J. World Maricul. SOC. 1 2 ( 2 ) :9-14 (1981)

PARASITES AND PARASITOSIS IN FISH CULTURE IN PORTUGAL

M. Carvalho-Varela,'" V. Cunha-Fer re i ra , l t2 M. P. Cruz e S i l v a , l r 2 M. T. Monteiro2 and M. S . Grazina-Frei tas2

ABSTRACT

This paper d e a l s wi th research work covering t h e per iod from May 1979 up t o May 1981 and p r e s e n t s r e s u l t s o f p a r a s i t e s and p a r a s i t o s i s diagnosed i n a t o t a l of 195 complete d i s s e c t i o n s of s i x f i s h spec ies from cul tured and f e r a l popula t ions i n Por tuga l : European e e l (Anguilla a n g u i l l a ) (49) ; mirror carp (Cyprinus c a r p i o s p e c u l a r i s ) (29) ; common grey m u l l e t (Mugil cephalus) (18) ; European p l a i c e (Pleuronectes pla- t e s s a ) (11); rainbow t r o u t (Salmo g a i r d n e r i ) ( 4 2 ) ; common sole (Solea s o l e a ) (46) .

A l i s t of protozoans and helminths i d e n t i f i e d with respec t ive i n c i -

A ) F e r a l f i s h : 1) European eel (17)--Echinorhynchus c l a v u l a 11.8% dence i s given:

and Rhabdochona a n g u i l l a 5.9%; 2 ) common grey mul le t (18)--Haploporus benedeni i 16.7%, Neoechinorhynchus sp. 5.6%, and Raphidascar is sp . 5.6%; 3) European p l a i c e (11) --Bothriocephalus sp. l a r v a e 9.1%, Contracaecum aduncum 9.1%, and Cryptocotyle l ingua 9.1%; 4) common s o l e (46)--Cucul- l a n e l l u s minutus 8.7%, Gyrodactylus e legans 4.3%, and Cestodes la rvae 2 .2%.

B) Cul tured f i s h : 1) European e e l (32)--Trichodina a n g u i l l a e 3.1% and Ich thyophth i r ius m u l t i f i l i i s 18.8%; 2 ) rainbow t r o u t (42)--Eimeria t r u t t a e 2.4%, Hexamita i n t e s t i n a l i s 4 .8%, Holophrya simplex 2.4%, and Trichodina t r u t t a e 4.8%.

The r e s u l t s show t h a t f e r a l f i s h harbor predominantly i n d i r e c t l i f e cyc le helminths , i n c o n t r a s t w i t h c u l t u r e d f i s h only a f f e c t e d with pro- tozoans, due mainly t o overcrowding and d e f i c i e n t management, which pro- p i t i a t e a s i g n i f i c a n t background i n f e c t i o n . I t w a s i n these specimens t h a t some l e s i o n s c h a r a c t e r i s t i c o f pro tozoos is were found.

k e n t r o P a r a s i t o l o g i a Universidade Tgcnica Lisboa, Escola Superior

2Laborat&io Servipos V e t e r i n s r i o s Por tos Pesca, I n s t i t u t e Nacional

Medicina Veter ingr ia , Rua Gomes F r e i r e , 1199 Lisboa, Por tuga l .

V e t e r i n s r i a , Doca Pedrousos, Por ta 65, 1400 Lisboa, Por tuga l .

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INTROWCTION

I n p r i v a t e l y owned i n t e n s i v e in land aquacul ture u n i t s i n Por tuga l t h e r e are four rainbow t r o u t (Salmo g a i r d n e r i ) farms, with a product ion o f about 600 MT/year, and t h r e e i n t h e planning o r bu i ld ing s t a g e s t o produce about 400-600 MT/year.

Regarding eel farms, t h e r e are on a semi- intensive s c a l e two u n i t s i n mid and southern Por tuga l , wi th an average t o t a l product ion o f about 150 MT/year i n t h e f i r s t phase and an es t imated t a r g e t of 300 MT/year, and another i n t h e developmental s t a g e , with an expected average produc- t i o n o f over 400 MT/year.

The ex tens ive brackish water c u l t u r e covers an a r e a of about 500 ha, with an average product ion o f about 0.4 MT/ha/year, e .g . , near ly 200 MT/ year from es tua r ine s p e c i e s , p a r t i c u l a r l y m u l l e t (Mugil s p p . ) , bream (Sargus sargus and o t h e r s p e c i e s ) , eel (Anguil la a n g u i l l a ) , g i l t head bream (Sparus a u r a t a ) , bass (Dicentrarchus l a b r a x ) and black s p o t t e d bass (D. p u n c t a t u s ) , common s o l e (Solea s o l e a ) and o t h e r pleuronectes .

For mollusc c u l t u r e t h e r e is an i n c r e a s i n g i n t e r e s t i n t h e recon- s t i t u t i o n of o y s t e r beds, p a r t i c u l a r l y Portuguese o y s t e r (Crassostrea angula ta ) and f l a t o y s t e r (Ostrea e d u l i s ) and, y e t , grooved c a r p e t - s h e l l product ion (Venerupis d e c u s s a t a ) , from which t h e r e is no a v a i l a b l e ca l - c u l a t i o n . Information is also lacking on f i s h farms or p r o j e c t s f o r in- d u s t r i a l mar icu l ture .

Concerning in land waters , t h e S t a t e Serv ices produce var ious spe- c i e s o f f i s h f o r res tocking , p a r t i c u l a r l y t h r e e m i l l i o n t r o u t f inger - l ings /year which also supply some i n d u s t r i a l t r o u t c u l t u r e . They have a l s o two p i l o t - p l a n t s o f t r o u t c u l t u r e s i t u a t e d i n t h e nor th with a t o t a l product ion o f about 50 MT/year t o encourage and t r a i n t h e poten- t i a l f i s h farmers.

The c u l t u r e of some s p e c i e s i n t h e process of domest icat ion con- f r o n t s us with new d i s e a s e e n t i t i e s and management problems t h a t w e must l e a r n t o t rea t and d e a l w i t h , some d i s e a s e s t h a t are not apparent i n n a t u r a l ecosystems b u t which can assume epidemic f e a t u r e s i n enclosed f i s h e r i e s , p a r t i c u l a r l y enc losures wi th high overcrowding.

p a r a s i t e s and t h e i r pathogenic e f f e c t s i n f e r a l f i s h , which w i l l provide us with background knowledge u s e f u l f o r f i s h farming as w e l l as an in- creased awareness of t h e paras i tocoenos is i n t h e a q u a t i c ecosystem, has emphasized t h e r e a l i n t e r e s t of p a r a s i t e s a s b i o l o g i c a l t a g s , when they are used t o h e l p d e f i n e both t h e taxonomical s t a t u s and t h e e t h o l o g i c a l and zoogeographical f e a t u r e s of t h e i r h o s t s .

I t i s also necessary t o bear i n mind t h a t t h e i d e n t i f i c a t i o n of

Thus, t h e main a i m s o f t h i s s tudy are: t o compare t h e p a r a s i t e fauna i n f e r a l f i s h having r e a l c u l t u r e p o t e n t i a l i t y i n Western Europe, with t h e p a r a s i t e fauna i n c u l t u r e d f i s h i n P o r t u g a l , and t o determine which p a r a s i t e s can be pathogenic i n e i t h e r environment.

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MATERIALS AND METHODS

From May 1979 t o May 1981, 195 samples of 6 s p e c i e s , both from f e r a l f i s h (92) and from c u l t u r e d (103) f i s h populat ions were examined f o r p a r a s i t e s . The samples from f e r a l f i s h w e r e obtained from mater ia l landed i n Lisbon P o r t , and w e r e from s e v e r a l f i s h i n g zones of Portuguese Cont inenta l Coast. The c u l t u r e d samples included Anguil la angui l la (European e e l ) , Cyprinus c a r p i o s p e c u l a r i s (mir ror carp) and S a l m g a i r d n e r i (rainbow t r o u t ) . The samples came from Eirolac-Nazar6, Post0 Aquicola da Azambuja and Postos Aquicolas de Covas ( e e l ) , Vi la do Conde and Manteigas ( c a r p ) , and Vis i tur i s -Viseu and T r u t i c u l t u r a do Paul- Tortozendo ( t r o u t ) . A l l f i s h tanks were made o f concre te .

A f t e r weighing, measuring and determining t h e f i s h age (whenever p o s s i b l e ) , a complete p a r a s i t o l o g i c a l f i s h d i s s e c t i o n was followed, as w e l l as p r e p a r a t i o n , observa t ion and i d e n t i f i c a t i o n of i s o l a t e d speci- mens according t o methods recommended by Hoffman (1967) and Bauer e t a l . (1973) . H i s t o l o g i c a l s e c t i o n s were a l s o examined.

RESULTS AND DISCUSSION

The frequency, percentages and i d e n t i f i c a t i o n of p a r a s i t e s found i n t h e 6 f i s h species examined are given i n Tables 1 and 2 .

Table 1. P a r a s i t i s m o f T o t a l Examined Fish

F ish Examined P a r a s i t i z e d %

F e r a l : Anguil la a n g u i l l a (L.) (European e e l ) 1 7 2 11.8

s t r i p e d m u l l e t ) 18 4 2 2 . 2 Mugil cephalus (Common grey mul le t o r

Pleuronectes p l a t e s s a (L . ) (European p l a i c e ) 11 3 27.3

Solea s o l e a (L.) (Common s o l e ) 46 6 13.0

Cultured: Anguil la a n g u i l l a (L.) (European ee l ) 32 Cyprinus c a r p i o s p e c u l a r i s ( L . ) (Mirror

carp) 29 S a l m g a i r d n e r i Richardson (Rainbow

t r o u t ) 4 2

6 18.8

- -

5 11.9

T o t a l 195 26 1 3 . 3

Although i n t h e p r e s e n t s tudy t h e number o f specimens examined a r e n o t s u f f i c i e n t f o r a s t a t i s t i c a l a n a l y s i s , t h e r e s u l t s show t h a t f e r a l f i s h harbor predominantly heteroxenous o r i n d i r e c t l i f e cycle helminths-- t h e monogenetic ( G y r o d a c t y l u s e legans) being t h e s i n g l e exception--in c o n t r a s t w i t h c u l t u r e d f i s h only a f f e c t e d by protozoans with d i r e c t l i f e cyc les .

i n concre te tanks and had f i l t e r e d e f f l u e n t , thereby hindering access by The semi- intensive and i n t e n s i v e f i s h farms s tudied were contained

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and p r o l i f e r a t i o n o f s u s c e p t i b l e in te rmedia te h o s t s . explana t ion f o r the above f ind ings .

This i s t h e main

Table 2. P a r a s i t e s and Their Frequency i n T o t a l Hosts (bracketed num- b e r s denote examined f i s h , F = frequency)

Feral Cultured

0 k3 !. 3 rl 0

W 9 as B u a o m 4

4 C I O 8 P 3 u 1

a m 2 2 z vi * n f uvl vi 4 9 c S E

4 HOStS

0 rl

o m n l m m * m 11 $ 3 .* .1 .3 3

c c

1 1 = m m 3

5 5 3 1 1 - 4 -* -1

g s 3 % 1 g g 2 Parasites L171 1181 [111 [461 [321 [291 [421

F % F % F % F % F % F % € %

Protozoa 1 2 . 4 2 4.8 1 2 . 4

- - - - - - - - - - _ _ Eimeria truttae Hexamita intestinalis - - - - - - - - - - - _ Holophrya simplex - - - - - - - - - - _ _ Ichthyophthirius multifiliis - - - - - - - - Trichodina anguillae - - - - - - - -

6 18.8 - - - - 1 3.1 - - - -

2 4 . 8 - - - - - - - - - - _ _ T. truttac?

Monogenoidea

Digenoidea

_ _ _ _ _ _ 2 4 . 4 - - - - - - Gymdactyl us el eyans

- - _ _ _ _ cryptocotyle lingua (metacercariael - - - - 1 9.1 - - Haploporus benedenii - - - - _ _ _ _ 3 16.7 - - - -

Cestoda - _ _ _ _ _ 1 2 . 2 - - - - - - Cestodes (larvae) Bothriocephalus sp. (larvae) _ _ _ _

Contracaecum aduncum Cucullanellus minutus Rhabdochona anguillae

- - _ _ _ _ 1 9.1 - - NematOda - - _ - - - 1 9.1 - - _ _ _ _

_ _ _ _ _ _ 4 8 . 7 - - - - - - 1 5 . 9 - - - - - - - - _ - - -

- - - - - - 1 5 . 6 - - - - Raphidascaris sp. (larvael - -

Echinorhynchus clavula 2 11.8 - - - - - - Neoechinorhynchus sp. - - 1 5 . 6 - - - -

Acanthocephala - - _ - - - - - - - - -

Also, t h e low l e v e l s of i n t e n s i v e o r ex tens ive i n f e c t i o n of f e r a l f i s h helminths explained by t h e incommensurate extension o f t h e respec- t i v e t e r r i t o r i e s and migra t ions , which l e a d to a l o w d e n s i t y of in fec- t i v e p a r a s i t i c e lements , o r i g i n a t e a degree of p a r a s i t i s m by helminths much lower than t h a t found i n confined o r overcrowded environments where, given a favorable e c o l o g i c a l condi t ion , o v e r t helminthic pathogenesis i s manifested (Cruz e S i l v a e t a l . 1973) .

I n e a r l y s t u d i e s p r i o r t o t h i s work, t h e fol lowing protozoans were i d e n t i f i e d i n Por tuga l : Ich thyophth i r ius m u l t i f i l i i s , i n Anguilla an- g u i l l a from t h e same f i s h farm, and a l s o from o t h e r f reshwater f i s h spe- cies such as Carass ius a u r a t u s , L e b i s t e s r e c t i c u l a t u s , Molliennesia l a t i p i n n a , M. sphenops and Xiphophorus h e l l e r (Mendes e t a l . 1980); T r i - chodina a n g u i l l a e , i n A . a n g u i l l a from a p i l o t - p l a n t i n Alcochete (Men- des e t a l . 1980).

Previous r e p o r t s o f o t h e r he lminth ic s p e c i e s i n So lea s o l e a f i shed i n t h e Portuguese Cont inenta l Coast are: Entobdel la s o l e a e (Van Beneden and Hesse, 1864) Johnston, 1929, c i t e d by Kearn and Vasconcelos ( 1 9 7 9 ) ;

Contracaecum magnum Smedley 1934, mentioned by Rodrigues e t a l . (1975): Acanthocephaloides i n c r a s s a t u s (Molin, 1858) Meyer, 1933, was found i n t h e s a m e f i s h species i n t h e North Afr ican A t l a n t i c Coast by Rodrigues e t a l . (1975).

To t h e b e s t o f our knowledge, t h e fol lowing p a r a s i t i c s p e c i e s a r e reported i n Por tuga l f o r t h e f i r s t t i m e : Eimeria t r u t t a e Leger and Hesse, 1919, Hexamita i n t e s t i n a l i s Dujardin, 1841, Holophrya simplex Schewiakoff, Trichodina t r u t t a e Mtller, 1937 (Pro tozoa) ; Gyrodactylus e legans Nordmann, 1832 (Monogenoidea); Cryptocotyle l ingua (Crepl in , 1825) Fischoeder, 1903, Haploporus benedeni i ( S t o s s i c h , 1887) Looss 1902 (Digenoidea); Contracaecum aduncum (Rudolphi, 1802) R a i l l i e t and Henry, 1912, Cucul lane l lus minutus (Rudolphi, 1819) Tornquis t , 1931, Rhabdo- chona a n g u i l l a e Spaul , 1927 (Nematoda); Echinorhynchus c l a v u l a Dujardin, 1845 (Acanthocephala) .

W e a l s o confirm t h e absence o f t h e protozoan Myxosoma c e r e b r a l i s i n t r o u t c u l t u r e i n Por tuga l . This f i n d i n g makes t h i s country a p r i v i l e g e d p lace f o r t r o u t c u l t u r e i n Europe, where t h e myxosporidian i s widespread. Accordingly, r i g i d c o n t r o l measures should be implemented (Machado-Cruz e t a l . 1980).

LITERATURE CITED

Bauer, 0. N . , V. A. Mussel ius , and Yu. A. S t re lkov . 1973. Diseases of Pond Fishes ( i n Russian) . Engl i sh t r a n s l a t i o n by U.S. Department o f t h e I n t e r i o r and Nat ional Science Foundation, Washington, D.C. 220 pp.

Cruz e S i l v a , J. A . , M. M. Afonso-Roque, and M. M. Mendonsa. 1973. A s helmintoses como f a c t o r de fundamental importzncia s a n i t d r i a nos animais selvagens e m c a t i v e i r o . Revis ta Portuguesa Cidncias V e t e - r i n s r i a s 68(428) :260-274.

Univers i ty of C a l i f o r n i a P r e s s , Beverly H i l l s . 486 pp.

Kearn, G. C . , and M. E. Vasconcelos. 1979. Prel iminary l i s t o f Mono- genean p a r a s i t e s of Portuguese marine f i s h e s , with a note on (Eno- p locoty le minima) T a g l i a n i , 1912. Boletim I n s t i t u t o Nacional In- vest igap3o Pescas , L i s b o a , Por tuga l 1:25-36.

Machado-Cruz, J . , M. H . Galhano, and J. Costa-Eiras. 1980. The prophy- l a x i s o f (Myxosoma c e r e b r a l i s ) . The Portuguese case. Presented a t t h e Seminar on Actual Problems o f Oceanography i n Por tuga l (INVOTAN), Lisbon, Por tuga l , November 1980 ( i n p r e s s ) .

t i r i o s e e m Portugal . Ext rac to i n Proceedings I1 Congress0 I n t e r - national V e t e r i n s r i a Lingua Portuguesa, Lisboa, Por tuga l , 21-25 Julho 1980, p. 170.

1980. A Tricodinose e m Por tuga l . Ext rac to i n Proceedings I1 Con- gresso I n t e r n a c i o n a l V e t e r i n d r i a Lingua Portuguesa, Lisboa, Portu- g a l , 21-25 Julho 1980, p . 170.

Hoffman, G. H. 1967. P a r a s i t e s o f North American Freshwater F ishes .

Mendes, A. M . , M. Carvalho-Varela, and R. M. Bessa. 1980. A I c t i o f -

Mendes, A. M . , M. C. P e l e t e i r o , R. M. Bessa, and M. Carvalho-Varela.

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Rodrigues, H. O . , M. Carvalho-Varela, S. S. Rodrigues, and R. Crist6faro. 1975. Nova contribuiSZo para o estudo dos Nemat6deos de peixes do Oceano Atlsntico--Costa Continental Portuguesa e Costa do Norte da zfrica. Mem6rias Instituto Oswaldo Cruz 73 (1/2) :127-134.

Rodrigues, H. O., D. Noronha, and M. Carvalho-Varela. 1975. Alguns

Mem6rias Instituto Oswaldo Acantocgfalos de peixes do Oceano Atl^antico--Costa Continental Por- tuguesa e Costa do Norte da Africa. Cruz 73(3) :209-214.

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