Page 1



*Department of Zoology and Applied Entomology, Imperial College of Science and Technology, London, S.W.7. INTRODUCTION

THE helminths of birds have, during the last 150 years, been the subject of a large number of papers and monographs, and the European fauna is thus reasonably well known. In Britain, however, very few collections from wild birds have been made. In 1844 both Bellingh am and Thompson published papers on parasites of birds in Ireland. In 1911 the Grouse Disease Committee published a report which included information on the helminthic fauna and Meggitt (1916) reported on the parasites of sparrows collected in the Midlands. Since 1920 several authors have presented papers on avian helminths but most of these are lists of the parasites of domesticated birds, e.g., Lewis (1930) Foggie (1933), Davies (1938), Owen (1951) and Soliman (1955) who were all concemed with domestic duck. Almost the only records of helminths of wild Anatids in Britain are those of Rosseter (1891, 1898, 1911), who described several species of the genus Hymenolopis from duck, and of Baylis (1928, 1939) who published a list of helminths collected from British vertebrates. Many of the foreign papers on helminths of wild birds have included information on the parasites of Anseriformes and other fresh water birds but few have been concerned exclusively with these hosts. In North America, Gower (1938) examined a large number of duck (mostly Mallard) that were shot in Michigan. He only commented on the trematode fauna (flukes) and did not consider the cestodes (tapeworms) or nematodes (roundworms). Later, (1939) Gower published a list of the helminths which had been recorded from duck up to 1939. Schiler (1951) *Present Address. Department of Zoology, University College of Rhodesia and Nyasaland, Salisbury, Southern Rhodesia.



examined Anseriformes from Alaska and included wild geese and swans as well as duck. Schiller (1955) published a paper on the helminths of Eider duck, also taken in Alaska. In Europe, Bezubik (1956) published the results of a survey of the helminth fauna of wild duck in Poland. Bezubik collected his material over a period of five years (1949-1954) and was able to obtain fowl all the year round. It was possible therefore to report on the seasonal fluctuations of the helminths observed. Czaplinski (1956) described the Hymenolopids of Polish Anseriformes collected between 1950-1955. A large proportion of Czaplinski's material was, however, taken from domestic birds killed in local abattoirs. As large numbers of wild duck are migratory, visiting the British Isles only during the winter months, it was decided to examine as many birds as possible in order to ascertain what parasites are being introduced from Europe. The level of infection (both the percentage of birds infected and the number of parasites per host) tends to be at its peak in July and August, gradually falling off throughout the autumn to a minimum in the spring and early summer. Consequently, a direct comparison of the infections found in duck killed in England with those in duck killed in Poland is impossible. T h e following species of duck were taken at Nacton Decoy, near Ipswich, Suffolk; Anas platyrhyncha platyrhyncha L. (Mallard), Anas penelope L. (Widgeon), Anas crecca crecca L. (Teal), Anas acuta acuta L. (Pintail), and Spatula clypeata L. (Shoveler). Specimens of Gallinula chloropus chloropus L. (Moorhen) from Great Glemham, Saxmundham, Suffolk were also examined. EXAMINING


It is essential to carry out the post mortem examination within a few hours of the death of the host as the worms soon become macerated. This is especially true of the cestodes which may loose their scolices and thus become impossible to identify. T h e eyes and nostrils were examined as well as the internal organs. Leeches were discovered in the nostrils of two of the Mallard and were identified as Theromyzon tessulatum. T h e birds were opened and,aftertheair sacs had been looked at,the viscera were removed. T h e trachae, bronchi, lungs, Oesophagus, crop, gizzard, intestine, intestinal caeca, rectum, cloaca, bursa Fabricii, gall bladder, bile ducts, liver, kidneys, Ureters, and oviduct were all scrutinised. T h e organ under examination was opened, spread out in a black dissecting dish and then gently washed with a jet of water from a wash bottle. T h e worms tend to float out from their place of attachment and can be easily seen against the dark background. T h e intestine was always divided into three equal parts so that

31 the locations of the parasites could be recorded more easily The worms were collected with a seeker, pipette or paint brush and transferred to a Petri dish to be thoroughly cleaned. HELMINTHS FROM FRESH WATER BIRDS


Trematodes were fixed in cold formal-acetic under slight coverslip pressure to prevent the worms curling up. As soon as the specimens were dead the cover-slips were removed. After 12-24 hours in fixative the trematodes were washed in water and stored in 70% alcohol. Notocotylid material was examined under cover-slip pressure, in water, while still alive so that the pattern of the ventral glands could be discerned. After fixation the glands can be seen before dehydration or after staining with picro-nigrosin. Erlich's haematoxylin, and Aceto-carmine were used for staining trematodes but the latter was found to give the more satisfactory results. Cestodes were fixed in hot Bouin-Hollande. The fixative was heated in a small boiling tube and the cestodes dropped into the tube from a pipette. After vigorous, horizontal shaking for about 30 seconds, the worms are extended uniformly along their whole length. Specimens were left infixativefor 3-4 hours and then stored in 70% alcohol. Formal-acetic was also used when large quantities of worms were available. Hydrochloric carmine was used for staining all the cestodes and gave excellent results. Cestode hooks were mounted in Berlese's fluid and detached from the scolex before they were measured and drawn. Nematodes werefixedeither in hot formalin (4%) or hot alcohol (70%). The latter gave better results. Specimens were cleared in lactophenol for examination. Sectioned platyhelminth material was stained with haematoxylin and eosin after the usual paraffin wax sectioning process. THE FOLLOWING IS A LIST OF THE HELMINTHS RECOVERED FROM EACH OF THE HOST SPECIES.

1. Anas platyrhyncha platyrhyncha L. Trematodes : Apatemon gracilis (Rudolphi, 1819) Szidat, 1928. Typhlocoelum sisowi (Skrjabin, 1913) Dollfus, 1948. Echinostoma revolutum (Frรถlich, 1802) Looss, 1899. Echinoparyphium westsibiricum Issaitschikoff, 1924. Hypoderaeum conoideum (Bloch, 1782) Dietz, 1909. Psilochasmus longicirratus Skrjabin, 1913. Notocotylus triserialis Diesing, 1839. Notocotylus imbricatus (Looss, 1893) Szidat, 1935. Catatropis verrucosa (Frรถlich, 1789) Odhner, 1905. Uniserialis gippyensis Beverley-Burton, 1958.



Prosthogonimus ovatus (Rudolphi, 1803) LĂźhe, 1909. Prosthogonimus cuneatus (Rudolphi, 1809) Braun, 1901. Schistogonimus rarus (Braun, 1901), LĂźhe, 1909. Metorchis xanthosomus (Creplin, 1846) Braun, 1902. Total : 14 species. Cestodes : Hymenolopis abortiva (Von Linstow, 1904) Von Linstow, 1905. Hymenolopis anatina (Krabbe, 1869) Cohn, 1901. Hymenolopis collaris (Batsch, 1786) Fuhrmann, 1908. Hymenolopis compressa (Linton, 1892) Skrjabin, 1914. Hymenolopis coronula (Dujardin, 1845) Railliet, 1899. Hymenolopis echinocotyle Fuhrmann, 1907. Hymenolopis gracilis (Zeder, 1803) Railliet, 1899. Hymenolopis megalops (Creplin, 1829) Parona, 1899. Hymenolopis octacantha (Krabbe, 1869) Railliet, 1899. Hymenolopis paramicrosoma Gasowska, 1931. Hymenolopis parvula Kowalewski, 1904. Hymenolopis spiralibursata Czaplinski, 1956. Hymenolopis tenuirostris (Rudolphi, 1819) Railliet, 1899. Hymenolopis venusta (Rosseter, 1897) Railliet & Henry, 1909. Haploparaxis furcigera (Rudlophi, 1819) Fuhrmann, 1908. Diorchis nyrocae Yamaguti, 1935. Fimbriaria fasciolaris (Pallas, 1781) Wolffhugel, 1900. T o t a l : 17 species. Nematodes : Amidostomum skrjabini Boulenger, 1926. Epomidiostomum uncinatum (Lundahl, 1848) Seurat, 1918. Porrocaecum crassum (Deslongchamps, 1824) Railliet & Henry, 1912. T o t a l : 3 species. The total number of helminth species recovered from Mallard was 34.


Anas penelope L. Trematodes : Apatemon gracilis Typhlocoelum sisowi Notocotylus imbricatus T o t a l : 3 species. Cestodes : Hymenolopis anatina Hymenolopis echinocotyle Ligula intestinalis (Linneus, 1758). T o t a l : 3 species.



Nematodes : Epomidiostomum uncinatum T o t a l : 1 species. The total number of helminth species recovered from Widgeon was 7. 3.

Anas crecca crecca L. Tremadotes : Apatemon gracilis Hypoderaeum conoideum Notocotylus imbricatus Total: 3 species. Cestodes : Hymenolopis anatina Hymenolopis compressa Hymenolopis echinocotyle Hymenolopis megalops Hymenolopis paramicrosoma Fimbriaria fasciolaris Total : 6 species. Nematodes : Epomidiostomum uncinatum T o t a l : 1 species. T h e total number of helminth species recovered from Teal was 10.


Anas acuta acuta L. Trematodes : Typhlocoelum sisowi Echinostoma revolutum Psilochasmus longicirratus Notocotylus imbricatus Catatropis verrucosa Prosthogonimus ovatus T o t a l : 6 species. Cestodes : Hymenolopis Hymenolopis Hymenolopis Hymenolopis Hymenolopis Hymenolopis Hymenolopis

anatina compressa coronula echinocotyle gracilis megalops octacantha



Hymenolopis solowiowi Skrjabin, 1914. Hymenolopis venusta Fimbriaria fasciolaris Anomotaenia ciliata Fuhrmann, 1913. T o t a l : 11 species. Nematodes : Epomidiostomum uncinatum Porrocaecum crassum T o t a l : 2 species. To total number of helminth species recovered from Pintail was 19. 5.

Spatula clypeata (L.). Trematodes : Psilochasmus longicirratus Notocotylus triserialis Notocotylus imbricatus Catatropis verrucosa Prosthogonimus ovatus T o t a l : 5 species. Cestodes : Hymenolopis echinoctyle Hymenolopis floreata Meggitt, 1930. Hymenolopis liophallos (Krabbe, 1869), Railliet, 1899. Hymenolopis octacantha Echinocotyle rosseteri Blanchard, 1891. T o t a l : 6 species. Nematodes : Epofnidiostomum uncinatum Total : 1 species. The total number of helminth species recovered from Shoveler was 12.


Gallinula chloropus chloropus (L.). Trematodes : Echinostoma revolutum Notocotylus gibbus (Mehlis, 1846) Kossack, 1911. Total : 2 species. Cestodes: None. Nematodes : Amidostomum sp. Total : 1 species. T h e total number of helminth species recovered from Moorhens was 3.



Of the duck, Mallard, Pintail and Shoveler were found to carry a wider variety of helminth species than Widgeon or Teal. This feature may be correlated with the idea that Widgeon and Teal are mainly vegetable feeders. DĂźring the survey the crop and gizzard Contents from each bird were examined and the remains of molluscs were recovered several times from Mallard, Pintail and Shoveler. It was possible to identify the shells of Assiminea grayana, Scrobicularia plana, Littorina rudis and Hydrobia ulvae. All these species are littoral or brackish water forms which were presumably ingested while the fowl were feeding on the estuaries. No remains of fresh water snails were recovered and Assiminea grayana was the only mollusc found once in Widgeon and once in Teal. DISTRIBUTION OF THE H E L M I N T H F A U N A I N THE B O D Y OF THE H O S T . 1.


Three trematodes were found exclusively in this region, they are : A. gracilis, E. westsibiricum and P. longicirratus. Cestodes recovered in this location are : F. fasciolaris, H. venusta and E. rosseteri. 2.



No trematodes or nematodes were found in the median region of the intestine. H. floreata, H. paramicrosoma and Ii. tenuirostris were all recovered from this location but their ränge probably includes the more anterior and posterior parts of the intestine. 3.


H. conoideum and E. revolutum apparently prefer the posterior part of the gut as does H. anatina. The majority of the cestode species are not confined to a Single region of the intestine. H. echinocotyle and II. parvula tend to inhabit the anterior half of the intestine while H. coronula and H. octacantha are more often found posteriorly. H. collaris, H. compressa, H. gracilis, H. solowiowi and H. spiralibursata occur along the entire length of the intestine. 4.


The species occurring in the posterior part of the intestine may also be present in the rectum. They are : H. conoideum, E. revolutum and II. anatina. H. furcigera was found in the anterior part of the rectum as well as in the intestinal caeca. 5.


H. megalops occurs exclusively in the cloaca. Occasionally P. ovatus and P. cuneatus are recovered from this location but it is not the normal habitat for these two species.

36 6.


H. abortiva was always found in the narrow, distal region of the intestinal caeca. H. echinocotyle and II. furcigera have been recovered from this site although it is possible that the worms may have moved into the caeca after the death of the host. Notocotylus triserialis, N. imbricatus, C. verrucosa and N. gibbus were all found exclusively in the caeca. 7.


This structure is only present in young duck as it atrophies when the fowl become mature. P. ovatus, P. cuneatus, S. rarus and U. gippyensis all occur in this location. 8.



T. sisowi was found in the trachea, or, more rarely, in the lungs. One specimen of this species was recovered from the bursa Fabricii. 9.


The only species recovered from this location was M. xanthosomus. 10.


Amidostomine nematodes viz. : A. skrjabini and E. uncinatum were recovered exclusively and in comparatively large numbers from the lining of the gizzard. These nematodes appear to cause a certain amount of mechanical damage to the gizzard wall. The following descriptions are of two species of helminths which were both recovered from birds in Suffolk. Genus Notocotylus Diesing, 1839. Notocotylus gibbus (Mehlis, 1846) Kossack, 1911. DESCRIPTION.

The body is flattened and oval in shape. 1.3mm. long and 0.7-1.4 mm. wide. On the ventral surface there are three rows of glands which can be seen while the animal is alive but which become invisible after dehydration and Clearing. The three rows of ventral glands are characteristic of the genus Notocotylus. There are eleven glands in each of the lateral rows and four or five glands in the median row. The mouth is surrounded by an oral sucker and is terminal in position. As is usual in the family Notocotylidae the pharynx and ventral sucker are both absent. T h e short Oesophagus leads to the intestinal bifurcation. T h e two long intestinal caeca extend to the posterior region of the body.



The two testes are irregularly oval in shape, extracaecal and lie in the posterior third of the body. Vasa deferentia connect the testes with the vesicula seminalis. The latter is elongate and sinuous, median in position proximally but distally forming several loops to the right hand side before passing to the base of the cirrus sac. The latter is flask-shaped with conspicuous muscular walls, and contains the internal vesicula seminalis and the cirrus. T h e cirrus is armed with conspicuous spines. T h e ovary lies inside the intestinal caeca in the testicular region, and is round or oval in shape. Mehlis' gland lies immediately anterior to the ovary. The uterus has large, transverse slings that extend laterally to the intestinal caeca. At the level of the cirrus sac the slings become smaller and the uterus passes forward to the muscular metraterm. The latter opens with the cirrus at the common genital pore which lies just posterior to the intestinal bifurgation. T h e vitelline follicles are irregulär in shape and lie in two extra caecal bands which extend from the level of the testes into the anterior half of the body. The uterus is filled with numerous, thin shelled, operculate eggs which bear long polar filaments. Host. Gallinula chloropus chloropus (L.). Location. Intestinal caeca. Locality. Great Glemham, Saxmundham, Suffolk. Notocotylus gibbus was first found in the Moorhen and the Coot by Mehlis in 1846. It has subsequently been recorded several times from these hosts in Europe and from the American Coot in America. N. gibbus has previously been recorded from Moorhen in Argyllshire. Trematodes belonging to the family Notocotylidae often inhabit the intestinal caeca of birds and are easily recognised as they are coral pink in colour with a white mass of eggs in the centre of the body. The worms tend to congregate in the tips of the intestinal caeca. The Moorhens probably become infected with N. gibbus by eating metacercariae which encyst on or in fresh water snails. Genus Hymenolopis Weinland, 1858. Hymenolopis abortiva (Von Linstow, 1904) Von Linstow, 1905. DESCRIPTION.

The body is short. Entire specimens measure up to 2.27mm. and consist of a scolex, neck and strobila. The scolex bears a comparatively long rostellum which can be partially retracted into the rostellar sac. The expanded apex of the rostellum carries 10 hooks which measure 34-35pt long. T h e scolex also bears four rather shallow suckers that tend to protrude from the sides of the scolex. The latter narrows posteriorly to merge with the short neck. The immature proglottids are wider than they are long while those in the mature region of the strobila are more elongate.



The genital pores are unilateral and situated on the right hand side of the body. The cirrus and vagina open into a shallow genital atrium. The rudiments of the male genitalia are visible in the 13th or 14th proglottid behind the scolex. The three testes, characteristic of the genus Hymenolopis, are spherical and are arranged at the points of an inverted triangle in the posterior part of the proglottid. The external vesicula seminalis is anterior and becomes evident in proglottid 20. It increases in size in the next two proglottids and then atrophies so that no trace is apparent in the 24th proglottid. The cirrus sac is slender and elongate lying obliquely across the anterior part of the proglottid. The cirrus is unarmed. The female genitalia only arises when the male genitalia is fully functional. The ovary is first visible in the 22nd proglottid. In the 23rd the testes have degenerated and the ovary is fully developed, with two spherical lobes joined by a narrow isthmus. The vitellarium lies between the lobes of the ovary. The vagina is a slender duct which leads to the receptaculum seminis. The latter is clearly visible in proglottid 22. In the 23 rd proglottid the U shaped uterus is formed and in the succeeding proglottids the eggs become differentiated and the uterus extends towards the margins of the proglottid. Host. Anas platyrhyncha platyrhyncha L. Location. Intestinal caeca. Locality. Nacton Decoy, Near Ipswich, Suffolk. Hymenolopis abortiva was first described by Von Linstow in 1904 from the Mallard. Rosseter (1911) found this species in English domestic duck but called it H. upsilon as he was not aware of Von Linstow's description. H. abortiva is one of the smallest species of the genus Hymenolopis and generally occurs in large numbers in the narrow, distal part of the intestinal caeca. This species is unusual in that the reproductive Organs arise and atrophy in only six or seven proglottids and that the female reproductive complex replaces the male genitalia so quickly. The U shaped uterus is conspicuous and characteristic. The gravid proglottids are shed before the eggs are fully formed.


I wish to thank Professor B. G. Peters under whose supervision this work was carried out. I am most grateful to the Suffolk Naturalists' Society for making the Morley Bursary available to me, also to the Earl of Cranbrook, who obtained the Moorhens for me. I wish to thank the Warden, Mr. F. J. Bingley, and the Staff at Fiatford Mill Field Centre for providing accommodation and encouragement during the winter months while material was being collected.




Baylis, H. A., (1928). Ann. Mag. Nat. Hist. (10), 1, 329-343. (1939). Ibidem. (11), 4, 473-498. Bellingham, O'B., Ibidem. 13, 335-340, 422-430. Bezubik, B., (1956). Acta. Parasit. Polon., 4, 407-510. Czaplinski, B., (1956). Ibidem. 4, (8), 175-373. Davies, T . I., (1938). Welsh J. Agric., 14, 280-287. Foggie, A., (1933). Scot. Nat., 200, 60-64. Gower, W. C., (1938). Mich. State. Coli. Agri. Expt. Sta. Mem. 3, 94pp. (1939). Amer. Midland Nat. 22, (3), 580-628. Lewis, E. A., (1930). J. Helminth, 8, (1), 1-18. Meggitt, F. J., (1916). Parasitology, 8, (4) 390-410. Owen, R. W., (1951). J. Helminth, 25, 105-130. Rosseter, T . B. (1891). Bull. Soc. Zool. France, 16, (8), 224-229. (1898). J. Quekett Micr. Club, 7, 10-23. (1911). Ibidem. 11, 147-160. Schiller, E. L., (1951). Amer. Midland Nat., 46, (2), 444-461. (1955). J. Parasit., 41, (1), 79-88. Soliman, K. N., (1955). J. Helminth, 29, (1/2), 17-26. Thompson, W., (1844). Ann. Mag. Nat. Hist., 13, 430-440.


T h e order of birds which contains the family

BURSA FABRICII. A small bursa which opens into the cloaca and lies dorsal to the distal part of the rectum. T h e bursa Fabricii atrophies when the bird becomes mature and is not apparent in individuals that have over-wintered. CESTODA. (Tapeworms). A class of the phylum Platyhelminthes. T h e cestodes are endoparasites that have no gut. CIRRUS. T h e eversible male organ which is often armed with spines. CIRRUS SAC. T h e muscular sac which contains the retracted cirrus and the internal vesicula seminalis. COMMON GENITAL PORE.

I n t h e class T r e m a t o d a t h e m e t r a t e r m

and cirrus usually open close together at the common genital pore.


HELMINTHS FROM FRESH WATER BIRDS VESICULA SEMINALIS (Seminal Vesicle). The vas deferens often becomes dilated before entering the cirrus sac to form a reservoir for the spermatozoa.


In the class Cestoda the cirrus and vagina often open into an atrium of variable depth and muscularity.


GRAVID. With the uterus filled with eggs in varying stages of development. HELMINTH. A term which usually refers to the parasitic members of the phyla Platyhelminthes and Nematoda. VESICULA SEMINALS. (Seminal Vesicle). That part of the dilated vesicula seminalis which lies inside the cirrus sac.


In birds there are two intestinal caeca or diverticula which open into the gut at the junction of the intestine and the rectum. In the trematodes the gut bifurcates behind the Oesophagus to form two blindly ending caeca.


The oviduct in the trematodes and cestodes is dilated to form the " ootype " which is surrounded by the secretory cells of Mehlis' gland.


In some trematodes the cercariae (last larval stage to be produced by the intermediate host) encyst and become metacercariae before becoming infective to the definitive host.


METRATERM. In the trematodes the distal part of the uterus is known as the metraterm which may or may not be glandulär and /or cuticularised. NEMATODA. (Roundworms). A phylum that shows little affinity with any other. Many nematodes are free living. In most of the trematodes (digenetic) the mouth is surrounded by a sucker the muscles of which are clearly demarcated from the parenchyma.


PHARYNX. If present in the trematodes the pharynx is a globular or sub-globular muscular organ that lies between the prepharynx and the Oesophagus. The strobila of the cestodes consist of a chain of proglottids or segments each of which, at maturity, contains at least one set of reproductive organs.


SEMINIS. In the trematodes the receptaculum, if present, is formed by a diverticulum from the oviduct. In the cestodes the vagina becomes dilated to form a receptaculum.


A muscular sac into which the rostellum can be wholly or partially withdrawn.




ROSTELLUM. A muscular structure situated at the apex of the scolex in many cestodes (Cyclophyllidea). The rostellum often carries rostellar hooks. SCOLEX. T h e anterior " head " of a tapeworm which is attached to the gut wall of the host. STROBILA. The body of a tapeworm excluding the head and neck. The strobila is made up by a series of proglottids. (Flukes). A class of the phylum Platyhelminthes which contains ecto- and endoparasites.



qibbus. .oral


a n t e r i o r qland of lateral


.anterior qland of median


O 3


Notocotylus gibbus (Mehlis, 1846) Kossack, 1911. External f e a t u r e s . T h e t h r e e rows of v e n t r a l glands are characteristic t h e genus Notocotylus Diesing, 1839.




The duct leading from the testes to the cirrus.

In the trematode family Notocotylidae several genera have ventral glands. The arrangement of the glands is of diagnostic importance. When everted the glands appear as hemispherical protuberances but when they are retracted they become small transverse slits.


SUCKER. Most of the digenetic trematodes have a muscular sucker which is median and ventral in position.


(Vitellaria). by the vitelline follicles.


T h e yolk cells are produced





cirrus n genital


metraterm .cirrus





qlttnd .vitel line duct

.ovary .testis .intestinal



Internal anatomy.



Hymenolepis abortiva (Von Linstow, 1904) Von Linstow, 1905. i . Entire specimen. \}g- 2. Hooks from the scolex. V.V- 3• Scolex with the rostellum partly everted. pß- 4• Proglottid with fully developed male genitalia. f'g- 5. Proglottid with fully developed female genitalia.


Some Helminths from Fresh Water Birds in Suffolk  
Some Helminths from Fresh Water Birds in Suffolk