sheltered sandy bay near the island of Sylt in the North Sea. Mean biomass in ... On experimental mussel beds, fucoid cover enhanced mud accumulation and ...
HELGOL,~NDER MEERESUNTERSUCHUNGEN Helgol~inder Meeresunters. 48, 243-256 (1994)
Effects of Fucus 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 in t h e W a d d e n S e a A. Albrecht & K. Reise Biologische Anstalt Helgoland, Wattenmeerstation Silt; D-25992 List, Federal Republic of 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 enhanced 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.
INTRODUCTION 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 drifting 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 elite s t r u c t u r e s in t e r m s of the 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 (Dittmann, 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 birds ( S w e n n e n et al., 1989; Zwarts, 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). T h e p h e n o m e n o n of Fucus vesiculosus g r o w i n g o n intertidal m u s s e l b e d s w a s first d e s c r i b e d by N i e n b u r g (1925, 1927) for t h e K 6 n i g s h a f e n Bay of Sylt. S i n c e then, t h e coo c c u r r e n c e of F. vesiculosus a n d m u s s e l a g g r e g a t i o n s (large b e d s or d r i f t i n g clusters) o n soft s e d i m e n t s has b e e n r e p o r t e d b y s e v e r a l a u t h o r s from d i f f e r e n t l o c a t i o n s a l o n g t h e N o r t h S e a coast ( W o h l e n b e r g , 1937; N i e n h u i s , 1970; v a n d e n H o e k et al., 1979). In this association, F. vesiculosus lacks a h o l d f a s t a n d g a s vesicles, a n d is a t t a c h e d to t h e s u b s t r a t u m by b y s s u s t h r e a d s of t h e m u s s e l s . R e p r o d u c t i o n is v e g e t a t i v e b y m e a n s of f r a c t i o n e d thalli. D u e to m u d a c c u m u l a t i o n in t h e m u s s e l b e d , t h e a l g a e a r e g r a d u a l l y 9 Biologische Anstalt Helgoland, Hamburg
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 column. Nienb u r g (1925, 1927) d e s c r i b e d the reciprocal effect of mussels a n d fucoids on e a c h other as beneficial for both parties. H e b e l i e v e d that F. vesicutosus p r e v e n t e d the m u s s e l s from sinking into the mud, w h e r e a s mussels 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 with their byssus threads. In the p r e s e n t study, investigations a b o u t the possible effects of fucoid cover on mussels are 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 an additional p h y s i c a l a n d biological structure in the mussel b e d community. This structure could function as food for herbivores a n d a h a b i t a t for e p i f a u n a (Nicotri, 1980), as substrate for e p i p h y t e s (Kangas et al., 1982) or as shelter against 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 complexity. Results w e r e o b t a i n e d b y parallel s a m p l i n g of covered a n d u n c o v e r e d b e d s in the tidal zone of K6nigshafen n e a r Sylt. The hypothesis that p a t c h e s of F. vesiculosus significantly alter siltation a n d the composition of the species a s s e m b l a g e , w a s t e s t e d experimentally. MATERIAL A N D METHODS Study site Investigations w e r e carried out in " K 6 n i g s h a f e n ' , the s a m e shallow tidal b a y n e a r the island of Sylt, North 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. The distribution a n d size of m u s s e l b e d s in the a r e a have b e e n subject to g r e a t variation since the early reports from the b e g i n n i n g of the century. S u c h fluctuations were c a u s e d by severe winters (Ziegelmeier, 1964, 1970) a n d p r e s u m a b l y eutrophication (Reise et al., 1989). Two locations in the b a y which 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 the 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 an e x p o s e d site with mussel b e d s e x t e n d i n g along 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 part of K6nigshafen a n d is thus more sheltered, with m u s s e l b e d s b e i n g situated slightly further upshore. Both locations are sandy, but the 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 portion of coarse (0.36-0.6 ram) a n d a lower p o r t i o n of fine {0.09-0.15 ram) s e d i m e n t (Austen, 1992). Algal biomass 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 growth (100 % surface cover; visual 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 replicate 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 with seawater, blotted a n d w e i g h e d (fresh weight), a n d then d r i e d for three 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 organic content as ash-free dry weight. Siltation experiment A field e x p e r i m e n t was d e s i g n e d to test w h e t h e r Fucus vesiculosus cover e n h a n c e s m u d accumulation on m u s s e l beds, a n d w h e t h e r this affects m u s s e l density. From m u s s e l
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 - clumps of mussels with a n d without attached algae were removed with a shovel. T h e y were a r r a n g e d in beds of approximately lm 2, four with a n d three without algae, at a distance of a b o u t 2 m from each other a n d situated in the direct vicinity of the natural beds. C l u m p s of mussels 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, subsequently, served as a reference to m e a s u r e the height 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 by p r o b i n g a ruler 10 times into the m u d of the central area (0.3 m 2) of each mussel bed. The initial density of mussels (> 10 m m shell length) was arranged into 200 individuals on 1000 c m 2 with a n approximate error of - 50. Mussel spat was not considered 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. The vertical position of mussels in 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), semi-epifaunal (2/3 to '/3) or epifaunal (< '/3 of shell buried in mud). The experiment was started on July 3rd 1991 a n d t e r m i n a t e d on July 18th 1992. Throughout 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 designed to be free of fucoids. After July 1992, the e x p e r i m e n t a l beds were left u n a t t e n d e d . In N o v e m b e r 1992, these beds were completely covered by 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 samples each were t a k e n from mussel 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 during J u n e to August 1990. Sampling procedure was selective, in that samples were t a k e n in pairs of two from directly adjacent areas of the same mussel 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 differentiating the two plots. A box corer of 500 cm 2 surface area was used to take samples d o w n to a d e p t h of 15 cm, below which no living m a c r o f a u n a occurred. If present, algae were cut off the surface and treated separately: a n y a d h e r i n g epifauna was w a s h e d off a n d r e t a i n e d in a sieve (500 ~m m e s h size) to be identified a n d counted. The s e d i m e n t portion of the sample was w a s h e d a n d sieved (500 ~m) a n d the residues from the sieve transferred into sorting dishes from which animals were extracted alive. All taxa, except oligochaetes and gammarids, were identified to species level u s i n g a stereo microscope. H e a v y recruitm e n t of Carcinus m a e n a s a n d N e r e i s diversicolor occurred d u r i n g the s a m p l i n g period; therefore these species were roughly grouped 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 nonparametric U-test of Wilcoxon, Mann & Whitney (Sachs, 1984). Differences were considered 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. Usually, abundances are given as means (~) and standard deviations (SD). For comparison of macrofaunal assemblages, two indices were calculated: (a) Shannon-
246
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W i e n e r - I n d e x H = - X Pi * In Pi, with Pi b e i n g the portion of a species' (ni) n u m b e r of individuals b a s e d on the total n u m b e r of individuals (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 Algal cover Patches within mussel b e d s c o v e r e d entirely by Fucus vesiculosus h a d a biomass 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 beds in 1990 was estimated at 60 % in O d d e w a t t an d 70 % in M 6 w e n b e r g w a t t . T h e following year in June, surface c o v e r in the m u s s e l b e d areas r e a c h e d 95 and 55 %, respectively. With 70 % cover as an overall mean, fucoid biomass on m u s s e l b e d s in KSnigshafen was a p p r o x i m a t e l y 400 g ash-free dry w e i g h t m -2 in s u m m e r .
Siltation experiment Within 5 days after setting-up the e x p e r i m e n t a l mussel beds, the distribution of mussels h ad 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 . During this time, w e a t h e r conditions h ad b e e n constantly calm. In the 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. Thick diatom growth was visible on the m u d surface in the interspaces. In the p r e s e n c e of fucoids, mussels formed a continuous m o n o l a y e r , w i t h most individuals buried in m u d by about two-thirds of their shell length. W h e n p r o b i n g the m u d d ep t h after 4 w e e k s in August, a smell of h y d r o g e n sulfide was apparent. In the course of the e x p e r i m e n t all mussel beds b e c a m e larger. Initially, the m e a n size was 1.1 m 2. Six months later the m e a n size w as 1.6 m 2, with no s i g n i f i c a n t difference b e t w e e n treatments. H o w e v e r , m u s s e l beds without fucoid cover h ad t w i c e the m u s s e l density of beds with algae. M e a n density of mussels was 119 --- 12 an d 61 ___ 21, respectively, (July, 1992) on 1000 cm 2 in the centre of beds: Taking the a r e a l i n c r e a s e of each mussel b e d into account, m u s s e l n u m b e r s had d e c r e a s e d by t h e e n d of the e x p e r i m e n t (after 1 year) by 15 ___ 10% without fucoid cover and by 54 _+ 18 % with fucoid cover. This difference was significant at the 5 % - l e v e l (U-test). E x p e r i m e n t a l mussel beds c o v e r e d by Fucus vesiculosus a c c u m u l a t e d more sedim e n t than the bare b e d s (Fig. 1). Initially, the h e i g h t of m u d was 95 ___ 6 ram. With algal cover, s e d i m e n t h e i g h t in 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 July 1992. Intermittently, the net gain of s e d i m e n t at o n e b e d was 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 and further to 22 _+ 23 m m in July 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 In the experiment, it was a l r e a d y o b s e r v e d that mussels u n d e r n e a t h fucoid co v er w e r e positioned primarily in the mud, w h i le in the a b s e n c e of Fucus vesiculosus most mussels w e r e positioned in clumps a b o v e the m u d surface. Th e r e l a t i v e position of mussels to the s e d i m e n t surface w a s r e c o r d e d in replicate samples t a k e n from m u s s e l
Effects of F u c u s o n m u s s e l s 150
247
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Fig. 1. Height of m u d surface in experimental mussel beds, 4 beds with and 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 each are plotted per site and date (average standard demation 9.5 ram). Initial h e i g h t varied b e t w e e n 84 and 105 mm and was standardized to the m e a n of 95 mm 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 cover, 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 40 % 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 . In 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 .
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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 cove 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. Abundance 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. The position is recorded as the percentage of individuals in infaunal position (> 2/3 of shell length sunk into the mud), semiepifauna] (2/3 to 1/3) and epifaunal (< I/3). Asterisks assign significance level after U-test Mussels
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Without Pucus (~ + SD) 122 3 17 81
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