Studies on Gyrocotyle rugosa Diesing, 1850, A Cestodarian Parasite of the Elephant Fish, Callorhynchus milii
Observations on the Life Cycle of Gyrocotyle
Observations on the Life Cycle of Gyrocotyle
The life cycle of only one Cestodarian is known; it is that of Amphilina foliacea (Rud.) parasitic in the body cavity of. the sturgeon in Europe. Eggs of Amphilina foliacea pass out through the abdominal pores of the ganoid host. They contain a ciliated lycophore but do not hatch until eaten by amphipods (Gammarus or Dikerogammarus). The lycophore penetrates into the body cavity of the amphipod, loses its cilia, and gradually becomes an organism resembling the adult. Sturgeons become infected by ingestion of infected amphipods (Janicki, 1930).
The order Amphilinidea is quite distinct from the Gyrocotylidea in many respects. Amphilinids never occur in the digestive tract but are parasites of the body cavity. There is evidence that when the host is a teleost fish adult worms bore through the body wall and presumably liberate eggs only after thus leaving their host. At least specimens of Gephyrolina paragonopora have been found protruding from the body wall of their host, an Indian siluroid fish. Baer (1951) states: "One might be inclined to interpret such facts as indicating that the adult worms are free-living or, at least, that they escape from their host when their uterus is filled with eggs and that the latter are liberated when the worm disintegrates." Possibly the digestive tract is a secondary location for Cestodarians.
The life cycle of Gyrocotyle is unknown. There is at present no evidence as to the manner in which the definitive host is infected. It has been presumed that eggs pass out in the faeces and that some food animal serves as intermediate host, as is the case for most intestinal helminths. However, Lynch observed almost all stages from lycophore to adult either within the parenchyma of adult worms or in the spiral valve of the host. Yet there must be some part of the life cycle outside the host. The following observations may or may not be relevant to the life cycle.
One of the first impressions one receives from collection of numerous specimens of Gyrocotyle rugosa is the absence of small specimens. Of 34 specimens in 13 hosts, all were of large size and contained eggs in the uterus. No half-grown or quarter-grown individuals were found. Lynch found that infections with G. urna or G. fimbriata usually involved only adult specimens. However, of 104 rat fishes (Hydrolagus) examined by him, seven had mass infections "of small juvenile worms, seven to 203 in a host." Such conditions suggest an immunity by which the presence of adults prevents establishment of additional specimens at least of easily visible size. The large surface area of the adult worms suggests that the immunity might be largely determined by available space. As noted above, large page 7 numbers of postlarval stages are of common occurrence in the spiral valve of the elephant fish. The presence of a few adults seems to prevent the development of these larvae. Presumably, the numerous juveniles found by Lynch would follow multiple exposure by a host uninfected by adults, and only a limited number of these could become adult because of space limitations. The actual fate of the numerous postlarval individuals is, however, unknown. Almost microscopic in size and without cilia, they would not seem well adapted to infect another final host directly. Apparently few if any of them attain appreciable size within the elephant fish so long as adult worms are present If the latter should leave the host, possibly some of the postlarval forms would replace them.
The spontaneous departure from their living host by parasites is not common except for the purpose of dissemination of eggs. The fact that only the eggs in the terminal coils of the uterus of G. rugosa and none of the eggs of G. urna or G. fimbriata are ready to hatch casts some doubt that adult Gyrocotyle normally leaves the host for dispersal of its eggs. Yet there is evidence that adult Gyrocotyle can live in sea water at least for some days. Watson (1911, p. 365) states that G. fimbriata can "live for some days free." Lönnberg (1891, p. 14) notes that a specimen was found floating free in the sea off the coast of Sweden and that in the Museum at Christiana is a specimen found free on the bottom of the Bergen Fiord. One of the early records of adult "Gyrocotyle rugosa" was from a bivalve mollusc, "Mactra edulis"* from the coast of Chili. Since such a finding has not been confirmed, it has been concluded by most authors that the record involved some error or accident, as is more obviously the case in the record of Gyrocotyle from an African antelope (Diesing, 1850). It does seem evident that Gyrocotyle has unusual longevity in cold sea water, and the possible role in the life cycle of this ability seems worth further investigation. A mature individual of G. rugosa contains thousands of eggs ready to hatch, and it is known to be able to leave a dead host. Whether its eggs normally pass out in the faeces of the host has not been demonstrated.
The intestinal content near the anus of an elephant fish infected with six adult G. rugosa was examined. Three smears revealed no eggs or larvae. Pour smears of scrapings of the wall of the spiral valve near its middle revealed one living, postlarval stage with everted haptoral disc. It was not measured, but was evidently three or four times larger than the lycophore.
Numerous hatched larvae were exposed to: (1) a snail, Buccinulum multilincatum; (2) a hermit crab; (3) a bivalve mollusc, Aulacomya maoriana; (4) mucus from the spiral valve of the elephant fish; and (5) two pieces cut from the spiral valve. No immediate change in behaviour or distribution of the larvae was noted except in the watch glass containing the mucus. Although not markedly attracted to the mucus, the lycophores reacted positively to contact with it. Upon contact they remained or returned until thoroughly enmeshed. Within the mucus they frequently bent the body or revolved with gradually slowing movement. After about an hour, the mucus was filled with many hundreds of larvae. It was then killed and preserved. Slides made of this mucus show larvae so crowded together as to form in places almost a solid mass. In contrast, no larvae adhered to mucus secreted by the snail equally exposed to the lycophores.
The total thickness of the wall of the spiral valve was about 1.474 mm. Of this thickness, the inner half (0.804 mm.) was mucosa thrown into deep folds of flask-shaped pockets, the mucous glands. The mucus-secreting cells were limited to the globular, basal portion of the glands. Although these glands contained mucus, there was no evidence that larvae were being attracted to it. An occasional egg, still unhatched, occurred within a gland, and a single larva free in the lumen was found there.
Of 22 larvae studied from sections of the spiral valve, 14 were found within the muscular layers. 4 were within blood vessels. 2 were within mucosal tissue, and 1 was free in a mucous gland. Those within the blood vessels had probably previously penetrated into the muscular layers. Of the 14 larvae in the muscular layers, 7 had penetrated less than 0.1 mm., and the deepest penetration was 0.165 mm. from the cut edge of the tissue. The distance of the point of penetration from the outer (coelomic) surface of the piece of tissue varied from 0.067 to 0.502 mm., but only four larvae had entered more than 0.2 mm. from that surface and only two were in the inner (mucosal) half of the tissue. The four larvae in blood vessels had more varied locations, showing that locomotion within the vessel was more rapid. Two of these larvae were 0.603 mm. from the outer surface; two others were almost 3 mm. from the nearest cut edge.
These observations indicate that, although lycophore larvae will collect in large numbers in mucus from the spiral valve of the elephant fish, when exposed to a cut piece of the spiral valve, (1) they prefer the muscular layers to the mucosa, and (2) are capable of penetrating not only into the tissues hut also into the blood vessels of that organ. Considering this attraction of these larvae to tissues of the final host, their ability to enter blood vessels, and their later appearance in almost as small a size in scrapings of the mucosa. the possibility is suggested that their larvae normally penetrate the gills or some surface area of the elephant fish, be carried to the intestine where they emerge into the lumen, and then for the first time make use of their powerful hooks for anchorage. Their reaction to the gills of the elephant fish, possibilities of which had not occurred to me when fresh material was available, would be of Interest to observe. Some experiment which would expose intact gill surface without the distraction of free blood or other tissues is suggested.
Numerous larvae were still living in sea water after 6½ hours. Some were active after 18 hours. All were dead when examined about 34 hours after hatching. Under natural conditions. the larvae probably can live at least 24 hours.
Five days after exposure to larvae, the soft parts of the snail, bivalve, and hermit crab were examined after crushing between slides. No larval stages of Gyrocotyle were observed.
The few experiments recorded above indicate that the eggs G. rugosa hatch immediately in sea water and possibly within the spiral valve of the host; that the lycophore larvae were not attracted to and did not penetrate one species of bivalve, one species of hermit crab, and one species of snail; that they were attracted by, penetrated into. and remained in large numbers in scrapings of mucus page 10 from the spiral valve of the elephant fish; that they also penetrate into the tissues and blood vessels of cut pieces of the spiral valve itself. This attraction to a part of the definitive host suggests a direct life cycle.
Unfortunately, Callorhynchus does not live well in captivity. Furthermore, it is so omnivorous in food habits that it could theoretically be infected from almost any sort of intermediate host. Specimens of elephant fish examined by me had been feeding largely on molluscs (both bivalves and snails) or on Crustacea.
Gyrocotyle rugosa is the most favourable species for life cycle studies because its lycophore larvae are so easily obtained in very large numbers.
* Dollfus (1923, p 216) notes that the correct name for this mollusc is Mulinia edulis.