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Effects ofFucus vesiculosus covering intertidal mussel beds in the Wadden Sea

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HELGOL,~NDER MEERESUNTERSUCHUNGEN Helgol~inder Meeresunters. 48, 243-256 (1994)

E f f e c t s of

F u c u s v e s i c u l o s u s

c o v e r i n g i n t e r t i d a l m u s s e l

b e d s i n t h e W a d d e n S e a

A. Albrecht & K. Reise

Biologische A n s t a l t Helgoland, W a t t e n m e e r s t a t i o n Silt; D-25992 List, Federal R e p u b l i c o f G e r m a n y

ABSTRACT: The brown alga Fucus vesiculosus forma mytili (Nienburg) Nienhuis covered about 70 % of mussel bed (Mytilus edulis) surface area in the lower intertidal zone of K6nigshafen, a sheltered sandy bay near the island of Sylt in the North Sea. Mean biomass in dense patches was 584 g ash-free dry weight m -2 in summer. On experimental mussel beds, fucoid cover e n h a n c e d mud accumulation and decreased mussel density. The position of mussels underneath algal canopy was mainly endobenthic (87 % of mussels with > 1~ of shell sunk into mud). In the absence of fucoids, mussels generated epibenthic garlands (81% of mussels with < I/3 of shell buried in mud). Mussel density underneath fucoid cover was 40 to 73 % of mussel density without algae. On natural beds, barnacles (Balanidae), periwinkles (IAttorina littorea) and crabs (particularly juveniles of Carcinus maenas) were significantly less abundant in the presence of fucoids, presumably because most of the mussels were covered with sediment, whereas in the absence of fucoids, epibenthic mussel clumps provided substratum as well as interstitial hiding places. The endobenthic macrofauna showed tittle difference between covered and uncovered mussel beds. On the other hand, grazing herbivores - the flat periwinkle LittoHna mariae, the isopod Jaera albi[rons and the amphipods Gammarus spp. - were more abundant at equivalent sites with fucoid cover. The patchy growth of Fucus vesiculosus on mussel beds in the intertidal Wadden Sea affects mussels and their epibionts negatively, but supports various herbivores and increases overall benthic diversity.

I N T R O D U C T I O N

T h e m u s s e l M y t i l u s edulis L. g e n e r a t e s d r i f t i n g c l u m p s a n d b i o g e n i c r e e f s in t h e W a d d e n Sea. T h e s e m u s s e l b e d s a r e a b u n d a n t in t h e l o w e r tidal z o n e a n d s u b t i d a l l y ( V e r w e y , 1954; R i e s e n & Reise, 1982; D a n k e r s & K o e l e m a i j , 1989; O b e r t & M i c h a e l i s , 1991), c o n s t i t u t i n g e c o l o g i c a l e l i t e s t r u c t u r e s in t e r m s of t h e h i g h n u m b e r of a s s o c i a t e d s p e c i e s ( D i t t m a n n , 1990), b i o m a s s a n d s e c o n d a r y p r o d u c t i o n (Asmus, 1987), f o r a g i n g site for b i r d s ( S w e n n e n et al., 1989; Z w a r t s , 1983), r e m i n e r a l i z a t i o n , a n d o x y g e n c o n s u m p t i o n ( D a m e & D a n k e r s , 1988; A s m u s et al., 1990).

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244 A. A l b r e c h t & K. Reise

b u r i e d in s e d i m e n t whilst s i m u l t a n e o u s l y g r o w i n g u p w a r a s m tl~e w a t e r c o l u m n . N i e n - b u r g (1925, 1927) d e s c r i b e d t h e r e c i p r o c a l effect of m u s s e l s a n d fucoids on e a c h o t h e r as b e n e f i c i a l for b o t h parties. H e b e l i e v e d t h a t F. vesicutosus p r e v e n t e d the m u s s e l s from s i n k i n g into t h e m u d , w h e r e a s m u s s e l s e n a b l e d s t e a d y g r o w t h of the a l g a b y h o l d i n g it firm w i t h their b y s s u s threads.

In the p r e s e n t study, i n v e s t i g a t i o n s a b o u t the p o s s i b l e effects of f u c o i d cover on m u s s e l s a r e e x t e n d e d to the a s s o c i a t e d m a c r o f a u n a of m u s s e l beds. T h e m a c r o a l g a e r e p r e s e n t a n a d d i t i o n a l p h y s i c a l a n d b i o l o g i c a l structure in the m u s s e l b e d c o m m u n i t y . This structure could function as food for h e r b i v o r e s a n d a h a b i t a t for e p i f a u n a (Nicotri, 1980), as s u b s t r a t e for e p i p h y t e s (Kangas et al., 1982) or as s h e l t e r a g a i n s t p h y s i c a l stress a n d p r e d a t i o n (Dean & Connell, 1987), thus i n c r e a s i n g overall h a b i t a t c o m p l e x i t y .

Results w e r e o b t a i n e d b y p a r a l l e l s a m p l i n g of c o v e r e d a n d u n c o v e r e d b e d s in the tidal zone of K 6 n i g s h a f e n n e a r Sylt. T h e h y p o t h e s i s t h a t p a t c h e s of F. vesiculosus significantly alter siltation a n d the c o m p o s i t i o n of the s p e c i e s a s s e m b l a g e , w a s t e s t e d e x p e r i m e n t a l l y .

MATERIAL A N D M E T H O D S

S t u d y s i t e

I n v e s t i g a t i o n s w e r e c a r r i e d out in " K 6 n i g s h a f e n ' , the s a m e shallow t i d a l b a y n e a r the i s l a n d of Sylt, N o r t h Sea, w h e r e N i e n b u r g (1925) first s t u d i e d the Fucus-Mytilus association. T h e distribution a n d size of m u s s e l b e d s in t h e a r e a h a v e b e e n s u b j e c t to g r e a t v a r i a t i o n since the e a r l y reports from the b e g i n n i n g of t h e century. S u c h fluctua- tions w e r e c a u s e d b y s e v e r e w i n t e r s ( Z i e g e l m e i e r , 1964, 1970) a n d p r e s u m a b l y e u t r o p h i - cation (Reise et al., 1989).

Two locations in t h e b a y w h i c h are c h a r a c t e r i z e d b y different p h y s i c a l p r o p e r t i e s w e r e c h o s e n for this study. T h e " O d d e w a t t " at t h e e a s t e r n o p e n i n g of the b a y r e p r e s e n t s a n e x p o s e d site with m u s s e l b e d s e x t e n d i n g a l o n g the low w a t e r line; the " M 6 w e n b e r g - watt" is l o c a t e d in the central p a r t of K 6 n i g s h a f e n a n d is thus m o r e s h e l t e r e d , w i t h m u s s e l b e d s b e i n g s i t u a t e d slightly further u p s h o r e . Both locations are s a n d y , b u t t h e O d d e w a t t is c h a r a c t e r i z e d b y a h i g h e r p o r t i o n of c o a r s e (0.36-0.6 ram) a n d a l o w e r p o r t i o n of fine {0.09-0.15 ram) s e d i m e n t (Austen, 1992).

A l g a l b i o m a s s

Thalli of Fucus vesiculosus w e r e c l i p p e d at the s e d i m e n t surface from p a t c h e s with d e n s e g r o w t h (100 % surface cover; v i s u a l estimation) on m u s s e l b e d s in M 6 w e n b e r g - watt. T w e n t y r e p l i c a t e s a m p l e s of 0.25 m 2 w e r e t a k e n b e t w e e n M a y a n d J u n e 1990. In the laboratory, the thalli w e r e w a s h e d w i t h s e a w a t e r , b l o t t e d a n d w e i g h e d (fresh weight), a n d t h e n d r i e d for t h r e e d a y s at 80 ~ (dry weight), 6 samples, e a c h w e i g h i n g 25 g (dry weight), w e r e c o m b u s t e d for 5h at 520 ~ to d e t e r m i n e the o r g a n i c c o n t e n t as a s h - f r e e d r y weight.

S i l t a t i o n e x p e r i m e n t

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Effects of F u c u s on mussels 245 beds in M 6 w e n b e r g w a t t - which display a mosaic of fucoid cover - c l u m p s of mussels with a n d without a t t a c h e d algae were r e m o v e d with a shovel. T h e y w e r e a r r a n g e d in b e d s of a p p r o x i m a t e l y lm 2, four with a n d three w i t h o u t algae, at a distance of a b o u t 2 m from each other a n d situated i n the direct vicinity of the n a t u r a l beds. C l u m p s of m u s s e l s were placed together, with a n a d h e r i n g layer of mud, u p o n circular sheets of plastic foil which, s u b s e q u e n t l y , served as a reference to m e a s u r e the h e i g h t of s e d i m e n t a c c u m u - lation. This was d e t e r m i n e d b y p r o b i n g a ruler 10 times into the m u d of the c e n t r a l area (0.3 m 2) of each m u s s e l bed. The initial density of mussels (> 10 m m shell length) was a r r a n g e d into 200 i n d i v i d u a l s o n 1000 c m 2 with a n a p p r o x i m a t e error of - 50. M u s s e l

spat was n o t c o n s i d e r e d in the counts, b e c a u s e it was insignificant c o m p a r e d to the n u m b e r of individuals.

T h e vertical position of m u s s e l s i n the s e d i m e n t was categorized as either i n f a u n a l (> 2/3 of shell s u n k into the mud), s e m i - e p i f a u n a l (2/3 to '/3) or e p i f a u n a l (< '/3 of shell b u r i e d in mud).

T h e e x p e r i m e n t was started on July 3rd 1991 a n d t e r m i n a t e d on J u l y 18th 1992. T h r o u g h o u t the e x p e r i m e n t the drift algae e n c o u n t e r e d were r e m o v e d from the three beds d e s i g n e d to b e free of fucoids. After July 1992, the e x p e r i m e n t a l b e d s w e r e left u n a t t e n d e d . In N o v e m b e r 1992, these b e d s were completely c o v e r e d b y F. v e s i c u l o s u s again.

C o m p a r i s o n of m a c r o f a u n a

At both locations - O d d e w a t t a n d M b w e n b e r g w a t t - 12 replicate s a m p l e s e a c h w e r e t a k e n from m u s s e l b e d patches covered with F u c u s v e s i c u l o s u s a n d from u n c o v e r e d patches d u r i n g J u n e to A u g u s t 1990. S a m p l i n g p r o c e d u r e was selective, in that s a m p l e s were t a k e n in pairs of two from directly a d j a c e n t areas of the s a m e m u s s e l b e d that was only partly algae-covered. Thus, fucoid growth was the only obvious p a r a m e t e r differ- e n t i a t i n g the two plots.

A box corer of 500 cm 2 surface area was u s e d to take s a m p l e s d o w n to a d e p t h of 15 cm, below w h i c h no living m a c r o f a u n a occurred. If present, algae were cut off the surface a n d treated separately: a n y a d h e r i n g e p i f a u n a was w a s h e d off a n d r e t a i n e d i n a sieve (500 ~m m e s h size) to b e identified a n d counted. T h e s e d i m e n t p o r t i o n of the sample was w a s h e d a n d sieved (500 ~m) a n d the residues from the sieve t r a n s f e r r e d into sorting dishes from which a n i m a l s w e r e extracted alive. All taxa, except oligochaetes a n d gammarids, were identified to species level u s i n g a stereo microscope. H e a v y recruit- m e n t of C a r c i n u s m a e n a s a n d N e r e i s d i v e r s i c o l o r occurred d u r i n g the s a m p l i n g period; therefore these species were r o u g h l y g r o u p e d into size classes.

Statistics

Differences in faunal densities (and in vertical position of

NIytilus individuals)

between algae-covered and uncovered mussel aggregations were tested with the non- parametric U-test of Wilcoxon, Mann & Whitney (Sachs, 1984). Differences were consi- dered significant at different levels and marked by asterisks in the following fashion:

* 0.05 -- p > 0.02, ** 0.02 -> p > 0.002, *** 0.002 -> p.

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246 A. A l b r e c h t & K. Reise

W i e n e r - I n d e x H = - X Pi * In Pi, w i t h Pi b e i n g the portion of a species' (ni) n u m b e r of in- dividuals b a s e d on the total n u m b e r of i n d i v i d u a l s (N): Pi = ni/N; (b) E v e n n e s s e -- H / i n S, with S b e i n g the total n u m b e r of species.

RESULTS A l g a l c o v e r

Patches within m u s s e l b e d s c o v e r e d entirely by F u c u s vesiculosus h a d a b i o m a s s of 4811 ___ 909 g fresh w e i g h t or 1050 --- 187 g dry w e i g h t m -2 ( n = 20), c o r r e s p o n d i n g to 584 "4- 104 g ash-free dry w e i g h t m -2 in M a y to J u n e 1990. Fucoid surface c o v e r of m u s s e l b e d s in 1990 w a s e s t i m a t e d at 60 % in O d d e w a t t a n d 70 % in M 6 w e n b e r g w a t t . T h e following y e a r in J u n e , surface c o v e r in t h e m u s s e l b e d areas r e a c h e d 95 a n d 55 %, respectively. With 70 % c o v e r as an o v e r a l l m e a n , fucoid biomass on m u s s e l b e d s in K S n i g s h a f e n w a s a p p r o x i m a t e l y 400 g a s h - f r e e dry w e i g h t m -2 in s u m m e r .

S i l t a t i o n e x p e r i m e n t

Within 5 days after s e t t i n g - u p the e x p e r i m e n t a l mussel beds, t h e distribution of mussels h a d c h a n g e d from the initial e v e n a r r a n g e m e n t . D u r i n g this time, w e a t h e r conditions h a d b e e n constantly calm. In t h e a b s e n c e of fucoid cover, m u s s e l s a g g r e g a t e d into e p i b e n t h i c garlands. T h i c k d i a t o m g r o w t h was visible on the m u d surface in t h e interspaces. In the p r e s e n c e of fucoids, m u s s e l s f o r m e d a continuous m o n o l a y e r , w i t h most i n d i v i d u a l s b u r i e d in m u d by a b o u t two-thirds of their shell length. W h e n p r o b i n g the m u d d e p t h after 4 w e e k s in A u g u s t , a smell of h y d r o g e n sulfide w a s a p p a r e n t .

In the course of the e x p e r i m e n t all m u s s e l b e d s b e c a m e larger. Initially, the m e a n size w a s 1.1 m 2. Six m o n t h s l a t e r the m e a n size w a s 1.6 m 2, with no s i g n i f i c a n t d i f f e r e n c e b e t w e e n treatments. H o w e v e r , m u s s e l b e d s w i t h o u t fucoid c o v e r h a d t w i c e the m u s s e l density of b e d s with algae. M e a n d e n s i t y of mussels was 119 --- 12 a n d 61 ___ 21, respectively, (July, 1992) on 1000 cm 2 in the centre of beds: T a k i n g the a r e a l i n c r e a s e of e a c h m u s s e l b e d into account, m u s s e l n u m b e r s h a d d e c r e a s e d by t h e e n d of t h e e x p e r i m e n t (after 1 year) by 15 ___ 10% w i t h o u t fucoid c o v e r a n d by 54 _+ 18 % w i t h fucoid cover. This d i f f e r e n c e w a s s i g n i f i c a n t at the 5 % - l e v e l (U-test).

E x p e r i m e n t a l m u s s e l b e d s c o v e r e d by F u c u s vesiculosus a c c u m u l a t e d m o r e sedi- m e n t than the b a r e b e d s (Fig. 1). Initially, the h e i g h t of m u d was 95 ___ 6 ram. With a l g a l cover, s e d i m e n t h e i g h t i n c r e a s e d until D e c e m b e r to 123 ___ 19 ram, d e c r e a s i n g t h e r e a f t e r to 84 _+ 10 m m in J u l y 1992. Intermittently, the n e t g a i n of s e d i m e n t at o n e b e d w a s up to 47 ram. Without algal cover, the h e i g h t of m u d d e c r e a s e d to 41 + 10 turn in D e c e m b e r a n d further to 22 _+ 23 m m in J u l y 1992.

V e r t i c a l p o s i t i o n of m u s s e l s

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E f f e c t s of F u c u s o n m u s s e l s 247 150 m m

I00

50

o

July Oec./Ja.. July

1991 1992

Fig. 1. H e i g h t of m u d surface in experimental mussel beds, 4 b e d s with a n d 3 without fucoid cover, m e a s u r e d at irregular intervals b e t w e e n July 1991 a n d July 1992. M e a n values of 10 m e a s u r e m e n t s e a c h are plotted p e r site a n d date (average s t a n d a r d demation 9.5 ram). Initial h e i g h t v a r i e d

b e t w e e n 84 a n d 105 m m a n d was s t a n d a r d i z e d to the m e a n of 95 m m to facilitate comparison

b e d s i n M 6 w e n b e r g w a t t t h a t c o m p r i s e d a m o s a i c of b a r e p a t c h e s a n d p a t c h e s w i t h f u c o i d c o v e r ( T a b l e 1). U n d e r n e a t h f u c o i d c o v e r , t h e d e n s i t y of m u s s e l s w a s o n l y 4 0 % of t h e d e n s i t y w i t h o u t a l g a e , a n d m o s t m u s s e l s h a d s u n k i n t o t h e m u d . I n t h e p r e s e n c e of f u c o i d s , 87 % of m u s s e l s ( > 1 0 r a m ) w e r e b u r i e d i n m u d w i t h > 1/3 of t h e i r s h e l l l e n g t h ( e n d o b e n t h i c g r o w t h ) . In t h e a b s e n c e of f u c o i d s , 8 1 % of m u s s e l s w e r e b u r i e d i n m u d w i t h < */3 of s h e l l l e n g t h , m o s t of t h e m b e i n g c l u m p e d t o g e t h e r i n e p i b e n t h i c g a r l a n d s , o f t e n 2 to 3 m u s s e l l e n g t h s i n h e i g h t .

F a u n a o f m u s s e l b e d s w i t h / w i t h o u t f u c o i d c o v e r

A t t h e t w o i n v e s t i g a t e d sites, p a i r e d s a m p l e s f r o m p a t c h e s of m u s s e l b e d s c o v - e r e d w i t h d e n s e g r o w t h of P u c u s v e s i c u l o s u s a n d p a t c h e s f r e e of f u c o i d a l g a e r e v e a l e d s t r i k i n g d i f f e r e n c e s i n e p i f a u n a l s p e c i e s c o m p o s i t i o n ( T a b l e 2), w h e r e a s t h e r e w e r e n o

Table I. A b u n d a n c e and position of A4ytilus edulis (> i0 m m shell length) in patches with (n =

6 sites) and without (n = 6) Pucus vesiculosusin K6nigshafen, June 1991. T h e position is recorded as

the percentage of individuals in infaunal position (> 2/3 of shell length sunk into the mud), semi- epifauna] (2/3 to 1/3) and epifaunal (< I/3). Asterisks assign significance level after U-test

Mussels With Pucus Without Pucus Significance

(~ + SD) (~ + SD)

Ind./400 cm 2 49 -+ 16 122 • 24 "~ "

% infaunal 19 - 15 3 +- 7 '

% semi-epifaunal 68 ___ 19 17 • 21 * ~

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2 4 8 A. A l b r e c h t & K. R e i s e

0 m

m ,bl ~

~ -

0

0

t~

:0

:0

+I +l ~ +I

r

+] 0 ~ l - H

~N

p~ r

0

. : . . . . . . . : :

(,~ ~1 ~-~ ~1 0 ~ ~ "~ Ot ~ ~_'~ ~

+ 1 + 1 + 1 o +1 + 1 ~ + 1 + 1 + 1 o + 1 ~ + 1 + 1

+1 +1 +1 +~ +1 +1 +1 +~ +1 +1 o ~ +1 +1 +1

~

~--N ~ ,~ ~'~ .'~ .e.~l "~ ,.0 ~.~ ~..~1 u.~ ~lqD ~1 ~ ,..0

+1 +1 +1 o +1 +1 +1 +1 ~ +1 +[ +1 +1 +1 +1

~.,

~-~

~ ~

.~.~~

"~

+[ o o o o o + I § o § 2 4 7 2 4 7 +l + l o + l + l + l +l

~ ~ ~

+l

0

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Effects of Fucus o n m u s s e l s 2 4 9

"<'e-

r~ r

O'~-

tu

,-!

t~

:o

r~

-I-I +l q-I +l +l +1+1 + 1 4 - 1 o + l J r l + l + l §

Lr~ cqr" D'~ ~t~ 0"~ ~ oh-, ,.~~ r ~ o.~ ".~ ~0 ~ ~---~ o~ ~,.~ ..~ r +1 + 1 4 - 1 q - I + l q-lq-I -H o o + 1 o 4 - 1 q - l q - l q - l q - l o + l - t - I - H o - I - I

4-1+1-1-1 +1 +1

o

9 =~ ~ ~ ~ .~

~

~

-t-I-H q - l q - I + l - I - I o +1 + l o - H o o q - I J d - H o - H

+1 +1 o o o + 1 o + 1 o o + 1 o o + 1 + 1 o o +1

~ b.. o o ~t~ o ' ~ o o

~ ' ~

~ ' ~ .~

, ~ ~

~

~ O ~

d ~

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250 A. A l b r e c h t & K. Reise

c o n s p i c u o u s d i f f e r e n c e s w i t h r e s p e c t to i n f a u n a (Table3). Total s p e c i e s n u m b e r w a s always h i g h e r on b a r e m u s s e l beds. Polychaetes, in particular, w e r e less r e p r e s e n t e d on Fucus-covered b e d s w i t h r e g a r d to n u m b e r s of individuals. A b u n d a n c e s of s e v e r a l s p e c i e s (primarily epifauna) differed significantly in relation to a l g a l c o v e r (Fig. 2): m u s s e l s (Mytflus edulis), c o m m o n p e r i w i n k l e s (Littorina littorea), shore c r a b s (Carcinus maenas) a n d b a r n a c l e s (including Balanus crenatus, Elminius modestus a n d Semi- balanus balanoides) w e r e m o r e a b u n d a n t on u n c o v e r e d m u s s e l beds. For Carcinus maenas, this distribution w a s most p r o n o u n c e d in the O - g r o u p of crabs (< 1 c m c a r a p a c e width).

T h e isopod Jaera albifrons a n d the flat p e r i w i n k l e Littorina mariae a t t a i n e d h i g h e r densities on b e d s w i t h fucoid cover, the latter occurring e x c l u s i v e l y on plots w i t h fucoids present. D i f f e r e n c e s b e t w e e n c o v e r e d a n d u n c o v e r e d b e d s w e r e q u a l i t a t i v e l y t h e s a m e at both i n v e s t i g a t i o n sites, b u t w e r e r e f l e c t e d m o r e clearly in the O d d e w a t t , w h i c h h a d a h i g h e r n u m b e r of s p e c i e s as w e l l as individuals. At this e x p o s e d sRe, a g r e a t e r p e r c e n - t a g e of animals w a s f o u n d directly on the algae. T h e diversity i n d e x H w a s h i g h e r in the O d d e w a t t (1.86) t h a n in the M 6 w e n b e r g w a t t (1.45). W h e n c o m p a r i n g d i v e r s i t y a n d e v e n n e s s on m u s s e l b e d s w i t h (F) a n d w i t h o u t (O) F. vesiculosus, b o t h p a r a m e t e r s w e r e h i g h e r on c o v e r e d beds, r e g a r d l e s s of location (HF = 1.88; H o = 1.68 a n d eF = 0.56; e o = 0.48). T h e s a m e holds true if the s p e c i e s u s i n g the m a c r o a l g a e as h a b i t a t (mainly Littorina spp., Gammarus spp. a n d Jaera albifrons) are d i s r e g a r d e d in the calculation, in o r d e r to assess their i m p a c t on diversity m e a s u r e s . In that case HF = 1.41 as c o m p a r e d to H o = 1.34, a n d eF = 0.44 as c o m p a r e d to e o = 0.39.

i n d . m -2

*** Mytilus edulis

** Littorina littorea

*** Carcinus maenas

* Balanidae

*** Gammarus spp.

*** Jaera albifrons

III ... ~ ~ ~ . . . .

" i . . . . ~ ~ . . .

0 20 4 0 60 8 0

w i t h F u c u s ~ w i t h o u t F u c u s J

6 1 8 2

1 9 2 4

8 9 3

1 4 0 7

129

1151

151

I O 0 %

Fig. 2. Relative abundance of macro-epifauna, differing significantly on mussel beds with/without fucotd cover. Means and standard deviations (n = 24) and total numbers [individuals m -2] corre-

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Effects of F u c u s on m u s s e l s 251

DISCUSSION

All i n t e r t i d a l m u s s e l b e d s in K 6 n i g s h a f e n are at l e a s t p a r t l y c o v e r e d w i t h F u c u s vesiculosus. N o g r o w t h h a s b e e n r e p o r t e d on s u b t i d a l b e d s . In 1988, P a r u s e l (1990) e s t i m a t e d F. vesiculosus surface cover in the O d d e w a t t to b e 50 %. In 1990 a n d 1991 it w a s 60 a n d 95 % and, at the s e c o n d site, M 6 w e n b e r g w a t t , fucoid cover d e c l i n e d from 70 to 55 %. Thus, t h e r e is c o n s i d e r a b l e i n t e r a n n u a l a n d intersite variation, b u t f u c o i d s s e e m to h a v e b e e n p r e s e n t in t h e a r e a a l w a y s (see also N i e n b u r g , 1927; W o h l e n b e r g , 1937; K o r n m a n n , 1952; Reise, 1977; Reise et al., 1989). By t a k i n g s a m p l e s of b e n t h i c m a c r o - f a u n a s e l e c t i v e l y from p a r t l y a l g a e - c o v e r e d m u s s e l b e d s , w e c o u l d o p t i m i z e t h e i n f o r m a - tion g a i n in r e l a t i o n to s a m p h n g effort, w h i c h is p a r t i c u l a r l y t i m e - c o n s u m i n g i n m u s s e l beds. Also, it w a s p o s s i b l e to a s s e s s the effects of fucoid cover on m u s s e l b e d s at d i f f e r e n t levels b y c o m p a r i n g c o v e r e d a n d u n c o v e r e d plots (a) w i t h i n s i n g l e m u s s e l b e d s , (b) of m u s s e l b e d s at o n e l o c a t i o n a n d (c) of all m u s s e l b e d s i n d e p e n d e n t of l o c a t i o n . T h e following d i s c u s s i o n will focus on a l g a l - c o v e r effects o b s e r v e d at b o t h i n v e s t i g a t i o n sites, n e g l e c t i n g d i f f e r e n c e s in s p e c i e s c o m p o s i t i o n w h i c h are d u e to e x p o s u r e or t i d a l level.

A l g a l cover

O u r estimates of biomass refer to the above-ground thalli of P. vesiculosus. T h e r e is a

considerable a m o u n t of thalli buried in m u d . Judging from the dark colour a n d fragile

nature, most of these thalli s e e m to consist of d e a d tissue. However, on resampling

6 clipped plots 33, a n d again 41 days later, a daily regrowth of about 4 g dry weight m -2

w a s calculated. Thus, w h a t appears to be d e a d tissue s h o w e d a conspicuous potential for

growth. Accordingly, our biomass figures w e r e too low. At least part of the e m b e d d e d

thalli constitute v i a b l e biomass. With its h i g h b i o m a s s a n d g r o w t h p o t e n t i a l , F. ve- siculosus r e p r e s e n t s a n i m p o r t a n t factor on i n t e r t i d a l flats a p a r t from its s t r u c t u r a l effects: with a total m u s s e l b e d a r e a in K 6 n i g s h a f e n of 46 000 m 2 , a n d a n a v e r a g e F. vesiculosus cover of 70 %, t h e total d r y w e i g h t of this m a c r o a l g a in t h e b a y a m o u n t s to 34 000 k g or 19 000 k g a s h - f r e e d r y w e i g h t in summer.

M u s s e l a b u n d a n c e

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252 A. Albrecht & K. Reise

b y fucoids c o m p a r e d to e p i b e n t h i c clumps a n d g a r l a n d s i n the a b s e n c e of algae. We a s s u m e that mussels are suffocated b y m u d in the association with F. vesiculosus. This result is in fact the opposite of w h a t N i e n b u r g (1925, 1927) proposed, a n d constitutes a strong a r g u m e n t a g a i n s t his hypothesis of the F u c u s - M y t i l u s assocation r e p r e s e n t i n g a m u t u a l relationship.

Mussels are p r e y e d u p o n b y e i d e r d u c k s (Somateria mollissima) as well as other birds (oyster catchers, H a e m a t o p u s ostralegus, a n d h e r r i n g gulls, Larus argentatus), w h i c h m i g h t r e s p o n d n e g a t i v e l y to the p r e s e n c e of fucoids. K e t z e n b e r g (1990) o b s e r v e d f e e d i n g b e h a v i o u r of these ducks, a n d f o u n d no difference in f e e d i n g activity o n fucoid-covered a n d u n c o v e r e d beds. Also, Albrecht (1991) c o m p a r e d l e n g t h - f r e q u e n c y distributions of m u s s e l p o p u l a t i o n s on fucoid-covered mussel b e d s with those on u n c o v e r e d sites, b u t reported no differences. If m a c r o a l g a l cover significantly r e d u c e d p r e d a t i o n (by birds as well as crabs), o n e w o u l d expect differing size spectra of mussels, b e c a u s e normally p r e d a t i o n is selective for certain size groups. Thus, mussels do n o t s e e m to profit from r e d u c e d p r e d a t i o n u n d e r n e a t h fucoid cover.

S t r u c t u r a l i n f l u e n c e of a l g a l c o v e r

The algal cover m a y h a v e beneficial effects b y buffering h e a t stress, or as protection a g a i n s t desiccation d u r i n g s u m m e r low tides. However, i n the area of i n v e s t i g a t i o n this did not s e e m to b e effective. T h e r e d u c e d a b u n d a n c e of b a r n a c l e s is likely to b e a c o n s e q u e n c e of the decrease in b a r e m u s s e l surface area p r o j e c t i n g into the water, a n d thus of the latter's d e c r e a s e d availability as substratum. Apart from that, the F. ves- iculosus thalli w h i c h are m o v e d b a c k a n d forth b y w a v e action m a y interfere with larval s e t t l e m e n t a n d the d e v e l o p m e n t of barnacles, as has b e e n d e s c r i b e d for rocky shores (Menge, 1976).

Several species seek shelter from p r e d a t i o n u n d e r algal' cover or i n seagrass b e d s (Wilson et al., 1990). The s a m e was expected for 'crabs, Carcinus maenas, i n relation to fucoids, especially since the shore crab s p e n d s most of its j u v e n i l e lifetime in m u s s e l b e d s (Ropes, 1968; Eriksson & Edlund, 1977; Scherer & Reise, 1981). O n i n t e r t i d a l flats, m a i n l y birds (gulls a n d oyster catcher - Zwarts, 1983) a n d fish (e.g. flounder - J e n s e n & J e n s e n ,

1985) prey on crabs, a n d it s e e m s likely that C. m a e n a s w o u l d hide u n d e r the d e n s e cover of algae to e s c a p e them. However, our results r e v e a l the opposite, viz. the a b u n d a n c e of C. m a e n a s was h i g h e r on m u s s e l b e d s free of m a c r o a l g a e . This refers p a r t i c u l a r l y to small crabs, b e c a u s e j u v e n i l e s ~ 10 m m carapace w i d t h comprised a p p r o x i m a t e l y 65 % of the p o p u l a t i o n in our study. It has to b e m e n t i o n e d that s a m p l i n g at tow tide does not always reflect conditions at high tide. D u r i n g s u b m e r s i o n , fucoid thalli project into the w a t e r column, l e a v i n g a n accessible s e d i m e n t surface u n d e r n e a t h . O n m u s s e l b e d s without F. vesiculosus, w h e r e e p i b e n t h i c a l l y g r o w i n g m u s s e l s form a system of interstices b e t w e e n them, small crabs m i g h t in fact find b e t t e r h i d i n g places t h a n u n d e r a n algal v e g e t a t i o n w h e r e crevices a n d niches are mud-filled.

A b u n d a n c e of g r a z i n g h e r b i v o r e s

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Effects of F u c u s on m u s s e l s 253

p a r t l y f o u n d as e p i f a u n a directly on the a l g a l thalli. F e e d i n g on a d u l t fucoids b y h e r b i v o r e s w a s d e s c r i b e d for Littorina obtusata (van D o n g e n , 1956; Williams, 1990b), for the i s o p o d Idothea balUca (Haahtela, 1984) or - u n d e r c i r c u m s t a n c e s of t e m p o r a l s t a r v a t i o n - for Carcinus m a e n a s (Janke, 1990). H o w e v e r , f i l a m e n t o u s g r e e n s a r e g e n e r - ally p r e f e r r e d as food b y grazers, w h e n g i v e n the a l t e r n a t i v e to fucoids, b e c a u s e t h e l a t t e r s u c c e e d in d e t e r r i n g g r a z e r s b y m e c h a n i c a l as w e l l as c h e m i c a l d e f e n s e m e c h a n i s m s (Nicotri, 1980; W a t s o n & Norton, 1985; H a y & Fenical, 1988). H e r b i v o r e g r a z i n g on j u v e n i l e fucoids, w h i c h h a s b e e n d e s c r i b e d for r o c k y shores (Lubchenko, 1983; C h a p - man, 1990; J a n k e , 1990), finds no p a r a l l e l on i n t e r t i d a l s e d i m e n t s b e c a u s e t h e r e are no y o u n g fucoids present, as r e p r o d u c t i o n occurs solely v e g e t a t i v e l y . T h e F. vesiculosus thalli in K 6 n i g s h a f e n s h o w e d g r a z i n g m a r k s w h i c h h a v e b e e n o b s e r v e d to o r i g i n a t e from G a m m a r u s spp., b u t field- a n d l a b o r a t o r y e x p e r i m e n t s of Reise a n d A s m u s & A s m u s (unpubl.) also d e m o n s t r a t e d the p r e f e r e n c e of g a m m a r i d s for f i l a m e n t o u s g r e e n a l g a l species. H a a g e (1975), J a n s s o n & Wulff (1977), C a t t a n e o (1983) a n d Williams (1990b) all m e n t i o n the i m p o r t a n c e of e p i p h y t i c d i a t o m s on fucoids for s e v e r a l g r a z i n g h e r b i v o r e s . H o w e v e r , the q u e s t i o n as to w h a t e x t e n t fucoids, on t h e one h a n d , a n d e p i p h y t i c micro- a n d m a c r o a l g a e , on t h e other, c o n t r i b u t e to the diet of t h e a b u n d a n t g r a z i n g s p e c i e s is as yet u n a n s w e r e d a n d h a s to r e m a i n t h e s u b j e c t of further i n v e s t i g a t i o n s .

H i g h e r p e r c e n t a g e s of g r a z i n g o r g a n i s m s f o u n d directly on t h e a l g a e at our e x p o s e d study site m i g h t i n d i c a t e the a d d i t i o n a l utilization of the thalli as h a b i t a t a n d for p r o t e c t i o n a g a i n s t m e c h a n i c a l stress, w h i c h b e c o m e s m o r e p r o n o u n c e d t h e m o r e e x p o s e d the location. Nicotri (1980) d e s c r i b e s such v a r y i n g s i g n i f i c a n c e s of h o s t a l g a e as h a b i t a t a n d food source for e p i f a u n a l grazers. Also, r e d u c e d p r e d a t i o n p r e s s u r e of fish a n d s h r i m p on a m p h i p o d s a s s o c i a t e d w i t h m a c r o a l g a e w a s d o c u m e n t e d b y N e l s o n (1979) a n d S t o n e r (1979, 1980).

For Littorina mariae, the a s s o c i a t i o n w i t h fucoids is i m p e r a t i v e (Williams, 1990a; this study). Williams d e s c r i b e s not only s p a t i a l b u t also t e m p o r a l l i n k a g e of L. mariae to its host a l g a e , in that the life history of the p e r i w i n k l e is s y n c h r o n i z e d with that of t h e a l g a e . H e also m e n t i o n s a p a r t i c u l a r b o n d of L. m a r i a e to fucoids, b e c a u s e the snail d e p o s i t s its e g g m a s s e s on the a l g a l thalli (in contrast to the c o m m o n p e r i w i n k l e , w h i c h d e p o s i t s its e g g s into the water). This w a s also o b s e r v e d in our study. T h e fact that Littorina fittorea r e a c h e d h i g h e r d e n s i t i e s on m u s s e l b e d s free of F. vesiculosus is surprising, w h e n t a k i n g into a c c o u n t that food a n d fe~ding m e c h a n i s m s are similar to Littorina mariae - in t h a t d i a t o m s as well as e p h e m e r a l or j u v e n i l e m a c r o a l g a e are p r e f e r r e d foods ( L u b c h e n k o , 1978, 1983; Lein, 1980; E n r i g h t et al., 1983; Petraitis, 1983; W a t s o n & Norton, t985; Imrie et al., 1990). H o w e v e r , the c o m m o n p e r i w i n k l e is k n o w n to g r a z e on a b r o a d r a n g e of surfaces, a n d in K 6 n i g s h a f e n it p r e f e r a b l y a s s o c i a t e s w i t h solid s u b s t r a t a ( W i l h e l m s e n & Reise, 1994). B e c a u s e L. littorea is l a r g e r a n d its shell projects m o r e from the s u r f a c e t h a n that of L. mariae, its p r e s e n c e on the a l g a l thalli s w a y i n g w i t h the w a v e s a n d currents m i g h t b e m o r e difficult to m a i n t a i n . F u r t h e r m o r e , the s h a d i n g effects of fucoids m a y limit the g r o w t h of u n d e r s t o r e y a l g a e (juvenile m a c r o a l g a e a n d diatoms) and, thus, also t h e food s u p p l y for p e r i w i n k l e s on c o v e r e d m u s s e l b e d s ( C h a p m a n , 1990; Parusel, 1990).

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254 A. A l b r e c h t & K. R e i s e

e n h a n c e s e d i m e n t a t i o n w h i c h l e a d s t o s u f f o c a t i o n of p a r t of t h e m u s s e l p o p u l a t i o n , c a u s i n g t h e r e m a i n i n g i n d i v i d u a l s to g r o w m o s t l y e n d o b e n t h i c a l l y . T h e r e f o r e , t h e s u b - s t r a t u m a r e a f o r e p i b i o n t s , f o r i n s t a n c e b a r n a c l e s , is r e d u c e d , a n d so is t h e i n t e r s t i t i a l s p a c e b e t w e e n m u s s e l s t h a t is u s e d b y o t h e r c o m m u n i t y m e m b e r s a s m i c r o h a b i t a t . S e c o n d l y , f u c o i d c o v e r s e r v e s - d i r e c t l y o r i n d i r e c t l y - a s f o o d for h e r b i v o r e s . W h i l e d i r e c t c o n s u m p t i o n of P. v e s i c u l o s u s a p p e a r s to b e l e s s i m p o r t a n t , e p i p h y t i c g r o w t h of d i a t o m s a n d f i l a m e n t o u s g r e e n a l g a e o n l =. v e s i c u l o s u s - t h a l l i p r o v i d e s f o o d f o r s e v e r a l g r a z i n g s p e c i e s .

T h e m a c r o a l g a l c o v e r of m u s s e l b e d s w i t h P. v e s i c u l o s u s p a r t l y i n c r e a s e s h a b i t a t c o m p l e x i t y t h r o u g h a d d i t i o n of a c a n o p y s t r u c t u r e , b u t , a t t h e s a m e t i m e , r e d u c e s u n d e r s t o r e y h a b i t a t c o m p l e x i t y b y e l i m i n a t i o n of l i v i n g s p a c e c a u s e d b y s e d i m e n t a c c u m u l a t i o n .

M a c r o b e n t h i c e n d o f a u n a is little i n f l u e n c e d b y f u c o i d c o v e r o n m u s s e l b e d s , b u t o v e r a l l m a c r o b e n t h i c d i v e r s i t y is i n c r e a s e d .

A c k n o w l e d g e m e n t s . We thank Dirk Schories who, during the s u m m e r of 1990, h e l p e d to collect the samples, a n d Elisabeth Herre w h o assisted with calculations a n d drawings during data analysis. The study was supported b y the Federal Environmental Agency, the Environmental Natural Research Plan of the Minister for the Environment, Nature Conservation and Nuclear Safety of the Federal Republic of G e r m a n y (grant 10 802 085/01) and the State of Schleswig-Holstein. This is publication no. 128 of the project "Ecosystem Research W a d d e n Sea".

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Austen, I., 1992. Geologisch-sedimentologische Kartierung des K6nigshafens (List/Sylt). - M e y n i a n a

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exp. mar. Biol. Ecol. 118, 207-216.

Dankers, N. & Koelemaij, K., 1989. Variations in the mussel population of the Dutch W a d d e n Sea in relation to monitoring of other ecological parameters. - Helgolhnder M e e r e s u n t e r s . 43, 529-535. Dean, R. L. & Connell, J. H., 1987. Marine invertebrates in an algal succession. IIL M e c h a n i s m s

linking habitat complexity with diversity. - J. exp. mar. Biol. Ecol. I09, 249-273.

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Enright, C., Krailo, D., Staples, L,, Smith, M., V a u g h a n , C., Wardl D., Gaul, P. & Borgese, E., 1983. Biological control of fouling algae in oyster aquaculture. - J. Shellfish Res. 3, 41-44.

Eriksson, S. & Edlund, A., 1977. On t h e ecological energetics of O-group Carcinus rnaenas (L.) from a shallow s a n d y bottom in Gullmar Fjord, Sweden. - J. exp. mar. Bio], EcoL 30, 233-248. Haage, P., 1975. Quantitative investigations of the Baltic Fucus belt macrofauna. 2. Quantitative

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E f f e c t s of F u c u s o n m u s s e l s 255

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Figure

Table I. Abundance and position of A4ytilus edulis (> i0 mm shell length) in patches with (n = 6 sites) and without (n = 6) Pucus vesiculosusin K6nigshafen, June 1991
Fig. 2. Relative abundance of macro-epifauna, differing significantly on mussel beds with/without fucotd cover

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