SEASONAL OCCURRENCE AND MATURATION
OF BATHYBOTHRIUM RECTANGULUM (CESTODA: AMPHICOTYLIDAE) IN BARBEL BARBUS BARBUS (PISCES)
OF THE JLHLAVA RIVER, CZECH REPUBLIC
SCHOLZ T. & MORAVEC F.*
Summary:
Seasonal dynamics of the tapeworm Bathybothrium rectangulum (Bloch, 1782), a parasite of barbel (Barbus barbus), was studied from April 1992 to June 1993 in the Jihlava River (the Danube basin), Czech Republic. Although the cestodes occurred in fish throughout the year, their maturation exhibited a marked seasonality with new infections (recruitment) in summer (July), growth and maturation in autumn and winter; worms with ripe eggs left the fish hosts from May to July. Smaller fish (size
≤ 35 cm) were more frequently infected with cestodes than larger ones, although mean intensity reached its maximum in 35.5- 4 0 cm long fish.
KEY WORDS : Bathybothrium rectangulum, Barbus barbus, seasonal patterns, maturity, host-size dependence.
Résumé : INCIDENCE SAISONNIÈRE ET MATURATION DE BATHYBOTHRIUM RECTANGULUM (CESTODA : AMPHICOTYLIDAE) CHEZ LE BARBEAU, BARBUS BARBUS (PISCES), DE LA RIVIÈRE JIHLAVA, RÉPUBLIQUE TCHÈQUE l'évolution saisonnière de l'helminthe Bathybothrium rectangulum (Bloch, 1782), parasite du barbeau (Barbus barbus), a été étudiée d'avril 1992 à juin 1993 dans la rivière Jihlava (bassin du Danube), République tchèque. Bien que les cestodes soient présents chez le poisson tout au long de l'année, leur maturation est marquée par un net caractère saisonnier — nouvelles infestations (recrutement) en été (juillet), croissance et maturation en automne et hiver; les vers porteurs d'oeufs mûrs quittent le poisson- hôte de mai à juillet. Les poissons les plus petits (taille ≤ 35 cm) ont été plus souvent infestés par les cestodes que les plus grands, encore que le pic d'intensité soit maximal pour les poissons longs de 35,5 à 40 cm.
MOTS CLÉS : Bathybothrium rectangulum, Barbus barbus, modes saisonniers, maturation, taille-dépendance.
INTRODUCTION
T
h e t a p e w o r m BATHYBOTHRIUM RECTANGULUM( B l o c h , 1 7 8 2 ) (Pseudophyllidea: Amphicoty
lidae) is a specific intestinal parasite o f barbel (BARBUS s p p . ) a n d related g e n e r a o f cyprinid fish, occurring in Palaearctic Region (Lühe, 1 9 1 0 ; J o y e u x &
Baer, 1 9 3 6 ; Protasova, 1977; Moravec & Amin, 1978;
Van Maren, 1 9 7 9 ; Dubinina, 1 9 8 7 ; Scholz, 1 9 8 9 « ) . Despite its relatively c o m m o n o c c u r r e n c e , there are only very limited data o n the o c c u r r e n c e a n d life his
tory o f this parasite ( s e e Chubb, 1 9 8 2 ) . With the e x c e p tion o f brief information about t h e o c c u r r e n c e o f this tapeworm in barbel from Podebrady, B o h e m i a (Srämek, 1901) and Central and Eastern Balcan Mountains (Kaka- cheva-Avramova, 1 9 7 3 ) , the only data describing the seasonal periodicity o f o c c u r r e n c e a n d maturation o f B . RECTANGULUM w e r e p r o v i d e d b y K u l a k o v s k a y a ( 1 9 5 9 ) . T h e s a m e author (Kulakovskaya, 1 9 6 3 ) also
* Institute of Parasitology, Academy of Sciences of the Czech Repu
blic, Branišovská 31, 370 05 Česke Budějovice, Czech Republic.
Fax: 00 42 38 47743. Tel.: 00 42 38 41158. E-mail Lscholz@paru.cas.cz.
r e p o r t e d c o p e p o d s MACROCYCLOPS ALBIDUS a n d MEGA- CYCLOPS VIRIDIS as experimental intermediate hosts o f this tapeworm.
H o w e v e r , data b y K u l a k o v s k a y a ( 1 9 6 3 ) originated from a different geographical region. It is k n o w n that seasonal patterns in the o c c u r r e n c e a n d maturation o f helminths o f freshwater fish c a n b e influenced b y local ecological conditions a n d c a n differ even in rela
tively c l o s e localities ( s e e C h u b b , 1 9 8 2 for review).
Considering the specificity o f B . RECTANGULUM a n d the fact that barbel has b e c o m e endangered o r even extinct fish s p e c i e s in most localities in Central Europe, m o r e detailed data o n the e c o l o g y o f this c e s t o d e parasite appear to b e o f m o r e than regional importance. In this paper, data o n t h e o c c u r r e n c e a n d maturation o f B. RECTANGULUM from barbel (BARBUS BARBUS) in the J i h lava River, South Moravia, Czech Republic, are pre
sented.
MATERIALS AND METHODS
S
amples o f barbel, BARBUS BARBUS L., w e r e taken monthly by electrofishing from the Jihlava River near the village o f Biskotipky ( n e a r Rosice uParasite, 1996, 3, 39-44
39
SCHOLZ T. & MORAVEC F.
B r n a ; the D a n u b e River system) in South Moravia, C z e c h R e p u b l i c ( s e e M o r a v e c a n d Scholz, 1 9 9 4 , 1 9 9 5 ) . A total o f 177 barbel, ranging b e t w e e n 14-51 c m in total length ( a g e 1-7 y e a r s ) w a s e x a m i n e d monthly from April 1992 to J u n e 1 9 9 3 (Table I ) ; in addition, a sample o f 1 8 b a r b e l ( s i z e 1 2 - 4 7 c m ) w a s e x a m i n e d in May 1 9 9 4 .
evaluate s e a s o n a l c h a n g e s in maturation, t h e w o r m s w e r e stained with S c h u b e r g s c a r m i n e a n d divided into t h e following groups: g r o u p I: juvenile w o r m s ( o n l y s c o l i c e s o r u n s e g m e n t e d w o r m s ) ; II: maturing w o r m s ( s e g m e n t a t i o n present, genitalia d e v e l o p i n g ) ; III: mature w o r m s (genitalia d e v e l o p e d , n o e g g s pre
sent); I V a : gravid w o r m s , without ripe e g g s , uterus small, oval in s h a p e ; IV gravid, with ripe eggs, uterus large, l o b a t e ; I V c : d e s t r o b i l i z e d w o r m s . A total o f 1,315 w o r m s w a s evaluated (Fig. 2 ) . T h e material h a s b e e n d e p o s i t e d in the helminthological c o l l e c t i o n o f the Institute o f Parasitology, ASCR, in C e s k e Budejo- vice (Coll. No. C-17).
RESULTS
O C C U R R E N C E O F B.
rectangulum
I N B A R B E LO
ut o f 1 9 5 b a r b e l (BARBUS BARBUS) e x a m i n e d , 9 8 ( p r e v a l e n c e 5 0 . 3 % ) w e r e infected with a total o f 1,690 w o r m s ( m e a n intensity 1 7 . 3 , range 1-222; a b u n d a n c e 9 - 1 ) .A survey o f p r e v a l e n c e , intensity a n d m e a n intensity o f B . RECTANGULUM i n f e c t i o n in individual m o n t h s a m p l e s is given in T a b l e I a n d Figure 1. BATHYBO- THRIUM RECTANGULUM o c c u r r e d in b a r b e l throughout the year with p r e v a l e n c e r e a c h i n g its m a x i m u m in s u m m e r 1 9 9 2 , declining to lowest values in winter a n d
Year and month
No. o f barbel examined
No. o f barbel infected
Prevalence (%)
Intensity of infection (mean, range)
Body length of barbel in cm
(mean, range)
Abundance
1992
April 12 6 50 11 (2- 3 2 ) 34 (22-50) 5.3
May 14 10 71 4 ( 1 - 16) 32 (19-43) 2.6
June 11 6 55 5 ( 1 - 16) 37 (24-47) 2.4
July 12 9 75 21 ( 1 - 4 6 ) 30 (21-35) 15.4
August 12 9 75 6 ( 1 - 23) 28 (22-36) 4.3
September 12 4 33 16 ( 3 - 3 3 ) 26 (21-35) 5.2
October 13 7 54 27 ( 1 - 6 9 ) 29 (18-49) 14.4
November 12 8 67 22 (3- 9 3 ) 29 (19-47) 14.8
December 15 7 47 38 (1-222) 33 (28-46) 17.8
1993
January 13 5 38 22 ( 4- 7 7 ) 37 (28-51) 8.4
February 10 5 50 24 ( 1- 8 2 ) 35 (30-51) 12.1
March 10 3 30 27 (15- 4 4 ) 35 (24-45) 8.0
April 10 6 60 9 ( 1- 18) 29 (14-35) 5.6
May 10 4 40 9 ( 1- 2 6 ) 35 (30-40) 3.7
June 11 3 27 66 (10- 96) 30 (16-42) 18.0
1994
May 18 7 39 8 ( 1- 25) 32 (12-48) 3.1
Total 195 98 50 17 ( 1-222) 28 (14-51) 9.1
Table I. — Survey of Barbus barbus examined from the Jihlava River and their infection with Bathybothrium rectangulum.
4 0 Parasite, 1996, 3, 39-44
T h e fishes w e r e transported live to the Institute o f Para-
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sitology in C e s k e Budejovice a n d 1-2 days after their capture w e r e e x a m i n e d b y routine helminthological e x a m i n a t i o n as outlined b y Bykhovskaya-Pavlovskaya ( 1 9 6 9 ) .
Planktonic invertebrates w e r e s a m p l e d monthly from J u l y t o D e c e m b e r 1 9 9 2 a n d in May 1 9 9 4 t o s e a r c h for
larvae o f B . RECTANGULUM. T h e invertebrates e x a m i n e d w e r e as follows: CANDONA CANDIDA, CYPRIDOPSIS VIDUA,
CYCLOCYPRIS GLOBOSA a n d HEPRETOCYPRIS REPTANS (Ostra- c o d a , 2 6 3 s p e c i m e n s ) , MACROCYCLOPS ALBIDUS ( 4 4 5 ) , EUCYCLOPS SERRULATUS ( 1 , 3 2 9 ) , ACANTHOCYCLOPS VER- NALIS ( 7 ) , PARACYCLOPS AFFINIS ( 4 ) , ECTOCYCLOPS PHALE- RATUSD), MEGACYCLOPS GIGAS ( 1 ) ( C o p e p o d a , 1,787), and PARACANTHA TRUNCATA (Cladocera, 1 3 2 ) . Survey o f other b e n t h i c invertebrates, w h i c h w e r e e x a m i n e d for the p r e s e n c e o f helminth larvae a n d w e r e free o f B . REC
TANGULUM infection, is given b y M o r a v e c & Scholz ( 1 9 9 4 ) .
T h e tapeworms found were fixed under slight coverslip or slide pressure with 4 % formaldehyde. In order to
Fig. 1. — Seasonal variation of prevalence (points), mean intensity (circles) and abundance (asterisks) of infection of barbel with Bathy- bothrium rectangulum in the Jihlava River. Mean intensity and abundance expressed as log (x + 1). Vertical bars around mean intensity data are standard deviations.
early spring ( M a r c h ) . M e a n intensity o f infection and a b u n d a n c e fluctuated irregularly without any distinct seasonal pattern (Fig. 1) with the e x c e p t i o n that lowest values occurred in late spring (May) and early s u m m e r ( J u n e ) .
S E A S O N A L I T Y O F M A T U R A T I O N
Proportion o f w o r m s in different states o f maturity in monthly samples indicated the e x i s t e n c e o f a pro
n o u n c e d seasonal cycle in the maturation o f B . REC
TANGULUM (Fig. 2 ) . J u v e n i l e w o r m s (group I ) , w h i c h represented 9 0 % o f w o r m s evaluated, occurred exclu
sively in July. Maturing w o r m s w e r e r e c o v e r e d from July to March with the highest proportion ( 7 9 - 1 0 0 % )
from August to J a n u a r y (Fig. 2 ) . Mature w o r m s w e r e found in O c t o b e r , from J a n u a r y to April and in J u n e , with higher proportions ( 9 8 % ) only in March. Gravid w o r m s o f different states o f maturity (groups I V a - c ) o c c u r r e d only from April to J u l y in e a c h years ( 1 9 9 2 , 1993 and additional sample in 1 9 9 4 ) , with the e x c e p tion o f eight t a p e w o r m s containing immature eggs (group I V a ) found in O c t o b e r . W o r m s with fully deve
loped, ripe eggs containing motile o n c o s p h e r e s w e r e o b s e r v e d only from May to July, with the highest fre
q u e n c y in J u n e (Fig. 2 ) .
S I T E O F L O C A T I O N
T h e anterior third o f the intestine was found to b e the preferred site o f location o f B . RECTANGULUM tape
worms. A total o f 1,021 o f 1,089 s p e c i m e n s evaluated (93-8 % ) w e r e localized in this part o f the gut; 4 8 and 20 tapeworms (i. e. 4.4 and 1.8 %, respectively) w e r e found in the middle and posterior thirds. T h e anterior third o f the gut harboured a majority o f tapeworms in all month samples (from 7 8 % in N o v e m b e r up to 100 % in S e p t e m b e r and D e c e m b e r ) , with the e x c e p tion o f J u n e w h e n 7 3 % o f tapeworms, represented by gravid tapeworms occurred in the posterior third o f the intestine.
R E L A T I O N S H I P B E T W E E N I N F E C T I O N
O F B. rectangulum I N F E C T I O N A N D H O S T S I Z E T h e infection o f B . RECTANGULUM was influenced by the size o f fish (Fig. 3 ) - P r e v a l e n c e was highest in smaller barbel (size 2 0 . 5 - 2 5 c m ) and its value d e c r e a s e d in larger fish s p e c i m e n s . Mean intensity increased from fish smaller than 20.5 c m to fish 2 1 - 2 5 c m long. In larger fish, its value fluctuated without any significant pattern, reaching its m a x i m u m in fish 3 5 . 5 - 4 0 c m long.
T h e smallest barbel infected was 18 c m long ( a g e 3 y e a r s ) ; the largest o n e measured 50 cm ( a g e 7 years).
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SCHOLZ T. & MORAVEC F.
Fig. 2. — Seasonal cycle of maturation of Bathybothrium reclangulum in barbel in the Jihlava River. Data are expressed as percentages of the total number of tapeworms found per month: I: scolices (black); II: maturing worms (white); III: mature worms (stippled, small points); IVa - gravid worms with infertile eggs (stippled, large points); IV b: gravid worms with ripe eggs (horizontally hatched); IVc: des- trobilized gravid worms (vertically hatched). Numbers below axis x represent numbers of tapeworms evaluated.
42 Parasite, 1996, 3, 39-44
Mémoire
Fig. 3. — Relationship of prevalence (points) and mean intensity of infection (asterisk) with Bathybuthrium rectangulum to body length of barbel from the Jihlava River. Mean intensity expressed as log (x + 1), with vertical bars representing a standard deviation.
Figures on the top represent number of fish in individual size groups; figures below intensity curve represent absolute values of mean intensity (mean number of worms per infected fish).
E X A M I N A T I O N O F P L A N K T O N
O u t o f 2 , 1 8 2 planktonic invertebrates, only o n e female o f the c o p e p o d MACROCYCLOPS ALBIDUS, e x a m i n e d in O c t o b e r 1 9 9 2 , w a s found to b e infected with o n e pro
c e r c o i d , w h i c h m o r p h o l o g i c a l l y c o r r e s p o n d s t o the larvae o f BATBYBOTHRIUM RECTANGULUM as d e s c r i b e d by Kulakovskaya ( 1 9 6 3 ) .
T h e p r o c e r c o i d m e a s u r e d 4 2 9 x 1 6 6 urn. It p o s s e s s e d a rectangular s c o l e x , 134 um wide, with s h a l l o w late
rally situated bothria, n u m e r o u s c a l c a r e o u s c o r p u s c l e s ( a b o u t 1 2 - 1 9 pm in d i a m e t e r ) filling the b o d y a n d an e l o n g a t e c e r c o m e r containing six e m b r y o n a l h o o k s .
DISCUSSION
I
n the J i h l a v a River, BATBYBOTHRIUM RECTANGULUM e x h i b i t e d a p r o n o u n c e d annual c y c l e o f maturation with the recruitment in s u m m e r (July), growth and maturation in the autumn and winter months, a n d production o f e g g s at the late spring and at the b e g i n ning o f s u m m e r (May-July). D u e to overlapping o f old g e n e r a t i o n a n d n e w l y a c q u i r e d t a p e w o r m s in J u l y 1992, the parasite o c c u r r e d in b a r b e l throughout the year.
Kulakovskaya ( 1 9 5 9 ) o b s e r v e d very similar s e a s o n a l patterns in the o c c u r r e n c e a n d maturation o f B . REC
TANGULUM in BARBUS BARBUS and B. MERIDIONALISPETENYI
in different localities o f the ex-USSR with the recruit
ment taking p l a c e in s u m m e r (June-August) and gravid w o r m s b e i n g released from the hosts in May-June. Dif
ferences b e t w e e n individual localities w e r e thought to d e p e n d o n their g e o g r a p h i c a l position; l o w e r water temperatures w e r e c o n s i d e r e d to h a v e delayed matu
ration (Kulakovskaya, 1 9 5 9 ) . In s o m e localities, the recruitment o c c u r r e d w h e n gravid w o r m s w e r e still present, similarly to the situation in the Jihlava River in J u l y 1 9 9 2 .
Finding several gravid w o r m s in barbel s a m p l e d in O c t o b e r 1 9 9 2 indicates the possibility o f a c c e l e r a t e d growth and sexual d e v e l o p m e n t o f s o m e s p e c i m e n s in the s a m e year o f their recruitment. T h e d e c r e a s e o f water temperature in N o v e m b e r a n d D e c e m b e r m a d e it impossible for these w o r m s to c o m p l e t e their sexual maturation.
Seasonal patterns in maturation have also b e e n found in other tapeworms parasitizing freshwater fish in mid- latitude r e g i o n s o f E u r o p e ( a l m o s t all c o n t i n e n t a l E u r o p e and Ukraine according to C h u b b , 1 9 8 2 ) . In pseudophyllideans, seasonality in the o c c u r r e n c e and maturation h a v e b e e n r e p o r t e d in BOTBRIOCEPBALUS ACHEILOGNATHI, B. CLAVICEPS, TRIAENOPHORUS NODULOSUS, EUBOTHRIUM CRASSUM and E. RUGOSUM (for e x t e n s i v e review s e e C h u b b , 1 9 8 2 ) . In C z e c h Republic, s e a s o nality in maturation has b e e n found in BOTBRIOCE
PBALUS CLAVICEPS (Moravec, 1 9 8 5 ) , TRIAENOPHORUS NODU
LOSUS (Ergens, 1 9 6 6 ; Moravec, 1 9 7 9 ) , PROTEOCEPHALUS PERCAE ( M o r a v e c , 1 9 7 9 ; Scholz, 1 9 8 6 ) , P. TORULOSUS ( S c h o l z , 1 9 8 9 6 ; Scholz & Moravec, 1 9 9 4 ) . In most c a s e s w o r m s b e c a m e gravid in late spring and early summer.
T h e finding o f o n e p r o c e r c o i d , w h i c h r e s e m b l e s those o f B . RECTANGULUM as d e s c r i b e d b y K u l a k o v s k a y a ( 1 9 6 3 ) , in the c o p e p o d MACROCYCLOPS ALBIDUS d e m o n s trated that they m a y serve as intermediate hosts o f this tapeworm. T h i s c o p e p o d s p e c i e s has already b e e n p r o v e d to serve as an e x p e r i m e n t a l intermediate host o f B . RECTANGULUM (Kulakovskaya, 1 9 6 3 ) .
Higher p r e v a l e n c e o f B . RECTANGULUM t a p e w o r m s in smaller fish from the Jihlava River c o m p a r e d to larger barbel might indicate that smaller fish c o n s u m e more plankton, including c o p e p o d s . Heavier intensity o f infection in s o m e larger barbel might b e e x p l a i n e d by larger amount o f food c o n s u m e d , including planktonic animals; piscivory d o e s not s e e m to play an important role in the parasite transmission and accumulation o f parasites in larger fish s p e c i m e n s since forage fish represent o n l y a negligible c o m p o n e n t o f barbel diet (Losos ET AL., 1 9 8 0 ; M o r a v e c & Scholz, 1 9 9 5 ) .
Evaluation o f the distribution o f t a p e w o r m s in the digestive tract o f fish s h o w e d that BATBYBOTHRIUM REC
TANGULUM preferred the anterior part o f the intestine as its site o f location. Although the value o f these data
Parasite, 1996, 3, 39-44
43
may b e limited by the fact that the fish w e r e e x a m i n e d 1-2 days after their capture, the p r e s e n c e o f tape
w o r m s firmly attached with their s c o l e x in the intes
tinal epithelium does not support the assumption about unnatural migration o f the w o r m s in captivity. In addi
tion, similar patterns in the site o f location ( p r e f e r e n c e for the anterior part o f the digestive t u b e ) has b e e n reported in other fish tapeworms.
ACKNOWLEDGEMENTS
T
h e authors are indebted to Mr. J o s e f Melkus and o t h e r officials o f the Association o f Moravian F i s h e r m e n in B r n o a n d N o v a V e s u Oslavan for their permission to take s a m p l e s o f fish and assistance in capturing the fish. Our thanks are also d u e to Mrs. M. Holinkova and I. Husakova, Institute o f Parasitology, AS CR, for their e x c e l l e n t technical assistance. Dr. J . Leps-, Faculty o f Biological S c i e n c e s , University o f South B o h e m i a , C e s k e Budejovice, is a c k n o w l e d g e d for advice and a n o n y m o u s referees for their constructive criticism and valuable remarks. This work was supported by the grant no. 6 2 2 1 0 o f the Aca
d e m y o f S c i e n c e s o f the C z e c h Republic and b y the grant n o . G Z 4 5 . 3 1 3 / 2 - I V / 6 a / 9 3 o f Bundesministerium fur Wissenschaft und Forschung, Austria.
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Reçu le 2 novembre 1994 Accepté le 26 juillet 1995
44 Parasite, 1996, 3, 39-44
