailouviana, Heterosiphonia (Dasysiphonia) japonica, Porphyra sp., Ceramium virgatum (rubrum), Polysiphonia sp., Fucus vesiculosus, Elachista fucicola, Sargassum muticum and Dictyota dichotoma. In July and August, these drifting macroalgae could cover the Vaucheria-bed but were removed again by rough weather. No smothering of Vaucheria was detected.

Discussion
This study refers the beginning displacement of the most characteristic benthic species in the European Wadden Sea, the lugworm Arenicola marina, from the lower shore by an invasive alga forming dense turfs and accumulating mud where loose sand prevailed before. This benthic regime shift raises several questions. What may cause the spatial gap between Vaucheria-algae at the upper shore and the recent spread at the lower shore? How could feeble algae establish between sediment reworking lugworms, and then even displace such vigorous worms? Could the invading Vaucheria endanger the lugworm population? While the impact of V. cf. velutina on A. marina and its associated fauna is clearly negative, dense algal turfs also offer a novel type of habitat for other benthos. Who bene ts from the algal turf?

Contest between invading Vaucheria and resident Arenicola
In the Wadden Sea, species of the genus Vaucheria are common at upper shores, particularly on estuarine mud ats and in salt marshes (i.e., Simons 1975;Polderman 1979 a,b;Krieg et al. 1988). At the lower shore, Vaucheria was unknown until we discovered V. cf. velutina at and below low tide level near the island of Sylt in summer 2020 (Rybalka et al., submitted; Reise et al., submitted). In addition, we found V. longicaulis at the lower shore for the rst time in the Wadden Sea (Rybalka et al., submitted). However, this second taxon was only found since September 2020, occurred in small patches only, and effects on other benthos were not investigated. We regard both as recent invaders, possibly introduced from coasts where they also occur at lower shores. If correct, the recent spread at and below low tide level cannot be explained by niche expansions from the upper shore. What could explain the gap in the vertical distribution of Vaucheria at mid shore between high and low tide level?
As shown, lugworm abundance at mid shore is higher than at lower shore. A general pattern with a belt of young worms at upper shore, high adult density at mid shore and low densities further offshore is generally known for the Wadden Sea (i.e., Farke et al. 1979;Flach and Beukema 1994;Reise et al. 2001).
Lugworm exclusion experiments (Volkenborn et al. 2009) and observations at patchy freshwater seeps avoided by lugworms (Zipperle and Reise 2005) have shown that in the absence of bioturbating lugworms, tube-builders and species requiring a more stable sediment surface took advantage. This implies that a small alga dependent on a rm rooting in sediment could be suppressed where lugworm bioturbation is high. We suggest that this may be responsible for the disjunct occurrence of turf-building Vaucheria in the Wadden Sea, and why the introduced taxa could only establish at the lower shore where lugworm abundance is low. However, this hypothesis still needs to be tested by transplant experiments.
Initial growth of Vaucheria was observed on slightly elevated sand waves of the lower shore (Reise et al., submitted). These may offer a window of opportunity for the invader where deposition prevails over erosion. Once Vaucheria succeeded in getting anchored, its growth habit may constitute a preadaptation to displace lugworms. We suggest the key mechanism is clogging feeding funnels with felted rhizoids and long laments as could be observed directly (Fig. 1). Clogging curtails the nutrition of lugworms. Instead of fueling microalgae at funnels with upwelling burrow water (Chennu et al. 2015), lugworms now supply Vaucheria with nutrients while this alga is inhibiting the downward slide of surface sediment. This will be aggravated by shading of the sediment surface once Vaucheria attained high coverage, which inhibits diatom growth at sediment surface, a major food of lugworms (Rijken 1979;Retraubun et al. 1996;Engel et al. 2012).
Such antagonistic mechanisms have also been proposed for interactions between intertidal seagrass Zostera and Arenicola. Seagrass is much larger but otherwise similar to V. cf. velutina with a mesh of roots and narrow blades. At high lugworm density and sheltered conditions, bioturbation may suppress seed germination and young Zostera, while dense growth of seagrass may inhibit lugworm feeding by roots and by shading of benthic microalgae (Philippart 1994;Valdemarsen et al. 2011;Suykerbuyk et al. 2012;Goerlitz et al. 2015). Similar as with V. cf. velutina on lugworm ats, also sharp boundaries and mosaic patterns are common (Eklöf et al. 2011). Juvenile lugworms may aggregate in patches of seagrass when avoiding to intermingle with adults (own observations). For this ephemeral phenomenon, no correspondence occurred at sites with V. cf. velutina because juvenile lugworms rarely occur at the lower shore. Another antagonistic relation occurs between lugworms and clusters of Spartina-grass at the upper shore (van Wesenbeeck et al. 2007).
Lugworm bioengineering intensity may reach a tipping point, probably conditional on ambient hydrodynamics, above which sediment stabilizing Vaucheria have to give way to sediment destabilizing lugworms. This could explain the emergent mosaic pattern of plateaus with a dense algal turf and few lugworms alternating with bare sand bioturbated by lugworms which aggregated at patches not yet occupied by the turf. Apparently, instead of swimming away, lugworms simply move their feeding funnels away from spreading algal turfs and thereby aggregate with their neighbors doing the same. Such aggregates with concerted sediment reworking activity may in turn retard a further spread of young algae. The consequence are arising depositional plateaus generated by sediment stabilizing algae, alternating with eroding pits still intensively reworked by lugworms.
Such a mosaic pattern is even more conspicuous in Vaucheria-beds of the previous year, here in the form of muddy hummocks covered by dense turf, alternating with troughs where lugworms persevere and the algal turf remains patchy. There, height differences have become more pronounced. Nevertheless, at the oldest part of the bed, a coherent turf of elongated algae has taken over. There hummocks and troughs have leveled out. Most likely, this is an effect of preceding winter storms (Reise et al., submitted). In addition, at the central part of the bed, hydrodynamics is lower than at elevated edges. This may result in a more even deposition of ne organic particles and in turn raise sul de concentrations in the sediment. This could cause the last lugworms to leave the place. Such a complete displacement of lugworms may take three years because the mosaic pattern of the antagonists is slowing down the takeover of Vaucheria. Where hydrodynamic conditions are stronger, the mosaic pattern may perpetuate.
Mosaic patterns are a recurrent phenomenon caused by aggregate settlement of space occupants or by clonal growth of plants or colonial animals. This spatial organization may be dynamic due to life time limitations or disturbances or remain in a quasi-permanent state (Remmert 1991;Rietkerk and van de Koppel 2008;van de Vijsel et al. 2020). The mosaic of an introduced Vaucheria alternating with resident Arenicola demonstrates that such patterns emerge spontaneously and do not require joint evolutionary history. The scale of patches is probably predetermined by hardly discernable, parallel sand waves separated by slight depressions. Both, Vaucheria and Arenicola respond to these in opposite ways and then modify and reinforce the pattern by antagonistic bioengineering and positive feedbacks.
Threat to the lugworm population?
Could the displacement of senior lugworms at the lower shore by Vaucheria destabilize the entire population? Numerically, the share of lugworms dwelling at the lower shore in the Wadden Sea may be small (Beukema and de Vlas 1979). Although sedentary during most of its life, lugworms migrate occasionally, not only as juveniles but also as adults (Reise 1985;De Cubber et al. 2019). The latter may migrate downslope to avoid crowding, escape cold spills or predation (Farke et al. 1979;Reise et al. 2001). At the lower shore, abundances were 4-times lower than around mean tide level and young worms were notably absent. On the other hand, the lower sandy shore accommodates the largest and presumably oldest worms. Even if these worms contribute disproportionally to gamete production, their effect on population size would remain marginal because of density dependence at the mid shore population center (Flach and Beukema 1994;Reise et al. 2001). The role of senior lugworms at lower shore for the entire population could be a reinsurance in the case of rare, exceptionally harsh winters causing high mortality in the intertidal zone as observed in winter 1998/99 (Reise et al. 2001).

Provision of novel habitat
Meiofauna seems indifferent to algal turf colonizing bare sand. For this size group, however, better taxonomic resolution would have been required than shown in Table 2. On the other hand, juveniles of the intertidal macrofauna when still of meiofaunal size, show a clear preference for the algal turf. The novel habitat functions as nursery. Altogether, ten species of young bivalves were encountered in the algal turf.
Of particular abundance were juveniles of the small mud snail Peringia ulvae with up 10 individuals per cm² in June, crawling at the green laments and feeding on epiphytes such as sessile diatoms but not on V. cf. velutina itself. This constitutes a spontaneous mutual bene t for Vaucheria getting cleaned and for P. ulvae nding additional food. More generally, juvenile macrofauna likely found shelter in the algal turf against epibenthic predators such as shrimp (Crangon crangon).
For tube-dwelling spionid polychaetes which occurred with more than two individuals per cm² in dense algal turf not only shelter against epibenthic predators may have been important but also the sediment stabilizing effect of V. cf. velutina. Young growth of Vaucheria did not su ce. Perhaps the canopy of algal laments was too thin or since June no signi cant larval settlement had taken place. On tidal ats in the Firth of Forth (Scotland) with a low density of lugworms a similar preference of spionid polychaetes for patches of Vaucheria was observed, comprising even the same species (Pygospio elegans, Polydora cornuta and Streblospio benedicti) (Bolam and Fernandes (2002;pers. communication).
Of special interest is the obligatory feeding of the tiny sea slug Alderia modesta on cushions or turfs of Vaucheria (Hartog 1959;Seelemann 1967;Rasmussen 1973;Ligthart 2009). Similar to Elysia, also A. modesta saves chloroplasts from their diet for photosynthesis on their own (kleptoplasty: Clark et al. 1990;Rumpho et al. 2011). With the appearance of V. cf. velutina at the lower shore of the Wadden Sea, A. modesta could widen its narrow niche at salt marshes of the upper shore down to the subtidal zone. This was already observed in the Oosterschelde (Rhine delta) where V. longicaulis is spreading since 1993 (Ligthart 2009). Whether A. modesta would be capable of stopping the Vaucheria invasion at the lower shore, remains to be seen. In summer 2020 its abundances were too low for thinning out algal turfs.
However, under con ned lab conditions few individuals could completely wipe out Vaucheria (own observations). The role of other mesoherbivores such as gammarid amphipods also needs further investigation. Large herbivores, such as brent geese or widgeon were not yet observed grazing at low shore Vaucheria.
On close investigation, a cocktail of negative, neutral and positive effects on residents may always be the case with invaders (Thieltges et al. 2006). Super cially, there is some similarity of the Vaucheria-turf with episodic mats of green algae on tidal ats in response to eutrophication. These suffocated endobenthic fauna underneath but provided habitat to opportunists and epibenthic snails such as Peringia ulvae (i.e., Nicholls et al. 1981;Reise 1983;Raffaelli et al. 1999;Bolam et al. 2000). However, Vaucheria is not ephemeral and attract a rich small fauna (Bolam and Fernandes 2002;this study). This follows the generalization of Crooks (2002) that invaders increasing habitat complexity entail higher abundances and species richness in residents. Although leaves of seagrass are taller and broader and roots go deeper than in V. cf. velutina, effects of Zostera on associated fauna are strikingly similar, i.e., high abundances of tube-building spionid polychaetes and epibenthic mud snails (i.e., Reise 1978;Orth et al. 1984;Reise et al. 1994;Philippart 1995) and inhibition of lugworms (see above). Mixing of seagrass beds and Vaucheria was not observed. As beds of Zostera are declining on tidal ats of northern Sylt (Dolch and Reise 2010), the novel habitat of Vaucheria at the lower shore may offer a partial compensation for certain species.

Conclusions And Outlook
An alien alga is displacing a resident keystone bioengineer at the lower shore of the Wadden Sea. Converely, where lugworm density is high, spread of Vaucheria may be inhibited. Vaucheria and Arenicola cannot coexist and arrange in a mosaic fashion until the latter is expelled completely. A habitat of bare loose sand and reworked by lugworms is transformed into bumpy mud, hold together by a felt of rhyzoids and covered by a dense turf of thin laments. Lugworms and their benthic associates are eventually driven out while other benthos nds shelter under a lamentous canopy, bene ts from stabilized sediment or algal food. Presumably, the invasion will proceed as there is ample bare sandy sediment at the lower shore equivalent to what has already been vegetated near the island of Sylt. Similar occurrences of Vaucheria velutina are known from lower shores of Florida (Gallagher and Humm 1981) and the southern Paci c (Wilcox 2012; Womersley1987) but species identity still has to be con rmed by molecular genetics Declarations Figure 2 Turf of Vaucheria cf. velutina in Blidsel Bay, July 2020 with lugworm fecal mound. Right: Algal tuft cleaned from sediment with green laments above and a felt of pink rhizoids below. Thicker than rhizoids are entangled tubes of spionid worms