Observations on the trematode parvatrema affinis, causative agent of crawling tracks of macoma balthica

Netherlands Journal of Sea Research 8 (1) : 108-115 (1974)

OBSERVATIONS ON THE TREMATODE P A R V A T R E M A A F F I N I S , C A U S A T I V E A G E N T OF C R A W L I N G T R A C K S OF M A C O M A B A L T H I C A by C. S W E N N E N

(Netherlands Institutefor Sea Research, Texel, The Netherlands) and HILDA

L. C H I N G

(Department of Zoology, Universityof British Columbia, Vancouver,Canada) CONTENTS

Io I n t r o d u c t i o n .

. . . . . . . H i s t o r i c a l r e v i e w o f t h e species . Methods and materials . . . . . Descriptions . . . . . . . . 1. S p o r o c y s t s . . . . . . . 2. C e r c a r i a e . . . . . . . . 3. M e t a c e r c a r i a e . . . . . . 4. A d u l t s . . . . . . . . . g. Comparisons with previous reports . VI. Incidence of infection . . . . . . . . . . . . . VII. Discussion . . . . . . . . VIII. Summary . . . . . . . . IX. References II. III. IV.

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108 108 109 109 I09 110 110 111

112 112

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

SWF.NNEN (1969) observed that Macoma balthica (L.) which produced crawling tracks on sand were 100% infected with a trematode, while those normally buried in sand had a much lower infection rate. The trematode was not named but belonged to the family Gymnophatlidae. In this paper, the trematode will be described as Parvatrema afinis (Jameson and Nicoll, 1913) James, 1964 and compared with earlier descriptions. The incidence of infection in clam hosts of various ages, collected at different tidal levels will be presented. II. HISTORICAL

JAMESON&

REVIEW

OF THE

SPECIES

NICOLL (1913) described Gymnophallus affnis from the intestine of Melanitta nigra; the host ducks were stated to come from the Netherlands (Zwarte Water, near the former Zuiderzee). SFLIKMAN (1953) reported on the life cycle of this species from Kandalaksha Bay

PARVATREMA

AFFINIS

109

in the White Sea. He found cercariae and metacercariae within sporocysts in Macoma balthica. In experimental feedings of the metacercariae to Sterna paradisea, Haematopus ostralegus, Larus argentatus, and Fells domestica, SELIKMAN obtained adults similar to those described by JAMESON• NICOLL. SELIKMANconsidered the larval stages of G. affnis to be identical to MARKOWSKfS (1937) Metacercaria morula from Macoma balthica in the Baltic Sea although MARKOWSKIdid not describe the cercarial stage or conduct any experimental infections to obtain adults. JAMES (1964) examined specimens of Gymnophallus affnis in the British Museum (Natural History) collected from Melanitta nigra in Kent in 1936 and 1937. He himself found the species in Haematopus ostralegus occidentalis in Swansea, South Wales. JAMEStransferred the species to the genus Parvatrema because of its minute body size and the presence of a large genital pore. LOOS-FRANK (1971) found the larval stages of P. affnis in Macoma balthica and the adults in Melanitta nigra, M. fusca, Haematopus ostralegus, Somateria mollissima, and Larus argentatus in the southern part of the North Sea. III. METHODS AND MATERIALS Specimens of Macoma balthica were collected at various tidal levels of mud flats and localities along the Dutch coast as described by SWENNEN (1969) and HULSCHER (1973). Observations of the trematodes were made on living material and supplemented by preparations of fixed metacercariae in situ (within sporocysts in host tissue) and fixed, stained adults. The adult stage was obtained after experimental infection with metacercariae of young ducks, Anas platyrhynchos. The infected ducks were examined after 4 hour, 24 hour, and 1 week. IV. DESCRIPTIONS 1. S P O R O C Y S T S

Although there are no sporocysts within the gills, velum, siphons, intestine, or muscles, all available space within the gonads and digestive gland of infected Macoma balthica is filled with the immobile, white sacs of this parasite (see SWENNEN, 1969: Plate II, Fig. 1). The sporocysts are variable in size and rounded at both ends; 16 sporocysts gave a range of 250 to 2,200 ~tm by 250 to 425 ~tm with most sporocysts about the body size of 612 by 350 ~tm. The number of sporocysts varies and is dependent upon the size and age of the host (Table I).

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&

HILDA

TABLE

L.

CHING

I

Relation of shell length of 4 infected specimens of Macoma balthica to number of sporocysts of Parvatrema a~nis. Shell length (mm)

Number of sporocysts

6.0 13.8 18.2 23.2

52 353 2,111 3,457 2. C E R C A R I A E

Sporocysts with germ balls and cercariae were rarely present. Therefore, the cercarial development into the metacercarial stage must be very rapid. Most sporocysts contained only metacercariae. Thus Macoma balthica serves as both first and second intermediate hosts for Parvatrema affnis. 3. M E T A C E R C A R I A E

The number of metacercariae varies according to the sporocyst size. For instance, 7 sporocysts ranging in length from 250 to 2,200 ~m contained 2 to 246 metacercariae; in sporocysts of average size (612 by 350 ~m), there are about 40 metacercariae. Measurements of at least I0 specimens are gathered in Table II. T h e b o d y (Fig. I) is entirely spined, oval with r o u n d e d anterior end and pointed posterior end (almost round w h e n contracted); body length a n d width w h e n alive 150 to 204 by 95 to 170 ~m; preserved TABLE II

Comparison of morphological data of Parvatrema a~inis. Markowski (1937)

Selikman (1053)

Swennen ~ Ching (1974)

Host

Shell length (mm) 5-13 6.0-23.2 Sporocysts Number 40-500 52-3,457 Size (/~m) 500-1,000 X ? 155 X 77 250-2,200 X 250-425 Metacercariae Numb. per sporocyst 46* 3-16 2-246 (40) Size (/~m) 150 × 90 168-244 × 96-144 150-204 × 95-170 Oral sucker (/~m) 54 X 60 56-72 45-55 Ventral sucker (/~m) 35 × 35 20-40 19-32 Pharynx (#m) 16 x 16 12-19 x 12-16 * According to figure.

PARVATREMA

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91 to 120 by 71 to 91 Ezm. Oral sucker with lateral papillae, mouth opening surrounded by symmetrically placed sensory papillae, oral sucker twice the size of ventral sucker, transverse diameter when alive 56, preserved 45 to 55 Ezm. Ventral sucker with crenelated opening, transverse diameter when alive 28, preserved 19 to 32 ~m. Pharynx

Fig. 1. Free-hand drawing ofphotomicrograph of live metacercaria with genital pore. well developed, 12 to 19 by 12 to 16 Ezm; prepharynx and oesophagus not distinct. Ceca not lined with cellls; short, inflated sacs 12 to 26 ~zm in length diverging obliquely or transversely from pharynx. Genital pore measuring 13 to 23 ~zm across, transverse slit on the ventral surface, slightly anterior to ventral sucker. Testes diagonal, posterior to ventral sucker; right testis may be at level of ventral sucker, oval to round, each testis 14 to 19 by 9 to 16 ~zm. Ovary slightly larger than testes, dextroanterior to ventral sucker, 16 to 23 by 13 to 21 Ezm. Vitellaria small, compact, occasionally fused to form dumb-bell shape, dorsal to and overlapping ventral sucker. Excretory vesicle V-shaped with bicornutate ends at sides of oral sucker or pharynx. Flame cells, at least 10 on each side. 4. ADULTS

In experimental feedings of metacercariae to young ducklings, adult trematodes were found most numerous in the small intestine. Egg production began as early as 4 hours after infection with 10 to 29 eggs produced after 24 hours in the host. Adults recovered after one week in a duckling appeared somewhat degenerate but contained many more eggs. Adults measured alive were slightly larger, 160 to 250 ~m in length, but were otherwise similar to the metacercarial stage. However, the round seminal vesicle of 26 by 13 ~tm, prominently filled with sperm, lies anterodorsal to the ventral sucker and may almost equal

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& HILDA

L.

CHINO

it in size. The seminal vesicle is surrounded by few prostatic cells before joining the genital atrium and the wide genital pore. The vitellaria become crescentic or irregular in shape. Eggs, mainly in the hind body, are very large, 18 to 27 by 10 to 17 ~m. V. COMPARISONS WITH PREVIOUS REPORTS SELIKMAN (1953) reported smaller sporocysts, 155 by 77 ~tm, and only 3 to 16 metacercariae per sporocyst in M. balthica with shell lengths ranging from 5 to 13 m m (Table II). The small size of the sporocysts may be due to the smaller maximum size of the clams in Kandalaksha Bay. It is not known if there are smaller sporocysts in younger, smaller clams, but their numbers definitely increase with increasing size of the host, as shown in Table I. Measurements of metacercariae given by SELIKMAN (1953) and MARKOWSKI (1937) compare favourably with the present ones (Table II). MARKOWSKIdescribed a genital sucker in the metacercaria which we have not been able to find. Any one of the structures anterior to the ventral sucker may have been construed as one such as the contracted genital pore, shallow genital atrium, curved uterus, wide prostatic duct, or even the round seminal vesicle. The vitellaria show variable shapes most probably due to age and different methods of fixation. MARKOWSKI described the organs as compact with curved edges while SELIKMANpictured them as a single dumb bell organ. Although we have observed the vitellaria to be usually compact with smooth edges, a few specimens do show single, bi-lobed organs. In adults, the vitellaria vary greatly from compact to highly irregular shapes. JAMESON & NICOLL (1913) described them as crescentic. Both JAMESON & NICOLL (1913) and JAMES (1954) observed very small Parvatrema affnis with respective lengths of 130 to 190 vtm and 140 vm in comparison to other specimens which were 200 to 250 by 110 to 130 ~m. With such enormous numbers present in infections in bird hosts, a wide range of body sizes would be expected. There appears to be some body shrinkage due to fixation but sucker ratios and egg sizes remain remarkably constant in all reports of the species. VI. INCIDENCE OF I N F E C T I O N The incidence of infection of Macoma balthica with Parvatrema affnis is summarized in Table III. In subtidal or lower parts of the tidal flats, the incidence is very low but in the higher parts of the tidal flats, it ranges from 1.5 to 20~/o. As the depth distribution of M. balthica in the

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PARVATREMA AFFINIS TABLE

III

Incidence of infection of Macoma balthica with Parvatrema aflinis in the Dutch coastal waters. The data from Schiermonnikoog are according to HULSCHER (1973).

Locality North Sea Off Texel Off Kijkduin Wadden Sea Scheer Vlieter Balgzand Schiermonnikoog Terschelling Texel

Den Helder Wieringen Rhine Delta Beach of Rozenburg

Depth (m)

Date

6-12 8-15

.Number examined

Incidence (%)

1965 1965

65 53

0 0

5-9 2-4 < MSL < MSL > MSL > MSL > MSL > MSL > MSL > MSL > MSL > MSL > MSL > MSL

1966 1968 1967-1972 1967 Jun. 1967 Aug. 1967 Apr. 1955 Aug. 1968 Apr. 1968 Oct. 1968 Dec. 1968 Jul. 1973 May 1957 Jun. 1957

162 290 5000 534 3588 52 72 110 234 48 199 91 137

0 1 < 1 < 1 12.3 15.0 13.4 16.6 5.4 7.2 6.2 1.5 11.0 14.6

> MSL

March 1958

59

20.3

Dutch coastal waters ranges from the upper half of the tidal zone to 15 to 20 m subtidal, only a small fringe of the Macoma population is a f f e c t e d - - t h a t dwelling in the u p p e r p a r t of the tidal zone. F u r t h e r , t h e i n c i d e n c e i n c r e a s e s w i t h shell l e n g t h (age) ( T a b l e I V ) . T h e s m a l l e s t i n f e c t e d c l a m h a d a shell l e n g t h o f 6.0 m m a n d was o v e r a y e a r old.

TABLE

IV

Incidence of infection with Parvatrema a~inis according to shell length (age) of Macoma balthica from the higher part of the tidal zone, the Mok, Texel; all samples of 1968.

Shell length (ram) < 6 6-10 11-15 16-20 21-25

Age (years)

Injection (%)

0

0

1-2 2-3 ~ 3 ~ 4

1 3 15 32

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VII. DISCUSSION The distribution of Parvatrema aj~nis in the North, Baltic, and White Seas appears limited to a single intermediate host, Macoma balthica, and definitive hosts such as birds which use this mollusk in their diet. It seems reasonable to expect this parasite to be reported elsewhere in the boreal North Atlantic and Arctic which is the range for Macoma

balthica. Previous authors gave the following incidences of infection of Parvatrema affnis in M. balthica: MARKOWSKI (1937), 0.7% at a depth of 25 to 30 m in the Baltic Sea; SELmMAN (1953), not exceeding 6.6% in the middle and lower levels of sandy shores of the White Sea; and LOOS-FRANK (1971), 7.5% in the tidal zone of the southern part of the North Sea. The single figures for the incidence of infection can be misleading without the correlation of host size and age to the host distribution at various tide levels. HULSCHER (1973) also found positive correlation between the infection rate of P. affnis and the shell length (age) of Macoma balthica. In high intertidal flats, he found 5 to 44% of the clams in the size range of 11 to 20 mm to be infected. Further, these larger, older infected clams in the upper tidal flats exhibited surfacing and crawling behaviour. DINEEN (personal communication), working with M. balthica in River Ythan estuary, Scotland (North Sea) found that the surfacing and crawling behaviour is in response to an oxygen shortage stimulus caused by the large density of the metacercariae. Parvatrema affnis can be regarded as a successful parasite because the sporocyst, cercarial, and metacercarial stages are confined to one intermediate host. This host harbours a massive infection of minute but well developed larvae which are capable of immediate egg production in the definitive host. The infected clams produce crawling tracks on the sand, unusual behaviour that possibly attracts the definitive hosts to eat them. That parasites may alter the behaviour of the intermediate hosts and thus increase chances of predation by the definitive hosts has been reviewed recently by HOLMES & BETHEL (1972). In the summer months, large numbers of infected clams have been found dying on the sand surfaces (HuLsCHER, 1973). Although the mortality of infected clams is high, it can be surmised from the massive infections of single clams that only a few need to be eaten in order to maintain the life cycle in that locality. VIII. SUMMARY Stages in the life cycle of Parvatrema affnis were studied and compared

PARVATREMA AFFINIS

115

with previous descriptions by MARKOWSKI (1937) a n d SELIKMAN (1953). T h e cercariae quickly develop into m e t a c e r c a r i a e a n d r e m a i n within the sporocysts which heavily parasitize the i n t e r m e d i a t e host, Macoma balthica in the tidal zone o f the W a d d e n and N o r t h Seas. T h e a d u l t stage, recovered from e x p e r i m e n t a l infections o f Anas platyrhynchos is similar to t h a t described b y JAMESON & NICOLL (1913) and JAMES (1964). Older, larger clams in the u p p e r littoral zones were most highly infected with P. aflinis. These infected clams exhibited surfacing and crawling tracks on the sand, changes in the b e h a v i o u r o f the hosts which m a y increase risk of p r e d a t i o n by birds, the definitive hosts. IX. R E F E R E N C E S

HOLMES,J. C. & W. M. BETHEL,1972. Modification of intermediate host behavior by parasites.--J. Linn. Soc., Zool. 51: 123-149. HULSCHER,J. B., 1973. Burying-depth and trematode infection in Macoma balthica.-Neth. J. Sea Res. 6 (1-2): 141-156. JAMES, B. L., 1964. The life cycle of Parvatrema hornoeotecnumsp. nov. (Trematoda: Digena) and a review of the family Gymnophallidae Morozov, 1955.--Parasitology 54: 1--41. JAMESON,H. L. & W. NmOLL, 1913. On some parasites of the scoter duck (Oedemia nigra) and their relation to the pearl-inducing trematode in the edible mussel (Mytilus edulis).--Proc, zool. Soc. Lond. 12: 53-63. LOos-FP.ANK,B., 197 I. Zur Kenntnis der gymnophalliden Trematoden des Nordseeraumes. IV. ~bersicht tiber die gymnophalliden Larven aus MoUusken der Gezeitenzone.--Z. ParasitKd. 36: 206-232. MARKOWSKI,S., 1937. ~ber die Trematodenfauna der baltischen MoUusken aus der Umgebung der Halbinsel Hel.--Bull. int. Acad. pol. (B) 1937 (2) : 285-317. SELIKMAN,E. A., 1953. (On the life cycle of the bird trematode, Gymnophallus aflinis Jameson & Nicoll, 1913).--Dokl. Akad. Nauk 91:989-992 (in Russian). SWENNEN, C., 1969. Crawling-tracks of trematode infected Macoma balthica (L.).-Neth. J. Sea Res. 4 (3) : 376-379.