Parasite communities of the Schlei Fjord (Baltic coast of ... · Parasite communities of the Schlei Fjord (Baltic coast of northern Germany) V. Kesting, S. Gollasch & C. D. Zander*

HELGOL.$NDER MEERESUNTERSUCHUNGEN Helgol~nder Meeresunters . 50, 477-496 (1996)

Parasi te c o m m u n i t i e s of the Sch le i Fjord

(Baltic coast of n o r t h e r n G e r m a n y )

V. Kesting, S. Gollasch & C. D. Zander*

Zoologlsches Institut und Zoologisches Museum der Universitfit; Martin-Luther-King-Platz 3, D-20146 Hamburg, Germany

ABSTRACT: The parasite faunas of snails, mussels, crustaceans and small-sized fishes were investigated over a period of six months in the Schlei fjord, on the Baltic coast of Schleswig-Holstein. Two sites differing in salinities were compared: Missunde with 5-9 %o and Olpenitz with 12-20 %~ Pre- valences, number of host-parasite combinations, numbers of core and secondary species were generally higher in Olpenitz than in Missunde. In the latter site, only prevalences of cestodans in planktic copepods and the number of rare species were apparent . Specificity of parasites was relatively high in snails, mussels and fishes, but lower in benthic crustaceans. Parasites may survive in an extreme envi ronment like brackish water by means of special strategies which differ from those ac- quired in the marine milieu: suspension of specificity, adaptat ion to hosts which are genuine brackish water species, extension of host spectra, and shortening of life-cycles. Although the parasi te communities of the Schlei fjord were primarily influenced by the prevailing salinities, the influence of other factors, e.g. environmental stress, was also confirmed. Whereas generally low prevalences in Missunde may contradict Thienemann 's biocoenotic rule. planktic parasites infested their hosts often at higher rates than in Olpenitz. This phenomenon is explained by the poorer envi ronmenta l condition of the ben tha l zone in Missunde compared to that of the pelagial or the bentha l zones of Olpenitz.

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

T h e Sch le i f jo rd in n o r t h e r n S c h l e s w i g - H o l s t e i n h a s b e e n i n t e n s i v e l y i n v e s t i g a t e d in

r e g a r d to t he c o m m u n i t i e s of b e n t h o s , p l a n k t o n a n d n e k t o n (Nel len , 1967; R h e i n h e i m e r ,

1970; Schr i eve r , 1974; Del l ing , 1975). T h e S c h l e i is a b r a c k i s h - w a t e r a r e a w h i c h e x t e n d s

for 42 k m f r o m S c h l e s w i g w h e r e sa l in i t i e s a r e 0 %o to t h e in f lux in to t h e Bal t ic S e a w i t h

15 -18 %0 (Fig. 1). Add i t iona l ly , t h e w a t e r s a r e s e v e r e l y p o l l u t e d b y t h e w a s t e - p r o d u c t s of

f a r m i n g w h i c h c a u s e a p e r m a n e n t e u t r o p h i c a t i o n w i t h r e g u l a r p h y t o p l a n k t o n b l o o m s in

s p r i n g a n d s u m m e r ( R h e i n h e i m e r , 1970) a n d l a r g e m u d d e p o s i t i o n o n t h e b o t t o m .

T h e ab io t i c f ac to r s m e n t i o n e d g ive r ise to a r i ch h e r b i v o r o u s a n d d e t r i t i v o r o u s f a u n a

w h i c h is e x p l o i t e d b y s e v e r a l s m a l l f i sh s p e c i e s ( S c h m i d t - M o s e r & W e s t p h a l , 1981; A n t -

ho lz e t al., 1991; Z a n d e r & W e s t p h a l , 1992). T h e e x t r e m e c o n d i t i o n s of b r a c k i s h w a t e r s

a r e r e s p o n s i b l e for a s p e c i e s - p o o r b u t i n d i v i d u a l - r i c h f a u n a , e s p e c i a l l y in t h e m i d d l e p a r t

of t h e S c h l e i w h e r e sa l in i ty is on ly 6 - 8 %o. Th i s c o r r e s p o n d s to t h e si te of s p e c i e s min i -

m u m a c c o r d i n g to R e m a n e (1958) a n d fo l lows t h e l a w of T h i e n e m a n n (1939) b e c a u s e low

sa l in i t i e s m e a n e x t r e m e ab io t i c c o n d i t i o n s for b o t h m a r i n e as we l l as l i m n e t i c o r g a n i s m s .

* Addressee for all correspondence

�9 Biologische Anstalt Helgoland, Hamburg

478 V. Kesting, S. Gollasch & C, D. Zander

KAPPELN

t I Sk in

~ O L P E N I T Z - -

_ OSTSEE

Fig. 1. Map of Schleswig-Holstein (inset) and of the Schlei fjord (enlarged) presenting the sampling sites of Missunde and Olpenitz. Ostsee = Baltic Sea. From Zander & Westphal (1991)

Recent parasitological investigations in the Schlei fjord concentrated on single parasites in regard to their prevalences and life-cycles (Zander et al., 1984; Kreft, 1991), or on species compositions in single host groups (Wendland, 1985; Zander & Westphal, 1991; Gollasch, 1992; Kesting, 1992; Gollasch & Zander, 1995). The present s tudy under takes a synthesis of parasite communit ies of several host groups with the aim of analys ing the compound communi ty of this area in the sense of Esch et al. (1990). The quest ion as to how different salinities such as those encountered in the Schlei fjord inf luence the species composit ion and prevalence of the respective parasite communit ies was of special interest. For the analysis the groups of snails, mussels, crustaceans and fishes were considered. These are primary, secondary or final hosts and, additionaily, represent groups of different mobility. Another aim of this study was to elaborate the ma in hosts within the cycles of he lminth parasites. It may be assumed that in extreme habitats like brackish waters other hosts are preferred than are preferred in the mar ine milieu.

SAMPLING SITES, MATERIAL AND METHODS

Samples were taken at two sites of the Schlei fjord which clearly differ in their prevail ing salinities. "Missunde" is located at the influx of the "Ornumer Noor" into the "Missunde Enge" (Fig. 1), present ing salinities of 5-9 %o. "Olpenitz" lies at the southern

Parasite communit ies of the Schlei Fjord

Table 1. Compilation of host species from the Schlei fjord

479

GASTROPODA Hydrobia ulvae (Pennant) H. stagnalis Baster FI. neglecta Muus Littorina saxatilis (Olivi) L. s. tenebrosa Montagu L. littorea (L.) L. obtusata (L.)

BIVALVIA Mya arenana L. Mytilus edulis L. Cerastoderma edule (L.) C. aculeatus (Reeve)

PISCES Pomatoschistus microps Kroyer P. minutus (Pallas) Gasterosteus aculeatus L. Pungitius pungitius (L.)

COPEPODA Temora longicornis Mfiller Eurytemora affinis (Poppe) E. hirundo Giesbrecht Acartia tonsa Dana Oithona similis Claus

AMPHIPODA Gammarus duebeni Liljeborg G. zaddachi Sexton G. locusta L. Microdeutopus gryllotalpa Costa Corophium insidiosum Crawford

ISOPODA Jaera albifrons Leach Motea chelipes Pallas I. baithica Pallas Sphaeroma rugicauda Leach S. hooked Leach

DECAPODA Crangon crangon L.

edge of the "Olpeni tzer Noor" and attains salinities of 12-20 %o.

The samples were taken every four weeks from April to September 1991 and combi-

ned plankton, benthos, fishes and, additionally, phyton in Olpenitz. Plankton was extracted from 100 1 water which was poured through a net of 55 p m meshsize. Most of the

benthos and all fishes were sampled by means of large hand nets with 2-5 m m meshsize which were drawn fast over the bottom. Snails were extracted from the bot tom by means of a corer with an opening of 10 cm 2. Phytal fauna was obtained only in Olpenitz, by

loosening Fucus ves iculosus thalli from the substrate, and transferred under water into a

10 1 PVC box. Snails and phytal fauna were t ransported alive to the laboratory; benthos and plankton were fixed in 70 % ethanol, fishes in 4 % Formalin.

All potent ia l hosts were de te rmined to the species level and carefully examined by means of a s tereomicroscope in order to find parasites. The most important hosts are com-

piled in Table 1. Parasites were separa ted from their hosts and treated with lactic acid in order to clear organs for determination.

The following parameter and index were used. Preva lence = part of a host population which was infested by a specific parasite. In most cases, the mean p reva lence was

calculated from the prevalences of the six samples col lected during the invest igat ion period. Only in four selected digeneans, which were conspicuously abundant in two or three

different hosts, were the monthly p reva lences p resen ted separately. In order to eva lua te the impor tance of the infestation rates the core-satel l i te concept of Holmes & Price (1986)

was used: core species = preva lence > 60 %; secondary species = 40-60 %; satelli te spe-

480 V. Kesting, S. Gollasch & C. D. Zander

DIGENEA Podocotyle atomon Asymphyllodora demeli Hirnasthla interrupta Microphallus claviformis M. papillorobustum Maritrema subdolum Cercaria microphallidarum no. 4 Diplostomum spathaceum Cryptocotyle concavum C. lingua Brachyphallus crenatus Hemiurus communis Magnibursatus caudofilamentosa Psilochasmus oxyurus Psilostomum brevicolle Acanthostomum imbutiforme Mesorchis denticulatus Cercaria ephemera

TURBELLARIA Paravortex cardii Explanations: M = Missunde O = Olpenitz Oe = Oehe-Schleim0nde * KREFT (1991); # WENDLAND (1985)

Snails, Snails, 1. int. 2. int. host host

Mussels Plankto- Benthic Fishes Birds nic crus- crusta- taceans ceans

, : O "

O M IIIIIIlItllllllltllltll~ N~ ~

I g@~r . . . . ~ ~y

0

0 M # ~ 0 j: . ~ O ' O

O

O M # O # O #

0 M #

M* O'M*

1. intermediate host 2. intermediate host

IIIIIIIIIIIIIIl!!llli 13. intermediate host ~N~r Finat host I

Fig. 2. Compilation of digenean and turbellarian parasite life-cycles and their presence at different host levels. The respective evidence was gained by former and present investigations in the Schlei

fjord and is marked accordingly

cies = 5-40 %; rare species = prevalence < 5 %. The specificity index (SI, Rohde, 1982) was calculated as:

x (i,j) x (i, j) SI = s + Y . - -

n (j) h (i,j) n (j) where x(i,j) = n u m b e r of parasite specimen of species i in host species j; n (j) = n u m b e r of host specimen of species j; h (i,j) = range of host species j infested by parasite i.

RESULTS

Prevalences and cycles

In total, 33 diverse parasites represent ing eight taxonomic classes were found dur ing present and former studies in the Schlei fjord (Figs 2, 3) (Wendland, 1985i Kreft, 1991; Zander & Westphal, 1991). The most important group were digeneans , compris ing as many as 18 species (Fig. 2), followed by acanthocephalans with 5 species (Fig. 3). The ment ioned studies, when combined, were able to pursue complete life-cycles of six digeneans, but the development of Podocotyle atomon was the only complete one in the

Parasite communit ies of the Schlei Fjord 481

CESTODA Hymenolepis sp. Schistocephalus sp. Proteocephalus percae

NEMATODA Pseudanisakis truncata ,,Hysterothylacium sp.

ACANTHOCEPHALA Polymorphus botulus Acanthocephalus sp. Corynosoma sp. Pomphorhynchus laevis Neoechinorhynchus rutili

COPEPODA Thersitina gasterostei Caligus lacustris

MICROSPORIDIA

Plankto- Benthic Mussels Fishes Fishes nic cru- crusta- (interm. (final

staceans ceans hosts) hosts)

M O? M? O? M?

iii!i!iii!ii~!M!i!i!i!i!i!i!

M I iili! i'!~i~!i~!iii[~i i!iiii~

Seals Birds

0 M ~!!j:[i i~!! ii iiii~iiii ii O ~":~:~ :: ii~ ~ ~

: O iiii!:~iii~iiiii:-i~!iii!i[ ~",ii i:iiiili;',i ~:!i

Glugea anomala 0 M O M

MYXOSPORIDIA Henneguya sp. 0 * M *

Explanations: 1. in termedia te host

[ ; : 12. in termedia te host [!~i!~ii: '~:ii:~i,!~ii:i i4~;~ii: ~, F i nal h o st I

M = Missunde O = Ofpeni tz * ZANDER & WESTPHAL (1991)

Fig. 3. Compilation of parasite life cycles of diverse groups and their presence at different host levels. The respective evidence gained by earlier and present investigations in the Schlei fjord is

marked accordingly

present study. The description of infestation follows the five different host groups: snails, mussels, planktic and benthic crustaceans, and fishes (Figs 4-8).

The snails were represented by Littorina spp. in Olpenitz and Hydrobia spp. in O1- penitz as well as in Missunde. Infestation by d igeneans was found only in Olpenitz (Fig. 4). Highest prevalences (more than 20 %) were caused by the microphallids Micro- phallus claviformis and Maritrema subdolum in Hydrobia spp. Lower values were attain- ed by Podocotyle atomon and Psilochasmus oxyurus in Littorina spp.; Cryptocotyle concavum and the other three parasites were of lesser importance (Fig. 4). Some Hydrobia specimens harboured not only cercariae but also metacercariae of M. daviformis and M. subdolum which indicate their role as 1. as well as 2. in termediate host.

Four mussel species were investigated, but only Cerastoderma edule was present in Olpenitz as well as in Missunde and infested by the turbel lar ian Paravortex cardii (Fig. 5). The d igenean Himasthla interrupta which at ta ined prevalences of 1-6 % was the most important parasite of mussels, whereas Asymphyllodora demeli played a less conspicuous role (Fig. 5).

CO

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Fig

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val

ence

s of

sn

ail

par

asit

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rom

tw

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of

the

Sch

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fjor

d. T

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nd

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tern

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86):

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ht

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lite

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.<

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0)

(0)

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107

177

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Par

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Fig

. 5.

Pre

val

ence

s of

mu

ssel

par

asit

es f

rom

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ites

of

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):

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96

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1968

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Fig

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s of

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atel

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lpen

itz p

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n,

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= O

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itz b

enth

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sund

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ntho

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Mar

itrem

a su

bdol

urn

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roph

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avifo

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pillo

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H

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tero

thyl

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m s

p.

Aca

ntho

ceph

alus

sp.

P

olym

orph

us b

otul

us

Hos

t spe

cies

and

site

; O

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enitz

phy

ton,

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B =

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enitz

ben

thos

, M

= M

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bent

hos

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Fig

. 7.

P

rev

alen

ces

of p

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ites

of

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thic

cru

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ean

s fr

om

tw

o si

tes

of t

he

Sch

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fjor

d. T

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dif

fere

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kg

rou

nd

p

atte

rns

mar

k t

he

val

ues

ac

cord

ing

to

th

e co

re-s

atel

lite

-sp

ecie

s co

nce

pt

(Ho

lmes

& P

rice

, 19

86):

w

hit

e =

rare

sp

ecie

s,

ligh

t =

sate

llit

e sp

ecie

s,

med

ium

=

seco

nd

ary

sp

ecie

s, d

ark

= c

ore

spec

ies


Host species and site; P. P. P. P. M = Missunde mi- mi- mi- mi- O = Olpenitz crops crops nutus nutus

(M) (O) (M) (O)

N 101 194 72 2

Podocotyle atomon 2 i i: ! Brachyphallus crenatus Hemiurus communis Diplostomum spathaceum 0.4 Cryptocotyle concavum (kidney cysts) 10 83~ ii Cryptocotyle concavum (dermal cysts) 2 15 1 Magnibursatus caudofilamentosa Proteocephalus percae 8 0.3 Schistocephalus sp. 2 1 0.6 Hysterothylacium sp. 2 1 Corynosoma sp. 12 3 Pomphorhynchus laevis Thersitina gasterostei Glugea sp.

G. G. P. P. acu- acu- pun- pun-

leatus leatus gitius gitius (M) (O) (M) (O)

33 40 1 57

2 5 2 ~ o 6 , 2

11 8

2 35 14

3 5 4

8

19 ii!:.!:~!i!]i ~ i ~ i . 16 3 5

Fig. 8. Prevalences of parasites of small-sized fishes from two sites of the Schlei fjord. The different background patterns mark the values according to the core-satellite-species concept (Holmes & Price, 1986): white = rare species, light = satellite species, medium = secondary species, dark = core

species

Planktic hosts comprised four calanoid and one cyclopoid copepod species which were infested in Olpenitz as well as in Missunde (Fig. 6). They were parasitized by early developmenta l stages of cestodans which were not determinable . Probably, they were larvae of Schistocephalus sp. and/or Proteocephalus percae which were found in fishes, their 2. in termediate hosts (Fig. 8). It was conspicuous that prevalences of copepods seem- ed to be higher in Missunde than in Olpenitz (Fig. 6).

Benthic crustaceans comprised 11 species and, therefore, were the largest host group (Fig. 7). They were 1. or 2. intermediate hosts of several helminths. Microphallid digeneans, especially Niaritrema subdolum, at tained the highest prevalences (63 % max.) in as many as 10 hosts in Olpenitz and three in Missunde. Idotea chelipes which harboured 6 parasites, and Sphaeroma hookeri with 5 parasites were further important hosts (Fig. 7). Gammarus spp. were not only infested by the bird parasites Microphallidae but also in high prevalences by Podocotyle atomon which lives in fishes as final hosts. Remarkably, Crangon crangon harboured this parasite, too. Not only microphallids were found in Mis- sunde but also the less specialized nematode Hysterothylacium as well as the cestodan Hymenolepis which was only found in Gammarus zaddachi (Fig. 7).

The host group fishes comprised two gobies and two sticklebacks. They harboured as many as six d igeneans and seven other parasites (Fig. 8). The highest prevalences were at ta ined by Cryptocotyle concavum, Thersitina gasterostei and Podocotyle atomon at the Olpenitz site. Thersitina gasterostei, C. concavum, Proteocephallus percae and Pomphorhynchus laevis dominated in Missunde where clearly lower prevalences than in Olpenitz prevailed. C. concavum appeared as metacercar iae cysts in the kidneys of gobies or in the skin of gobies as well as sticklebacks. The intensities of cysts clearly

4 8 6

/

V. K e s t i n g , S. G o l l a s c h & C. D. Z a n d e r

1.1H

%

o A. M. J. J. A. S.

Prevalence of P. atomon in L. saxalil/s

%

Prevalence o! P. alomon in lishes

FH ! J

C

6 %

Prevalence of ,~ alomon in Crustacea

Fig. 9. Life-cycle of Podocotyle atomon p r e s e n t i n g m o n t h l y p r e v a l e n c e s in Olpen i t z o v e r s ix m o n t h s at all t h ree hos t levels�9 Exp lana t ions : C = cercar ia , E = egg , FH = final host, IH = i n t e r m e d i a t e host ,

M = m i r a c i d i u m

P a r a s i t e c o m m u n i t i e s of t h e Sch le i F jord 487

/

(?. 0 M

-.... t0 %

in /-I slagnal/s

I. IH

t.,

A. ~ . J. J. X. . Prevalence of C. concavum

in ~ re~crops ( kidneys )

% I O0 I

A. M. J. J. A. S.

Prevalence of C. concavum

in fishes ( skin )

Fig. 10. Life-cycle of Cryptocotyle concavurn present ing monthly prevalences in Olpenitz over six months at two host levels. Explanations see Fig. 9.

l

V. Kes t ing , S. Go l l a s ch & C. D. Z a n d e r

/

3 %

1

0 i i i i i

A. M. J. J. A. S.

Prevalence of M, clavitorm/s in Crustacea

30 % 2o~ Io

~ ~ 3 ~. k. _ Prevalence of M. subdo/um in Crustacea

488

J

/ /

1./2. IH

%

A

Prevalence o! /l,,f clav//orm/s

in /-/stagnal/s

%

A. M. J. J. ,~. S.

Prevalence of A~. subdolum

in H sfagnal/k

\ \ \ \

cMO C i:

2. IN

! CMS

Fig. 11. Life-cycles of Micropl~allus claviformis and Maritrema subdolum present ing monthly prevalences in Olpenifz over six months at two host levels. For explanations see Fig. 9 and, additionally:

CMC = cercaria of Microphallus claviformis CMS = cercaria of Maritrema subdolum.

Tab

le 2

, C

om

par

iso

n o

f p

aras

ite

spec

ies

spec

tra

at f

ive

ho

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om

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ites

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the

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he

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p <

5 %

)

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t p

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Ex

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siv

ely

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y

Ex

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siv

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y

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t p

ara

site

O

lpen

itz

Mis

sun

de

sp

p,

Olp

enit

z M

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enit

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itz

spp

, O

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itz

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. sp

p.

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17

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Table 3. Comparison of parasite prevalences at two sites of the Schlei fjord. The higher prevalences in Olpenitz are significant (p < 1%)

Joint host- parasite

combination

Fishes 11 Benthic crustaceans 8 Copepods 2 Mussels 1 Snails 0

Sum 22

Equal Prevalence Prevalence prevalences higher in higher in

Olpenitz Missunde

2 7 2 1 6 1 2

1

5 14 3

differed in these two microhabitats: In P. microps as many as 2000 k idney cysts were found in a specimen, whereas maximally 17 dermal cysts were found in Casterosteus aculeatus. Adult flukes of P. atomon were found in the middle or hind part of the intestine with maximally 100 specimens. Remarkably, Diplostomum spathaceum appeared exclusively in Missunde, whereas Brachyphaflus crenatus and Proteocephalus percae at tained larger prevalences in this site than in Olpenitz (Fig. 8).

Some of the most a b u n d a n t d igeneans could be analysed regarding their fluctuations in diverse hosts during the course of half a year. P. atomon was found in Littorina saxatilis (1. in termediate host), benthic crustaceans (2. intermediate hosts) and fishes (final hosts) (Fig. 9). The prevalences of this parasite peaked in Littorina and benth ic crustaceans in June as well as in August /September . Nearly all fishes were infested in May; thereafter prevalence decreased to zero by September.

Cryptocotyle concavum at tained peaks in Hydrobia stagnafis (1. in termedia te host) in June and a still larger one in August (Fig. 10). All Pomatoschistus microps, the main 2. in termediate host, were infested dur ing the whole year by kidney cysts with the ex- ception of July when prevalences lay below 100 %,. Dermal cysts were less f requent but a t ta ined similar values in all four fish hosts dur ing April to August, becoming rarer in Sep- tember (Fig. 10). Prevalences of the microphallids Maritrema subdolum a nd Microphal- lus daviformis were extremely high in their 1. in termediate host HydroMa stagnalis with more than 30 % in late summer (Fig. 11). The increase of infestation be ga n earlier (July) in M. subdolum than in M. daviformis which peaked in August in the 2. in termediate hosts, benthic crustaceans. In comparison with M. subdolum, the prevalences at ta ined by M. daviformis in benthic crustaceans were very low and fluctuated dur ing the half year (Fig. 11).

A n a l y s i s of s i tes a n d c o m m u n i t i e s

The differences be tween the parasite faunas of Olpenitz (30 species) a nd Missunde (20 species) were not extremely great because 17 parasites were present at both sites (Table 2). Subsequently, only 3 (Diplostomum spathaceum on Pomatoschistus microps, Pomphorhynchus laevis on Gasterosteus aculeatus, Hymenolepis sp. on Gammarus zaddachi) were exclusively present in Missunde at low salinities, whereas 13 combinat ions were characteristic for Olpenitz.


Table 4. Comparison of the dominances of paraslte-i~ost combmahons at two sites of the Schlei fjord according to the core-satellite-concept (Holmes & Price, 1986). The differences between the sites are

highly significant (p ~ 0.1%)

Olpenitz/Missunde

Core Secondary Satellite Rare Host-parasite species species species species combinations

O M O M O M O M O M

Fishes 2 0 4 0 9 5 5 12 20 17 Benthic crustaceans 1 0 3 0 17 4 12 6 33 10 Copepods 0 0 0 0 0 1 3 3 3 4 Mussels 0 0 0 0 2 0 4 1 6 1 Snails 0 0 0 0 8 0 10 0 18 0

Sum 3 0 7 0 36 10 34 22 80 32

Parasites from Olpenitz phyton which were not found in the benthos were rare spe-

cies such as Acanthocephalus sp. in Idotea chelipes and Polymorphus botulus in Sphaeroma hookeri, or first host specialists such as Podocotyle atomon and Psilochasmus oxyurus in Littorina spp.. This group of first host specialists is also decisive for 3 d igeneans present in HFdrobia spp. from the benthos only (Table 2).

A comparison of prevalences of parasites in the two sites may reveal further differences (Table 3). Four teen out of 22 joint host-parasite combinations a t ta ined higher

values in Olpeni tz but only three were of h igher p reva lences in Missunde: Proteoce- phalus percae/Poma toschistus microps, Brachyphallus crena tus/ Gasterosteus aculea tus, Maritrema subdolum/Jaera albifrons. Five combinations were considered to be similar in the two sites: cestode larvae in copepods, Hysterothylacium sp. and Schistocephalus sp.

in Pomatoschistus microps and Microphallus papillorobustum in Sphaeroma hookeri. Totally, 80 parasi te-host combinations were found in Olpeni tz but only 32 in Mis-

sunde (Table 4). Three of them were core species of more than 60 % preva lence which occurred only in Olpenitz: Cryptocotyle concavum (kidney cysts)/Pomatoschistus microps, Thersitina gasterostei/Gasterosteus aculeatus and A/laritrema subdolum/ Mothea chelipes. Also secondary species with 40-60 % preva lence were not present in Missunde but occurred in 7 combinations from Olpenitz: Podocotyle atomon in Pomato- schistus microps, Gasterosteus aculeatus and Pungitius pungitius; Cryptocotyle concavum (dermal cysts) in Gasterosteus aculeatus; Maritrema subdolum in Gammarus zaddachi, Mothea balthica and Sphaeroma hookeri. Despite genera l ly low preva lences in Missunde some of the 10 satellite species of this site are worth mentioning: these were

fish-infesting parasites which represent core species in Olpenitz. Contrarily, the main

hosts of Maritrema subdolum changed in Missunde: Jaera albffrons, Sphaeroma hookeri and S. rugicauda, the latter being a secondary species in Olpenitz.

The specificity index (Rohde, 1982) revea led parasite specialists, especial ly in snarls and fishes, as wel l as generalists, especial ly in benthic crustaceans (Table 5). The only ex-

ception regard ing snail parasites is Maritrema subdolum which at tained a low index of 0.86. All D igenea and Hysterothylacium sp. a t ta ined values of below 0.84 in benth ic crus-

taceans; Maritrema subdolum again p resen ted the min imum (0.68). Only Ces toda and

Acanthocepha la a t ta ined indices of 1 because they were present in only one host species


Table 5. Specificity indices {Rohde, 1982) regarding parasite prevalences in single hosts and host communities IS (comm.)]

S (prev.) < 0.71 0.71-0.80 0.81-0.90 0.91-0.95 0.96-1.00 N S (comm.)

Fishes 1 4 2 6 13 0.93 Benthic crustaceans 1 2 2 3 8 0.86 Plankton t 1 0.91 Mussels 1 2 3 0.93 Snails 2 2 4 8 0.95

Sum 2 2 9 7 13 33 0.92

with low prevalences. The fish parasites partially were specialists like Cryptocotyle concavum (kidney cysts) or, to a lesser degree, Thersitina gasterostei and Schistocephalus sp. Generalists were Podocotyle atomon (index = 0.69), Cryptocotyle concavum (dermal cysts; = 0.84) and Hysterothylacium sp. (= 0.84). The benthic crustaceans presen ted the lowest specificity; the snails a t ta ined the highest values of the 5 host groups (Table 5).

DISCUSSION

H o s t - p a r a s i t e r e l a t i o n s h i p in t he b r a c k i s h e n v i r o n m e n t

Parasitism is characterized by the peculiarity that the existence of parasites does not depend on the direct envi ronmenta l effects only but also on those effects which limit the distribution of their hosts. The compound communit ies (Esch et at., 1975) invest igated in the Schlei fjord were especially rich in hosts that are called genu ine brackish-water species, e.g. Pomatoschistus microps, or euryhal ine species like Gasterosteus aculeatus (Remane, 1958). The parasite's problem may be its adaptat ion to brackish water, even when its ma in host of the mar ine envi ronment is absent. Consequently, two al ternatives are possible: Dominance of parasites without complicated life-cycles, e.g. Thersitina gasterostei and, if complete cycles are performed, presence of generalists which do not prefer special hosts, e.g. Hysterothylacium sp. The large n u m b e r of 18 d igeneans found in the Schlei fjord combined with lower numbers of less specialized cestodes, nematodes and acanthocephalans or parasites without cycles seems to contradict this assumption.

Strategies which may help to adapt parasites to the brackish env i ronmen t and its community can be compiled in 4 points:

1. Suspension of specificity. For instance, the copepod Thersitina gasterostei clearly prefers Gasterosteus aculeatus to Pungitius pungitius in mar ine and freshwater, but not in the brackish-water milieu of the Elbe and Eider rivers (Mbller-Buchner, 1987). Podo- cotyle atomon was found especially in Littonna saxatilis in the North and Baltic Sea (MacKenzie & Gibson, 1970; Zander et al., 1993). L. littorea which was also an important 1. host in the Schlei fjord was only very seldomly infested in the North or open Baltic Sea (Werding, 1969; Lauckner, 1984). Kidney cysts of Cryptocotyle concavum in its ma in host Pomatoschistus microps indicate a specialized coevolution (Zander et al., 1984) which was not found in P. minutus in the W Baltic (Zander et al., 1993) but was found in the Schlei fjord (Kreft, 1991). Kennedy (1975) interpreted the p h e n o m e n o n of specificity

Parasite communi t ies of the Schlei Fjord 493

breakdown as alteration of host suitability or as reduced immune defence under stress conditions.

2. Adaptat ion to hosts which are genu ine brackish-water species. Pomatoschistus microps, Gammarus zaddachi, Idotea chelipes and Hydrobia stagnalis are genu ine brackish-water species represent ing the host levels - fishes, benthic crustaceans and snails - in the Schlei fjord. These species were also conspicuous in that they harboured the most parasite species. This t rend has already been recorded (Wendland, 1985; Kreft, 1991; Zander & Westphal, 1991; Gollasch & Zander, 1994). Contrarily, Pomatoschistus mmutus, Gammarus locusta and Hydrobia ulvae were the most important hosts in the Lfi- beck Bight (W Baltic Sea with more than 10 %o salinity) (Zander et al., 1993, 1994; Stroh- bach pers. comm.). Gammarids which play this role in the Kiel Bight are Gammarus ocea- nicus and G. salinus (Voigt, 1991). Genu ine brackish-water species such as the isopods Sphaeroma hookeri and S. rugicauda were, in addit ion to Jaera albifrons, the only benthic crustacean hosts in Missunde. This site of low salinity creates a characteristic section of the "species min imum" (Remane, 1958) in the Schlei fjord. The results of this investigation emphasize the adaptat ion of parasites to an extreme brackish-water milieu such as that in the Schlei fjord. The stress caused by brackish water may be he ightened by a steep decrease and sudden fluctuations of salinity.

3. Extension of host spectra. The shrimp Crangon crangon as host for d i g e n e a n parasites was first observed in the Schlei fjord (Podocotyle atomon: Gollasch & Zander, 1995) and, thereafter, at other sites of the W Baltic (Microphallidae: Gollasch et al., 1996). Helminths have not been detected in the North Sea shrimp populat ion where shrimps are of high commercial importance and have been intensively invest igated (Tiews, 1954). The abundance of C. crangon in the shallow sand bottoms of the W Baltic Sea is generally as high as in the North Sea (Winkier, 1994) and, therefore, this species may be an ideal alternative host for diverse helminths in order to guarantee an accomplishment of their life-cycles. Another example is the microphallid d igenean Maritrema subdolum which is a genu ine brackish-water species that is able to extend its spectrum of final hosts to fish-eating birds by using fish as 3. in termediate or transport hosts (Reimer, 1963).

4. Shortening of life-cycles. The genu ine brackish-water parasites, Microphallus daviformis and Maritrema subdolum, developed a different strategy to reach their final bird hosts. Because their cercariae can encyst in their 1. hosts - snails (Deblock et al., 1961; Reimer, 1963) - as also found in this investigation, they can miss out the second-host level - the crustaceans. This strategy is widely distr ibuted among microphallid d igeneans and is most perfectly developed by Microphaflus pygmaeus (Werding, 1969),

Therefore, the conditions for successful complet ion of the complicated he lmin th life- cycles seem to be present in the brackish milieu. Four of these life-cycles that disregard birds could be analysed quanti tat ively in this study. Gulls and terns from Oehe- Schleimiinde, a na ture reserve nea r the site of Olpenitz, harboured among other helminths adult Maritrema subdolum as well as Cryptocotyle concavum but not Microphal- lus claviformis (Kreft, 1991). The prevalence fluctuations of these three parasi tes and Podocotyle atomon in in termediate hosts were similar to those found at other sites (MacKenzie & Gibson, 1970; Zander et al., 1984, 1994). The cycle of the fish d i g e n e a n Podocotyle atomon is interrupted in Missunde due apparent ly only to the absence of the first host Littorina saxatilis or L. fittorea.

494 V. Kesting, S. Gollasch & C. D Zander

C o m m u n i t y a n a l y s i s

The parasite communit ies of the Schlei fjord were prel iminari ly in f luenced by the prevai l ing salinities at the two sites of Olpenitz and Missunde. According to Esch et al. (1988), the habitat quality can be judged by analysing which kind of he lmin th parasite cycles is present. Hence, eight species of Olpenitz and seven of Missunde were autoge- nic parasites which perform their whole cycles in the water. Twelve species of both sites were allogenic parasites which change from water to air, birds be ing their final hosts. These relations may indicate less favourable habitat conditions in Olpenitz and in Mis- sunde than in undis turbed envi ronments (Esch et al.. 1988). The n u m b e r of parasite species was, according to Remane's (1958) rule of species minimum, lower in Missunde than in Olpenitz, albeit without significance. Contrarily, the n u m b e r of host-parasite combinat ions was significantly higher in Olpenitz. This may indicate that the existence of parasites may not depend on salinities in the same way as it does for hosts.

Additionally, the presence of core and secondary species in Olpenitz and their absence in Missunde were of high significance. Core species were rare in Olpenitz - two fish parasites and one crustacean parasite - but these were accompanied by seven secondary species. A similar situation was found in the Ltibeck Bight with 10-16 %, salinity where a guild of five goby species was infested by two secondary parasite species (Zan- der, 1993). In contrast to the Schlei fjord, the parasite communit ies of st icklebacks of the Elbe and Eider rivers showed no remarkable change of core species number s at different salinities, inc luding freshwater (M611er-Buchner, 1987).

Generally, prevalences were higher in Olpenitz than in Missunde. This seems to contradict the biocoenotic rule of T h i e n e m a n n (1939) which claims increas ing populat ion densities and decreasing species numbers in extreme ecosystems. This s i tuat ion is apparent in brackish waters at 5-8 %,, salinity such as prevail in Missunde. Here the rare species domina ted over the satellite species, whereas in Olpenitz a reverse situation was found. The only evidence for Th ienemann ' s rule may be demonstra ted by early cestode larvae infest ing planktic copepods (Gollasch & Zander, 1995), or plerocercoids of Proteo- cephalus percae infesting Pomatoschistus microps with higher intensit ies in Missunde than in Olpenitz (Kesting, 1992). These results may indicate that in Missunde not only salinity is responsible as stress factor but also pollution in general . This causes a deposition of mud on the bottom which influences especially the bentha l zone of Missunde but to a lesser degree the pelagial zone where the cestodes complete their cycles.

Evidence of a better situation in the pelagial zone of Missunde ma y be given by planktic parasites such as Thersitina gasterostei, whose prevalence is one of the highest values of this site, or mero-planktic ones like Brachyphallus crenatus which is a satellite species at this site but a rare species in Olpenitz. Further evidence of drastical changes in the env i ronmenta l conditions in the benthal zone of Missunde may be given by the infestat ion of Pomatoschistus microps by Cryptocotyle concavum which decreased strongly be tween 1978 (Zander et al., 1984) and 1991. This negat ive t r end was intensi- fied by the infestation of the i . in termediate host of this parasite, Hydrobia spp., which was found in 1984 (Wendland, 1985) but not in 1985/1986 (Kreft, 1991) nor in the present investigation. Therefore, we may conclude that dur ing the last 16 years a clear deterio- ration of ecological conditions has occurred. Such results are only avai lable if long-term monitor ing can be performed.

P a r a s i t e c o m m u n i t i e s of t he Sch le i Fjord

Acknowledgement. We thank C. Berger for improving the English text.

495

LITERATURE CITED

Antholz, B., Meyer-Antholz, W. & Zander, C, D., 1991. Feeding activities of two euryhal ine small- sized fish in a western Baltic brackish fjord. - Helgol6nder Meeresunters . 45, 287-300.

Deblock, S., Capron, A. & Ros6, F., 1961. Contribution ~ l '6tude des Microphallidae Travassos, 1920 (Trematoda). La genre Maritrema Nicoll, 1907, cycle 6volutif de M. subdolum Jaegerski61d 1909. - Parassitologia 3, 105-119.

Delling, D., 1975. Un te r suchungen am Oligohal inikum der Schlei. I. Haddebyer und Selker Noor als Beispiele oligohaliner Lebensr~iume. - Kieler Meeresforsch. 31, 1t 1-150.

Esch, G. W., Gibbons, J. W. & Bourque, J. E., 1975. An analysis of the relationship be tween stress and parasitism. - Am. Midl. Nat. 93, 339-353.

Esch, G. W., Kennedy, C. R., Bush, A. O. & Aho, J. M., 1988. Patterns in helminth communi t ies in freshwater fish in Great Britain: alternative strategies for colonization. - Parasitology 96, 519-532.

Esch, G. W., Shostak, A. W., Marcogliese, D. J. & Goater, T. M., 1990. Patterns and processes in helminth parasite communities: an overview. In: Parasite communities: patterns and processes. Ed. by G. W. Esch, A. O. Bush & J. M. Aho. C h a p m a n & Hall, London, 1-19.

Gollasch, S., 1992. Populat ionsdynamik und Parasitenbefall von Bivalvia, benthischen und plankti- schen Crustacea in der Ostseef6rde Schlei. Dipl.-Arb., Univ. Hamburg, 175 pp.

Gollasch, S. & Zander, C. D., 1995. Population dynamics and parasitation of planktonic and epi- benthic crus taceans in the Baltic Schlei fjord. - Helgol~inder Meeresunters . 49, 759-770.

Gollasch, S., Winkler, G., Strohbach, U. & Zander, C. D., 1996. Digene Parasiten der Nordseegar- nele, Crangon crangon (L., 1758), (Decapoda, Crustacea) aus der westl ichen Ostsee. - Seev6gel 17, 3-4.

Holmes, J. C. & Price, P. W., 1986. Communi t ies of parasites. In: Communi ty ecology: Patterns and processes. Ed. by D. J. Anderson & J. Kikkawa. Blackwell, Oxford, 187-213.

Kennedy, C. R., 1975. Ecological animal parasitology. Blackwell, Oxford, 163 pp. Kesting, V., 1992. Un te r suchungen zur Parasi tenfauna von Kleinfischen und Schnecken der Ost-

seef6rde Schlei. Dipl.-Arb., Univ. Hamburg , 183 pp. Kreft, K. 1991. Befalls- und Populat ionsdynamik ausgew6hl te r d igener Trematoden und ihrer Wirte

in der Schlei. Diss., Univ. Hamburg, 289 pp. Lauckner, G., 1984. Impact of trematode parasi t ism on the fauna of a North Sea tidal fiat. - Hel-

gol6nder Meeresunters . 37, 185-199. MacKenzie, K. & Gibson, D., 1970. Ecological studies of some parasites of plaice Pleuronectes pla-

tessa L. and flounder Platichthys [lesus (L.). - Syrup. Br. Soc. Parasitol. 8, 1-42. M611er-Buchner, J., 1987. Unte r suchungen zur Paras i tenfauna drei- und neuns tachl iger Stichlinge

(Gasterosteus aculeatus L. und Pungitius pungitius [L.]) aus EIbe, Eider und Schlei. Diss., Univ. Hamburg, 230 pp.

Nellen, W., 1967. Okologie und Fauna (Makroevertebraten) der brackigen und hyper t rophen Ost- seef6rde Schlei. - Arch. Hydrobiol. 63, 273-309.

Reimer, L. W., 1963. Zur Verbreitung von Adulti und Larvenstadien der Fam. Microphallidae Viana, 1924 (Trematoda, Digenea) in der mit t leren Ostsee. - Z. Parasitkde 23, 253- 273.

Remane, A., 1958. Okologie des Brackwassers. - Binnengew~isser 12, 1-216. Rheinheimer, G., 1970. Chemische, mikrobiologische und planktologische U n te r suc hunge n der

Schlei im Hinblick auf deren Abwasserbelas tung. - Kieler Meeresforsch. 26, 105-216. Rohde, K., 1982. Ecology of marine parasites. Univ. Queens l and Press, St. Lucia, 245 pp. Schmidt-Moser, R. & Westphal, D., 1981. Interrelation be tween invertebrate p lankton and larval fish

development in the Schlei fjord, western Baltic. - Kieler Meeresforsch. (Sonderh.) 5, 202-210. Schriever, G., 1974. Die sessile, hemisessi le und vagile Har tbodenfauna der Schlei im 6kologischen

Vergleich. - Kieler Meeresforsch. 30, 80-90. Th ienemann , A., 1939. Grundzfige einer a l lgemeinen Okologie. - Arch. Hydrobiol. 35, 267- 285. Tiews, K., 1954. Die biologischen Grundlagen der Biisumer Garnelenfischerei. - Ber. dt. wiss.

Kommn Meeresforsch. 13, 235-269.

496 V. Kes t ing , S. Go l l a s ch & C. D. Z a n d e r

Voigt, M. O. C., 1991. Community structure of the helminth parasite fauna of gamrnarids (Crusta- cea: Amphipoda) in Kiel Bay, western Baltic Sea. - Meeresforsch. 33, 266- 274~

Wendland, W., 1985. Ober das Auftreten digener Trematoden und ihrer Zwischenwirte Schnecken, Crustacea und Kleinfische in der Schlei unter besonderer Beriicksichtigung der Microphalliden. Dipl.oArb., Univ. Hamburg, 136 pp.

Werding, B., 1969. Morphologie, Entwicklung und Okologie digener Trematoden-Larven der Strandschnecke Littorina littorea. - Mar. Biol. 3, 306-333.

Winkler, G., 1994. Zur Populationsdynamik und Ern~ihrungsbiologie von Crangon crangon L. (Cru- stacea; Crangonidae) in der Lfibecker Bucht (Siidwestliche Ostsee). Dipl.oArb., Univ. Hamburg, 90 pp.

Zander, C. D., 1993. The biological indication of parasite life-cycles and communities from the Lti- beck Bight, SW Baltic Sea. - Z. angew. Zool. 79, 377-389.

Zander, C. D. & Westphal, D., 1991. Kleinfischparasiten der Ostseef6rde Schlei und ihre Einbindung in die Nahrungskette. - Seev6gel 12, 4-8.

Zander, C. D. & Westphal, D., 1992. Nahrungsbeziehungen von vier euryhalinen Kleinfischarten der Ostseef6rde Schle i . - Zoot. Jb. (Syst. C)kol. Geogr. Tiere) 119, 339-364.

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}inder Meeresunters. 47, 81-111.

Zander, C. D., Groenewold, S. & Strohbach, U., 1994. Parasite transfer from crustacean to fish hosts in the Lfibeck Bight, SW Baltic Sea. - Helgol~nder Meeresunters. 48, 89- 105.

Zander, C. D., Kollra, H. G., Antholz, B., Meyer, W. & Westphal, D., 1984. Small-sized euryhaline fish as intermediate hosts of the digenetic trematode Cryptoco ty le concavum. - Helgol~nder Mee- resunters. 37, 433-443.

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Parasite communities of the Schlei Fjord (Baltic coast of ... · Parasite communities of the Schlei Fjord (Baltic coast of northern Germany) V. Kesting, S. Gollasch & C. D. Zander*