Sewage, green algal mats anchored by lugworms, and the effects on Turbellaria and small Polychaeta

Helgoland Marine Research, May 2019

On sandy tidal flats at the Island of Sylt (North Sea) ephemeral mats of green algae covered wide areas in the vicinity of sewage outflows. Algae became anchored in the feeding funnels of lugworms (Arenicola marina) and thus were able to resist displacement by tidal currents. Below the algal mats anoxic conditions extend to the sediment surface. After about one month a rough sea removed all algae. Polychaetes endured this short-term environmental deterioration, while the more sensitive Turbellaria decreased in abundance and species richness. Diatom-feeders were affected most, predators to a medium extent, and bacteria-feeders the least affected. Rare and very abundant species were more affected than moderately abundant ones. None of the turbellarian species increased in abundance and none colonized the algal mats above the sediment. In a semicontrolled experiment with daily hand-removal of drift algae from a 100-m2 plot within an extensive field of algal mats, this cleaned "island

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Sewage, green algal mats anchored by lugworms, and the effects on Turbellaria and small Polychaeta

H E L G O ~ E R MEERESUNTERSUCHUNGEN Helgot~nder Meeresunters. S e w a g e , g r e e n a l g a l m a t s a n c h o r e d b y l u g w o r m s , a n d t h e e f f e c t s o n T u r b e l l a r i a a n d s m a l l P o l y c h a e t a * 0 Biologische Anstalt Helgoland (Litoralstation); D-2282 List/Sylt, Federal Republic of Germany and II. Zoologisches Institut, UniversitAt Gfittingen; D-3400 G~ttingen, Federal Republic of Germany O n sandy tidal fiats at the Island of Sylt (North Sea) e p h e m e r a l mats of g r e e n algae covered wide areas in the vicinity of sewage outflows. Algae b e c a m e anchored in the feeding funnels of lugworms (Arenicola marina] a n d thus were able to resist dispIacement by tidal currents. Below the algal mats anoxic conditions extend to the sediment surface. After about one m o n t h a rough sea r e m o v e d all algae. Polychaetes endured this short-term environmental deterioration, while the more sensitive Turbeilaria decreased in a b u n d a n c e a n d species richness. Diatom-feeders were affected most, predators to a m e d i u m extent, and bacteria-feeders the least affected. Rare and very a b u n d a n t species were more affected than moderately a b u n d a n t ones. None of the turbellarian species increased in a b u n d a n c e a n d n o n e colonized the algal mats above the sediment. In a semicontrolled e x p e r i m e n t with daily h a n d - r e m o v a l of drift algae from a 100-m2 plot within a n extensive field of algal mats, this d e a n e d "'island" served as a refuge to Turbellaria escaping from their algal covered habitat. Here a b u n d a n c e d o u b l e d relative to initial conditions a n d was 5-times h i g h e r t h a n below algal mats. - K a r s t e n R e i s e I N T R O D U C T I O N i n c r e a s i n g l y c o m m o n p h e n o m e n o n i n s h e l t e r e d m a r i n e b a y s ( P e r k i n s & A b b o t t , 1972; T u b b s , 1977; W h a r f e , 1977; M i c h a e l i s , 1978; N i c h o l l s e t aL, 1981; a n d r e f e r e n c e s t h e r e i n ) . A m m o n i u m a n d n i t r a t e a r e c r u c i a l w h i l e p h o s p h a t e is n o t ( H a r l i n & T h o r n e M i l l e r , 1981) . A l o n g i n t e r t i d a l s e d i m e n t a r y s h o r e s , w i d e a r e a s of f o r m e r o p e n m u d l a n d s a r e c o v e r e d b y c o n t i n u o u s m a t s of f i l a m e n t o u s a n d m e m b r a n o u s a l g a e ( C h l o r o p h y c e a e : Enteromorpha spp., Ulva spp.), 10 to 15 c m i n t h i c k n e s s . T h e u n d e r l y i n g s e d i m e n t b e c o m e s a n o x i c , r e d u c i n g a n d t o x i c h y d r o g e n s u l f i d e a c c u m u l a t e s ( W h a r f e , 1977) . T h e m a c r o f a u n a of t h e s e s e d i m e n t s s u f f e r s l o s s e s b u t s o m e s n a i l s c o l o n i z e t h e a l g a l m a t s . W a d i n g b i r d s f o r a g e e l s e w h e r e b u t b r e n t g e e s e a n d w i g e o n s a c c e p t t h e s e g r e e n a l g a e as f o o d ( N i c h o l l s e t al., 1981; T u b b s , 1977). B e c a u s e a l g a l m a t s c o v e r i n g i n t e r t i d a l s e d i m e n t s a r e l i k e l y to e x p a n d f u r t h e r as e u t r o p h i c a t i o n of t h e s e a i n c r e a s e s , a c l o s e e x a m i n a t i o n of t h e i r e f f e c t s o n b e n t h i c f a u n a * This work was supported by a grant from the Deutsche Forschungsgemeinschaft (Re 425/3). is advisable. In this study, the response of m e i o b e n t h i c T u r b e l l a r i a a n d of small Polychaeta to e p h e m e r a l g r e e n a l g a l cover on s a n d y flats is d o c u m e n t e d . T u r b e l l a r i a are very rich i n species o n s a n d y tidal flats a n d comprise bacteria-feeders, diatom-feeders a n d predators. T h e y are often overlooked b y r o u t i n e s a m p l i n g b e c a u s e m a n y disintegrate or form u n r e c o g n i z a b l e cell-masses in p r e s e r v e d s e d i m e n t samples. Sorting of living, a n i m a l s is required. Species identification, however, is relatively easy a n d the sensitive response of T u r b e l l a r i a to short-term e n v i r o n m e n t a l d e g r a d a t i o n m a k e s this group well suited for i n v e s t i g a t i o n s into p o l l u t i o n effects on a taxon rich i n species. While the larger polycha.etes are a b l e to survive u n d e r the a l g a l mats, T u r b e l l a r i a suffer severe losses a n d / o r escape w h e n conditions get worse. Trophic groups, rare a n d a b u n d a n t species r e s p o n d differently. AREA AND METHODS Two study sites d e v e l o p i n g algal cover d u r i n g s u m m e r w e r e selected i n K6nigshafen, a shallow tidal b a y at the I s l a n d of Sylt (North Sea). Hydrography, s e d i m e n t s a n d m a c r o f a u n a of the area h a v e b e e n described b y W o h l e n b e r g (1937), 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 a n d y flats are relatively coarse g r a i n e d ( m e d i a n 456 ~ n , phi = 1.14, sorting coefficient 1.5). O r g a n i c c o n t e n t is ca 0.4 % (dry weight). Salinity r e m a i n s close to 31. A n n u a l m e a n t e m p e r a t u r e is ca 10 ?C, s u m m e r a v e r a g e is 15.1, w i n t e r a v e r a g e 4.5. T i d a l r a n g e is 1.7 m. Site 1 i n the i n n e r part of K 6 n i g s h a f e n is at m i d tide level, Site 2 i n the outer part of K 6 n i g s h a f e n close to low tide level. Both are a d j a c e n t to m i n o r domestic s e w a g e effluents. In summer, the outflow close to Site 1 is fed b y about 1000 p e o p l e a n d s e w a g e is almost untreated. Close to Site 2 the outflow is fed b y about 7000 p e o p l e a n d s e w a g e is m e c h a n i c a l l y treated (low particle load b u t h i g h c o n c e n t r a t i o n s of a m m o n i u m a n d phosphate; see Otte, 1979) . At Site 1 s a m p l i n g was d o n e after a m o n t h of coherent a l g a l cover (17 J u l y 1981) . S e d i m e n t cores of 2 cm2/0-5 cm w e r e t a k e n directly u n d e r n e a t h algal mats (n ~ 5), from small o p e n interspaces t e m p o r a r i l y u n c o v e r e d (n --- 5), a n d from a b a r e r e g i o n 150 m apart from the other s a m p l e positions a n d about 20 m outside the algal field (n ~ 5). In addition, pieces of algal mat w e r e cut out for investigation. T u r b e l l a r i a a n d small Polychaeta were sorted w h i l e alive without s i e v i n g the s e d i m e n t cores. To s a m p l e larger polychaetes, cores of 10 cm2/0-5 cm were w a s h e d t h r o u g h a 0.5-ram sieve. At Site 2, two a d j a c e n t plots, 10 ? 10 m, w e r e marked. A l g a l strands w e r e first n o t i c e d on 23 J u l y 1981, a n d from J u l y 28 on they w e r e r e m o v e d from one of the plots b y h a n d each day u n t i l A u g u s t 26. Drift algae were collected a n d d u m p e d a b o u t 50 m away. This kept the e x p e r i m e n t a l plot r e a s o n a b l y free from algal cover w h i l e the a d j a c e n t control was covered b y a coherent mat with only small interspaces from A u g u s t 5 onward. S a m p l i n g was d o n e at the b e g i n n i n g of e x p e r i m e n t to d o c u m e n t the initial conditions (July 28), a n d thereafter every 10 days o n the c l e a n e d plot. O n A u g u s t 26 the a l g a l area also was sampled. T e n cores of 2 cm2/0-2 cm were t a k e n e a c h time, a n d pieces of algal mats w e r e cut out. N o n - p a r a m e t r i c tests are a p p l i e d to the sets of s a m p l e s (Wilcoxon r a n k s u m U-test; Kruskal-Wallis m u l t i p l e c o m p a r i s o n H-test). P ~ 0.05 is r e g a r d e d as not s i g n i f i c a n t (ns). Diversity is expressed as D------(Zp~)-i a n d H ' = - ~pilnpi, w h e r e Pi is the relative proportion of species i from the total of i n d i v i d u a l s . E v e n n e s s was m e a s u r e d with a m o d i f i e d H i l l ' s ratio p r o p o s e d b y Alatalo (1981) , w r i t t e n as (D -- 1) / (exp H ' -- 1), w h e r e exp H ' is the a n t i l o g a r i t h m of H'. C o m p a r e d to Pielou's e v e n n e s s this m e a s u r e is less affected b y species richness. Species i d e n t i t y i n T u r b e l l a r i a is u s u a l l y confirmed b y i n s p e c t i o n of the complex reproductive organs. J u v e n i l e s c a n n o t always b e a s s i g n e d to a species w i t h certainty. In the p r e s e n t study, this is the case i n the g e n e r a Proxenetes (3 spp.) a n d Promesostoma (6 spp.). J u v e n i l e s comprised 72 % a n d 37 %, respectively. In c a l c u l a t i n g diversity i n d i c e s a n d plotting species versus a b u n d a n c e class, these j u v e n i l e s w e r e a s s i g n e d in proportion to the species b e i n g p r e s e n t as adults. G u t a n a l y s e s a n d f e e d i n g observations h a v e b e e n carried out on T u r b e l l a r i a at Site 2 since J u n e 1980 (see Reise, 1983) , a n d categories g i v e n i n T a b l e 5 are b a s e d on that study. RESULTS G r e e n a l g a l m a t s o n s a n d y t i d a l f l a t s G e r m l i n g s of Bnteromorpha spp., attached to s a n d grains, increase i n l e n g t h i n early summer, get branchy, a n d f i n a l l y b e c o m e p l a i t e d to tresses b y tidal currents a n d wave action. These strands of g r e e n a l g a e drift b a c k a n d forth w i t h the tides a n d finally b e c o m e deposited i n sheltered areas, or storms pile t h e m u p a l o n g the shoreline. However, since 1979, algal strands h a v e r e m a i n e d o n s a n d y flats. Explosive growth i n J u n e / J u l y led to the formation of thick algal mats, covering w i d e areas in the intertidal zone at the Island of Sylt. U s u a l l y t h e y stayed there u n t i l the e n d of A u g u s t w h e n storms r e m o v e d them. Enteromorpha spp. are the first to take root, t h e n other algae join the mats (i.e. Ulva spp., Cladophora spp., Chaetomorpha spp., Porphyra spp.). O n s a n d y flats, strands of g r e e n a l g a e m a y find a hold o n t u b e - c a p s of polychaetes (i.e. Lanice conchilega Pallas) a n d mollusc shells. However, i n the p r e s e n t case, algae b e c a m e p r i m a r i l y a n c h o r e d b y the s e d e n t a r y p o l y c h a e t e Arenicola marina (L.). This deposit feeder p o p u l a t e s the s a n d y flats with a m e a n d e n s i t y of 40 m -2 (Reise, 1981) . T o g e t h e r w i t h surface s e d i m e n t , strands of a l g a e slide d o w n the f e e d i n g f u n n e l s a n d h e a d shafts a n d thus b e c o m e "'rooted" i n 12 to 20 cm d e p t h (Fig. 1). This certainly is u n i n t e n d e d b y the l u g w o r m s b e c a u s e they shift their h e a d shafts into n e w positions once d o g g e d b y algae. W h e n a l g a e h a v e g r o w n into coherent mats, A. marina fixes t h e m to the s e d i m e n t with its b a c k w a r d s o r i e n t e d activity too. D u r i n g low tide, casts are p i l e d o n top of the a l g a l mats, thus b u r y i n g t h e m at these spots. Primarily it is the l u g w o r m p o p u l a t i o n w h i c h p r e v e n t s the g r e e n a l g a l m a t s from drifting to more sheltered flats. This conclusion is d e r i v e d from a l u g w o r m e x c l u s i o n e x p e r i m e n t started i n J u n e 1979 at Site 1. At three 4 - m2 plots, g a u z e of 1 m m m e s h was i n s e r t e d horizontally into the g r o u n d a p p r o x i m a t e l y 10 cm deep, The g a u z e b l o c k e d the w a y to the surface a n d thus forced the worms to move out at the sites. In J u l y 1981, the entire s e d i m e n t at Site 1 was covered b y thick a l g a l mats except the three plots where a l g a e found no a n c h o r a g e b e c a u s e A. marina was excluded. In 1981 w h e n this i n v e s t i g a t i o n was carried out, coherent mats were a p p a r e n t at Site 1 from the m i d d l e of J u n e to the e n d of August. At Site 2, algal strands w e r e first noticed o n J u l y 23. A l r e a d y 12 d a y s later, c o h e r e n t m a t s c o v e r e d a b o u t 50 % of t h e surface. W i t h i n a f e w days, c o v e r a g e w a s a l m o s t total, e x t e n d i n g o v e r a b o u t 2 ha. A t t h e e n d of A u g u s t , s t o r m s r e m o v e d all a l g a l c o v e r . P o l y c h a e t a w i t h a n d w i t h o u t a l g a l c o v e r O n e m o n t h of a l g a l c o v e r at S i t e 1 d i d n o t s i g n i f i c a n t l y affect t h e c o m p o s i t i o n of t h e p o l y c h a e t e a s s e m b l a g e ( T a b l e 1). T h i s s t a t e m e n t is i n p a r t c o m p e l l e d b y t h e h i g h v a r i a t i o n w i t h i n sets of s a m p l e s . M o r e e x t e n s i v e s a m p l i n g of s m a l l p o l y c h a e t e s m i g h t h a v e r e v e a l e d a s i g n i f i c a n t i n c r e a s e in j u v e n i l e Capitella capitata. In t h e e x p e r i m e n t at Site 2 no s i g n i f i c a n t d i f f e r e n c e s b e t w e e n t r e a t m e n t s (U-test) or o v e r t h e p e r i o d of 30 days o n t h e c l e a n e d a r e a (H-test) w e r e o b s e r v e d ( T a b l e 2). D i v e r s i t y a n d e v e n n e s s are r e l a t i v e l y h i g h u n d e r a l g a l c o v e r b e c a u s e Pygospio elegans loses its d o m i n a n c e . H o w e v e r , t h e d e c r e a s e in a b u n d a n c e of this s p e c i e s is not s i g n i f i c a n t (U-test, P = 0.25). T u r b e l l a r i a w i t h a n d w i t h o u t a l g a l c o v e r G r e e n a l g a l m a t s h a v e a d v e r s e effects on all b e n t h i c T u r b e l l a r i a . A t Site 1, s a m p l e s w e r e t a k e n o n e m o n t h a f t e r t h e o n s e t of a l g a l c o v e r ( T a b l e 3). Small, t e m p o r a r i l y o p e n p a t c h e s p r o v i d e n o r e s c u e . A b u n d a n c e a n d s p e c i e s r i c h n e s s a r e s i g n i f i c a n t l y h i g h e r o n t h e b a r e flat (U-test, P < 0.001), D i v e r s i t y is l o w e r in t h e a l g a l field, e v e n n e s s h i g h e r . T h i s is b e c a u s e t h e d o m i n a n t s p e c i e s o n t h e b a r e flat (Cheliplanilla caudata, Cicerina brevicirrus, Promesostoma rostratum) lose t h e i r d o m i n a n c e b e l o w a l g a l cover. N o Turb e l l a r i a w e r e f o u n d w i t h i n t h e f l o a t i n g a l g a l mats. E v e n o n t h e b a r e flat, a b u n d a n c e w a s b a c t e r i a - f e e d e r s (2.8-fold). D i a t o m - f e e d e r s a l s o i n c r e a s e d s i g n i f i c a n t l y i n t h e i r p r o p o r t i o n r e l a t i v e to t h e o t h e r t r o p h i c g r o u p s {U-test, P < 0.05). T h e s p e c i e s p a r t i c u l a r l y a f f e c t e d b y a l g a l c o v e r w e r e t h e t h r e e d i a t o m - f e e d i n g M a c r o s t o m u m pus111um, Pogalna sueclca a n d P o s t m e c y n o s t o m u m p i c t u m . O n t h e c l e a n e d a r e a , t h e r e l a t i v e p r o p o r t i o n of p u s l l l u m w i t h i n t h e t u r b e l l a r i a n a s s e m b l a g e i n c r e a s e d s i g n i f i c a n t l y (U-test, P < 0.05}. T h i s is a l s o i n d i c a t e d for P. sueclca (P = 0.06), w h i l e A r c h i l o p s i s unipunctata is o n a s l i g h t l y i n c r e a s i n g t r e n d (P -----0.09). T h e d i f f e r e n c e i n s p e c i e s r i c h n e s s is c o n s p i c u ous, b u t d i v e r s i t y is o n l y s l i g h t l y h i g h e r o n t h e c l e a n e d flat b e c a u s e of a l o w e v e n n e s s c o m p o n e n t . B a s e d o n t h e c o m p l e t e s p e c i e s a b u n d a n c e d a t a ( T a b l e 5}, g r a p h s of s p e c i e s v e r s u s a b u n d a n c e c l a s s ( g e o m e t r i c i n t e r v a l s } a r e p r e s e n t e d for {1) T u r b e l l a r i a at t h e o n s e t of a l g a l g r o w t h {start of e x p e r i m e n t } , {2) T u r b e l l a r i a b e l o w a l g a l c o v e r o n e m o n t h later, a n d {3} T u r b e l l a r i a o n t h e c l e a n e d p l o t {Pig. 2}. Initially, t h e t u r b e l t a r i a n a s s e m b l a g e w a s c h a r a c t e r i z e d b y a h i g h e v e n n e s s w h e r e s p e c i e s w i t h a m o d e r a t e n u m b e r of i n d i v i d u a l s d o m i n a t e d . U n d e r a l g a l c o v e r m o s t s p e c i e s h a v e o n l y f e w i n d i v i d u a l s a n d n o n e a r e v e r y a b u n d a n t . C h a n c e of s u r v i v a l u n d e r a l g a l c o v e r is c a l c u l a t e d p e r g e o m e t r i c a b u n d a n c e c l a s s (initial c o n d i t i o n s are s e t to 100 %}. I n d i v i d u a l s of i n i t i a l l y r a r e s p e c i e s as w e l l as t h o s e of i n i t i a l l y v e r y a b u n d a n t s p e c i e s h a v e a l o w c h a n c e of survival, w h i l e i n d i v i d u a l s of m o d e r a t e l y a b u n d a n t s p e c i e s h a v e a m o r e t h a n 50 % c h a n c e (Pig. 2). O n t h e e x p e r i m e n t a l p l o t f r e e of a l g a e t h e r e a r e m a n y r a r e s p e c i e s a n d f o u r w h i c h f a c i l i t a t e d d i s p e r s a l . (2) P r o m e s o s t o m a r o s t r a t u m o c c u r r e d w i t h t h r e e m a t u r e a n d initial conditions July 28 Pig. 2. Number of species (abscissa) versus geometric abundance class (ordinate) of Turbellaria at the beginning and end of experiment (see Table 5), and chance of survival for individuals subject to algal cover. Number of species present initially are set to 100 % (first two classes are taken together to obtain a comparative number of individuals) and the fraction of species present below the algae are assumed to be survivors 2 j u v e n i l e i n d i v i d u a l s in t h e s a m p l e s from A u g u s t 16. O n l y 10 days later, t h e r e w e r e 20 m a t u r e P. rostratum. (3) S p e c i e s richness i n c r e a s e d from 26 to 36 in the s a m e interval. T h e s e o b s e r v a t i o n s a n d other d a t a p r e s e n t e d in T a b l e 4 i n d i c a t e a substantial i m m i g r a tion of T u r b e l l a r i a from t h e a l g a l c o v e r e d fiat into t h e insular e x p e r i m e n t a l plot free of a l g a e . This i m m i g r a t i o n c a u s e d a d e c r e a s e in e v e n n e s s b e c a u s e a b u n d a n t s p e c i e s further i m p r o v e d t h e i r d o m i n a n c e . Rare species did not b e c o m e m o r e c o m m o n but other rare s p e c i e s arrived. W h i l e d i a t o m - f e e d e r s and predators d o u b l e d their n u m b e r s since the initiation of e x p e r i m e n t , t h e r e w a s no significant i n c r e a s e i n b a c t e r i a - f e e d e r s on the c l e a n e d plot (Table 4). D I S C U S S I O N G r e e n a l g a l m a t s T h e m a c r o a l g a e and s e a g r a s s e s of K 6 n i g s h a f e n w e r e i n v e s t i g a t e d in 1924 to 1926 by N i e n b u r g (1927). H e p r o v i d e d a m a p of the v e g e t a t i o n . Regions w i t h g r o w t h of Hnteromorpha spp. b e t w e e n April and J u l y w e r e l o c a t e d close to the h i g h tide line, just above the Zostera noltii b e l t (his Z. nana). Dense growth of Chaetomorpha linum was o b s e r v e d i n two m u d d y bights. All in all, only small patches were covered (< 1 ha). Later, W o h l e n b e r g (1937) a n d K o r n m a n n (1952) also m e n t i o n these g r e e n a l g a e b u t report n o excessive growth either. T h e p r e s e n t g r e e n a l g a l mats occur from the Zostera noltii b e l t on downwards, w h e r e n o g r e e n algal growth was observed earlier. A c c o r d i n g to N i e n b u r g ' s map, Site 1 was v e g e t a t e d b y a small variety of Zostera marina (his Z. angustifolia), a n d Site 2 was without a n y macrophytes. I h a v e no direct e v i d e n c e that the p r e s e n t algal mats are c a u s e d b y s e w a g e effluents. However, this is very likely b e c a u s e (1) they were a b s e n t from the flats i n earlier times w h e n no or little s e w a g e e n t e r e d the bay, (2) they occur i n J u l y - A u g u s t w h e n s e w a g e load is more t h a n d o u b l e d b e c a u s e of the tourist season, (3) their proximity to the two outflows is a p a t t e r n w h i c h has consistently b e e n observed e l s e w h e r e i n the W a d d e n Sea, a n d has b e e n r e p e a t e d l y reported from other r e g i o n s (see r e v i e w s i n H a r l i n & Thorne-Miller, 1981; Nicholls et al., 1981) . Sewage m a y not b e the only agent, a n d favourable weather, particularly a calm sea, is a n o t h e r prerequisite (Perkins & Abbott, 1972) . U n d e r the h y d r o g r a p h i c conditions i n KSnigshafen, a b u n d a n c e of Arenicola marina is important, as it k e e p s the algal mats on the s a n d y flats i n spite of the strong tidal currents. Without the a n c h o r a g e provided b y the l u g w o r m s ' f e e d i n g funnels, the g r e e n algal mats w o u l d b e c o n f i n e d to more s h e l t e r e d sites or get w a s h e d out of the bay. A. marina is a b u n d a n t o n almost all s a n d y tidal flats along E u r o p e a n coasts, a n d outside Europe other l u g w o r m species m a y p l a y a similar role. Thus, the u n i n t e n d e d "rooting" of g r e e n algae b y l u g w o r m s m i g h t h a p p e n e l s e w h e r e w h e n e n h a n c e d e u t r o p h i c a t i o n causes explosive growth of these algae. P o l y c h a e t a b e l o w a l g a l m a t s O n e m o n t h or less of a l g a l cover c a u s e d n o m e a s u r a b l e losses i n p o l y c h a e t e s at b o t h sites, a n d no species i n c r e a s e d significantly. Nicholls et al. (1981) who i n v e s t i g a t e d m u d d y fiats covered b y g r e e n algal mats from M a y to D e c e m b e r each year, f o u n d striking effects on polychaetes. All species were less a b u n d a n t b e l o w algal mats except two, Capitella capitata a n d Scolelepis fuliginosa, w h i c h b e c a m e e x t r e m e l y n u m e r o u s . As m a n y of these species occur also at Site 1 a n d 2, the difference is l i k e l y to lie i n the d u r a t i o n of algal cover (1 m o n t h versus 8 months). C o m p a r e d to the smaller Turbellaria, polychaetes show more s t a m i n a w h e n their h a b i t a t is s u b j e c t e d to adverse conditions. T u r b e l l a r i a b e l o w a l g a l m a t s T u r b e l l a r i a are a b u n d a n t a n d diverse on s a n d y flats. A l o n g - t e r m d e c l i n e i n a b u n d a n c e at Site 1 coincides with the year w h e n algal mats w e r e observed for the first time. However, the u n u s u a l l y severe w i n t e r of 1979 w i t h its ice cover l a s t i n g 67 days at Site 1, where n o r m a l l y there is n o n e or one lasting less t h a n a week, m a y be a n o t h e r cause. At Site 2, a l g a l cover was observed in 1981 for the first time. Here a v e r a g e a b u n d a n c e a n d species richness of T u r b e l l a r i a is g e n e r a l l y high: 111 - 10 cm -2 a n d 83 species from J u n e 1980 to J u n e 1981 (Reise, 1983) . S a m p l e s d u r i n g the e x p e r i m e n t i n J u l y / A u g u s t 1981 g a v e a n a v e r a g e of 87 - 10 cm -2 a n d a total of 42 species. These T u r b e l l a r i a are very sensitive to e n v i r o n m e n t a l deterioration c a u s e d b y a n e p h e m e r a l a l g a l cover. All d e c l i n e d ; no species took a d v a n t a g e of the altered habitat. With respect to the s e d i m e n t this is not s u r p r i s i n g as anoxic conditions d e v e l o p e d b e l o w a l g a l cover, a n d there s e e m to b e n o T u r b e l l a r i a f a v o u r i n g p u r e l y anoxic s e d i m e n t s (Reise & Ax, 1979) . O n the surface, d i a t o m growth was p r o b a b l y i n h i b i t e d b y s h a d i n g (see Sullivan, 1976) . This m a y h a v e c a u s e d food shortage to diatom-feeders. O n the g r e e n a l g a e themselves, epiphytic diatoms w e r e observed. Snails, Hydrobia ulvae, grazed on these a n d not o n the g r e e n algae. Some ciliates a n d copepods were also present. Phytal Turbellaria, however, r e m a i n e d absent. P r o b a b l y the d u r a t i o n of algal mats o n the s a n d flats was too short for colonization. D i a t o m - f e e d i n g T u r b e l l a r i a d e c l i n e d d r a m a t i c a l l y w h e n covered b y g r e e n algae, w h i l e p r e d o m i n a n t l y b a c t e r i a - f e e d i n g species w e r e less affected. This m a y reflect the effects of g r e e n a l g a e on the respective food resources. O n the other hand, diatomfeeders are s u r f a c e - d w e l l i n g species a n d as such more sensitive to a n a e r o b i c conditions t h a n the d e e p e r d w e l l i n g bacteria-feeders. Predators show a n i n t e r m e d i a t e response. C o m p a r e d to the initial conditions one m o n t h earlier, algal cover c a u s e d h i g h losses i n rare a n d very a b u n d a n t species. T h e m o d e r a t e l y a b u n d a n t species did better. Therefore diversity a n d e v e n n e s s i n d i c a t e little change. This p a t t e r n of survival suggests that the i n i t i a l l y most a b u n d a n t species m a y b e r e g a r d e d as "'specialists", u n a b l e to cope with a c h a n g e i n habitat. M o d e r a t e l y a b u n d a n t species s e e m to i n c l u d e most " g e n e r a l ists", b e t t e r p r e p a r e d to survive altered conditions. A r e f u g e f r o m a l g a l m a t s The s e m i - c o n t r o l l e d field e x p e r i m e n t c o n d u c t e d at Site 2 r e v e a l e d that T u r b e l l a r i a w e r e a b l e to e s c a p e from their d e t e r i o r a t i n g habitat. T h e 100-m2 plot k e p t c l e a n of g r e e n algae was located right i n the m i d d l e of the algal field. W h a t was i n t e n d e d to b e a control area to the algal mats e v e n t u a l l y t u r n e d out to be a refuge for T u r b e l l a r i a i n n e e d of a n e w habitat. The c l e a n e d area was well w i t h i n reach, a n d e v e n more so w h e n a r o u g h sea facilitated dispersal. C o m p a r e d to initial conditions, the refuge is characterized b y a n i n c r e a s e d n u m b e r of rare species a n d some w h i c h b e c a m e extremely a b u n d a n t . T h e n u m b e r of m o d e r a t e l y a b u n d a n t species r e m a i n e d about the same. The c o r r e s p o n d i n g g r a p h of species versus geometric a b u n d a n c e class r e s e m b l e s that of m a c r o b e n t h o s u n d e r p o l l u t e d conditions, except that rare species are more significant (see G r a y & Pearson, 1982) . T h e fact that the control s e r v e d as a rescue a r e a fouled my e x p e r i m e n t which h a d b e e n d e s i g n e d to quantify the effects of algal cover o n Turbellaria. However, the i m p o r t a n c e of area size is h i g h l i g h t e d , a n d s h o u l d b e c o n s i d e r e d w h e n effects of a l g a l cover are e v a l u a t e d . If spatial refuges are nearby, c o n s i d e r a b l e n u m b e r s of T u r b e l l a r i a c a n survive the e p h e m e r a l h a b i t a t c h a n g e b y escape a n d later m a y recolonize. Purthermore, the o b s e r v e d escape r e s p o n s e m a y serve as a w a r n i n g , not to take d w i n d l i n g a b u n d a n c e s i n b e n t h o s s i m p l y as mortality u n l e s s the d e a d i n d i v i d u a l s are actually found. CONCLUSIONS Excessive growth of g r e e n a l g a e (Chlorophyceae) on the tidal flats of the W a d d e n Sea d u r i n g s u m m e r is attributed to e u t r o p h i c a t i o n b y a d j a c e n t s e w a g e effluents. Mats of t h e s e a l g a e c o v e r w i d e a r e a s o n s h e l t e r e d flats, a n d o n s a n d y flats a l g a e b e c o m e a n c h o r e d i n t h e f e e d i n g f u n n e l s of t h e a b u n d a n t p o l y c h a e t e Arenicola marina. A l g a l c o v e r e d s e d i m e n t s t u r n a n o x i c a n d a f f e c t t h e i n f a u n a . S t o r m s a r e a b l e to d i s l o c a t e t h e a l g a l m a t s , a n d s a n d y flats a r e u s u a l l y c o v e r e d for n o m o r e t h a n o n e m o n t h . S u c h s h o r t t e r m c o v e r is e n d u r e d b y p o l y c h a e t e s b u t t h e s m a l l e r T u r b e l l a r i a s u f f e r s e v e r e l o s s e s . In t h i s s p e c i e s - r i c h t a x o n , a b u n d a n c e , s p e c i e s r i c h n e s s a n d d i v e r s i t y d e c r e a s e d w h i l e e v e n n e s s i n c r e a s e d , c o m p a r e d to t h e b a r e s a n d flat a r e a s . P a r t i c u l a r l y a f f e c t e d w e r e d i a t o m - f e e d e r s ; m o d e r a t e l y a b u n d a n t s p e c i e s s u r v i v e d b e t t e r t h a n t h e r a r e a n d v e r y a b u n d a n t o n e s . N o n e of t h e s p e c i e s w a s a b l e to t a k e a d v a n t a g e of t h e h a b i t a t a l t e r a t i o n . P r e v e n t i n g a l g a l g r o w t h o n a n e x p e r i m e n t a l p l o t w i t h i n a n e x t e n s i v e f i e l d of a l g a l m a t s d e m o n s t r a t e d t h e c a p a b i l i t y of s o m e T u r b e l l a r i a to m o v e o u t a n d t a k e a d v a n t a g e of n e a r b y r e s c u e a r e a s . T h i s is t h e first s t u d y u s i n g t h e s e n s i t i v i t y of T u r b e l l a r i a to d o c u m e n t e f f e c t s of p o l l u t i o n . 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Karsten Reise. Sewage, green algal mats anchored by lugworms, and the effects on Turbellaria and small Polychaeta, Helgoland Marine Research, 151, DOI: 10.1007/BF01983854