HELGOI~NDER MEERESUNTERSUCHUNGEN Helgol~nder Meeresunters. 37, 185-199 (1984)

Impact of t r e m a t o d e p a r a s i t i s m o n the fauna of a N o r t h

Sea t idal flat

G. L a u c k n e r

Biologische Ans ta l t He lgo land (Litoralstation];

D-2282 List/Sylt, Federal Republ ic of G e rm 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, depict ing the d igenean parasites of the common periwinkle, Littorina littorea, and their life cycles, as an example. On the German North Sea coast, L. fittorea is first intermediate host for 6 larval trematodes represent ing 6 d igenean 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 and polychaetes, those of R. roscovita in molluscs; Iv[. pygmaeus has an abbreviated life cycle; C. lebouri encysts free on solid surfaces; and the fish t rematode P. atomon utilizes benthic crustaceans, mainly amphipods, as second intermediate hosts. On the tidal flats of the K6nigshafen (Sylt), up to 77 % of the periwinkles have been found to be infested by larval trematodes. Maximum infestations in individual samples were 23 % for C. lingua, 47 % for H. etongata and 44 To for R. roscovita. The digeneans cause complete 'parasitic castration' of their carriers and hence exclude a considerable proportion of the snails from the breeding population. Infestation reduces the longevity of affected hosts, and size-related, t rematode-induced differential mortality causes changes in the normal size- frequency 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 evidence 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.

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

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 in 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 ,

that 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 in 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

ana lyses .

T h e p u r p o s e of th i s s t u d y is to 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 rva l t r e m a t o d e s on

severa 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 da 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 i ts d i g e n e a n p a r a s i t e s as a n e x a m p l e .

© Biologische Anstalt Helgoland, Hamburg

186 G. Lauckner

THE INVESTIGATION AREA

The K6nigshafen (Fig. 1) is a shal low lees ide bay s i tuated at the nor thern tip of the

Isle of Sylt (55°3'N 8°25'E). At low tide, l a rge areas of sand and mud flats, as wel l as mussel beds, are uncovered . Dur ing this t ime the flats are f r equen ted by sea birds that

. . . . : " : :" : :. ; . : . ~ .:,!.-:..:...: i ; ' : : : ~

f:!7 ";7[j , ~t "" /̂ ̀""% *"" "<" I:7:' ' } T f ~

I i S

0 :! 500 1000 I J .,,J m

Fig. 1. The 'K6nigshafen' at List, North Sea, Isle of Sylt (Federal Republic of Germany), showing Stations 1 and 2

feed on the bot tom inver tebrates . The islet of Uth6rn is a wi ld l i fe preserve provid ing roost ing and b reed ing places for a species-r ich avifauna. Major ep i faunal e lements of

the fiats are - in terms of b iomass - the b lue mussel , Myti lus edulis, the common cockle, Cardium (Cerastoderma} edule, and the per iwinkle , Littorina littorea,

The eco logy of the K6nigshafen has b e e n s tud ied by Woh lenbe rg (1937). However ,

excep t for a few brief notes (Lauckner, in Biologische Anstal t Helgoland , Jahresber icht 1974, 1978) and two more gene ra l publ ica t ions refer r ing only in part to mater ia l from

that area (Werding, 1969; Lauckner 1971), there have been no studies on the para- s i tofauna of the K6nigshafen.

MATERIALS AND M E T H O D S

Per iwinkles and mol luscan second in t e rmed ia t e hosts - main ly Myti lus edulis and

Cardium (Cerastoderma) edule - w e r e hand-co l l ec t ed at low tide. Juven i l e flatfish were

Impact of t rematode paras i t i sm on t idal-f lat fauna 187

dip-net ted dur ing ebb tide. The col lec ted inver tebra tes were t ransferred to the labora-

tory and main ta ined in aerated, dai ly c h a n g e d sea wate r unti l examinat ion . Per iwinkles

were a l lowed to defeca te for at least 24 h in order to faci l i tate recogni t ion of recent ly established, immature d i g e n e a n infestations. By means of a ca l iper rule, the sp indle

height of Lit torina l i t torea was measu red to the neares t 1/10 mm, and ind iv idua ls were

subsequent ly g rouped in 1.0 m m size intervals. The resul t ing multi~modal s i ze - f requency distributions (which represen t ove r l app ing year classes) were d issec ted into thei r normal

components by means of a computer p rogram based on the me thod out l ined by A k a m i n e

(1982). Bivalves used in the infestat ion and survival exper iments were col lec ted from tidal

flats outside the K5nigshafen, i.e. from sites wi th low overal l t r ematode p reva lence . All individuals were acc l imated to laboratory condi t ions (20 °C, 30Too S, 16:8 h day /n igh t

rhythm) for at least 5 days prior to the exper iments .

Cryp toco ty l e l i ngua infestat ion in juven 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 tudied

more thoroughly in the author 's laboratory by Ke l l e -Emden (1979). The methods

descr ibed in detai l in that pape r have b e e n adopted in the present invest igat ion.

RESULTS

Six species of larval t rematodes r ep resen t ing 6 d i g e n e a n famil ies have b e e n

reported from North Sea pe r iwink les (Werding, 1969), and all of these occur in Lit tor ina

l i t torea from the KSnigshafen. Thei r life cycles are summar i zed in Figure 2. All excep t

Podoco ty le a tomon uti l ize sea birds as def ini te hosts. The first three species are of

Life cycles of Littor~na parasites

Cryptocotyle lingua (Heterophyidae): L. littorea .~ Fishes .~ Sea birds

Himasthla elongata (Echinostomatidae}: Molluscs

L. 11ttorea ~ Annelids ~ Sea birds

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

considerable concern because they employ commerc ia l ly impor tant ver tebra tes or

invertebrates as second in t e rmed ia t e hosts. The other three, which occur in low preva-

lence, wil l not be cons idered in detail .

In the K6nigshafen, t r ematode infestat ion of pe r iwink les may reach enormous

levels. At most stations sampled, overal l infestat ion pe rcen t ages in adul t L. f i t torea were

188 G. L a u c k n e r

8 0 - - 0

/i \ ~+,~++,-'"-" I "X~,_,.N°n -infested I I I I I I

4] ./,/#•///i~,,.?. Cercerio lebouri I I I I I l

4 1 I Microphallus pygmeeus

20- O

12-

~ /*- onicola roscovito

t.L I I i [ I

t

• .

Himesthle elongate I~/l "six I I~

32 t o

24. ~o

I I I I I i

12 14 16 18 20 22 2/. Host-shell height (mm)

Fig. 3. L i t t o r i n a l # t o r o a . Length-f requency dis t r ibut ion and t rematode infestation of sample taken at Station 1 (see Fig, 1)

Impact of t rematode parasi t ism on tidal-flat fauna 189

well above 50 %, with a m a x i m u m of 77 % observed in a snai l sample (Fig. 3) t aken from a mussel b a n k near the ent rance of the bay, a favourite roosting and feed ing place of gulls Larus spp., oystercatchers Haematopu$ ostralegus and Eider ducks Somateria mollissima. M a x i m u m infestat ion inc idences recorded for ind iv idua l paras i te species in Littorina samples from the area were 23 % for Cryptocotyle lingua, 44 % for Renicola

roscovita and 47 % for Himasthla elongata. A more de ta i led analysis of the dynamics of trematode infestat ion in l i t torines from the K6nigshafen will be g iven e lsewhere (Lauck- her, in preparation).

Most of the infestat ions encoun te red were mature and the resul tant host pa thology severe. Gonad atrophy ( 'parasitic castration') was apparen t in almost all infested hosts, as was penis reduct ion in males. The larval d igeneans differ with respect to their pathogenici ty in the first in te rmedia te host (for review of l i terature see Lauckner, 1980). Since each species exhibi ts a dist inct preference for certain host-size classes (Fig. 3), the resultant paras i te -produced differential mortal i ty of infested hosts causes s ignif icant distortions of the or iginal s ize-f requency dis t r ibut ion of the L. fittorea populat ion. In extreme cases (Fig. 4), grotesque mul t imoda l d is t r ibut ion pat terns arise, which cannot be resolved into ind iv idua l normal components represen t ing successive year classes. Simi-

20- o

/\ >, 0 0 o Total sample 0 0 t X

"" o _ o -,o c r

8- 0 • I. ut

o/ ° 4-

- 0 o s Y / / / ~ a r a s r ~ l z e a y / / A O \ / 0 " 0 0 / .o / / / / 6 ind iv idualsY/ / /A ' / /e . \

0 / " ~ J " % 1 ~/,/2~ 1"1/////, , , , . . / . . H . / / / / / / ~ V / / / ~ I I I I I 1 I i I I I I

10 20 Host-shel l height (rnm)

Fig. 4. Littorina littorea. Grotesque distortion of length-frequency distribution caused by parasite- produced differential mortality, Sample taken at Station 2 (see Fig, 1)

lafly, no reproducible von Bertalanffy growth parameters can be computed for such affected per iwinkle populat ions.

As a consequence of these erratic deviations, no mortali ty est imates can be made from analyses of the changes of the per iwinkles ' s ize-frequency distr ibution. However, s imultaneous collection of l iv ing snails and dead shells form the same locality provides a rough idea of the amount of differential mortali ty (Fig. 5a). The sample contains n 1 = 147 living L. Httorea and n2 -- 167 dead shells. Combina t ion of both groups yields a size- frequency curve (Fig. 5b), which can be resolved into 3 normal components . Hence, the combined curves reflect, with a h igh degree of probabil i ty , the condi t ion that had existed prior to the onset of mortality. From the n u m b e r of (dead plus l iving) per iwink les in the whole sample minus the n u m b e r of dead shells, the mortal i ty - which is be l i eved to be

190 G. Lauckner

{3

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I t .

64-

60-

56-

52-

48-

44-

40- e----e

36- OdO 32--

28-- @ 2/.-

20-

16- /

12- / /

0 C , , , , 8 10

Living end deed/I combined / /

\

/ /

Living snails (total sample) Living snails (infested) Dead shells

• 0

I o °/°"e/• "-\ ./

12 14 16 I; 2~0 2'2 2'/, 8 10 I? Host-shell height (mm)

1

1'4 16

6~

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56

-52

-48

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-40

-36

-32

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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. l ingua 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. l ingua 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

Impact of t rematode parasi t ism on tidal-flat fauna 191

\

pr~ r'r',

Fig. 6. Herring (Clupea harengus) larva killed by encysting Cryptocotyle lingua metacercaria (arrow)

molluscs, the cercariae almost invar iab ly encyst in the foot musculature . In the Kbnigs- hafen, Mytilus edulis and Cardium edule, the ma in secondary host species, are 100 % infested with H. elongate metacercar iae. Frequent ly , the foot of these b ivalves is so r iddled with cysts that its vital funct ions are severely impa i red (Fig. 7).

Experiments were conducted to de te rmine the effect of H. elongate on byssus- thread production in young M. edulis. Uninfes ted mussels produced 31 + 17 threads wi th in 22.5 h and 62 + 26 threads wi th in 77.5 h. With in the same t ime intervals, ind iv idua l s infested with 116+66 cysts produced only 22 and 40 threads, respectively. The differences are statistically highly s ignif icant (Lauckner, 1983).

Cardium (Cerastoderma) edule is s imilar ly affected by H. elongate. The cockle normally lives ent i rely burrowed in the sediment , only the s iphon open ings be i ng vis ible at the substrate surface. In the K6nigshafen, numerous cockles can be seen which are partially or totally uncovered. Many have been spun together in bund le s by the byssus threads of mussels. Inspect ion of such cockles almost invar iab ly reveals the presence of large numbers of metacercarial cysts in the foot musculature .

When placed on sandy substratum, juven i l e cockles exper imenta l ly infes ted with H. elongate metacercar iae r emained at the sed iment surface for cons iderable time, whi le uninfested controls burrowed rapidly. The m e d i a n t ime ( ---- m e a n of log time) after which 50 % of the heal thy cockles were ent i re ly bur rowed was 12.5 min, as opposed to about 290 min required by the infested specimens. In order to de te rmine whether the effect exerted by the metacercar iae is mechan ica l or physiological, or both, another group of cockles was exper imenta l ly infested with cercariae of Renicola roscovita, which invade the palps rather than the foot. There was no devia t ion in the m e d i a n bur rowing t ime of this group from that of the un infes ted control. Therefore, the effect of H. elongate metacercariae on the bur rowing abi l i ty of cockles was in terpre ted as be i ng pure ly

mechanical .

192 G. L a u c k n e r

Fig. 7. Cardium edule. (a) Foot of juveni le individual (15.2 mm shell length) with extremely heavy natural t-timasthla elongata infestation showing dis t r ibut ion of 195 cysts; (b) en la rged portion of (a). Metacercariae, so dense ly packed that cysts deform each other, have almost entirely replaced host-

muscular 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 longata 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 cys 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 hos ts .

Impact of t rematode parasi t ism on t idal-f lat fauna 193

However , w h e n e x a m i n i n g na tura l ly infested 0-group cockles, it was found that 250

H. elongata cysts per host were not uncommon. Figure 7a, for example , shows the

distr ibution of 195 metacercar iae in the foot of a natural ly infested juven i l e cockle 15.2 mm in shell length. A cut-out of the same micrograph (Fig. 7b) shows that, in the most

heavi ly invaded port ion of the cockle ' s foot, the me tace rca r i ae are so dense ly packed

that they deform each other and have a lmost en t i re ly r ep laced the host 's muscu la r tissue. It is hard to unders tand how such an imals can stay a l ive - and in fact they do not survive

very long. The second important larval d i g e n e a n ut i l iz ing mussels and cockles as secondary

host is Renicola roscovita. Its sporocysts and cercar iae occur in up to 44 % of the L. littorea from the K6nigshafen, and mussels and cockles from that area are 100 % infes ted with the metacercar iae . In adul t hosts, the lat ter inhabi t main ly the palps, wh ich may

become as dense ly p a v e d as the foot by H. elongata. In very small cockles (Table 1, ' autumn spat'), R. roscovita metace rca r i ae encyst main ly in the man t l e m a r g i n and the visceral mass, which may be ~tue to the fact that the t iny palps of these small hosts do not

provide sufficient space to accomodate la rger numbers of larval worms.

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

Trematode Microhabitat species Foot Palps Gills Mant le Vis-

marg in ceral mass

Himasthla elongata Percentage of cysts

in summer spat 96.7 0 0 3.3 0 in autumn spat 97.0 0 0 3.0 0

Himasthla interrupta Percentage of cysts

in summer spat 0.5 0 0 99.5 0 in autumn spat 14.1 5.1 1.0 75.8 4.0

Renicola roscov~ta Percentage of cysts

in summer spat 0,6 71.7 2.1 10.5 15.1 in autumn spat 1,1 18.2 3.9 41,4 35.4

Total Total N u m b e r Mean n u m b e r n u m b e r (percentage) n u m b e r of of meta- of hosts of hosts metacerca-

cercar iae infested riae infested host -~

4,527 23 23 (100 %) 196.8 33 24 9 (37.5 %) 3.7

186 23 22 (95.7 %) 8.5 99 24 17 (70.8 %) 5.8

3,879 23 23 (100 %) 168.7 181 24 22 (91.7 %) 8.2

Both Himasthla and Renicola metace rca r i ae adverse ly affect the hea t to lerance of

their b iva lve hosts. As shown exper imenta l ly , the metace rca r i ae of Renicola, which grow

within the secondary host, have a phys io logica l ly more de t r imenta l effect on the cockle

than the non-growing Himasthla cysts (Lauckner, 1983). The impact of larval t rematodes on natural b iva lve popula t ions is difficult to

determine by direct f ie ld observat ion. However , the des t ruct ive act ion of these paras i tes

can be deduced from indirect ev idence (Table 2):

194 G. Lauckner

Table 2. Cardium edule. Intensity of trematode infestation in 0-group individuals

Summer spat Autumn spat

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

23 24 15.55 +- 2.05 6.86 ± 2.42

8,592 316 373.6 +-- 100.0 13.2 _+ 9.9

52.7 10.4 2.2 31.3

45.1 57.3 0 1.0

0-group C. edule from the K6nigshafen, 15.55 m m in m e a n shell length, were found to harbour an average of 373.6 metacercar ia l cysts w h e n examined at the b e g i n n i n g of the winter , i.e. at a t ime w h e n cercarial emiss ion by the first in te rmedia te hosts has ceased. These ind iv idua l s have b e e n t e rmed ' summer spat ' because they were members of the major spatfall occurr ing in June to July. In some years there is a second period of minor spatfall or diffuse s p a w n i n g occurr ing later in the year. These animals have accordingly b e e n te rmed ' a u t u m n spat' . They measured 6.86 nun in m e a n shell length and harboured, on the average, on ly 13.2 cysts w h e n examined by the end of the first growth period. Infestat ions with H. elongata (which is the - mechanica l ly - more deleter ious parasite} make up 52.7 % of the total infestat ions in the summer spat but only 10.4 % in the a u t u m n spat. H. interrupta, H. continua and Psilostomum brevicolle have their redial and cercarial stages in the gastropod Hydrobia ulvae (Loos-Frank, 1967, 1968}. H. interrupta metacercar iae occur in s ignif icant number s only in a u t u m n spat of C. edule. None of the juven i l e K6nigshafen cockles, inspected for encysted trematodes in the fol lowing spring, had metacercar ia l numbe r s fa l l ing into the range of the summer- spat counts ob ta ined dur ing the p reced ing a u t u m n {Table 2).

DISCUSSION

The pa thology of larval t rematodes in Littorina littorea has b e e n s tudied in detai l at the ind iv idua l level (Rees, 1936; Robson & Will iams, 1971a, b; Watts, 1971; and others). However, s tudies on the effects of d igeneans on Lit torinidae at the popula t ion level are scarce (for l i terature review see Lauckner, 1980).

Since the presence of rediae or sporocysts in L. littorea causes 'parasit ic castration', a cons iderable proport ion of pe r iwink les is, therefore, removed from the b reed ing popula- tion. It is obvious that infestat ion inc idences in excess of 50 %, as prevai l ing in the K6nigshafen, must have a profound effect on the popula t ion dynamics and recrui tment of the host species. The observed scarcity of Littorina veligers in p lank ton samples from the inves t iga t ion area (P. Martens, pers. comm.) may be a direct result of the trematode- caused reduct ion of the reproduct ive potent ia l of the per iwinkle .

It has b e e n sugges ted that infes ta t ion of L. littorea with Cryptocotyle lingua, Himasthla elongata and Renicola roscovita may account for increased host mortality in

Impact of t rematode parasi t ism on t idal-f lat fauna 195

the laboratory {Robson & Will iams, 1970}, bu t field data are lacking. Long- term observa- tions conducted at Sylt and in the Danish part of the Baltic Sea (Lauckner, in prep.} provide strong evidence for the assumpt ion that the popula t ion dynamics of L. llttorea in these waters are profoundly affected by larval d igeneans .

In the second in te rmedia te hosts, the pathology caused by the Littorina parasi tes is no less severe. The effects of C. lingua on fishes have b e e n s tudied on several occasions. S inde rmann & Rosenfield (1954) have shown that 0-group her r ing could be ki l led wi th in 15 days, and indiv iduals of Age Group I wi th in 30 days, by massive con t inuous exposure to cercariae of C. lingua. Mackenz ie (1968} ident i f ied massive infes ta t ion of young plaice with metacercar iae of that species as the possible cause of mortality. According to Kel le-Emden (1979), young flatfish less than 4 cm in l eng th are par t icular ly affected by C. lingua. A single C. lingua cercaria is sufficient to kil l a larval her r ing (Fig. 6). In the North and Baltic Seas, C. lingua is a very successful parasi te capable of m a i n t a i n i n g high spatial and temporal popula t ion stabil i ty in its in te rmedia te and final hosts (Lauckner, 1984; Lauckner, in prep.}. Therefore, its impact on the fish fauna of shal low inshore waters is obvious. The observat ion of 100 % C. lingua infestat ion in juven i l e flatfish from the K6nigshafen is a l a rming in v iew of the fact that the shal low parts of the Wadden Sea are important nursery grounds for plaice, dab and flounder.

Metacercar iae encys t ing in mar ine b iva lves are usua l ly regarded as harmless (for l i terature and discussion of controversial opin ions consul t Lauckner, 1983}. In contrast, detr imental effects of larval t rematodes on the genera l performance of mussels a nd cockles have clearly been demons t ra ted by Lauckner (1983). At tachment to the substrate by means of byssus threads is of vital impor tance for Mytllus edulis and for the formation of inter t idal banks (Maas Geesteranus , 1942}. The - commercia l ly unexp lo i t ed - mussel banks of the KSnigshafen are at present grossly depleted, which may be due, in part, to the ice winters of the p reced ing years, and to bird predation. But the ev idence presen ted in this study suggests that H. elongata infestat ions are an impor tant cont r ibu t ing factor reducing the success of the mussel in es tab l i sh ing banks in shallow shel tered waters.

Byssus-thread product ion by M. edulis has b e e n s tudied repea ted ly (Glaus, 1968; Reish & Ayers, 1968; Mah6o, 1970; Van Winkle , 1970; Martella, 1974; Mar t in et al., 1975; Al len et al., 1976; Cart & Reish, 1978; Price, 1980). Curiously, none of these authors has taken into considerat ion the possible effects of larval t rematodes on the byssal activity of their test individuals .

The deleterious effects of H. elongata on Cardium edule may be even more severe. Cockles rendered incapab le of bur rowing due to t rematode infestat ion of the foot fall an easy prey to birds and scavengers. Indiv iduals ly ing at the sed iment surface are frequently cemented, by means of the byssus threads of M. edulis, to shell fragments, pebbles, etc., in order to provide a solid subs t ra tum for the mussel ' s a t tachment . Such 'captured ' cockles rapidly die from desiccat ion dur ing ebb tide.

It may be added in paren theses that behav ioura l changes s imilar to those reported for the K6nigshafen cockles - i.e. ly ing at the sed iment surface ins tead of bu r rowing - have been observed in ind iv idua l s of Cardium lamarcki from shal low bays on the Danish Kattegat coast (i.e. nea r the en t rance of the Baltic Sea). Inspect ion of these an imals revealed high intensi t ies of infestat ion with H. elongata metacercar iae, and up to 34 % of the L. littorea from the same area harboured the rediae of that species.

Experiments de te rmin ing the possible effects of Renicola roscovita metacercar iae on

196 G. Lauckner

adul t b ivalves have not yet b e e n conducted, bu t it appears l ikely that, in heavi ly infested hosts, the proper funct ion of the palps as a part icle t ranspor t ing and sorting device may be impaired. At least juven i l e cockles are severely debi l i ta ted by R. ro$covita metacer- cariae, p robably by those encys ted in the gills and the visceral mass (Table 1).

The exper iments and observat ions reported above ma in ly reflect the effects of larval d igeneans on the second in te rmedia te hosts at the i n d i v i d u a 1 level. What are now the effects of metacercar ia l at tack on mussels, cockles and other susceptible hosts at the p o p u l a t i o n level?

The b iva lve species i nhab i t i ng the t idal flats have their b reed ing season in late spring, the resu l t ing major spatfalls occurr ing from late May to early August (Fig. 8).

30

20

~ Cardium edute

Mya arenaria

Mytilus edulis

Macoma baltlca

0 I I FM ' J ' j '~'

Time of sett l ing

- 3 0

-20

10

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 t ime interval coincides precisely with the period of major cercarial product ion in the pr imary host (Fig. 9). Hence, the young spat are overwhelmed with large numbers of cercariae immedia te ly after settl ing. Single or a few metacercar iae are sufficient to kill recent ly sett led b iva lve spat, a l though their abi l i ty to tolerate larger number s of larval t rematodes increases rapidly with size.

Since growth of the young bivalves is fast in the first summer, they do survive the ini t ia l per iod of major cercarial attack, provided that the n u m b e r of encys t ing metacer- cariae is not too high. In the second year, max imum growth occurs prior to the onset of cercarial invas ion and increases the capacity of the hosts to support addi t ional numbers of metacercar iae (Fig. 9). After the second summer, however, growth of the cockles slows down and can no longer keep up with the recurrent b o m b a r d m e n t by larval trematodes. In areas of modera te - to-h igh Himasthla and Renicola prevalence, the more heavily infested cockles usua l ly die dur ing or after their third summer. This is the so-called ' summer mortali ty ' , usua l ly be l i eved to be associated with pos t - spawning emaciation. However, mortal i t ies of this k ind have no th ing to do with the b reed ing cycle of Cardium and are not normal ly observable in areas devoid of larval t rematodes or other stress parasites.

As has been stated, j uven i l e Cardium edule from the K6nigshafen usual ly yield cons iderably fewer metacercar ia l cysts by the end of their first winter than individuals

Impact of t rematode parasi t ism on t idal-flat fauna 197

40~

' 3 0 -

~ 20~

~ 1 0

O- M J s

1 2

-o '

D M J S D M J S D

3 I 4. Host age

M J S D M J S

5. 6,

. 4 0

-30

2 0

~0

0 D Month

Summer

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

examined in the preceding a u t u m n (Table 2). There is no ind ica t ion that cockles or mussels are capable of s loughing off encysted H. elongata metacercar iae. Resorption of dead cysts may occur on rare occasions, and p resumab ly only in over -aged worms or in metacercariae ki l led by freezing. In fact, part ial resorption has only b e e n seen in metacercariae of Renlcola roscovita encysted in the palps. From the drastic a nd rather sudden decl ine of metacercar ia l counts in j uven i l e cockles it may, therefore, r easonably be concluded that none of the h ighly infested summer-spa t ind iv idua l s had survived their first winter. A concomitant dec l ine of metacercar ia l counts in the a u t umn- spa t individuals indicates that this host cohort has u n d e r g o n e a s imilar paras i te -caused mortality.

In the infestat ion exper iments conducted it became apparen t that the n u m b e r of metacercariae required to kill a juven i l e host may be qui te variable. This c i rcumstance reflects the microhabi ta t segregat ion displayed by the different species of metacercar iae (Table 1). A few cysts in the visceral mass or in nervous tissues are beyond doubt more deleterious than a much larger n u m b e r in the palps or the mant le margin. H. elongata invades almost exclusively the foot;/-/, lnterrupta cysts are largely conf ined to the man t l e margin, but in very small cockles they also occur in the foot. Renicola prefers the palps as encys tment site in larger hosts bu t the man t l e marg in in smal ler hosts. The fairly h igh percentage of Renicola cysts in the visceral mass cer ta inly accounts for the pa thogenic i ty of even low absolute number s of metacercar iae in these small hosts.

In conclusion, it has b e e n demons t ra ted that larval t rematodes do not only affect cockles and mussels at the ind iv idua l level bu t that - unde r ecological condi t ions prevai l ing in shallow bays such as the K6nigshafen - they even exert large-scale populat ion control over their mol luscan in te rmedia te hosts. At least they do account for the larger part of what the ecologist terms 'na tura l mortali ty ' .

It must be emphas ized that Hlmasth la and Renicola are not the sole t rematodes parasi t iz ing North Sea bivalves. At least 9 larval d i ge ne a ns occur in Cardium edu le and 6 in M f l l l u s edul is from the KSnigshafen (Lauckner, 1977}. Several are le thal disease agents. As the adults of all of these occur i n sea birds, it becomes progressively evident , w h i c h l ink of the littoral ecosystem is responsible for what may be te rmed an 'ecological disaster' . However, any at tempt to reduce sea bird a b u n d a n c e - at present the only conceivable measure that could be effective in restoring a ba l anced ecosystem

1 9 8 G . L a u c k n e r

i n t h e K 6 n i g s h a f e n - w o u l d i m m e d i a t e l y c a l l u p t h e b i r d p r o t e c t i o n i s t s w h o a r e e i t h e r

i g n o r a n t o r t o t a l l y u n a w a r e 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 l i t t o r a l f a u n a .

Acknowledgemen t s . I a m g ra t e fu 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, Mar scha 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 he co l lec t ion of the m a t e r i a l a n d t yped the m a n u s c r i p t .

L I T E R A T U R E C I T E D

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