HELGOLANDER MEERESUNTERSUCHUNGEN Helgol~inder Meeresunters. 48, 89-105 (1994)

Parasite transfer f r o m c r u s t a c e a n to fish hosts in t h e Lfibeck Bight, SW Baltic S e a C. D. Zander, S. Groenewold & U. Strohbach Zoologisches Institut und Zoologisches Museum der Universit~t; Martin-Luther-KingPlatz 3, D-20146 Hamburg, Federal Republic of Germany

ABSTRACT: Four helminth parasites out of 19 species found in the Liibeck Bight, Baltic Sea, were chosen for investigations on the transfer from invertebrate to small-sized fish hosts: larvae of the tapeworms Schistocephalus sp. and Bothriocephalus sp. (Cestoda) living in planktonic copepods as primary hosts; Podocotyle atornon (Digenea) and Hysterothylacium sp. (Nematoda) were found in benthic crustaceans, especially Garnmarus spp. These hosts were the prey of 3 gobiid fishes, Gobiusculus flavescens (feeding mainly on plankton), Pornatosctn'stus minutus (preferring benthos), and P. pictus (feeding more on plankton than benthos). Because the fishes selected smaller sizes of crustaceans, they ingested all stages of the copepods but only the smaller-sized groups of gammarids which were often less infested by parasites. In order to evaluate the probability for a fish to be parasitized by a helminth, an infestation potential index (IP) was calculated. Podocotyle atomon and Hysterothylacium sp. revealed an IP which was far lower in gobies than expected when the prevalences of the previous hosts were taken into consideration. The IP of tapeworm larvae was mainly influenced by the feeding pressure of the gobiid predators, which might change with developmental stage and season. It is concluded that parasite transfer to the next host decreases when sizes of prey and predator differ only moderately. This mechanism can reduce the numbers of parasites transferred to less suitable or wrong hosts.

INTRODUCTION Parasites are important c o m p o n e n t s in m a r i n e coastal ecosystems. M a n y helminths p r e s e n t complicated life cycles, infest different hosts and, therefore, c h a n g e their habitats several times. This biological c h a r a c t e r i s t i c can cause transportation from the w a t e r column to the bottom, or e v e n from a q u a t ic to terrestrial habitats (Odening, 1974; Reimer, 1983). The parasite communities in their r e s p e c t i v e hosts h a v e increasingly b e c o m e objects of research (Esch et al., 1990). First Esch et al. (1975) d e v e l o p e d an hierarchical co n cep t for parasite populations. T h r e e levels of parasite communities w e r e fixed: infracommunity in a single host, c o m p o n e n t co m m u n i t y in a host population, and c o m p o u n d c o m m u n i t y in a host biocoenosis. T h e analysis of c o m p o n e n t c o m m u n i t i e s helps in identifying important parasites. T h e flow of parasites through s e v e r a l hosts is the main object of c o m p o u n d c o m m u n i t y r e s e a r c h (Esch et al., 1990). Th e hosts are either directly infested by active larval stages (e.g. cercariae in Digenea), or by i n t e r m e d i a t e hosts, which are preyed*upon t o g e t h e r with passive larval stages (e.g. pro- or plerocercoids of Cestoda, m e t a c e r c a r i a e of D i g e n e a , larvae of N em at o d a, a c a n t h e l l a e of Acanthocephala). The transfer of larval parasites to the fish hosts b e c a m e plausible w h e n several 9 Biologische Anstalt Helgoland, Hamburg

90

C. D. Zander, S. G r o e n e w o l d & U. Strohbach

authors investigated the single-host levels a n d their prevalences (MacKenzie & Gibson, 1970; Reimer, 1970; Koie, 1979, 1983; Z a n d e r et al., 1984) but there is still a lack of results about fishes or birds feeding on infested preys. Snarls, planktonic a n d b e n t h i c crustaceans, as well as gobiid fishes of the Liibeck Bight (western Baltic Sea), h a r b o u r e d at least 19 species of d i g e n e a n s , cestodans, nematodes, a n d a c a n t h o c e p h a l a n s (Zander et al., 1993). The aim of this i n v e s t i g a t i o n was to elucidate their life cycles a n d host changes. In order to calculate probabilities of infestation and losses during the process from one host to the next, two pathways of parasite d e v e l o p m e n t were chosen: the prey-predator systems of copepods a n d fishes for Cestoda, as well as g a m m a r i d crustaceans a n d fishes for Podocotyle atomon (Digenea) a n d Hysterothylacium sp. (Nematoda). The presentation of the whole h e l m i n t h f a u n a of crustaceans from the Lfibeck Bight is i n c l u d e d in order to get information a b o u t the relative importance of the single parasite species.

MATERIAL AND METHODS

The investigations were performed in 1989 and 1990 off Dahmesh6ved, Lfibeck Bight, where salinityfluctuated between 9 and 15 %0 (Zander et al.,1993). All the material was sampled (mainly by S C U B A dives) very close to a stony pier. The gobiid fishes Pomatoschistus minutus (Pallas),Pomatoschistus pictus (Malta), and Gobiusculus flavesceils (Fabricius)were collected in a depth of 3-6 m with large hand-nets, and fixed in 4 % formaldehyde immediately after the diving operation had ended. A total of 461 gobies were sampled. The fishes were dissected for analysing prey components from the intestinaltracts,as well as parasites from the same organ and from the body cavity. The prey was assessed to relevant taxonomic groups and measured with a microsize device to the nearest 0.1 m m allowing it to b e a r r a n g e d into size classes of 2 mm. The parasites were assessed to the species level (Zander et al., 1993) of which the following 4 were chosen for the p r e s e n t studies: Bothriocephalus sp., Schistocephalus sp. (Cestoda), Podocotyle atomon (Rudolphi) (Digenea), a n d Hysterothylacium sp. (cf. auctum [Rudolphi]) (Nematoda). Plankton sampies were o b t a i n e d every 2-4 weeks from May to N o v e m b e r 1989 by p o u r i n g in situ 100 1 seawater through a net of 55 ~tm mesh-size. T h e copepods were selected out of the p l a n k t o n samples, a n d transferred into a m e d i u m consisting of 70 % ethanol, 25 % water, 5 % glycerine a n d 1-2 drops of borax-carmine. The parasites t h e n b e c a m e clearly visible, b u t could only b e identified to the level of larval stages of cestodes or nematodes. In 1990, the overgrown walls of the pier were scratched with a P E - t u b e into which the detached aufwuchs of the Mytilus girdle was collected; this i n c l u d e d b e n t h i c crustaceans. The samples were fixed in 4 % formaldehyde. The potential p r e y organisms of gobiid fishes - in particular g a m m a r i d s - were separated from the aufwuchs, identified to the species level, m e a s u r e d as described above in order to arrange t h e m in 2-mm size classes, and dissected in order to find larval hehninths. The following parameters were u s e d (partly according to Margohs et al., 1982): A b u n d a n c e : the m e a n n u m b e r of parasites in all specimens of a host population. I n t e n s i t y : the m e a n n u m b e r of parasites in the infested specimens of a host p o p u l a tion,

Parasite transfer: c r u s t a c e a n to fish hosts

91

P r e v a 1 e n c e : the p e r c e n t a g e of the host population w h i ch is parasitized. I n f e s t a t i o n p o t e n t i a 1 (IP): the p r e v a l e n c e of prey c o m p o n e n t s in a distinct size class, multiplied with the p e r c e n t a g e of organisms of the same size class w h i c h w e r e i n g e s t e d by the predators; the v a l u e s of e v e r y size class w h e n s u m m e d up result in the IP of the respective fish host. It expresses the probability of a predator to be infested by parasites p r e s e n t in its prey. A v a i 1 a b 1 e p r e y : the p e r c e n t a g e of a size class of a p r e y c o m p o n e n t found in the aufwuchs samples. I n g e s t e d p r e y : the p e r c e n t a g e of a size class of a prey c o m p o n e n t found in the guts of predators. RESULTS Copepoda A m o n g planktonic copepods, Acartia bifilosa p r e v a i l e d over Oithona similis, Eurytemora hirundoides and Centropages h a m a t u s (Table 1). W h e r e a s O. similis w as not parasitized, the 3 other species bore cestode an d n e m a t o d e larvae (probably Hysterothylacium sp.).

Table 1. Mean densities and prevalences of planktonic copepods from Dahmesh6ved, 1989 Host species

Paracalanus parvus Centropages hamatus Temora longicornis Eurytemora hirundoides Acartia bifflosa Acartia discaudata Oithona simflis

Density (N 100 1 - 1 ) 0.5 21.6 8.9 31.3 78.6 1.8 60.0

Oncosphaerae

Prevalence (%) Procercoids

5.1

7.9

1,9 3,8

3.5 6.0

Nematoda

0.5 1.1 0.6 1.0

Cestode larvae w e r e most a b u n d a n t in J u l y 1989 (5 % of copepods w e r e infested with oncosphaerae, 8 % with procercoids) (Fig. la). Lower p eak s of infestation w e r e found in April (oncosphaerae only) a n d October. P r e v a l e n c e s c a u s e d by n e m a t o d e larvae i n creas ed continuously until 3 % in summer, but t h e n stopped abruptly (Fig. la). The population of copepods was low until A u g u s t but i n cr eased extensively in a u t u m n (Fig. lb). Gobiusculus flavescens fed regularly on planktonic copepods in m e a n quantities of ca 100. In contrast, Pomatoschistus m i n u t u s only fed on this prey c o m p o n e n t in late s u m m e r and a u t u m n (Fig. lb). W h e n the c o p e p o d p r e v a l e n c e s and the f e e d i n g rates of fishes w e r e co m b i n ed , the result was a high potential of infestation (IP) of G. flavescens and also of P. m i n u t u s by cestodes at least in October (Fig. 2). A b u n d a n c e and intensity of cestodes m u s t be considered as very low b e c a u s e in g e n e r a l 1 or, at the most, only 2 parasites w e r e found per infested fish host.

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Parasite transfer: crustacean to fish hosts

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Benthic crustaceans, especially Gammaridae Young Garnmarus of less than 4 rnrn size, which cannot be d e t e r m i n e d to the species level, a n d Jaera albifrons were the most a b u n d a n t b e n t h i c crustaceans (Table 2). Garnrnarus oceanicus a n d G. salinus developed large populations, w h e r e a s several Gamm a r i d e a species a n d Idotea balthica were less a b u n d a n t . Microphallus papillorobusturn was present in 9 hosts; 6 hosts h a r b o u r e d other rnicrophallids, acanthellae or I-Iytherothylaciurn sp., but only 4 Garnmarus spp. harboured the d i g e n e a n Podocotyle atomon. Idotea balthica was not infested in the investigation area. The benthic g a m m a r i d crustaceans were bigger t h a n copepods a n d could, therefore, be a r r a n g e d into several size classes. The g a m m a r i d s were infested b y Podocotyle atornon and three microphalhd d i g e n e a n s in May 1990 (Fig. 3a), b u t the smallest sizes were not parasitized - though they were the most a b u n d a n t . Prevalences of only 1% were attained by P. atomon in the size classes of 6, 8 a n d 14 mm, w h e r e a s rnicrophallids were spread a m o n g single size classes attaining there approx. 0.5 % (Fig. 3a). The gobies preferred smaller crustaceans of 2 to 6 mm; Pomatoschistus rninutus very occasionally selected some individuals of 8 or 10 m m (Fig. 3b). Therefore, Gobiusculus flavescens must have a c c u m u l a t e d its very large P. atomon populations from the 6-ram size group of the transmitter only. P. atornon a n d two of the microphallids v a n i s h e d in July - but, simultaneously, n e m a t o d e larvae, which might be Hysterothylacium sp., a p p e a r e d (Fig. 4a). G a m m a r i d s of a maximal 8 m m were infested by rnicrophallids, but smaller as well as larger

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C. D. Zander, S. G r o e n e w o l d & U. Strohbach

96

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Fig. 4. Gammarid crustaceans in the food and parasite web of the Lfibeck Bight in July, 1990; a: Prevalence of infestation by helminth larvae with regard to different-sized hosts; b: Percentages of available prey and that ingested by gobiid fishes with regard to size individuals h a r b o u r e d n e m a t o d e larvae. The size distribution of g a m m a r i d s i n July was b e t w e e n 2 a n d 1 2 r a m with a p e a k at 6 m m (Fig. 4b). Size classes infested with nematodes were ingested by P. minutus, b u t not by G. flavescens (Fig. 4b). The S e p t e m b e r samples r e v e a l e d a spectrum of 5 parasite species i n gammarids: Podocotyle atomon, acantheUae a n d n e m a t o d e larvae, a n d 2 microphallid species (Fig. 5a). Within a size-range of 2-16 mm, the most infested group w a s 8-ram-large

Parasite transfer: crustacean to fish hosts

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98

C. D. Zander, S. G r o e n e w o l d & U. Strohbach

g a m m a r i d s (Fig. 5b). W h e r e a s lVlicrophallus flapillorobustum a t t a i n e d a h i g h e s t p r e v a lence of 1.7 %, P. atomon w e r e only p r e s e n t in the 8-ram class with 0.5 % p r e v a l e n c e (Fig. 5a). N e m a t o d a w e r e found in g a m m a r i d s of 6-10 m m with only 0.3 % p r e v a l e n c e , a c a n t h e l l a e w e r e only p r e s e n t in the 4-ram group. A m o n g available crustaceans, two p e a k s in 4- a n d 8-ram size classes w e r e a p p a r e n t (Fig. 5b). Pomatoschistus Rictus fed only on 2 - 6 - r a m individuals, w h e r e a s P. minutus s e l e c t e d even 10-ram-sized ones. Therefore, P. atomon m i g h t only infest P. minutus in this m o n t h - if one r e g a r d s g a m m a r i d s as transmitters. All p a r a s i t e s found in S e p t e m b e r w e r e p r e s e n t in October, e x c e p t P. atomon (Fig. 6a). The p a r a s i t e s w e r e c o n c e n t r a t e d in the 4- to 12-ram size groups, only the n e m a t o d e s a p p e a r e d in 6- to 8-mm l a r g e - h o s t s only. The total r a n g e of g a m m a r i d s c o m p r i s e d 2-18 mm; the 4 - 8 - r a m classes w e r e p r e y e d on b y P. rninutus (Fig. 6b). Therefore, this g o b y might b e infested b y a c a n t h o c e p h a l a n s as well as b y n e m a t o d e s . The p a r a s i t e s p e c t r u m c o m p r i s e d 5 c o m p o n e n t s in N o v e m b e r 1990 (Fig. 7a). N e m a t o d e a n d a c a n t h o c e p h a l a n l a r v a e a t t a i n e d p r e v a l e n c e s of 0.2-1.0 % in g a m m a r i d s of 6 - 1 6 - m m size. However, this s a m p l e was d o m i n a t e d b y m i c r o p h a i h d s attaining a highest p r e v a l e n c e of 5 % (Fig. 7a). The g a m m a r i d s r a n g e d from 2 to 20 m m a n d p e a k e d in the 4-ram group (Fig. 7b). The gobies s e l e c t e d p r e y of 4-10 ram, w h i c h w e r e simnltaneously the m a i n transmitters of n e m a t o d e s a n d a c a n t h o c e p h a l a n s . T h e size class of 6 ram, w h i c h w a s p r e f e r r e d b y Pomatoschistuspictus a n d P. minutus, was n o t infested b y n e m a t o d e s (Fig. 7b). W h e n the infestation potential (IP) of Podocotyle atomon was c o m p a r e d with the a b u n d a n c e s a n d intensities of 3 g o b y species, clear differences b e c a m e a p p a r e n t (Fig. 8). The h i g h e s t indices w e r e 2 % - w h i c h m e a n s that 50 p r e y ingestions w e r e n e c e s s a r y to infest P. pictus with a parasite. P. minutus a n d P. pictus can b e infested twice during the y e a r (May, S e p t e m b e r ) ; therefore, small populations of parasites can b e f o u n d 2 months later (July, N o v e m b e r ) in these hosts. In G. flavescens, this infestion p o t e n t i a l w a s lacking, b e c a u s e it did not f e e d on infested crustaceans in S e p t e m b e r (Fig. 8). All 3 fish hosts w e r e e x t r e m e l y infested b y Podocotyle atomon in May; this m a y be c a u s e d b y the infestations in early spring. The transmission rates of Hysterothylacium sp. are lower than those of P. atomon. The infestation potential (IP) was, for P. pictus, h i g h e s t in S e p t e m b e r (0.8 %), a n d for P. minutus, in July (0.4 %) (Fig. 9). Also, intensities a n d a b u n d a n c e s w e r e v e r y low - a n d not c o m p a r a b l e with rates y i e l d e d from other fish hosts of this area. P r e y of g o b i e s The a b u n d a n c e analysis (% numbers) of p r e y r e v e a l e d several differences b e t w e e n the 3 g o b y species (Fig. 10). Pomatoschistus minutus p r e f e r r e d benthic c r u s t a c e a n s such as harpacticoids or g a m m a r i d s , but also some calanoids; Gobiusculus flavescens fed mainly on plankton, a n d to a lesser d e g r e e on gammarids, but n e v e r on h a r p a c t i c o i d s ; P. pictus s e l e c t e d plankton, b u t b e n t h i c crustaceans (including harpacticoids) w e r e also important; Idotea balthica w a s insignificant for all gobies; mussels w e r e o n l y i n g e s t e d b y P. minutus (Fig. 10).

99

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Parasite transfer: crustacean

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Parasite transfer: c r u s t a c e a n to fish hosts

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DISCUSSION Microphallids, especially Microphallus papillorobustum a n d Maritrema subdolum, w e r e the most i m p o r t a n t parasites of benthic crustaceans in the L u b e c k Bight. The course to their final hosts, i. e. birds, could not be p u r s u e d in this investigation. Better information on h e l m i n t h transfer w a s o b t a i n e d from the fish parasites. It s e e m s that the values of the infestation potential (IP) are relatively low. The calculation of this i n d e x was b a s e d only on one stomach filling, with r e g a r d to size selection b y the fish host. Actually, at h i g h e r t e m p e r a t u r e s , e v e n 3-3.5 fillings p e r d a y can b e a s s u m e d in gobies (Meyer-Antholz, 1986). By calculation of the reciprocal of IP, the lowest n u m b e r of stomach fillings n e c e s s a r y for infesting a host b y a parasite b e c a m e a p p a r e n t . The reciprocals of C e s t o d a IP in Gobiusculus flavescens differed clearly in April or O c t o b e r 1989 (513 or 16, respectively). Therefore, the probability of infestation was h i g h e r in a u t u m n t h a n in spring for the t w o - s p o t t e d goby. This also applies to Pomatoschistus minutus. In contrast, intensities of C e s t o d a w e r e very low in both hosts - as was a l r e a d y found during 1990 t h o u g h p r e v a l e n c e s of c o p e p o d s w e r e still h i g h e r (Zander et al., 1993). A l a r g e plerocercoid of Schistocephalus sp. can fill up the b o d y - c a v i t y of its goby hosts totally, a n d allows no competitor. In contrast, as m a n y as four Bothriocephalus sp. plerocercoids w h i c h live in the stomachs of gobies can b e found (Zander et al., 1993). A s e a s o n a l i n c r e a s e of procercoid p r e v a l e n c e s in c o p e p o d s (Gollasch & Zander, unpubl.) m a y also i n c r e a s e the infestation rates in the next host - as was found in the brackish Schlei fjord (Zander & Westphal, 1991; Kesting, 1992). A third tapeworm, Proteocephalus percae (often found in the Baltic), was a b s e n t at D a h m e s h b v e d in the Lfibeck Bight. The analysis of the g a m m a r i d hosts of Podocotyle atomon a n d Hysterothylacium sp. e m p h a s i z e s the i m p o r t a n c e of p r e y - s i z e for the infestation of the next hosts. Pomatoschistus minutus s e l e c t e d far smaller g a m m a r i d s than a v e r a g e from the s u p p l y a v a i l a b l e in the L~ibeck Bight (Zander, 1990). This p h e n o m e n o n can b e confirmed by the p r e s e n t study, a n d a p p l i e d also to P. pictus a n d Gobiusculus flavescens. Consequently, parasites which infest only g a m m a r i d s , or other e q u a l - s i z e d crustaceans, have less c h a n c e of b e i n g transferred to gobiid fishes. Whereas, formerly, only g a m m a r i d s of at least 9 m m w e r e found to h a r b o u r Podocotyle atomon m e t a c e r c a r i a e in the Liibeck Bight (Zander & Dbring, 1989), this size-limit has d e c r e a s e d to 5 m m (Zander et al., 1993). G a m m a r i d hosts infested b y Hysterothylacium sp. L3-1arvae m e a s u r e d at least 7 m m ( Z a n d e r & Dbring, 1989) or 4.5 m m (this study). T h e isopod Jaera albi[rons which s e l d o m e x c e e d s 4 m m (Zander, 1990) a l r e a d y h a r b o u r e d n e m a t o d e l a r v a e by the time it h a d r e a c h e d the size of 1.5 mm. In the Schlei fjord, northern Schleswig-Holstein, Idothea spp. a r e also first i n t e r m e d i a t e hosts of Hysterothylacium sp. (Gollasch & Zander, unpubl.). It is h i g h l y p r o b a b l e that n e m a t o d e larvae found in the p l a n k t o n of the Lfibeck Bight ( Z a n d e r et al., 1993; this study, Fig. 1) could also b e Hysterothylacium sp. larvae. Koie (1993) s h o w e d that L3-1arvae of this p a r a s i t e first infest several b e n t h i c and planktonic c r u s t a c e a n s a n d are t h e n transferred to the next hosts, i n v e r t e b r a t e s a n d fishes. The transmittance of t a p e w o r m l a r v a e from the first (copepods) to the s e c o n d :intermediate hosts (fish), d e p e n d s first a n d foremost on the w a y s of life of the r e s p e c t i v e g o b y species. W h e r e a s Gobiusculus flavescens forages on p l a n k t o n d u r i n g its w h o l e life, only P. minutus a m o n g the Pomatoschistus spp. has a l o n g e r p e l a g i c p h a s e until r e a c h i n g a size of 30 m m (Zander & Hagernann, 1986). The a b u n d a n c e analysis of p r e y in 1989 a n d

104

C. D. Zander, S. G r o e n e w o l d & U. Strohbach

1990 revealed also strong preferences for b e n t h i c components, especially harpacticoids a n d gammarids, by sand gobies; whereas isopods were less exploited. P. pictus fed on smaller crustaceans - as indicated by the selection of smaller g a m m a r i d s a n d greater quantities of Jaera and, in particular, calanoids. A lot of factors may influence the life cycles of parasites, as was d e m o n s t r a t e d in the e e l - n e m a t o d e Anguillicola crassus (De Charleroy et al., 1990). Prevalences of several hosts within the respective cycles were considered e.g. Podocotyle atomon (McKenzie & Gibson, 1970), or Cryptocotyle concavum in Pomatoschistus microps (Zander et aL, 1984). Size selection c o n c e r n i n g i n t e r m e d i a t e hosts m a y only b e important for parasite transfer, w h e n size differences of prey a n d predator are moderate, as is the case b e t w e e n gobies a n d gammarids. In the case of great differences, e.g. b e t w e e n gobies a n d copepods or birds and gammarids, the real IPs simply imply the prevalences b e c a u s e size selection is irrelevant. This applies to the transmittance of tapeworms to gobies, a n d probably of microphaUid flukes to birds (see Figs 3-7). The m i n i m a l quantity of parasites transmitted from one host to the n e x t seems to be high, following the results of this investigation. In reality, the quantity must be even larger, b e c a u s e there is a great loss of parasite stages d u r i n g the d e v e l o p m e n t a l cycles. However, in addition to gammarids m a n y other crustaceans can infest fishes with Podocotyle atomon, a n d Hysterothylacium sp. can be transferred by m a n y invertebrates (MacKenzie & Gibson, 1970; Svendsen, 1990; Koie, 1993; Gollasch & Zander, unpubl.). The general threat to the existence of a parasite is not b e i n g able to infest the optimal host where it can mature. Whereas P. atomon m a t u r e d in all gobies of the L~ibeck Bight, Hysterothylacium sp. only did so in the larger Gobius niger, b u t not in small goby species (Zander et al., 1993). Another d a n g e r for parasites is lethal d a m a g e to its host by mass infestation. If gobies were able to overcome g a m m a r i d s larger than 10 mm, the infestation rates w o u l d increase e v e n further. Zoarces viviparus s p e c i m e n w h i c h fed on more a n d larger g a m m a r i d s in the L/ibeck Bight were maximally infested by 405 Podocotyle atomon a n d 95 Hysterothylacium sp. (Zander, 1991). This parasite load m a y b e lethal for small gobies: maximal n u m b e r s found were 32 Hysterothylacium sp. in Gobius niger or 130 Podocotyle atomon in Gobiusculus flavescens (Zander et al., 1993). Thus, it is possible that prey selection can partially reduce the transmittance of parasites to less suitable hosts.

Acknowledgements. Thanks are due to Heiko Blessin, Barbara JanBen and Dr. Ri~diger Kock for their help during the diving operations, to Jbrg Melander for supplying the 1989 plankton sample, to Fran~oise Marie-Claire and to Carol Berger for improving the English text. LITERATURE CITED Charleroy, L. de, Thomas, K., Belpaire, C. & Ollevier, F., 1990. The life cycle of Anyuillicola crassus. Dis. aquat. Org. 8, 77-84. Esch, G. W., Gibbons, J. W. & Bourque, J. E., 1975. An analysis of the relationship between stress and parasitism.- Am. Midl. Nat. 93, 339-353. Esch, G. W., Shostak, A. W., Marcogliese, D. J. & Goater, T. M., 1990. Patterns and processes in helminth parasite communities. In: Parasite communities:patterns and processes. Ed. by G. W. Esch, A. O. Bush & J. M. Aho. Chapman & Hall, London, 19 pp. Kesting, V., 1992. Untersuchungen zur Parasitenfauna von Kleinfischen und Schnecken der Ostseef6rde Schlei. Dipl.-Arb., Univ. Hamburg, 183 pp.

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Koie, M., 1979. On the morphology and life-history of Derogenes varicus (Mfiller, 1784) Looss, 1901 (Trematoda, Hemiuridae). - Z. ParasitKde 59, 67-78. Koie, M., 1983. Digenetic trematodes from Limanda limanda (L.) (Osteichthyes, Pleuronectidae) from Danish and adjacent waters, with special reference to their life histories. - Ophelia 22, 201-228. Koie, M., 1993. Aspects of the life cycle and morphology of Hysterothylacium aduncum (Rudolphi, 1802) (Nematoda, Ascaroidea, Anisakidae). - Can. J. Zool. 71, 1289-1296. MacKenzie, K. & Gibson, D., 1970. Ecological studies of some parasites of plaice, Pleuronectes platessa (L.) and flounder, Platichtys flesus (L.). - Syrup. Br. Soc. Parasit. 8, 1-42. Margolis, L., Esch, G. W., Holmes, J. C., Kuris, A. M. & Schad, G. A., 1982. The use of ecological terms in parasitology (report of an ad hoc committee of the American Society of Parasitologists). J. Parasit. 68, 131-133. Meyer-Antholz, W., 1986. Untersuchung fiber Verdauungsraten, Fref~rhythmen und lokomotorische AktivitSten der Strandgrundel, Pomatoschistus microps (Kroyer) (Gobiidae, Pisces), und ihre A n w e n d u n g zur Bestimmung der Tagesration. Diss., Univ. Hamburg, 152 pp. Odening, K., 1974. Ontogenese und Lebenszyklus bei Helminthen und ihre Widerspiegelung in der Wirtsklassifikation. - Zool. Anz. 192, 67-78. Reimer, L. W., 1970. Digene Trematoden und Cestoden der Ostseefische als natfirliche Fischmarken. -Parasit. SchrReihe 20, 144 pp. Reimer, L. W., 1983. Zur Entstehung der Lebenszyklen bei digenen Trematoden und Cestoden. Wissensch. - Z. phdag. Hochsch. Gfistrow (Math.-naturwiss. Fak.) 2, 293-306. Svendsen, S., 1990. Hosts of third stage larvae of Hysterothylacium sp. (Nematoda, Anisakidae) in zooplankton from outer Oslofjord, Norway. - Sarsia 75, 161-I67. Zander, C. D., 1990. Prey selection of the shallow water fish Pomatoschistus minutus (Gobiidae, Teleostei) in the SW Baltic Sea. - Helgol8nder Meeresunters. 44, 147-157. Zander, C. D., 1991. Akkumulation von Helminthen-Parasiten in Aalmuttern. - Zoarces viviparus (L.) (Teleostei) der SW Ostsee. - Seev6gel 12, 70-73. Zander, C. D. & D6ring, W., 1989. The role of gobies (Gobiidae, Teleostei) in the food web of the shallow habitats of the Baltic Sea. In: Proceedings of the 21st European Marine Biology Symposium, Gdansk, 1986. Ed. by R, Z. Klekowski, E. Styczinska-Jurewicz & L. Falkowski. Polish Academy of Sciences, Institute of Oceanology, Wroclaw, 499-508. Zander, C. D. & Hagemann, T:, 1986. Fluctuations of prey, abundance and biomass of gobies (Gobiidae, Pisces) in a shallow habitat of the western Baltic Sea. - Zool. Anz. 216, 289-304. Zander, C. D. & Westphal, D., 1991. Kleinfischparasiten der Ostseef6rde Schlei und ihre Einbindung in die Nahrungskette. - Seev6gel 12, 4-8. Zander, C. D., Kollra, G., Antholz, B., Meyer, W. & Westphal, D., 1984. Small-sized euryhaline fish as intermediate hosts of the digenetic trematode Cryptocotyle concavum. - Helgol~nder Meeresunters. 37, 433-443. Zander, C. D., Strohbach, U. & Groenewold, S., 1993. The importance of gobies {Gobiidae, Teleostei) as hosts and transmitters of parasites in the SW Baltic. - Helgol~nder Meeresunters. 47, 81-111.