FISHERIES RESEARCH BOARD OF CANADA. By Suguru Okada. From:. Syokubutu Oyobi Dobutu, Vol. 3, No. 8, pp , 1935.

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1 FISHES ARCHIVE FISHERIES RESEARCH BOARD OF CANADA Translation Series No. 121 f!.:kl. - -,-" r! 1 1 ON NEMATODES PARASITIC IN THE SWIM BLADDER OF OF THE SALMON AND TROUT FAMILY By Suguru Okada From:. Syokubutu Oyobi Dobutu, Vol. 3, No. 8, pp , Translated by the Bureau for Translations, Foreign Language Division, Department of the Secretary of State of Canada Edited by L. Margolis 1957

2 This is a preliminary translation prepared for the use of the Fisheries Research Board of Canada. It is not a"definitive English version of the article, and it has not been checked or approved by the author.

3 A species of nematode Cystidicola salmonicola (ISHII) is often found in great numbers in the swimming bladder of the salmon and trout family. The first study on this species was made in 1905 by Tokujiro Koshida who discovered it in the swim bladder of fry of trout at the present hatchery 1 and who reported that he had classified it as a species of Onuris. Following the above study, in 1917 Shigeyoshi Ishii made a detailed study on the same species at the same hatchery and named it Ancyracanthus salmonicola ISHII. However, Tsunenobu Fujita proposed in 1927 that it should be classified as gystidicola and corrected the name to Lystidicola salmonicola (ISHII)as above; and in 1931 pointed out errors in Ishii's observations and corrected them. The above studies more or less complete the morphological study of this parasite. However, there is still room for further study on the ecological and pathological phases such as its life history and its effects on the host. The writer started a study on these phases of this parasite. It_is his intention to publish a part of his study in this article. The writer here wishes to express his appreciation to Mr. Handa, the Director at Hokkaido salmon and trout hatchery, who offered facilities. He also expresses his appreciation to Drs. Inugai and Fujita for their kind assistance; I. Few Observations on Morphology Since there have been detailed accounts concerning the morphology of the parasite in the above theses, the present section will deal only with a few 'supplementary details. 1. Length: They measure 6 mm to 30 mm. They appear as if they are with hairs. The male is smaller in size compared to the female; the end of its tail coils approximately twice. 0# 2. The alimentary canal starts with the mouth which is located at the end of the head and is followed by the oral cavity, the vestibule, the esophagus, the intestines and the rectum and ends with the anus near the posterior end. 1 Hokkaido salmon and trout hatchery at Chitose Pura, Tanshin Koku, Hokkaido.

4 There is a well-defined demarcation (?) in the esophagus which divides it.into the anterior and the posterior sections (Fig. 1). Dr. Fujita made a comparison between the lengths of anterior and posterior esophagi of specimens from Salmo irideus GIBBONS of the salmon and trout hatchery in Sakata-Mura, Aomori Préfecture, from Oncorhynchus masou (BREVOORT) of the Chitose Hatchery in Hokkaido, and from OncoLimaphus keta (WALBAUM) of the Taranpaku Hatchery in Sakhalin. He found that the ratio became larger as he moved northward. Suspecting that such change depends on the species of host, the writer made measurements on the anterior and posterior esophagi of worms which are parasitic in Salmo irideus GIBBONS (approximately 50 cm), in onçorhynbus masou (approximately 10 cm) and in fry of OncorhyuLus keta (WALBAUM) (approxima'tely 15 cm) which were raised in the present hatchery. He then calculated the ratio. They are shown in Table 1.[p. 1452]. For a comparative purpose,.a part of Dr. Fujitals report is reproduced in Table 2. It shows the ratio between the anterior and the posterior esophagi of worms, which are parasitic in ôncorhynchus keta (WALBAUM), Oncorhynchus masou (BREVOORT) and Salmo irideus GIBBONS of Hokkaido. to be 1:2.8 or 1:3.0. The ratios are similar. Thus, it does not appear that the difference in ratio depends on the difference in the hosts. Dr. Fujita reports that whether this is due to chance, food, or climate requires further research On the size of this worm Dr. Fujita reported that of those found in Aomori Prefecture, Hokkaido and Sakhalin, those found in Aomori Prefecture were the largest, and that this should not be simply attributed to climate, but suggested that this might be related to the physical characteristics of the host and the food. At the present hatchery there are worms of all sizes - extending down from the size which Dr. Fujita found in worms collected in Aomori Prefecture - thus, the size has no relation to weather. This has already been stated by Dr. Fujita. The observations by the writer, suggest that the size of the worm is related to the size of the host - larger worms seem to be found among larger hosts. This is shown in Table 3. The table shows the measurements which were made on the 10 largest worms which were found in the swimming bladder of the fish.

5 4. The number of pepillae in the tail of the male varies greatly between different observers, although this is regarded as an important feature of classification. They agree on the point that there are 3-4 of unpaired papillae behind the genital opening: however, with respect to those which are situated in front of the genital opening, Ishii reports 9-11 pairs of paired papillae, while Dr. Fujita reports 6 pairs of paired and 4 of unpaired papillae in front of these. The. writer's observations seem to indicate that Ishii's case is more common.(fig. 2). II. Effects on the Host When these parasites become parasitic in the swim bladder, they can be seen through the surface of the swim bladder (Fig. 3). They are pa:ticularly numerous on the blind end; further, they are more numerous on the dorsal wall than on the ventral wall of the inner surface of the swim bladder. Thus, when the swim bladder is cut open and the worms are brought out and viewed under a hand magnifying glass they are much more numerous than outward appearance suggests. They range from a few worms to several hundreds and even to several. thousands. When a swim bladder with several hundred parasites is incised, a mucous 1 substance full of bodies of the worms appears. The microscopic examination of such substance shows a large number of cell fragments. The examination of that part of the structure of the swim bladder where the mucous substance was collected, shows that the pillar-like upper-skin structure has been destroyed or has fallen off (Fig. 4). The examination of the oral structure of this parasite shows that the cuticle is shaped like sharp teeth. probably eats away the structure (Fig. 5). starts at the blind end and proceeds forward. This sharp membrane It appears as though the erosion Inside the swim bladder, both mature worms and larvae are found. These larvae are large in size - measuring 5-10 mm. They can only be distinguished from the mature worms because of the incomplete development of their reproductive à 1 Dr. Fujita suggested that this might be for the most part a substance secreted from the reproductive organ of females in order to ease spawning.

6 organs. In the larvae of females there is a wen-like protuberance at the end of its tail. Thus, they can be distinguished very easily. When Oncorhya2hus masou (BREVOORT) become infested by several thousand worms, since their swim bladders are small in size, the interior of the bladder becomes full. In such cases, the number of la'rvae generally becomes extremely numerous. If we take a segment of a swim bladder with a small number of mature worms, we will find that the epidermis of the interior remains almost undamaged and that, because of the pressure exerted by the larvae, the interior is dented. The examination of the oral structure of the larvae shows that its development is incomplete and that teeth-like protuberances are not clearly defined (Fig. 6). Thus, it appears as though the larvae do not cause damage to the structure. The larvae molt once ih the swim bladder and become adults. At the time of molting, the outer cuticle separates crosswise into anterior and posterior portions near the front end. The posterior'portion comes off like a sheath - even the inside surface of the rectum comes off with it. In the female the wen-like protuberance at the tail end is cast off with the molt (Fig. 7). In the anterior portion, the molt turns inside out and stays attached to the oral portion. This seems to extend to the inner portion of the esophagus. The completion of molting in the anterior portion seems to require more time than in the posterior portion. With the completion of molting, the larvae assume an appearance of mature adults. It appears as though the oral section undergoes further development, the teeth appear and the worms are ready to inflict damage to the structure. It appears as though sexual union also occurs within the swim bladder. Spawned eggs- (Fig. 8) measure along the longer axis and along the shorter axis. They are right cylindrical in shape and have small protuberances at both ends, where there are two extremely long (0.6 mm) whip-like appendages. Spawned eggs are found along with the aforementioned. molts in the mucous substance. We do hot believe that the eggs hatch in the swim bladder. This is based on the fact that the larva is found folded in three within the eggshell and thatits body even at its longest will not exceed 0 15 mm if it hatches. Of the larvae which are found inside the swimmlng bladder ; even the smallest

7 - 5 - measures not less than 5 mm. Thus, it appears as though the hatching takes place after the eggs leave the swim bladdez.. In order to confirm this belief, an examination was made of the mucous substance, which was found in the excretion and at that portion of the throat where ductus pneumaticus opened. Of the twenty odd specimens infected by the worm, which were chosen from dead Salmo irideus (GIBBONS), only in one did we fird what appeared to be a molt in excreta which were found at the end of the rectum, and numerous relatively closely bunched eggs (more than 100) also at the end of the rectum. The shape and the size of the eggs were identical to those found in the swim bladder. Further, there was not a single similar nematode in the intestinal tracts. Therefore, there cannot be any doubt that the eggs are of the worm under discussion. There does not appear to be any differene in the extent of the development between larvae which were found in eggshells and which were found in the swim bladder. Thus, we can conclude that the eggs of the worm under discussion prassed through the digestive tracts without hatching. The examination of the area near the opening of the swim bladder duct indicated the presence of mucous substance in the neighbourhood of the gill. The microscopic exâmination of the substance showed a single egg. The examination of the inside of the swim bladder revealed the presence of mucous substance in several spots near the swim bladder duct. These observations seem to show that the mucous substance accumulates in the swim bladder and is expelled occasionally through the swim bladder duct and that (since the worms have not been observed in other organs than in the swimming bladder although the mucous substance contains eggs, molts and the worms) the worms escape back into the swim bladder and the eggs and molts are discharged. It appears that the discharge passes through the digestive tract and is expelled with the excretion. Thus, the eggs of the worm under consideration are often expelled to the outside world with the excreta during the life of the host and further there is no characteristic symptom of infection in the host at the beginning. Thus, the prevention of the propagation of this parasite is of considerable difficulty. If carcasses of the fish infested with this parasite are left in a hatchery, the swim bladder gradually putrifies and its contents are discharged outside. The discharge usually contains a large number of eggs, which does

8 - 6 - not seem to be much less th.an the amount expelled witn the excreta. Tnus it is not.entirely a useless preventive measure to remove carcasses immediately. It was discovered by Kbelda that the intermediate host of the worm was Gammarus. Since the Gammarus congregate on carcasses of andmals and eat them voraciously, it aids the propagation of the worm in cf._:éstion a great deal to leave carcases of fish. The worms are found in the northern part of Honshu, Hokkaido and Sakhalin. Their hosts! in addition to the aforementioned Oncorhvnchus keta (Walbaum), Oncorhynctus masou (BREVOORT), and Salmo irideus (GIBBONS), include Oncorhvnchus nerka and :Salveinus leucomaenis pluvius. It is believed that, of the 100 adult Salmo irideus (Gibbons), more than half are infected by this parasite. However,. the number of deaths, which. can be attributed to the infectioh, is at present relatively small - only one or two a month. Hoe-wer, at one time at this hatchery a large number of fry was infected and.killed. Good results were obtained after ponds had been dried and the Gammarus had been eradicated. References 1. Koshida, Tokujiro. On a nematode parasitic on fish of the salmon family. Hokkaido Syisan Zasshi, Vol. 5, No. 12, 2. Koshida, Tokujiro Survey of nematodes parasitic on fish reared in hatchery. The third report of the Hokkaido Suisan Shikenjo. 3. Ishii, Shigeyoshi On a nematode parasitic in the swim bladders of trout in Japan. Dobutsugaku Zasshi, Vol. 28, No Fujita, Tsunenobu Vermes parasitic on fish in Lake Biwa, (2). Dobutilsgaku Zasshi, Vol. 39, No Fujita, Tsunenobu On a nematode parasitic in the swim bladder of the salmon family. Dobutsugaku Zasshi, Dr. Natase Memorial Issue. 6. Ishii, Shigeyoshi Parasites on fish. of Japan. Iwanami Lecture Series on biology, No. 18. [page 1452] Fig. 1: a - Vestibulum b - Anterior esophagus c - Nerve ring. d - Posterior esophagus e - Intestines

9 - 7 - Table 1: a - Host b Salmo irideus (Gibbons) c Onçornyns masou (BREVVORT) d - Oncorhvnchus keta (Walbaum) Length of worm 2 - Length of anterior esophagus 3 - Length of posterior esophagus 4 - Anterior esophagus: Posterior esophagus ' In the No. 1 breeding ground, several year-old fry of Oncorhynchus keta (Walbaum) were reared mixed with those of Salim irideus (Gibbons). These were incised and examined under a microscope. However, only one of these was found to harbour in its swim bladder a single worm (d). Table 2: a - c - e Breeding centre Hokkaido Ho st Salmo milktschitsch Walbaum i - Oncorhynchus masou k (Brevoort) OnçorhygpLus keta (Walbaum)* b - d - f - h Aomori Prefecture Sakhalin Salmo irideus (Gibbons) Salmo irideus (Gibbons) Oncorhynchus (Walbaum) 1 - Length of worm 2 - Length of anterior esophagus 3 - Length of posterior esophagus 4 - Anterior esophagus: Posterior esophagus keta. Taken from the thesis of Dr. Fujita. In all cases, an average of 5 worms. Unit Mm. [page 1453] Table 3: a - Name of host b - Length of host c - Length of worm mm e - average mm' 1 - Oncorhynchus nerka 2 - Salmo irideus (Gibbons) 3 - Same as the preceding 4 - Salmo milktschitsch (Walbaum) 5 - Same as the preceding

10 Fig. 2. Morphology of tail In mature male. a - Papillae b - Folds in cuticle c - Tail d - Copulatory clasping hook e - Auxiliary copulatoryclasping hook ' [page 1454] Fig. 3. Exposed view of the swim bladder of Ôncorhynchus masou (Brevoort) to show the infection by worms. Approximately 300 worms were found. Fig. 4. Cross-sectional view of a healthy swim bladder structure a - Tunica externa b - Pillar-like single layer. Upper epithelium of interior surfaue of the swim bladder. c Adventitia connective tissue a+eind b will be missing where it is infectei by the worm. ced.: Resembles muscle structure; however, this is a connective tissue. e - Blood vessel f - Submucosa g - Dense connective tissue h - Flat single layer epithelium which covers the outmost layer of the swim bladder. Fig. 5.. Side view of area near the mouth of an adult worm. a - Vestibulum b - Anterior esophagus c - Nerve ring [rage 1455] Fig. 6. Side view of area near the mouth of immature worms. a - Vestibulum b - Anterior esophagus Fig. 7. Tail portion of larva molting. a - Lateral line b - Anus c - Anal muscle d - Molt of the inner surface of the rectum ' e - Molt f - Wen-like protuberance at the end of the tall of larvajemale.

Chapter 12 Part 2. The Worms Platyhelminthes, Nematoda & Annelida

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