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(Makerere University College Medical School, P.O. Box 2072, Kampala, Uganda) IN the summers of 1956 and 1957 I was able to spend a few weeks looking at larval trematodes from the Stour and other rivers near Fiatford, Suffolk. I had hopes of returning to study them more fully but a continuing period abroad is rendering this unlikely. This is therefore an account of these incomplete observations: they are recorded in case they may interest or assist the amateur microscopist who may encounter a larval trematode and wonder about its nature. T h i s introduction is more than usually personal intentionally: the literature is cluttered with brief descriptions purporting to be specific diagnoses and it is cssential to realise that none of the accounts that follow are to be taken as a specific designation nor are the n u m b e r s attached to the different forms more than my reference numbers. Anyone who reads them as species records will be placing on them a construction that the data will not bear. T h e trematoda, or flukes, comprise three subgroups. Here our concern is with the digenetic trematodes which are flattened, often leaflike, parasites of vertebrates when adult, with larval forms parasitic in molluscs with or without the addition of a third or even a f o u r t h host. T h e s e additional hosts may be molluscs, FIG. 1.

T h e digenetic trematode life cycle Adult fluke in V E R T E B R A T E

Metacercaria, free or

Egg in exereta

in M O L L U S C , L E E C H , F I S H , etc.


Miracidium in water

Cercaria in Water \ \ D a u g h t e r Redia of Sporocyst in M O L L U S C

Mother Redia ^

In M O L L U S C


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vertebrates, or such animals as insect larvae. FIG. 1 outlines the life cycle of digenetic trematodes and introduces the names of the various stages. Eggs are laid in the vertebrate host, pass out with the excreta, and hatch in water to release ciliated miracidia which penetrate molluscs. Development in a suitable host species through redia and sporocyst stages (or one of these) gives rise to cercariae which escape from the mollusc and encyst either free or after entering a second intermediate host. T h e encysted form is known as a metacercaria and is ingested by the final vertebrate host where it matures to the adult fluke. T h i s is the general scheme, but many species depart f r o m it to a greater or lesser extent. T h e British, and particularly English, larval trematode fauna of fresh water has been but little studied: for example, at the time of the work described here no records of any larval trematodes from Bithynia tentaculata in Britain had been published, yet, as may be seen f r o m this account, it is very heavily parasitised, at any rate in the Fiatford area. T h e Stour Valley provides an excellent region for the study of trematodes and it is to be hoped that more detailed and complete observations will be made there. In the account which follows a fairly fĂźll description is given of methods, some of the organisms found are described and illustrated, and then the distribution and abundance of the parasites in each species of host is considered.

Material and Methods Molluscan potential hosts were collected from the River Stour and its tributary the Brett in September, 1956, and July, 1957. On both occasions the main collection was of Bithynia tentaculata from D e d h a m Mill Pool. Some Lymnaea and Valvata were also taken there in 1956. Below Dedham Potamopyrgus jenkinsi was collected from the lower end of the boundary stream and various species at sites between Fiatford and D e d h a m Mills. In 1957 other sites were the Stour above Dedham, the junction of Brett and Stour and a series of stations up the Brett at Cherry Hill, Semer Bridge, and Chelsworth. T h e y are fully listed, together with t h e n u m b e r s of molluscs taken, in T a b l e 1 of the results. In addition ten leeches, Erpobdella octoculata, from Fiatford were examined for encysted metacercariae and none were found. Four roach and a dace from the Stour above Fiatford were dissected. T h e only adult parasite found was an unidentified flatworm, but two roach had encysted metacercariae. For collection of trematode larvae each snail was identified and measured. It was then left in a speeimen tube with a little filtered river water for two days. Any emerging cercariae could be seen against a dark background. Artificial strong illumination was used intermittently to speed emergence. T h e snail was crushed




in a little water and its tissues teased out under the binocular microscope. Rediae and cercariae, if present, were usually conspicuous; most were in the digestive gland. Encysted metacercariae were usually in smaller numbers, mainly in the mantle tissues. For detailed examination living cercariae were transferred in a drop of water to a slide and a very thin coverslip applied. Water was carefully abstracted from its edge using blotting paper until the cercaria was just prevented from moving. It was then examined chiefly by a 1/7" oil immersion objective with x l O and x 2 0 eyepieces. A green filter reduced eyestrain. As the water under the coverslip evaporated the cercaria was further compressed. T h e greatest detail could be seen in the last few minutes before the larva disintegrated. Vital staining by methylene blue was sometimes used. Measurements of living and preserved (5% formalin) material were made using an eyepiece micrometer. Fixed and stained cercariae are useless for identification purposes. Metacercariae were released from their cysts using fine entomological pins. Borax carmine staining was useful for them. T h e detailed structure of cercariae is hard to see; tracing out the excretory system is particularly tedious, taking many days, and is the reason for the incomplete descriptions. Results T h e parasites found are listed, by year and host in Tables I and II. Bithynia tentaculata was the most fully investigated mollusc. Its parasites are given in Table II. Five species of trematodes in 1956 were examined in some detail and are described in order. Observations on the remaining ones, from a variety of snails, were so scanty that they are reviewed by host spccies in the second part of this section. A.



Cercaria A





2 to 5).

This was found in two of the fifty Bithynia from Dedham. It had a relatively large body but the tail was much reduced. T w o suckers were present of which the ventral was larger. A small stylet was present by the oral sucker, from which the gut extended a short way caudally. A pharynx was seen. T w o stylet gland ducts were present but details of the glands and of flame cells could not be made out. T h e excretory vesicle was large, globular and distinct with a prominent epithelium. T h e tip of the stumpy tail was usually invaginated but was eversible. Locomotion was by a leech-like creeping. T h e cercariae developed in motile rediae in which the pharynx could be seen. T h e r e were twenty to thirty cercariae per redia. T w o were hyperparasitised as will be described below.

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T h i s microcercous cercaria corresponds exactly with the account of Cercaria micrura given by W e s e n b e r g - L u n d (1934) though less so with that of L u h e (1909). C. micrura is the larva of Sphaerostoma bramae, which has been recorded from the gut of the roach in Cambridgeshire (Dawes 1947). Closely related forms are recorded by Probert (1965A). 2



(FIGS. 5 t o 7).

T w o of the C. micrura rediae contained a cyst-Iike object. T h e snail involved showed no other evidence of a second parasite. T h e cysts were opaque and pigmented. One was serially sectioned and reconstructed from drawings; it was a strigeid metacercaria having the characteristic holdfast organ caudal to the vental sucker and anterolateral groves. T h i s stage is usually known as tetracotyle and may occur in a variety of hosts. M o r e precise identification is not possible f r o m the available material. T h e occurrence ot tetracotyle within other trematode rediae has been noticed by various workers. W e s e n b e r g - L u n d (1934) comments on it and says it was first seen by Steenstrup in 1842, whilst an adaptive modification of it was described by Cort, Olivier, and Brackett (1941). Hvperparasitism of Cercaria micrura has only been recorded once, to my knowledge, and this was by W e s e n b e r g - L u n d who found cercariaeum cysts within the rediae. 3.



(FIG. 10).

T h e body of this cercaria was ovoid, capable of great elongation, and its anterior part had a rough or spinous cuticle. T h e oral sucker was larger than the ventral and was armed with a stylet. T h e hind part of the oral sucker appeared to contain two large ovoid bodies known as the virgula organ. T h c r e were three pairs of stylet gland cells at the level of the ventral suckers. T h e i r Contents were granular and escaped along duets opening at the stylet base. A pharynx was present. T h e bicornuate exeretory vesicle opened at the base of the tail which, at rest, was rather shorter than the body. T h e cercaria swam head-first and rested with the tail upwards at an angle to the body. T h e cercariae were developing in small sporoeysts, each with two to seven or more cell masses or cercariae. T h e y were found in a single quite unusually large Bithynia tentaculata from D e d h a m . T h e presence of a stylet assigns this to the xiphidiocercaria group whilst the oral organ is characteristic of the 'virgula' subgroup. Quite a n u m b e r are described, mostly inadequately, f r o m Europe. M y form is similar to that described by W e s e n b e r g - L u n d (1934) as 'C. Helvetica I X Dubois'. It does not resemble Dubois' (1929) original description of that form at all closely however, and f u r t h e r speculation would be unprofitable.






(FIGS. 8 t o 9).

Another xiphidiocercaria, this was rather smaller than the preceding one and had no virgula organ. Of the two suckers, the ventral was small and in the posterior half of the body. T h e oral sucker was armed with a stylet having wing-like projections 1/3 of the way f r o m its tip. T w o large anterior stylet glands had ducts ending at its base and the coarsely granular secretion of these cells could be Seen passing u p the ducts. T h e remaining gland cells had very finely granular Contents and were either four or six in n u m b e r and difficult to distinguish. A pharynx was present T h e excretory vesicle was large, bicornuate and conspicuous T h e tributaries of the main excretory ducts are seen in the illustration. T h e vesicle opened at the base of the tail. T h i s was as long as the body when extended and contracted to half of that length. Swimming was with the oral sucker foremost. Cercariae attached to the substratum made penetrating movements with the stylet at a rate of 130 jabs each minute. T h i s form infected seven out of fifty R. tentaculata from D e d ham. Four were unusually large—it is possible that infaction may cause gigantism, as shown for Sabsnea ulvae by Rothschild (1941). It was the commonest form at D e d h a m in 1956. T h e r e were usually seven to eight cercariae in each sporocyst. T h i s xiphidiocercaria, with its length under 200 JA, a small rather posteriorly placed ventral sucker, and no finfold on its tail belongs to the 'microcotylae' subgroup of L u h e (1909) and the 'vesiculosa' division of Sewell (1922). It also fits the 'helvetica' group proposed by Dubois (1929) and is similar to his Cercaria helvetica X I I .








T h e body of this cercaria was more elongated than those of the preceding forms, and the tail was m u c h longer than the body. There was a large oval unarmed oral sucker. T h e ventral one was of variable size and often difficult to see. T w o black pigment spots were present a third of the way from the front of the body, and a pharynx at the same level. In addition the gut had a pre-[ pharyngeal wall thickening at the caudal end of the oral sucker. T h e whole cercaria was pigmented and opaque; gland cells were not clearly seen. T h e r e was an oval excretory vesicle. T h e tail bore a finfold for the whole of its length, wider near the tip. Locomotion alternated between intense swimming activity and slow creeping. T h e cercariae came f r o m a single specimen of Bithynia tentaculata and developed in rediae with elongated pharynges.

278 Transactions of the Suffolk Natnralists',

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In Europe a similar form has been recorded from B. tentaculata by Dubois (1929), Wesenberg-Lund (1934), and Probert (1965B) from Wales under the name Cercaria lophocerca, Fil. This is however a composite species and all that can be said is that my form may well be a member of the Opisthorchioidea. B.


Of 260 molluscs examined, eighty were infected by trematodes (sometimes more than one species at once) and the parasites belonged probably to a score or more different species, most of which could only be cursorily described. It was not possible to decide whether similar organisms in the two years were conspecific or merely closely related and therefore 1956 forms are referred to by capital letters and those found in 1957 by low er case letters. T h e various host species will be considered in turn. 1. Bithynia tentaculata in 1956 at Dedham Mill Pool yielded Cercariae A to E which have already been described. T h e fĂźll list of parasites is given in Table II. One snail contained sporocysts with around five germ balls each. Two molluscs had metacercariae encysted in the superficial tissues and mantle. The parasites had a ring of collar spines typical of echinostomes (FIG. 22). Only a few cysts were present in each host. Another encysted form occurred in vast numbers in a single Bithynia. It could not be further identified. Metacercaria F (FIGS. 15 to 17) was encysted in three of the snails. It was extracted from its cyst. T h e cuticle was spiny and part of the reproductive organs were visible. It resembled C. pali dinae impurae (larva of Asymphylodora tincae) as described by Wesenberg-Lund (1934). I n 1957 the Dedham B. tentaculata were less heavily parasitised. Five had a xiphidiocercaria (a) that could have been conspecific with C and one was infested with a virgulate xiphidiocercaria. T w o snails contained developing forms: one large sporocysts (e) and the other a redia (k). Three had large encysted metacercariae and one small one. Even those snails that were shedding cercariae produced rather few, and on dissection showed many immature forms, suggesting that in both years the majority of cercariae would be shed in the late summer. FIG. 24 shows a size-frequency histogram of the 1957 Bithynia samples examined and it is clear that the larger snails are most frequently infected with trematodes. This may be simply due to the larger specimens being older and therefore exposed to the possibility of infection longer, but some trematodes have been shown to produce gigantism in their snail hosts. Bithynia from several other sites were examined in 1957. From all sites encysted metacercariae of one form or another were taken. Those from the Stour between Dedham and Fiatford shed






: 1957

infected uninfected






8 Size




nearest FIG.






xiphidiocercariae of two species: (b) which was probably conspecific with (a), and a virgulate form (d). Virgulate xiphidiocercariae (c) were also shed by a snail from Chelsworth on the Brett. 2. Lymnaea pereger was heavily parasited both years. In 1956, nineteen of thirty specimens collected at the source of the boundary stream from the Stour were infected by echinostome cercariae. The same sample yielded a xiphidiocercaria and one unarmed monostome cercaria with three pigment spots (N). Other sites in both years yielded cysts of several types. Tetracotyle were common (FIG. 22) and resembled those encysted in type A rediae; xiphidiocercariae and echinostomes were found, and also several immature stages. 3. A few Lymnaea stagnalis from various sites shed xiphidiocercariae and furcocercariae. These last have forked tails which


280 Transactions of the Suffolk Naturalists', Vol. 13, Part 5 precede the body in swimming upwards. DĂźring periods of rest the cercaria sinks slowly, and by alternating between this and activity the cercaria maintains its position in the water. 4. Cercaria S (FIGS. 13 and 14) was a longifurcate distome cercaria brought to me in water containing Potamopyrgus jenkinsi. T h e Container was left for a day for more cercariae to emerge but none did so, and those present disappeared. On dissection, none of the snails contained sporocysts but the furcocercariae had shed their tails and were creeping amongst the molluscan tissues. Whether Potamopyrgus is ever a natural second intermediate host for this trematode is unknown and no more were found on dissecting other Potamopyrgus. No other molluscs usually occur in the Stretch of water from which the snails and cercariae came, and no parasites of Potamopyrgus jenkinsi are recorded in the literature (and indeed its rapid spread has been ascribed to this apparent immunity).

Only a few of the other molluscan species were dissected and the results are given in Table I. 5. In the course of the dissections some other parasites besides larval trematodes were encountered. One Bithynia from Dedham contained an unidentified nematode, and the shell of another contained two small leeches, Glossiphonia heteroclita. They may be more correctly termed micro-predators. The snail concerned was also shedding cercaria D. Much more common was the oligochaete worm, Chaetogaster limnaei which was found in 10% of the Bithynia and up to 75% of the Lymnaea pereger from the boundary stream. Some have considered this worm to be a parasite of snails whilst others have maintained that it is primarily a predator on trematode larvae. Not all the snails harbouring Chaetogaster here were otherwise parasitised, but the oligochaete was most abundant in the two most heavily infected samples of molluscs. Two roach, out of four taken at Fiatford, each had four metacercariae encysted subcutaneously. The cysts were surrounded by black pigment. Details of the morphology of this form (T) are given in FIGS. 18 to 21, and it is probably Posthodiplostomum cuticola, certainly a strigeid trematode. Discussion and Conclusion This very incomplete survey demonstrates how commonly larval trematodes may be found in East Anglia. Wesenberg-Lund (1934) considered that in Denmark Bithynia tentaculata was the most heavily infected freshwater snail as far as the number of trematode species was concerned, yet none had been recorded from England when the present work was done, though many have been



described since (see Nasir and Erasmus, 1965). It is clear that intensive work on a few species is needed, with füll descriptions of the cercariae and there are signs that in the years between the present observations and their reporting helminthology has b e c o m e a more populär study. T h e systematics of the groups are difficult however, a n d the literature in many ways confusing. Nevertheless, apart f r o m a good microscope, no apparatus is needed for their morphological study whilst very little is k n o w n about their behaviour or their effect o n molluscan ecology. This account therefore raises m a n y questions a n d answers few. It is to be h o p e d that someone may be able to find time for an intensive s t u d y of these fascinating animals a r o u n d Fiatford.

Summary A variety of trematodes f r o m the freshwater molluscs of the Stour are briefly described. A strigeid tetracotyle is recorded as a hyperparasite of Sphaerostoma rediae.



M y wärmest thanks are due to M r . F. J. Bingley, the W a r d e n of Fiatford Mill, for encouragement, facilities, and advice, and also to Miss J. Walker who was t h e n his assistant Warden. W o r k during 1957 was m a d e possible by the award of the Morley bursary. T h e H o n . M i r i a m Rothschild gave m u c h welcome encouragement, Dr. H. D . Crofton identified one species, and D r . C. A. W r i g h t kindly read the manuscript.

I References Cort, W. W., Olivier, L., and Brackett, S. (1941). Dawes, B. (1947). Society.


J. Parasitol

Trematoda of British Fishes.

27: 437-4S. London


Dubois, G. (1929). Bult. Soc. Neuchatel. Sei. Nat. 53: 3-177. Luhe, M . (1909). (In) Die Susswasserfauna Deutschlands 17. Nasir, P. and Erasmus, D . A. (1964). J. Helminthol 38: (3, 4) 245-68. Probert, A. J. (1965A).

J. Helminthol

39: (1) 35-52.

Probert, A. J. (1965B).

J. Helminthol

39: (1) 53-66.

Rothschild, M . (1941). Parasitology 33: 406-15. Sewell, R. B. S. (1922). Ind. J. Med. Res. 10, Supplement Cercariae Indicae. Wesenberg-Lund, C. (1934). 9: 5(3).

D. Kgl.





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Parasites Found

No. Exam.

Site Species D e d h a m Mill Pool Bithynia tentaculata Lymnaca pereger

50 16

See Table I I Xiphidiocercaria Cercaria Metacercaria Redia Motile sporocyst Nil


Creeping cercaria

Lymnaea auricularia Valvata piscinalis Boundary Stream at Sluice Potamopyrgus jenkinsi

Head of Boundary Stream near D e d h a m Lymnaea pereger 30 Echinostome Cercaria Xiphidiocercaria JULY,

D e d h a m Mill Pool Bithynia


Stour above Fiatford Bithynia tentaculata



Stour near D e d h a m Bithynia tentaculata






No. Infected

See Table II

Large metacercaria Xiphidiocercaria 5 Immature cercaria / E c h i n o s t o m e cercaria \ Tetracotyle metacercaria

i d m 1 n


b f


{Large metacercariae 6 1 3

Small metacercariae Furcocercaria Nil Nil

u r

4 8 1

Metacercariae Nil Nil


River Brett and Semer Bridge Lymnaea stagnalis


Tetracotyle metacercariae


River Brett at Chelsworth Bithynia tentaculata

6 5



Nil Xiphidiocercaria Encysted metacarcariae Young redia Tetracotyle metacarcariae Xiphidiocercariae Encysted echinostomes Nil

c h P n q t

Lymnaea stagnalis Lymnaea palustris Viviparus fasciatus Junction of Brett and Stour Bithynia tentaculata Potamopyrgus jenkinsi Planorbis vortex Tkeodoxus fluviatilis


Lymnaea stagnalis Valvata piscinalis Planorbis vortex

8 6 1

19 1 1




2 7 1 1 2 1 3 1 1


ig56: Fifty examined Microcercous cercaria Xiphidiocercaria Virgulate xiphidiocercaria Cercaria with pigment spots Echinocstome cysts Tetracotyle (hyperparasite) cyst Cysts Small cyst Sporocyst



1957: A D C E G B F H J




5 Xiphidiocercaria 1 Virgulate xiphidiocercaria

a d

3 1 1 1

b g e k

Large Small Large Redia

Cysts cyst Sporocyst with germ balls


M e a s u r e m e n t s w e r e m a d e of living s p e c i m e n s a n d m a t e r i a l p r e s e r v e d i n 5 % f o r m a l i n . T h e m e a n a n d r ä n g e of five i n d i v i d u a l s are given f o r fixed s p e c i m e n s ; all m e a s u r e m e n t s a r e in m i c r o n s ( t h o u s a n d t h s of a m i l l i m e t r e ) . PLATE


FIG. 2.

Cercaria A; a microcercous form from Bithynia

FIG. 3.

Tail of cercaria A with terminal portion expanded.

FIG. 4.

Redia with developing cercariae A. Living

Mean Cercaria A Body length 195 Body breadth 110 Tail length 37 Tail breadth 43 Ventral sucker 50 Oral sucker 46 Sporocyst A Length 1440 1440 Breadth 200 235 FIG. 5. Redia of A hyperparasitised by metacercaria B.


Fixed Range 150-230 65-150 27-52 39-54 46-62 46-58 1220-1770 184-284

FIG. 6.

Metacercarial cyst B extracted from redia.

FIG. 7.

Median sagittal section through metacercaria B. T h e globular organs are, from the top downwards, the oral sucker, pharynx, ventral sucker, and adhesive organ.

Encysted Length metacercaria B Breadth PLATE

FIG. 8.

Living 425 250


Xiphidiocercaria D from Bithynia


284 Transactions of the Suffolk Naturalists', FIG. 9.

Vol. 13, Part 5

Sporocyst of Cercaria D. Living


Fixed Range

Cercaria D

Body length Body breadth Tail length Tail breadth Ventral sucker Oral sucker Pharynx Stylet

143 57 120 17 20 30

135 78 85 23 22 31 10 19

119-150 69-92 73-115 19-27 19-27 27-35

Sporocyst D

Length Breadth

242 170

260 180

192-327 162-208

Virgulate xiphidiocercaria C from B.

FIG. 10.

Cercaria C

Body length Body breadth Tail length


173 62

\liext. 96contr.

Tail breadth Ventral sucker


140 85

115-177 68-88

130 17

112-139 15-19 23-31 X 23-31 35-42 X 31-42




Oral sucker

Sporocyst C


Stylet Virgula organs Length Breadth

15 (each) 250 100

255 125

242-262 100-142


FIG. 11.

Cercaria E from Bithynia

FIG. 12.

Redia with developing cercariae E.

Cercaria E

Body length Body breadth . Tail length Tail breadth . Oral sucker Ventral sucker .

Redia E FIG. 13.


35 17

Pigment spot Length Breadth




173 46 328 27 50 X 25 35 X 31

170 65 300 27 34 X 27 27 X 23 7

550 100

600 90

Body of furcocercaria S found in tissues of jenkinsi.

Fixed Range 120-210 40-80 265-345 23-31 32-35 X 20-21

very variable

550-650 65-120



FIG. 14.



Sketch of furcocercaria S before loss of tail.

Cercaria S

Body length Body breadth Oral sucker Ventral sucker Pharynx

Living 183 60 40 X 27 33 8

FIG. 15 •^Living encysted metacercariae F from FIG. 16

FIG. 17.

Metacercaria F after extraction from cyst.

Cyst F Metacercaria F


Bitliynia tentaculata.

Diameter Length Breadth Oral sucker Ventral sucker Pharynx

Living 285 590-640 280-330 127 142 62

Fixed 575 295 117 125 61


FIG. 18. /Subcutaneous cysts in roach of metacercaria T surrounded by FIG. 19. \ b l a c k pigment. FIG. 20.

Cyst (? capsule) with metacercaria T .

FIG. 21.

Freed metacercaria T .

Cyst T Metacercaria

FIG. 22.

Living 800 1150-1500 470-510


Length .. Breadth .

Living 400 270

Encysted echinostome metacercaria G, from Bithnia tentaculata. Living

Cyst G

1200 480 60 48 75 160

Encysted tetracotyle, or strigeid metacercaria Q, from Lymnaea pereger.

Metacercaria Q FIG. 23.

Diameter Length Breadth Oral sucker Pharynx Small ventral sucker Large postventral sucker

Mounted in Balsam

Outer diameter of cyst wall Inner diameter of cyst wall

300 200

Some Larval Trematodes in the Freshwater Fauna of the Flatford Mill Area  
Some Larval Trematodes in the Freshwater Fauna of the Flatford Mill Area