H E L G O I ~ N D E R MEERESUNTERSUCHUNGEN Helgol~nder Meeresunters. 37, 185-199 (1984)

I m p a c t of t r e m a t o d e p a r a s i t i s m o n t h e f a u n a of a N o r t h S e a t i d a l flat G. L a u c k n e r Biologische A n s t a l t H e l g o l a n d (Litoralstation]; D-2282 List/Sylt, Federal R e p u b l i c of G e r m a n y

ABSTRACT: The impact of larval trematodes on the fauna of a North Sea tidal flat is considered at the individual and at the population level, depicting the d i g e n e a n parasites of the common periwinkle, Littorina littorea, and their life cycles, as an example. On the G e r m a n North Sea coast, L. fittorea is first intermediate host for 6 larval trematodes r e p r e s e n t i n g 6 d i g e n e a n families Cryptocotyle lingua (Heterophyidae), Himasthla elongata (Echinostomatidae), Renicola roscovita (Renicolidae), Microphallus pygmaeus (Microphallidae), Podocotyle atomon (Opecoelidae} and Cercaria lebouri (Notocotylidae). All except P. atomon utilize shore birds as final hosts; adult P. atomon parasitize in the intestine of teleosts, mainly pleuronectid flatfish. Second intermediate hosts of C. lingua are various species of fish; the cercariae of H. elongata encyst in molluscs a n d polychaetes, those of R. roscovita in molluscs; Iv[.pygmaeus has an a b b r e v i a t e d life cycle; C. lebouri encysts free on solid surfaces; and the fish trematode P. atomon utilizes b e n t h i c crustaceans, mainly amphipods, as second intermediate hosts. On the tidal flats of the K6nigshafen (Sylt), up to 77 % of the periwinkles have b e e n found to be infested by larval trematodes. M a x i m u m infestations in individual samples w e r e 23 % for C. lingua, 47 % for H. etongata and 44 To for R. roscovita. The digeneans cause complete 'parasitic castration' of their carriers and h e n c e exclude a considerable proportion of the snails from the b r e e d i n g population. Infestation reduces the longevity of affected hosts, and size-related, t r e m a t o d e - i n d u c e d differential mortality causes c h a n g e s in the normal sizefrequency distribution of individual snail-age classes. Young flatfish Pleuronectesplatessa from the K6nigshafen are 100 % infested with metacercariae of C. lingua. Heavy infestation of the gills causes obstruction of blood vessels and respiratory impairment; metacercariae in the eyes and optic nerves cause visual and neurological disturbances. A single metacercaria is sufficient to kill a larval fish. MyO'lus edulis and Cardium (Cerastoderma) edule are 100 % infested with metacercariae of H. elongata. Heavy infestation impairs the byssus-thread production in mussels and affects the burrowing ability of cockles. Longevity and resistance to environmental - particularly thermal stress are reduced in bivalves infested with H. elongata and R. roscovita. There is e v i d e n c e that, in the study area, population size and age composition of the molluscs discussed are (indirectly} controlled by trematode parasites employing sea birds as final hosts, rather than directly by the predatory activities of these birds. INTRODUCTION T h e t r o p h i c d y n a m i c s of e c o s y s t e m s a r e u s u a l l y c o n s i d e r e d m a i n l y i n t e r m s of p r e d a t o r - p r e y r e l a t i o n s h i p s . A n o t h e r n o l e s s i m p o r t a n t c a t e g o r y of i n t e r r e l a t i o n s h i p s , t h a t of h o s t s a n d t h e i r p a r a s i t e s , h a s b e e n n e g l e c t e d i n m o s t of t h e p e r t i n e n t e c o s y s t e m analyses. T h e p u r p o s e of t h i s s t u d y is t o p r e s e n t e v i d e n c e of t h e i m p a c t of l a r v a l t r e m a t o d e s o n s e v e r a l m e m b e r s of t h e a n i m a l c o m m u n i t y of a N o r t h S e a t i d a l flat, d e p i c t i n g t h e c o m m o n p e r i w i n k l e , Littorina fittorea, a n d its d i g e n e a n p a r a s i t e s a s a n e x a m p l e . © Biologische Anstalt Helgoland, H a m b u r g

186

G. L a u c k n e r THE I N V E S T I G A T I O N A R E A

T h e K 6 n i g s h a f e n (Fig. 1) is a s h a l l o w l e e s i d e b a y s i t u a t e d at the n o r t h e r n tip of the Isle of Sylt (55°3'N 8°25'E). At low tide, l a r g e areas of sand and m u d flats, as w e l l as m u s s e l beds, are u n c o v e r e d . D u r i n g this t i m e the flats are f r e q u e n t e d by sea birds that

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Fig. 1. The 'K6nigshafen' at List, North Sea, Isle of Sylt (Federal Republic of Germany), showing Stations 1 and 2 f e e d on the bottom i n v e r t e b r a t e s . T h e islet of Uth6rn is a w i l d l i f e p r e s e r v e p r o v i d i n g roosting and b r e e d i n g p l a c e s for a s p e c i e s - r i c h avifauna. M a j o r e p i f a u n a l e l e m e n t s of the fiats are - in terms of b i o m a s s - the b l u e mussel, M y t i l u s edulis, the c o m m o n cockle, Cardium (Cerastoderma} edule, and the p e r i w i n k l e , Littorina littorea, T h e e c o l o g y of the K 6 n i g s h a f e n has b e e n s t u d i e d b y W o h l e n b e r g (1937). H o w e v e r , e x c e p t for a f e w brief notes (Lauckner, in B i o l o g i s c h e Anstalt H e l g o l a n d , J a h r e s b e r i c h t 1974, 1978) a n d two m o r e g e n e r a l p u b l i c a t i o n s r e f e r r i n g only in part to m a t e r i a l from that area (Werding, 1969; L a u c k n e r 1971), t h e r e h a v e b e e n no studies on the parasitofauna of the K6nigshafen.

MATERIALS AND METHODS P e r i w i n k l e s and m o l l u s c a n s e c o n d i n t e r m e d i a t e hosts - m a i n l y M y t i l u s edulis and Cardium (Cerastoderma) e d u l e - w e r e h a n d - c o l l e c t e d at low tide. J u v e n i l e flatfish w e r e

Impact of t r e m a t o d e p a r a s i t i s m on tidal-flat f a u n a

187

d i p - n e t t e d d u r i n g e b b tide. T h e c o l l e c t e d i n v e r t e b r a t e s w e r e t r a n s f e r r e d to t h e l a b o r a tory a n d m a i n t a i n e d in aerated, d a i l y c h a n g e d sea w a t e r until e x a m i n a t i o n . P e r i w i n k l e s w e r e a l l o w e d to d e f e c a t e for at l e a s t 24 h in o r d e r to facilitate r e c o g n i t i o n of r e c e n t l y established, i m m a t u r e d i g e n e a n infestations. By m e a n s of a c a l i p e r rule, the s p i n d l e h e i g h t of Littorina l i t t o r e a w a s m e a s u r e d to the n e a r e s t 1/10 mm, a n d i n d i v i d u a l s w e r e s u b s e q u e n t l y g r o u p e d in 1.0 m m size intervals. T h e r e s u l t i n g multi~modal s i z e - f r e q u e n c y distributions (which r e p r e s e n t o v e r l a p p i n g y e a r classes) w e r e d i s s e c t e d into t h e i r n o r m a l c o m p o n e n t s by m e a n s of a c o m p u t e r p r o g r a m b a s e d on the m e t h o d o u t l i n e d by A k a m i n e (1982). Bivalves u s e d in the i n f e s t a t i o n a n d s u r v i v a l e x p e r i m e n t s w e r e c o l l e c t e d from tidal flats outside the K5nigshafen, i.e. from sites w i t h l o w o v e r a l l t r e m a t o d e p r e v a l e n c e . All i n d i v i d u a l s w e r e a c c l i m a t e d to l a b o r a t o r y c o n d i t i o n s (20 °C, 30Too S, 1 6 : 8 h d a y / n i g h t rhythm) for at least 5 days prior to the e x p e r i m e n t s . C r y p t o c o t y l e l i n g u a infestation in j u v e n i l e P l e u r o n e c t e s p l a t e s s a has b e e n s t u d i e d more t h o r o u g h l y in the author's laboratory by K e l l e - E m d e n (1979). T h e m e t h o d s d e s c r i b e d in detail in that p a p e r h a v e b e e n a d o p t e d in the p r e s e n t i n v e s t i g a t i o n .

RESULTS Six s p e c i e s of larval t r e m a t o d e s r e p r e s e n t i n g 6 d i g e n e a n f a m i l i e s h a v e b e e n reported from North S e a p e r i w i n k l e s (Werding, 1969), a n d all of t h e s e occur in L i t t o r i n a littorea from the KSnigshafen. T h e i r life cycles are s u m m a r i z e d in F i g u r e 2. All e x c e p t P o d o c o t y l e a t o m o n utilize sea birds as definite hosts. T h e first t h r e e s p e c i e s are of Life cycles of Littor~na parasites Cryptocotyle lingua (Heterophyidae): L. littorea .~ Fishes .~ Sea birds Himasthla elongata (Echinostomatidae}: L. 11ttorea

Molluscs ~ Annelids

Renicola roscovita (Renicolidae): L. littorea .~ Molluscs

~ Sea birds • Sea birds

Microphallus pygrnaeus (Microphallidae}: L. littorea • (L. littorea) .~ Sea birds Cercaria lebouri (Notocotylidae): L. Httorea

• Sea birds

Podocotyle atornon {Opecoelidae}: L. fittorea .~ Amphipods

.~ Fishes

Fig. 2. Life cycles of digenetic trematodes utilizing Littorina littorea as first intermediate host c o n s i d e r a b l e c o n c e r n b e c a u s e t h e y e m p l o y c o m m e r c i a l l y i m p o r t a n t v e r t e b r a t e s or i n v e r t e b r a t e s as s e c o n d i n t e r m e d i a t e hosts. T h e other three, w h i c h occur in l o w p r e v a lence, will not b e c o n s i d e r e d in detail. In the K6nigshafen, t r e m a t o d e i n f e s t a t i o n of p e r i w i n k l e s m a y r e a c h e n o r m o u s levels. At most stations s a m p l e d , o v e r a l l i n f e s t a t i o n p e r c e n t a g e s in a d u l t L. f i t t o r e a w e r e

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well above 50 %, with a m a x i m u m of 77 % o b s e r v e d in a s n a i l s a m p l e (Fig. 3) t a k e n from a m u s s e l b a n k n e a r the e n t r a n c e of the bay, a favourite roosting a n d f e e d i n g p l a c e of gulls Larus spp., oystercatchers H a e m a t o p u $ ostralegus a n d Eider d u c k s Somateria mollissima. M a x i m u m infestation i n c i d e n c e s recorded for i n d i v i d u a l p a r a s i t e species i n Littorina s a m p l e s from the area were 23 % for Cryptocotyle lingua, 44 % for Renicola roscovita a n d 47 % for H i m a s t h l a elongata. A more d e t a i l e d a n a l y s i s of the d y n a m i c s of trematode infestation in littorines from the K 6 n i g s h a f e n will b e g i v e n e l s e w h e r e (Lauckher, in preparation). Most of the infestations e n c o u n t e r e d were m a t u r e a n d the r e s u l t a n t host p a t h o l o g y severe. G o n a d atrophy ('parasitic castration') was a p p a r e n t i n almost all infested hosts, as was p e n i s r e d u c t i o n in males. The larval d i g e n e a n s differ with respect to their p a t h o g e n i c i t y in the first i n t e r m e d i a t e host (for r e v i e w of literature see Lauckner, 1980). Since each species exhibits a distinct p r e f e r e n c e for certain host-size classes (Fig. 3), the resultant p a r a s i t e - p r o d u c e d differential mortality of infested hosts causes s i g n i f i c a n t distortions of the original s i z e - f r e q u e n c y d i s t r i b u t i o n of the L. fittorea p o p u l a t i o n . In extreme cases (Fig. 4), grotesque m u l t i m o d a l d i s t r i b u t i o n patterns arise, w h i c h c a n n o t b e resolved into i n d i v i d u a l n o r m a l c o m p o n e n t s r e p r e s e n t i n g successive year classes. Simi20-

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lafly, no r e p r o d u c i b l e v o n Bertalanffy growth p a r a m e t e r s c a n b e c o m p u t e d for such affected p e r i w i n k l e populations. As a c o n s e q u e n c e of these erratic deviations, no mortality estimates c a n b e m a d e from analyses of the c h a n g e s of the p e r i w i n k l e s ' s i z e - f r e q u e n c y distribution. However, s i m u l t a n e o u s collection of l i v i n g snails a n d d e a d shells form the same locality provides a rough idea of the a m o u n t of differential mortality (Fig. 5a). The s a m p l e contains n 1 = 147 living L. Httorea a n d n2 -- 167 d e a d shells. C o m b i n a t i o n of both groups yields a sizefrequency curve (Fig. 5b), w h i c h c a n b e resolved into 3 n o r m a l c o m p o n e n t s . Hence, the combined curves reflect, with a h i g h d e g r e e of probability, the c o n d i t i o n that h a d existed prior to the onset of mortality. From the n u m b e r of (dead plus living) p e r i w i n k l e s i n the whole sample m i n u s the n u m b e r of d e a d shells, the mortality - w h i c h is b e l i e v e d to b e

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Host-shell height (mm) Fig. 5. Littorina littorea. (a) Size-frequency distributions of living individuals and dead shells. (b) Both distributions combined, Sample taken from Ho Bugt, Esbjerg, Denmark primarily related to trematode parasitism - can be estimated. In the present case (a sample taken from Ho Bugt, Esbjerg, Denmark} it is in excess of 50 %. Concomitantly with the high prevalence of trematodes in L. littorea, infestations of second intermediate hosts with metacercariae may reach epizootic levels. Young flatfish collected in the tide pools and channels of the KSnigshafen were found to be 100 % infested with C. lingua in varying degrees of intensity. Up to 109 metacercariae of this digenean have been counted in plaice approximately 4 cm in length (Kelle-Emden, 1979). The site of the parasite within the fish body, rather than the absolute number of cysts per host, appears to determine the fate of the suscept, encystment in the gill tissue causing obstruction of blood vessels and respiratory impairment, and penetration of the eyes, optic nerves or other parts of the brain leading to visual or neural disturbances. A single metacercaria of C. lingua is sufficient to kill a larval fish (Fig. 6). H. elongata typically occurs in highest infestation rates in L. littorea from sheltered, shallow bays. It may be recalled that, in some parts of the K6nigshafen, up to 47 % of the periwinkle population are infested with the rediae of this species, which utilizes bivalves and, to a lesser extent, annelids and gastropods as second intermediate hosts. In

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Fig. 6. Herring (Clupea harengus) larva killed by encysting Cryptocotyle lingua metacercaria (arrow) molluscs, the cercariae almost i n v a r i a b l y encyst i n the foot m u s c u l a t u r e . In the Kbnigshafen, Mytilus edulis a n d Cardium edule, the m a i n s e c o n d a r y host species, are 100 % infested with H. elongate metacercariae. F r e q u e n t l y , the foot of these b i v a l v e s is so riddled with cysts that its vital functions are s e v e r e l y i m p a i r e d (Fig. 7). Experiments were c o n d u c t e d to d e t e r m i n e the effect of H. elongate on b y s s u s - t h r e a d production in y o u n g M. edulis. U n i n f e s t e d m u s s e l s p r o d u c e d 31 + 17 threads w i t h i n 22.5 h a n d 62 + 26 threads w i t h i n 77.5 h. W i t h i n the same time intervals, i n d i v i d u a l s infested with 1 1 6 + 6 6 cysts p r o d u c e d only 22 a n d 40 threads, respectively. T h e differences are statistically h i g h l y significant (Lauckner, 1983). Cardium (Cerastoderma) edule is similarly affected b y H. elongate. The cockle normally lives entirely b u r r o w e d i n the sediment, only the siphon o p e n i n g s b e i n g v i s i b l e at the substrate surface. In the K6nigshafen, n u m e r o u s cockles c a n b e s e e n w h i c h are partially or totally uncovered. M a n y have b e e n s p u n t o g e t h e r i n b u n d l e s b y the byssus threads of mussels. I n s p e c t i o n of such cockles almost i n v a r i a b l y reveals the p r e s e n c e of large n u m b e r s of metacercarial cysts i n the foot m u s c u l a t u r e . W h e n placed on s a n d y substratum, j u v e n i l e cockles e x p e r i m e n t a l l y i n f e s t e d with H. elongate metacercariae r e m a i n e d at the s e d i m e n t surface for c o n s i d e r a b l e time, w h i l e u n i n f e s t e d controls b u r r o w e d rapidly. T h e m e d i a n time ( ----m e a n of log time) after w h i c h 50 % of the h e a l t h y cockles were e n t i r e l y b u r r o w e d was 12.5 min, as opposed to a b o u t 290 m i n r e q u i r e d by the infested specimens. In order to d e t e r m i n e w h e t h e r the effect exerted by the m e t a c e r c a r i a e is m e c h a n i c a l or physiological, or both, a n o t h e r group of cockles was e x p e r i m e n t a l l y infested with cercariae of Renicola roscovita, w h i c h i n v a d e the palps rather t h a n the foot. There was no d e v i a t i o n in the m e d i a n b u r r o w i n g time of this group from that of the u n i n f e s t e d control. Therefore, the effect of H. elongate metacercariae on the b u r r o w i n g ability of cockles was i n t e r p r e t e d as b e i n g p u r e l y mechanical.

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Fig. 7. Cardium edule. (a) Foot of juvenile individual (15.2 m m shell length) with extremely heavy natural t-timasthla elongata infestation showing distribution of 195 cysts; (b) e n l a r g e d portion of (a). Metacercariae, so d e n s e l y p a c k e d that cysts deform each other, h a v e almost entirely replaced hostmuscular tissue In t h e b u r r o w i n g e x p e r i m e n t d e s c r i b e d , t h e c o c k l e s h a d b e e n c h a l l e n g e d w i t h a n u n c o u n t e d n u m b e r of 14. e l o n g a t a c e r c a r i a e . U p o n s u b s e q u e n t d i s s e c t i o n , t h e n u m b e r of m e t a c e r c a r i a l c y s t s p e r c o c k l e w a s f o u n d to b e i n t h e r a n g e of s o m e 30 to 55. T h i s w a s b e l i e v e d to b e a f a i r l y h i g h n u m b e r , w h i c h m a y h a v e o v e r c h a r g e d t h e s e s m a l l h o s t s .

Impact of t r e m a t o d e p a r a s i t i s m on tidal-flat f a u n a

193

H o w e v e r , w h e n e x a m i n i n g n a t u r a l l y i n f e s t e d 0 - g r o u p cockles, it w a s f o u n d that 250 H. elongata cysts p e r host w e r e not u n c o m m o n . F i g u r e 7a, for e x a m p l e , s h o w s the distribution of 195 m e t a c e r c a r i a e in the foot of a n a t u r a l l y i n f e s t e d j u v e n i l e c o c k l e 15.2 m m in shell length. A cut-out of t h e s a m e m i c r o g r a p h (Fig. 7b) s h o w s that, in t h e most h e a v i l y i n v a d e d portion of the c o c k l e ' s foot, the m e t a c e r c a r i a e are so d e n s e l y p a c k e d that they d e f o r m e a c h o t h e r a n d h a v e a l m o s t e n t i r e l y r e p l a c e d the host's m u s c u l a r tissue. It is hard to u n d e r s t a n d h o w such a n i m a l s can stay a l i v e - a n d in fact t h e y do not s u r v i v e very long. T h e second i m p o r t a n t larval d i g e n e a n u t i l i z i n g m u s s e l s a n d c o c k l e s as s e c o n d a r y host is Renicola roscovita. Its sporocysts a n d c e r c a r i a e occur in up to 44 % of the L. littorea from the K6nigshafen, and m u s s e l s a n d c o c k l e s from that a r e a are 100 % i n f e s t e d with the m e t a c e r c a r i a e . In a d u l t hosts, t h e latter i n h a b i t m a i n l y t h e palps, w h i c h m a y b e c o m e as d e n s e l y p a v e d as the foot by H. elongata. In v e r y s m a l l c o c k l e s (Table 1, ' a u t u m n spat'), R. roscovita m e t a c e r c a r i a e encyst m a i n l y in t h e m a n t l e m a r g i n a n d t h e visceral mass, w h i c h m a y be ~tue to t h e fact that t h e tiny p a l p s of t h e s e s m a l l hosts do not p r o v i d e sufficient space to a c c o m o d a t e l a r g e r n u m b e r s of larval worms.

Table 1. Cardium edule. Microhabitat selection (percentage distribution) of 3 larval trematodes in various body parts of juvenile cockles

Trematode species

Foot

Microhabitat Palps Gills M a n t l e Vism a r g i n ceral

mass

Himasthla elongata Percentage of cysts in summer spat in autumn spat

96.7 97.0

Himasthla interrupta Percentage of cysts in summer spat 0.5 in autumn spat 14.1 Renicola roscov~ta Percentage of cysts in summer spat in autumn spat

0,6 1,1

Total Total number number of m e t a - of hosts cercariae

Number Mean (percentage) n u m b e r of of hosts metacercainfested riae infested host -~

4,527 33

23 24

23 (100 %) 9 (37.5 %)

196.8 3.7

0 4.0

186 99

23 24

22 (95.7 %) 17 (70.8 %)

8.5 5.8

10.5 15.1 41,4 35.4

3,879 181

23 24

23 (100 %) 22 (91.7 %)

168.7 8.2

0 0

0 0

3.3 3.0

0 5.1

0 1.0

99.5 75.8

71.7 18.2

2.1 3.9

0 0

Both Himasthla a n d Renicola m e t a c e r c a r i a e a d v e r s e l y affect the h e a t t o l e r a n c e of their b i v a l v e hosts. As s h o w n e x p e r i m e n t a l l y , the m e t a c e r c a r i a e of Renicola, w h i c h g r o w within the s e c o n d a r y host, h a v e a p h y s i o l o g i c a l l y m o r e d e t r i m e n t a l effect on the c o c k l e than the n o n - g r o w i n g H i m a s t h l a cysts (Lauckner, 1983). T h e i m p a c t of larval t r e m a t o d e s on n a t u r a l b i v a l v e p o p u l a t i o n s is difficult to d e t e r m i n e by direct f i e l d observation. H o w e v e r , the d e s t r u c t i v e action of t h e s e p a r a s i t e s can be d e d u c e d from i n d i r e c t e v i d e n c e (Table 2):

194

G. L a u c k n e r Table 2. Cardium edule. Intensity of trematode infestation in 0-group individuals

Number of hosts inspected Host-shell length (mm; mean _+ standard deviation) Total number of cysts recovered Number of cyst hosts -1 (mean + standard deviation) Percentage of parasites involved Himasthla elongata Himasthla interrupta Renicola roscovita Himasthla continua and Psilostomum brevicotle

Summer spat

Autumn spat

23 15.55 +- 2.05 8,592 373.6 +-- 100.0

24 6.86 ± 2.42 316 13.2 _+ 9.9

52.7 2.2 45.1 0

10.4 31.3 57.3 1.0

0-group C. e d u l e from the K6nigshafen, 15.55 m m i n m e a n shell length, were found to h a r b o u r a n a v e r a g e of 373.6 m e t a c e r c a r i a l cysts w h e n e x a m i n e d at the b e g i n n i n g of the winter, i.e. at a time w h e n cercarial e m i s s i o n b y the first i n t e r m e d i a t e hosts has ceased. T h e s e i n d i v i d u a l s h a v e b e e n t e r m e d ' s u m m e r spat' b e c a u s e they were m e m b e r s of the m a j o r spatfall occurring i n J u n e to July. In some years there is a second period of m i n o r spatfall or diffuse s p a w n i n g occurring later i n the year. These a n i m a l s have a c c o r d i n g l y b e e n t e r m e d ' a u t u m n spat'. T h e y m e a s u r e d 6.86 n u n i n m e a n shell l e n g t h a n d h a r b o u r e d , o n the average, o n l y 13.2 cysts w h e n e x a m i n e d b y the e n d of the first growth period. Infestations with H. elongata (which is the - m e c h a n i c a l l y - more deleterious parasite} m a k e u p 52.7 % of the total infestations i n the s u m m e r spat b u t only 10.4 % i n the a u t u m n spat. H. interrupta, H. continua a n d Psilostomum brevicolle have their redial a n d cercarial stages i n the gastropod Hydrobia ulvae (Loos-Frank, 1967, 1968}. H. interrupta m e t a c e r c a r i a e occur i n s i g n i f i c a n t n u m b e r s only in a u t u m n spat of C. edule. N o n e of the j u v e n i l e K 6 n i g s h a f e n cockles, i n s p e c t e d for e n c y s t e d trematodes in the following spring, h a d m e t a c e r c a r i a l n u m b e r s f a l l i n g into the r a n g e of the s u m m e r spat counts o b t a i n e d d u r i n g the p r e c e d i n g a u t u m n {Table 2).

DISCUSSION T h e p a t h o l o g y of larval t r e m a t o d e s i n Littorina littorea has b e e n s t u d i e d i n detail at the i n d i v i d u a l l e v e l (Rees, 1936; Robson & Williams, 1971a, b; Watts, 1971; a n d others). However, studies on the effects of d i g e n e a n s o n Littorinidae at the p o p u l a t i o n level are scarce (for literature r e v i e w see Lauckner, 1980). Since the p r e s e n c e of r e d i a e or sporocysts i n L. littorea causes 'parasitic castration', a c o n s i d e r a b l e proportion of p e r i w i n k l e s is, therefore, r e m o v e d from the b r e e d i n g p o p u l a tion. It is obvious that infestation i n c i d e n c e s i n excess of 50 %, as p r e v a i l i n g i n the K6nigshafen, m u s t h a v e a p r o f o u n d effect o n the p o p u l a t i o n d y n a m i c s a n d r e c r u i t m e n t of the host species. The o b s e r v e d scarcity of Littorina veligers i n p l a n k t o n samples from the i n v e s t i g a t i o n area (P. Martens, pers. comm.) m a y be a direct result of the trematodec a u s e d r e d u c t i o n of the r e p r o d u c t i v e p o t e n t i a l of the p e r i w i n k l e . It has b e e n s u g g e s t e d that i n f e s t a t i o n of L. littorea with Cryptocotyle lingua, Himasthla elongata a n d Renicola roscovita m a y a c c o u n t for i n c r e a s e d host mortality in

Impact of t r e m a t o d e p a r a s i t i s m on tidal-flat f a u n a

195

the laboratory {Robson & Williams, 1970}, b u t field data are lacking. L o n g - t e r m observations conducted at Sylt a n d in the D a n i s h part of the Baltic Sea (Lauckner, i n prep.} provide strong e v i d e n c e for the a s s u m p t i o n that the p o p u l a t i o n d y n a m i c s of L. llttorea i n these waters are p r o f o u n d l y affected b y larval d i g e n e a n s . In the second i n t e r m e d i a t e hosts, the p a t h o l o g y c a u s e d b y the Littorina parasites is no less severe. The effects of C. lingua on fishes h a v e b e e n s t u d i e d on several occasions. S i n d e r m a n n & Rosenfield (1954) h a v e s h o w n that 0-group h e r r i n g could be k i l l e d w i t h i n 15 days, a n d i n d i v i d u a l s of A g e G r o u p I w i t h i n 30 days, by massive c o n t i n u o u s exposure to cercariae of C. lingua. M a c k e n z i e (1968} i d e n t i f i e d m a s s i v e i n f e s t a t i o n of y o u n g plaice with m e t a c e r c a r i a e of that species as the possible cause of mortality. A c c o r d i n g to K e l l e - E m d e n (1979), y o u n g flatfish less t h a n 4 cm i n l e n g t h are p a r t i c u l a r l y affected b y C. lingua. A single C. lingua cercaria is sufficient to kill a larval h e r r i n g (Fig. 6). In the North a n d Baltic Seas, C. lingua is a very successful parasite c a p a b l e of m a i n t a i n i n g high spatial a n d temporal p o p u l a t i o n stability i n its i n t e r m e d i a t e a n d final hosts (Lauckner, 1984; Lauckner, i n prep.}. Therefore, its i m p a c t on the fish f a u n a of s h a l l o w inshore waters is obvious. The o b s e r v a t i o n of 100 % C. lingua infestation i n j u v e n i l e flatfish from the K 6 n i g s h a f e n is a l a r m i n g i n v i e w of the fact that the s h a l l o w parts of the W a d d e n Sea are i m p o r t a n t n u r s e r y g r o u n d s for plaice, d a b a n d flounder. Metacercariae e n c y s t i n g i n m a r i n e b i v a l v e s are u s u a l l y r e g a r d e d as h a r m l e s s (for literature a n d discussion of controversial o p i n i o n s c o n s u l t Lauckner, 1983}. In contrast, d e t r i m e n t a l effects of larval t r e m a t o d e s on the g e n e r a l p e r f o r m a n c e of m u s s e l s a n d cockles have clearly b e e n d e m o n s t r a t e d b y L a u c k n e r (1983). A t t a c h m e n t to the substrate by m e a n s of byssus threads is of vital i m p o r t a n c e for Mytllus edulis a n d for the formation of intertidal b a n k s (Maas G e e s t e r a n u s , 1942}. The - c o m m e r c i a l l y u n e x p l o i t e d - m u s s e l b a n k s of the KSnigshafen are at p r e s e n t grossly depleted, w h i c h m a y b e due, i n part, to the ice winters of the p r e c e d i n g years, a n d to bird predation. But the e v i d e n c e p r e s e n t e d in this study suggests that H. elongata infestations are a n i m p o r t a n t c o n t r i b u t i n g factor r e d u c i n g the success of the m u s s e l i n e s t a b l i s h i n g b a n k s i n shallow s h e l t e r e d waters. Byssus-thread p r o d u c t i o n b y M. edulis has b e e n s t u d i e d r e p e a t e d l y (Glaus, 1968; Reish & Ayers, 1968; Mah6o, 1970; V a n W i n k l e , 1970; Martella, 1974; M a r t i n et al., 1975; A l l e n et al., 1976; Cart & Reish, 1978; Price, 1980). Curiously, n o n e of these authors has t a k e n into c o n s i d e r a t i o n the possible effects of larval t r e m a t o d e s o n the byssal activity of their test individuals. The deleterious effects of H. elongata o n Cardium edule m a y b e e v e n more severe. Cockles r e n d e r e d i n c a p a b l e of b u r r o w i n g d u e to trematode infestation of the foot fall a n easy prey to birds a n d scavengers. I n d i v i d u a l s l y i n g at the s e d i m e n t surface are frequently cemented, b y m e a n s of the byssus threads of M. edulis, to shell fragments, pebbles, etc., in order to provide a solid s u b s t r a t u m for the m u s s e l ' s attachment. Such 'captured' cockles r a p i d l y die from d e s i c c a t i o n d u r i n g e b b tide. It m a y be a d d e d in p a r e n t h e s e s that b e h a v i o u r a l c h a n g e s s i m i l a r to those reported for the K 6 n i g s h a f e n cockles - i.e. l y i n g at the s e d i m e n t surface i n s t e a d of b u r r o w i n g have b e e n observed i n i n d i v i d u a l s of Cardium lamarcki from shallow bays o n the D a n i s h Kattegat coast (i.e. n e a r the e n t r a n c e of the Baltic Sea). I n s p e c t i o n of t h e s e a n i m a l s r e v e a l e d high i n t e n s i t i e s of infestation with H. elongata metacercariae, a n d u p to 34 % of the L. littorea from the same area h a r b o u r e d the r e d i a e of that species. Experiments d e t e r m i n i n g the possible effects of Renicola roscovita m e t a c e r c a r i a e on

196

G. L a u c k n e r

a d u l t b i v a l v e s h a v e not yet b e e n conducted, b u t it a p p e a r s likely that, i n h e a v i l y infested hosts, the proper f u n c t i o n of the palps as a particle t r a n s p o r t i n g a n d sorting device m a y b e i m p a i r e d . At least j u v e n i l e cockles are s e v e r e l y d e b i l i t a t e d b y R. ro$covita metacercariae, p r o b a b l y b y those e n c y s t e d i n the gills a n d the visceral mass (Table 1). T h e e x p e r i m e n t s a n d o b s e r v a t i o n s reported a b o v e m a i n l y reflect the effects of larval d i g e n e a n s on the second i n t e r m e d i a t e hosts at the i n d i v i d u a 1 level. What are now the effects of m e t a c e r c a r i a l attack o n mussels, cockles a n d other susceptible hosts at the population level? The b i v a l v e species i n h a b i t i n g the tidal flats h a v e their b r e e d i n g season i n late spring, the r e s u l t i n g m a j o r spatfalls occurring from late M a y to early A u g u s t (Fig. 8).

30

~ Cardium edute Mya arenaria

- 30

Mytilus edulis Macoma baltlca -20

20

10

0

I

I FM

' J

' j

'~'

Time of settling

Fig. 8. Time of settling and average number of spat of several bivalve species on 20 dm ~ sediment area of a tidal flat. (Based on Baggerman, 1953)

This time i n t e r v a l coincides precisely with the period of major cercarial production in the p r i m a r y host (Fig. 9). Hence, the y o u n g spat are o v e r w h e l m e d with large n u m b e r s of cercariae i m m e d i a t e l y after settling. S i n g l e or a few metacercariae are sufficient to kill r e c e n t l y settled b i v a l v e spat, a l t h o u g h their a b i l i t y to tolerate larger n u m b e r s of larval t r e m a t o d e s increases r a p i d l y with size. Since growth of the y o u n g bivalves is fast in the first summer, they do survive the initial period of major cercarial attack, p r o v i d e d that the n u m b e r of e n c y s t i n g metacercariae is not too high. In the s e c o n d year, m a x i m u m growth occurs prior to the onset of cercarial i n v a s i o n a n d i n c r e a s e s the capacity of the hosts to support a d d i t i o n a l n u m b e r s of m e t a c e r c a r i a e (Fig. 9). After the second summer, however, growth of the cockles slows d o w n a n d c a n no l o n g e r k e e p u p with the r e c u r r e n t b o m b a r d m e n t by larval trematodes. In areas of m o d e r a t e - t o - h i g h H i m a s t h l a a n d Renicola p r e v a l e n c e , the more heavily infested cockles u s u a l l y die d u r i n g or after their third summer. This is the so-called ' s u m m e r mortality', u s u a l l y b e l i e v e d to b e associated with p o s t - s p a w n i n g emaciation. However, mortalities of this k i n d have n o t h i n g to do with the b r e e d i n g cycle of Cardium a n d are not n o r m a l l y o b s e r v a b l e i n areas devoid of larval trematodes or other stress parasites. As has b e e n stated, j u v e n i l e C a r d i u m e d u l e from the K 6 n i g s h a f e n u s u a l l y yield c o n s i d e r a b l y fewer m e t a c e r c a r i a l cysts b y the e n d of their first w i n t e r t h a n i n d i v i d u a l s

Impact of t r e m a t o d e parasitism on tidal-flat f a u n a

197

40~

.40

'30-

-30

-o'

~ 20~

20

~10

~0

O-

M

J

D

s 1

2

M

J

S 3

D M J S I 4. Host age

D

M

J

S 5.

D

M

J

S 6,

D

0 Month Summer

Fig. 9. Cardium edule. Relation between age, growth increment and major periods of cercarial attack (= crosshatched areas). (Based on Kristensen, 1957)

e x a m i n e d in the p r e c e d i n g a u t u m n (Table 2). T h e r e is no i n d i c a t i o n that cockles or mussels are c a p a b l e of s l o u g h i n g off e n c y s t e d H. elongata metacercariae. Resorption of dead cysts may occur on rare occasions, a n d p r e s u m a b l y only in o v e r - a g e d worms or i n metacercariae killed by freezing. In fact, partial resorption has o n l y b e e n s e e n i n metacercariae of Renlcola roscovita e n c y s t e d i n the palps. From the drastic a n d rather s u d d e n d e c l i n e of m e t a c e r c a r i a l counts i n j u v e n i l e cockles it may, therefore, r e a s o n a b l y be c o n c l u d e d that n o n e of the h i g h l y infested s u m m e r - s p a t i n d i v i d u a l s h a d s u r v i v e d their first winter. A c o n c o m i t a n t d e c l i n e of m e t a c e r c a r i a l counts i n the a u t u m n - s p a t i n d i v i d u a l s indicates that this host cohort has u n d e r g o n e a s i m i l a r p a r a s i t e - c a u s e d mortality. In the infestation e x p e r i m e n t s c o n d u c t e d it b e c a m e a p p a r e n t that the n u m b e r of metacercariae r e q u i r e d to kill a j u v e n i l e host m a y b e q u i t e variable. This c i r c u m s t a n c e reflects the m i c r o h a b i t a t s e g r e g a t i o n d i s p l a y e d b y the different species of m e t a c e r c a r i a e (Table 1). A few cysts i n the visceral mass or i n n e r v o u s tissues are b e y o n d d o u b t more deleterious t h a n a m u c h larger n u m b e r i n the p a l p s or the m a n t l e m a r g i n . H. elongata i n v a d e s almost exclusively the foot;/-/, lnterrupta cysts are l a r g e l y c o n f i n e d to the m a n t l e margin, b u t i n very small cockles they also occur i n the foot. Renicola prefers the p a l p s as e n c y s t m e n t site i n larger hosts b u t the m a n t l e m a r g i n i n s m a l l e r hosts. T h e fairly h i g h p e r c e n t a g e of Renicola cysts i n the visceral mass certainly accounts for the p a t h o g e n i c i t y of e v e n low absolute n u m b e r s of m e t a c e r c a r i a e i n these small hosts. In conclusion, it has b e e n d e m o n s t r a t e d that larval t r e m a t o d e s do not only affect cockles a n d mussels at the i n d i v i d u a l level b u t that - u n d e r ecological c o n d i t i o n s p r e v a i l i n g in shallow bays such as the K 6 n i g s h a f e n - they e v e n exert l a r g e - s c a l e p o p u l a t i o n control over their m o l l u s c a n i n t e r m e d i a t e hosts. At least they do a c c o u n t for the larger part of w h a t the ecologist terms ' n a t u r a l mortality'. It must b e e m p h a s i z e d that H l m a s t h l a a n d Renicola are not the sole t r e m a t o d e s parasitizing North Sea bivalves. At least 9 larval d i g e n e a n s occur i n C a r d i u m e d u l e a n d 6 i n M f l l l u s edulis from the K S n i g s h a f e n (Lauckner, 1977}. Several are l e t h a l d i s e a s e agents. As the adults of all of these occur i n sea birds, it b e c o m e s progressively evident, w h i c h l i n k of the littoral ecosystem is r e s p o n s i b l e for w h a t m a y b e t e r m e d a n 'ecological disaster'. However, a n y a t t e m p t to r e d u c e sea bird a b u n d a n c e - at p r e s e n t the only c o n c e i v a b l e m e a s u r e that could b e effective i n restoring a b a l a n c e d ecosystem

198

G. Lauckner

in the K6nigshafen ignorant

- would

or totally unaware

immediately

call up the bird protectionists

o f w h a t t h e i r ' p e t s ' a r e d o i n g to t h e m a r i n e

who are either littoral fauna.

A c k n o w l e d g e m e n t s . I a m g r a t e f u l to M. S~ihl for t e c h n i c a l a s s i s t a n c e a n d to J, M a r s c h a l l for p r e p a r i n g t h e d r a w i n g s . H. L a u c k n e r a s s i s t e d w i t h t h e c o l l e c t i o n of t h e m a t e r i a l a n d t y p e d t h e manuscript. LITERATURE

CITED

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