were encountered in both mud and sand, germ~g formation was restricted to sand: ... Investigations were conducted in K6nigshafen, a shallow tidal bay on the ...
HELGOLANDER MEERESUNTERSUCHUNGEN Helgol~nder Meeresunters. 47,275-285 (1993)
G e r m i n a t i o n and a n c h o r a g e of
Enteromorpha
spp. in
s e d i m e n t s of the W a d d e n S e a D. Schories & K. Reise Biologische Anstalt Helgoland, Watterrmeerstation Silt; D-25992 f_a'st, Federal Repubfic of Germany
ABSTRACT: Large quantities of filamentous green algae (Enteromorpha sppl) have regularly occurred on muddy and sandy tidal flats in K6nigshafen, on the island of Sylt (North Sea), since 1979 - covering the sediments in thick mats during the summer months. While spores of Enteromorpha were encountered in both mud and sand, g e r m ~ g formation was restricted to sand: However, mud snarls (Hydrobia ulvae Pennant) were overgrown with small Enteromorpha filaments in both habitats, about 50% of them at a muddy site and 20% at a sandy one. Filaments, several cm in length and still adhering to the snails, became tangled into clusters. At the sandy site, with abundant Arenicola marina L., these clusters slid into the feeding funne!s of lugworm burrows; the importance of this Secondary anchorage is demonstrated by afield experiment. We suggest that the primary and secondary attachment of Enteromorpha filaments provided by benthic fauna i s a n essential step in the development of green algal mats on sedimentary tidaI flats.
INTRODUCTION In earlier decades of this century, macroscopic g r e e n a l g a e were rarely p r e s e n t on the s a n d y or m u d d y intertidal flats n e a r the island of Sylt (Kuckuck, 1896-1903 u n p u b h Nienburg, 1927; Wohlenberg, 1937; Kornmann, 1952], b u t have regularly occurred in thick mats since 1979 (Reise, 1983; Reise et al., 1989). Within the last 25 years, excessive growth of green macroalgae has become an increasingly common p h e n o m e n o n a n d a problem in sheltered bays (Sawyer, 1965; Buttermoore, 1977; Fitzgerald, 1978; Montgomery & Soulsby, 198I; Sfriso et al., 1987; Raffaelli et al., 1989). O n tidal flats n e a r the island of Sylt, several species of g r e e n algae, n a m e l y Enteromorpha spp., Cladophora spp., Chaetomorpha sutoria (Berkeley) K o r n m a n n a n d Ulva spp. form d e n s e mats d u r i n g summer, which lead to dramatic c h a n g e s on epi- a n d e n d o f a u n a l a b u n d a n c e (Reise, 1983; Schories, 1991). Eutrophication in estuaries a n d coastal waters is w e l l - d o c u m e n t e d a n d m a y explain the extensive growth of certain macroalgae that take a d v a n t a g e of these conditions (Soulsby et al., 1982, 1985; Sfriso et aI., 1987). Culture experiments with Enteromorpha spores d e m o n s t r a t e d that the addition of sewage effluent to u n p o l l u t e d seawater stimulates growth (Ford et al 1983). Propagules of Enteromorpha species seem to germinate on a n y k i n d of solid substratum, i n c l u d i n g other plants. H o w e v e r . httle is k n o w n about how Enteromorpha propagules can develop in m u d d y a n d s a n d y intertidal areas where tidal currents a n d wave action move the surface s e d i m e n t to a n d fro. Linke (~ Biol0gische ~ s t a i t Helgoland, Hamburg
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(1939) a n d Nienhuis (1970) mention that mollusc shells, d e a d or alive (i.e. Cerastodenna edule L.), are colonized b y t h e s e algae, i m p l y i n g that a l g a l cover of an i n t e r t i d a l a r e a d e p e n d s on shell a b u n d a n c e . More d e t a i l e d information a b o u t p o s s i b l e substrata of Eateromorpha species occurring in the W a d d e n Sea is given b y K o e m a n & v a n d e n H o e k {1982a, b, 1984}. N i e n b u r g (1927} d e s c r i b e d the direct d e v e l o p m e n t of Entezomorpha g e r m l i n g s on s a n d grains, b u t he did not m e n t i o n w h e t h e r t h e s e g e r m l i n g s d e v e l o p e d f u r t h e r into adult plants. Reise {1983) d e s c r i b e d how g e r m l i n g s of Enteromorpha spp., a t t a c h e d to s a n d grains, i n c r e a s e d in l e n g t h d u r i n g summer, b r a n c h e d , a n d finally b e c a m e p l a i t e d into tresses b y tidal currents a n d w a v e action. Observations s h o w e d that t h e s e strands of g r e e n a l g a e b e c a m e a n c h o r e d in the f e e d i n g funnels of the l u g w o r m Arenicola marina, a n d h e n c e resisted d i s p l a c e m e n t b y tidal currents. The g e r m l i n g formation of Enteromorpha spp. in s a n d y a n d m u d d y i n t e r t i d a l areas is still a paradox. In this study, w e describe t h e d e v e l o p m e n t of y o u n g Enteromorpha spp. stages on intertidal soft bottoms in m o r e detail. W e p r o p o s e that b e n t h i c f a u n a can p l a y an essential role in Enteromorpha d e v e l o p m e n t b y p r o v i d i n g p r i m a r y a n d s e c o n d a r y anchorage. AREA A N D METHODS Habitat Investigations w e r e c o n d u c t e d in K6nigshafen, a shallow tidal b a y o n the island of Sylt in the N o r t h e r n W a d d e n Sea. H y d r o g r a p h y a n d m a c r o f a u n a h a v e b e e n d e s c r i b e d b y W o h l e n b e r g (1937} a n d Reise (1985), m a c r o a l g a e by N i e n b u r g {1927} a n d K o r n m a n n {1952), s e d i m e n t b y A u s t e n {I990}. 76 % of KSnigshafen Bay (total 4.8 krn 2} consists of s a n d y tidal a r e a s a n d 9 % of m u d d y areas. Two study sites w h e r e algal c o v e r develops during s u m m e r w e r e investigated. O n e site ["Tonnenlegerbucht") is l o c a t e d in a narrow e m b a y m e n t b e t w e e n the d i k e a n d a s a n d y spit with p r e d o m i n a n t l y m u d d y s a n d {organic content: 1.2 % of dry weight; silt content > 10 %; m e d i a n of particle size: 406 ~tm}. The relatively l a r g e m e d i a n of s e d i m e n t particles on the m u d flat is e x p l a i n e d b y t h e vicinity of t h e s a n d y spit containing coarse s e d i m e n t which, during w i n d y days, drifts onto the flat. T h e location is at m i d - t i d e level, h i g h l y sheltered, with a d o m e s t i c s e w a g e effluent that enters n e a r b y . The other site {"MSwenberg-Watt"} is l o c a t e d on an e x t e n s i v e s a n d y tidal flat at m i d - t i d e level {organic content: 0.04 % of dry weight; silt c o n t e n t < 4 %; m e d i a n of particle size: 324 ~m). Sampling 7 s a m p l e s of 5.3 cm2/0-0.5 cm d e p t h w e r e t a k e n r e g u l a r l y from e a c h site, to estimate the con~ent of y o u n g Enteromorpha filaments (> 0 1 m m length} g r o w i n g a t t a c h e d to s a n d grains. T h e s e d i m e n t cores w e r e t r a n s f e r r e d to Petri d i s h e s a n d i n s p e c t e d u n d e r 50fold r s a m p l e s of Hydrobia ulvae (6 s a m p l e s of 100 cm 2 sediment La m e s h of 1000 ~m} w e r e t a k e n a n d t h e n u m b e r of snails with a n d without a t t a c h e d Enteromorpha g e r m l i n g s d e t e r m i n e d . S a m p h n g w a s initiated on M a y 1st 1990 a n d c o n t i n u e d until the e n d of A u g u s t 1990. In the s a m e year, g r e e n t e t e r m i n e d b y t a k i n g a l g a e from 6 plots {samphng size v a r i e d n 2 d e p e n d i n g on g r e e n a l g a l cover of the area) a l o n g p e r m a n e n t
G e r m i n a t i o n a n d a n c h o r a g e of Enteromorpha spp.
277
transects at e a c h site. The plants w e r e w a s h e d in fresh w a t e r to remove the sediment, e p i f a u n a a n d salt from the algal filaments a n d then o v e n - d r i e d for 72 h at 70 ~ E i g h t e e n clusters of drifting, y o u n g Enteromorpha filaments, t a k e n at r a n d o m , were a n a l y s e d in t h e m i d d l e of M a y 1992 at the s a m e sites. Enteromorpha dry w e i g h t v a r i e d b e t w e e n 0.064 a n d 0.226 g cluster -1. The relation of sand grains to m u d s n a i l s as substrata of a t t a c h m e n t was also r e c o r d e d for these clusters of filaments.
Experiment At the s a n d y site, e x p e r i m e n t a l r e m o v a l of the l u g w o r m Arenicola m a n n a (144 _+ 25 individuals m -2, SD) took place b y inserting a sheet of g a u z e (mesh size 1 ram) horizont a l l y into the s e d i m e n t at 5 cm depth. The u p p e r layer of s e d i m e n t from fourteen 1-m 2 plots was r e m o v e d with a shovel, the g a u z e unfolded a n d t h e n covered with original surface sediment. I m m e d i a t e l y afterwards the g a u z e was r e m o v e d from the 7 plots w h i c h s e r v e d as controls; The r e m a i n i n g 7 plots' g a u z e b l o c k e d the vertical shafts of lugworms, forcing t h e m to l e a v e sideways, while on the similarly d i s t u r b e d controls t h e y r e m a i n e d in their b u r r o w s . A pilot e x p e r i m e n t s h o w e d that g r e e n a l g a e n e v e r a t t a c h e d to the b u r i e d g a u z e . Thus, t h e r e was no n e e d to i m p l a n t a substitute for the g a u z e at the control plots. :The e x p e r i m e n t was i m t i a t e d on M a y 1st, a n d t e r m i n a t e d o n J u l y 14th 1990, T h e effect of g r e e n algal cover w a s e v a l u a t e d b y t a k i n g p h o t o g r a p h s at r e g u l a r intervalsi and, with the h e l p of a g r i d (4900 units), the surface cover of g r e e n a l g a e on e a c h p l o t was estimated. A l g a l c o v e r from control a n d r e m o v a l sites were c o m p a r e d with n o n - p a r a m e t ric tests (U-test from W i l c o x o n , b i n o m i a l sign t e s t [Sachs, 198~]),
RESULTS
Enteromorpha g e r m h n g s Young p l a n t s of various macroscopic g r e e n algal g e n e r a (for e x a m p l e : Cladophora, Monostroma, Percursaria, Rhizodonium, Ulva) w e r e p r e s e n t at both sites, b u t r e m a i n e d rare in the s a m p l e s . :At no time during s a m p l i n g were m o r e t h a n 1'..9+_ 2.5 p e r c e n t of mudsnails at the m u d d y site o v e r g r o w n with young p l a n t s of a n y g e n e r a m e n t i o n e d
p r e s u m a b l y there w e r e still m o r e s p o r e s a n d small g e r m h n g s attached. A t t h e s a n d y site, the a b u n d a n c e of Enteromorpha g e r m h n g s g r o w i n g on shells or sand grains was always much lower. T h e r e w e c o u n t e d a m a x i m u m of 18 Enteromorpha filaments g r o w i n g o n a single shell, a n d a m a x i m u m of 9 filaments on a single s a n d grain. We could s h o w that in M a y 1990 spores of Enteromorpha w e r e a t t a c h e d to s a n d
and: not t h e m u d d y site. "mobile" s u b s t r a t u m Hydrobia ulvae occurred at both sites. In contrast to the s a n d y site,
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empty shells of mudsnails (with the exception of snails that had recently died) were n e v e r overgrown with Enteromorpha at the m u d d y site. The highest n u m b e r s of snails or sand grains overgrown with Enteromorpha filam e n t s were found in M a y at both sites (Fig. 1). At the s a n d y site, u p to 26 000 • 14 000 sand grains m -2 were found overgrown with Enteromorpha filaments, respectively 5700 • 5600 of the snarl shells m -2 were attached to Enteromorpha filaments. At the m u d d y site, n o n e of the s a n d grains, b u t 20300 • 5100 snail shells m -2 w e r e f o u n d with filaments. The total a b u n d a n c e of Enteromorpha g e r m l i n g s varied in relation to the n u m b e r of mudsnails present. Hydrobia densities m -2 were i n the same m a g n i t u d e at both sites: 31 000 • 4700 to 66 700 • 31 000 at the m u d d y site, a n d 24 000 • 5000 to 52 000 • 15 000 at the sandy site. Recnrits of 1990 were not considered. The p e r c e n t a g e of overgrown Hydrobia was m u c h higher at the m u d d y site t h a n at the s a n d y site (Fig. 2}. M e a n snarl size at the m u d d y site w a s 3.3 m m in J u n e a n d 3.9 m m i n September; at t h e s a n d y site, the size was 2.7 m m a n d 3.0 mm, respectively. There was no relation b e t w e e n shell size a n d degree of colonization by Enteromorpha filaments. C l u s t e r s of
Enteromorpha
filaments
Throughout the summer, the filaments of Enteromorpha spp., attached to s a n d grains or Hydrobia shells, increased in length, b u t these were rarely p r e s e n t in o u r s e d i m e n t or snail samples. In the latter two, most Enteromorpha filaments were very s m a l l (< 1 mm}. Only at sheltered, m u d d y sites, did we occasionally observe • a m e n t s of up to 20 cm l e n g t h attached to a m u d s n a i l on the s e d i m e n t surface. We assume that f i l a m e n t s > 1 m m easily become dislocated, together with their substratum (snail or s a n d grain), w h e n subject to tidal currents. From the b e g i n n i n g of M a y onwards, we found clusters of them d u r i n g low tide on the s e d i m e n t surface. T h e s e clusters m a y b e g e n e r a t e d (1) by snails with attached filaments, which crawl o n the s e d i m e n t surface, thereby passively e n t a n g l ing other filaments with or without their substratum, (2) b y tidal c u r r e n t s a n d waves which lift filaments together with the s a n d grains or snails up from the b o t t o m into the water column w h e r e they b e c o m e b r a i d e d to clusters and tresses. Similar to the results from s e d i m e n t samples, algal filaments within drifting d u s t e r s were exclusively attached to h y i n g mudsuails at the m u d d y site, a n d to b o t h snails a n d sand grains at the s a n d y site (Fig. 3). However, the proportion of snails to s a n d grains as substrata of a t t a c h m e n t increased from s e d i m e n t cores to clusters of a l g a e at the s a n d y site, indicating a higher chance of snail-attached filaments b e c o m i n g e n t a n g l e d in clusters. Green algal biomass Extensive growth of Enteromorpha s p p was recorded from May to the e n d of A u g u s t 1990 in K6nigshafen bay. Not only s a n d grains a n d mudsnails served Enteromorpha as primary substrata, b u t also polychaete tubes (i.e. built by Lanice conchflega Pallas) a n d cockles b e c a m e overgrown, b u t this did not develop into a high algal c o v e r in t h e bay. Only i n one restricted area (5600 m 2} of it were Enteromorpha filaments ( g r o w i n g o n the s a n d t u b e s of Lanice) able to form a d e n s e mat {97 __+43 g dw m-2; a total of 6 samples of 0.25 m 2 were r a n d o m l y taken) in Auqust. At the m u d d y site, the algal m a t w a s thickest in
Enteromorpha spp.
Germination and anchorage of
279
May
i, June mud flat
sandflat
July August n u m b e r o f mud s n a i l s In t h o u s a n d s / m 2
September
~ ~ T
1990
30
20
10
0
10
20
3O
Hydrobia ulvae with attached Enteromorpha- filaments
May
_
O, m
II o- I
o June mudflat
sandflat
0
July August tumber of sand ~ralns
September 1990
i
In t h o u s a n d s i
30
/ m 2 i
20
10
0
10
20
30
sand grainswith attached Enteromorpha filaments Figs::1:.:AbundanCe [means + 1SD) of Sand grains(abo~e)and Hydrobiaulvae ( b e l o w ) ~ attached Enterornorpha filamentsata muddy and a sandy sited ~ n g summer ig90
D. Schories & K. Reise
280 peroE 60 50 40 30 20 10 0 May
I~
~
muddy site
September
m l sandy site
Fig. 2. Percentages of Hydrobia ulvae in mud and sand with attached Enteromorpha filaments during summer 1990 {means +_ 1SD} The total number of snails found in each sample constitutes I00 %
M a y 1992
~ m l L
100%
28%
'\~~ muddy site
sandy site
~ Enteromorphafilaments mEnteromorpha filaments attached to Hydrobiau[vae attached to sand grains Fig, 3. A t t h e m u d ~ site; shell s of living mudsnafiSl Hydrobia ~vae, served a s the on!y subs~atum within clusters of:young Ente~omorphafilamentSi site; sand g~ainS were also overgrown by theSe a l g a e At both sites ~ubstrata o~her than m~d~Aails, Or Sand grains were not ~r~Senf ~ t h i n ~he dusters
Germination a n d a n c h o r a g e of Enteromorpha spp.
281
A n c h o r a g e of d r i f t i n g g r e e n a l g a e During ebb tide, drifting g r e e n a l g a e b e c o m e d e p o s i t e d in depressions of the s e d i m e n t surface. On the sand flats in the W a d d e n Sea, these depressions are mostly funnels of l u g w o r m burrows. Some of the algal filaments shde d o w n the f e e d i n g funnels t o g e t h e r with their a t t a c h e d s u b s t r a t a (sand grains a n d mudsnails). At the s a n d y site, w e found Enteromorpha tresses vertically e m b e d d e d in the s e d i m e n t d o w n to the d e p t h of burrows. There w e r e more algal tresses e m b e d d e d in the s e d i m e n t t h a n t h e r e w e r e l u g w o r m f e e d i n g funnels, a n d only a few w e r e actually e n c o u n t e r e d sticking out of functional h e a d shafts, From this, it follows that l u g w o r m s a b a n d o n h e a d shafts a n d funnels once these are c l o g g e d with algal tresses a n d m u s t build n e w shafts a n d funnels in a n e w position. The c o n s e q u e n c e of this is that a single l u g w o r m m a y a n c h o r s e v e r a l drifting algal clusters a n d p r e v e n t t h e m from further drifting. The result of this process is r e v e a l e d b y the l u g w o r m exclusion e x p e r i m e n t at the sandy site (Fig. 4). A l g a l cover
70 -I~percent cover I I f green algae
"/r -T-
60 * 50 40 30
'
2(1
May
,
,b
unmanipulated control ~
July
Arenicola marina -exclusion
Fig. 4. Experimental exclusion of the lugworm Arenicola marina leads to a lower coverage with Enteromorpha spp, filaments during the growing season, Asterisks (") denote differences at the level of p < 0.10 (Mann,Whitney U-test) b e c a m e significantly lower on plots without lugworms, c o m p a r e d with control plots with a m b i e n t l u g w o r m densities. During the time of investigation, the n u m b e r of l u g w o r m casts in the controls did not change. DISCUSSION The e n h a n c e m e n t of g r e e n algal b i o m a s s on s a n d y a n d m u a d y bottoms of the shallow sea is g e n e r a l l y ascribed to h i g h nutrient l o a d s in coastal waters, originating from
282
D. Schories & K, Reise
a n t h r o p o g e n i c sources (Harlin & Thome-Miller, 1981; Kautsky, 1982; Sfriso et al., 1987). High n u t r i e n t u p t a k e rates a n d a storage of excess nutrients support a n extensive growth of d e n s e algal mats (Kautsky, 1982; O'Brien & Wheeler, 1987; Thomas & H a r r i s o n 1987). However, the occurrence of these g r e e n algae on soft bottoms is still a paradox, b e c a u s e one w o u l d have expected to find a firm substratum on the surface to allow for germination u n d e r suitable hght conditions. Tidal currents a n d waves are likely to carry those thaUi away which are not attached to sohd objects. The p r e s e n t study p r o v i d e s some e v i d e n c e of h o w this paradox is overcome by species of Enteromorpha. We f o u n d a b u n d a n t spores i n both m u d a n d s a n d of the intertidal zone. G e r m l i n g formation occurred on sand grains of the surface layer, as described by N i e n b u r g (1927), b u t only at a s a n d y site a n d not in a n area with mud. Dayton (t975) s h o w e d that the total a b s e n c e of Hedophyflum plants from a site where t r a n s p l a n t e d adults survived, was very likely due to siltation of early post-settlement stages. Moss et al. (1973) s u g g e s t e d that silt was a major factor i n h i b i t i n g colonisation of Hirnanthafia, a n d attributed this to reduced hght p r e v e n t i n g germination. Norton (1978) showed that a n overlying layer of silt r e d u c e d light b y 98 % a n d inhibited d e v e l o p m e n t of microscopic gametophytes. We also suggest that r e d u c e d light conditions on sand grains e n v e l o p e d by silt w e r e the m a i n factor which i n h i b i t e d the germling formation of Enteromorpha spp. at our m u d d y site. A c o n s e q u e n c e of this would b e the a b s e n c e of y o u n g Enteromorpha plants at m u d d y sites. However, this is not the case, b e c a u s e hydrobiid snails provide a n alternative s u b s t r a t u m for germination. Hydrobia ulvae is a highly a b u n d a n t c o m p o n e n t of the intertidal f a u n a on both m u d a n d s a n d in the W a d d e n Sea (Linke, 1939; Reise, 1987), a n d elsewhere along E u r o p e a n coasts (Waiters & Wharfe, 1980). In the m u d d y area investigated in this study, H. ulvae t u r n e d t)ut to be the only s u b s t r a t u m suitable for germling formation of Enteromorpha. Thus, this snail may attain a key role in the g e r m l i n g formation, a n d later on m the d e v e l o p m e n t of g r e e n algae, on m u d d y bottoms in sheltered bays. At the s a n d y site investigated, the relation of overgrown m u d snails to s a n d grains c h a n g e d from spring to summer. H. ulvae b e c a m e more important as a s u b s t r a t u m . This m a y indicate a d i s a d v a n t a g e for g r e e n algal filaments attached to sand grains, once they have grown b e y o n d a certain length. Presumably they b e c o m e more easily dislocated a n d are t a k e n a w a y by the tidal currents, while filaments attached to h y d r o b i i d snails remain. This suggests that also on sand flats H. ulvae may attain a k e y role in Enteromorpha development. Present investigations in K6nigshafen bay s h o w that spores or microscopic stages of Enteromorpha spp. overwinter in m u d a n d s a n d a t t a c h e d to the shells of H. ulvae. Nearly all m u d snails were stocked with early p o s t - s e t t l e m e n t stages (Schories, in prep.). We do not suggest: a case of mutualism. In Petri dishes w e observed H. ulvae f e e d i n g
for H. ulvae. Nevertheless, H. ulvae m a y b e highly a b u n d a n t within algal m a t s (Nicholls et al., 1981; Soulsby et al., 1982). In n o n e of our samplings from Enteromorpha d u s t e r s or a l g a l m a t s did w e find high n u m b e r s of e m p t y Hydrobia shells or snails t h a t h a d recently died with lonq Enteromorpha filaments. Snails attached to Enteromorpha f i l a m e n t s a n d e n t a n g l e d i n d u s t e r s or mats were alive a n d e n g a g e d in epiphytic b r o w s i n g , p r o b a b l y
Germination and a n c h o r a g e of Enteromorpha spp.
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f e e d i n g on m i c r o a l g a e a n d bacteria. Thus, the effects of g r e e n a l g a e on H. ulvae m a y at b e s t be neutral, a n d at times certainly negative, w h e n a l g a e b e c o m e i m b e d d e d in the sediment, a r e w a s h e d ashore, or d e c a y u n d e r anoxic conditons. Some questions of the d e v e l o p m e n t of g r e e n a l g a e on sediments w e r e not c o n s i d e r e d in this study. It remains to b e p r o v e n that those filaments found a t t a c h e d to snails are the s a m e w h i c h later form thick algal mats. Overwintering filaments of Enteromorpha were found at the m u d d y site. These m a y also contribute to the formation of algal mats. At the s a n d y site, no overwintering filaments w e r e found. Drift algae, originating outside the study area, m a y also contribute to the g r e e n algal mats observed. Enteromorpha spp. are not only epizooic on H. ulvae on the tidal flats n e a r Sylt. In particular, cockles Cerastoderma edule (L.) are often b e a r d e d at their s i p h o n a l e n d with Enteromorpha spp. In 1988 a n d 1989, d e n s e cockle b e d s b e c a m e entirely o v e r g r o w n by g r e e n a l g a e a t t a c h e d to cockle shells. Most of these cockles suffocated a n d died. On a n o t h e r site in KSnigshafen, Enteromorpha spp. g e r m i n a t e d on the t u b e - c a p s of the a b u n d a n t p o l y c h a e t e Lanice conchilega (Pallas), a n d s u b s e q u e n t l y d e v e l o p e d into a c o h e r e n t algal cover, until storms in A u g u s t r e m o v e d most of it (1990 a n d 1991). O n the s h e l t e r e d m u d flat investigated, H. ulvae provided a sufficient s u b s t r a t u m for g e r m i n a t i o n a n d attachment, a n d a thick mat of Enteromorpha filaments p e r s i s t e d from J u n e to August. At the other site (the m o d e r a t e l y - e x p o s e d s a n d flat), H. ulvae w a s suitable for a t t a c h m e n t b u t did not provide sufficient a n c h o r a g e to resist the w a t e r m o v e m e n t s . As o b s e r v e d e a r h e r b y Reise (1983), a n d confirmed h e r e b y m e a n s of a field experiment, burrows of the l u g w o r m Arenicola marina p r o v i d e a s e c o n d a r y anchorage. B e c a u s e of the w i d e s p r e a d occurrence of A. marina on E u r o p e a n tidal flats, w e s u g g e s t this m o d e of a n c h o r a g e to be of g e n e r a l i m p o r t a n c e in the d e v e l o p m e n t of g r e e n algal mats. The algal strands sliding into feeding funnels are clearly a n u i s a n c e to the lugworms. This is e v i d e n t from the fact that worms shift h e a d - s h a f t s a n d funnels into n e w positions, once the former are c l o g g e d by algae. This very fact amplifies the i m p o r t a n c e of l u g w o r m s for the algae, b e c a u s e in this w a y a single w o r m m a y anchor s e v e r a l algal strands. In the study area, w e o b s e r v e d thick algal mats which h a d a p p a r e n t l y b e e n m a d e possible b y this m o d e of anchorage. W h e n these mats of g r e e n a l g a e start to decay, l u g w o r m s w e r e o b s e r v e d a b a n d o n i n g the sediment. We found no e v i d e n c e that lugworms f e e d on the g r e e n algae. Nor do f r a g m e n t s of g r e e n a l g a e s e e m to be a suitable food for l u g w o r m s (Hylleberg, 1975; Rijken, 1979). This is in contrast to n e r e i d polychaetes. W o o d i n (1977) d e s c r i b e s h o w Nereis vexillosa a n d Platynereis bicanaliculata attach pieces of drift a l g a e to their t u b e - c a p s a n d s u b s e q u e n t l y feed on the g r o w i n g thalli. She t e r m e d this "algal g a r d e n i n g " . A n o t h e r n e r e i d worm, N. brandti, pulls large strands of g r e e n a l g a e into its b u r r o w to f e e d on t h e m (Hylieberg & H e n r i k s e n , 1980}. W e o b s e r v e d N. diversicolor l i k e w i s e p u l l i n g filaments of Enteromorpha into its b u r r o w for s u b s e q u e n t consumption. Other p o l y c h a e t e s (Nereidae, Onuphidae} are k n o w n to d e c o r a t e their t u b e s with drift a l g a e (Pettiborne, 1963; Daly, 1973). In the present study, we have described two cases where benthic invertebrates p r o m o t e g r e e n algal d e v e l o p m e n t without r e c e i v i n g a n y clear b e n e f i t in return. The i m p o r t a n c e of H. ulvae as a primary, and A. marina as a secondary, m e a n s of a t t a c h m e n t only b e c a m e a p p a r e n t with the a d v e n t of coastal eutrophication. In the a b s e n c e of eutrophication as a precondition to the excessive growth of g r e e n algae, this n o n - t r o p h i c
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D. S c h o r i e s & K. R e i s e
l i n k in t h e e c o l o g i c a l w e b w o u l d b e a c u r i o u s c o i n c i d e n c e , l a c k i n g a n y g e n e r a l significance.
Acknowledgements. We gratefully acknowledge the help of A. Albrecht. The investigation was part of the project "Grfinalgenausbreitung im Wattenmeer (FKZ: 102 04 245)", supported by the Umweltbundesamt. It was also supported by the Ministry of Research and Technology (Publication No. 47 of the Wadden Sea Ecosystem Project).
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