Parasites as a Limiting Factor in Exploitation of Pacific Whiting, Merluccius productus

Z. KABATA and D. J. WHITAKER

Introduction Conispora meridionalis (Ev­ valves of unequal sizes. The spores are dokimova, 1977) (Sankurathri et aL, subconical in lateral view, the The parasite fauna of Pacific In press). posterior corners of the valves form­ whiting, Merluccius productus, like More important, however, are the ing sharp processes. The surfaces of that of most commercial fishes in the parasites belonging to the genus the valves are smooth and the suture eastern North Pacific, have not been Kudoa Meglitsch, 1947, which, lines very fine. The polar capsules are adequately studied. The extent of our because of their histozoic habits, are pyriform, of unequal sizes, one cap­ knowledge is best exemplified by the of direct concern to the fishing in­ sule being distinctly larger than the fact that, while Margolis and Arthur dustry. Grabda and Grabda (1975), other three. (1979) listed 10 parasite species who examined whiting taken by the Kudoa panijormis (Fig. IB) has recorded for this fish in Canadian Polish fishing fleet off California, spores subrectangular in polar view, waters, a small-scale survey carried recorded two species of Kudoa whjch with rounded valves and smooth sur­ out fairly recently in the Strait of they found in the musculature: Kudoa faces. Suture lines are devoid of ridges Georgia (Sankurathri et al., In press) clupeidae (Hahn, 1917) and Kudoa and are often somewhat sinuous. augmented that list to 22 species. In rosenbuschi (Gelormini, 1944). The Polar capsules are pyriform. Detailed view of the strong impact that some former has never been previously descriptions and measurements of of these parasites exert on the Pacific found in the genus Merluccius, but spores are given by Kabata and whiting fishery, this lack of attention the latter is known to occur in the Whitaker (1981). is regrettable. muscle of Merluccius hubbsi on the The spores of Kudoa are important The parasites of Pacific whiting on Patagonian shelf. Kabata and not only as the best clues to the identi­ which attention has been focused Whitaker (1981) put the validity of ty of the species; they also play a recently belong to the protozoan these records in doubt, because of prominent role in the life cycle of phylum Myxosporea. Sankurathri morphological differences and these parasites. The spore is the stage (1977) described Conispora renalis dissimilarity in the host-parasite rela­ that serves as the means of dispersal from the renal tubules of the whiting tionships. However, further studies in of the parasite and as the source of in­ in Georgia Strait. This species was Californian waters are needed to fection for new host individuals. found later to be identical with Myx­ allow a defiilltive conclusion in this Released from the musculature of oproteus meridionalis Evdokimova, matter. According to Kabata and dead fish, it must float in water and 1977, discovered in the urinary blad­ Whitaker (1981), the two species of make contact with the fish it is to in­ der of Merluccius hubbsi Marini, Kudoa infecting Pacific whiting off fect. The release could occur as the 1933, on the Patagonian shelf. Ev­ North American shores are Kudoa result of natural death of the host and dokimova's (1977) description, thyrsitis (Gilchrist, 1924) and Kudoa subsequent decomposition. It is also chronologically before that of panijormis (Kabata and Whitaker, likely that moribund fish would be Sankurathri, was incorrect in placing 1981). This paper concerns these two disposed of by predators. The spores, that species in Myxoproteus. It was species. with the digested remains of their necessary to place it in Conispora, host, would then be voided by the Morphology and Life while retaining Evdokimova's original predator. Whatever the mode of Cycle of Kudoa specific name. It is now known as release, being heavier than water, they Only the spores have been de­ gradually sink and are likely to des­ scribed in detail for the two species of cend to levels deeper than the habitat The authors are with [he Pacific Biological Sta­ Kudoa parasitic in Pacific hake. of their potential host. Kovaleva et aL tion, Fisheries Research Branch, Department of Kudoa thyrsitis (Fig. IA) is distin­ (1979) pointed out that the distribu­ Fisheries and Oceans, anaimo, B.C. V9R 5K6, Canada. guished by stellate spores, with four tion of the various Kudoa species in

47(2),1985 55 infection is more likely to deliver a concentrated dose of spores to the new host. It is currently presumed that Kudoa reaches its target site within the host via the intestinal tract and the cir­ A culatory system, but evidence sup­ porting this presumption is still cir­ cumstantial, at least for this particular myxosporean genus. The earliest stage known in the life cycle of Kudoa parasitic in Pacific whiting is a large trophozoite filling a sometimes substantial portion of a muscle fiber. In some instances the entire fiber is filled by the parasite to the point of becoming visibly dis­ tended. Observation with the naked eye reveals these fibers, or pseudo­ cysts, as white or black streaks. A new generation of spores develops within sporoblasts contained inside these relatively gigantic trophozoites. The distribution of pseudocysts in an individual host is not uniform. There are no significant differences between the right and the left side of the fish, but the number of infected muscle fibers tends to diminish from the anterior end toward the tail of the fish. The area most heavily infected is the dorsal musculature immediately behind the head; the lightest infection is found in the caudal peduncle. In view of the life history of Kudoa, this type of distribution is not unexpected. The sporoplasms (the infective agents carried within the spore) are released in the intenstine, penetrate the gut B wall, and enter the bloodstream. They are then carried by blood via the hepatic portal system, through the liver, heart, and gills, to the dorsal aorta. Along the latter they are Figure 1. - Unfixed spores in lateral and anterior view: (A) Kudoa transported in the posterior direction. thyrsitis; (B) Kudoa panijormis. (From Kabata and Whitaker 1981). The blood vessels branching off from the aorta near its origin have the greatest chance of receiving the proto­ zoan intruder. The number of para­ sites dwindles with their transport the Atlantic Ocean coincided with species of fish. (Atheresthes stomias towards the tail. areas of upwelling, in which the provides an example of such a demer­ Effect of Infection spores can be maintained by the sal host along the Pacific coast of on Muscle Tissue ascending currents at the depths in­ North America.) The Pacific whiting habited by their host species. The ex­ is cannibalistic and is often taken with Both species of Kudoa mentioned ceptions to this rule are provided by the remains of its conspecifics in the above penetrate individual muscle Kudoa parasitizing bottom-dwelling alimentary canal. The latter way of fibers. They do not appear to undergo

56 Marine Fisheries Review any division, once within these fibers. Judging from some very high inten­ sities of infection, some division prob­ ably occurs after the sporoplasm enters the blood vessel. In conse­ quence, a single sporoplasm could provide the means for infecting many muscle fibers. Within the confines of a fiber, the feeding stage (trophozoite) expands and its surface membrane de­ velops countless irregular villosities. The normal structure of the fiber is disrupted, and its tissue gradually breaks up and is replaced by the parasite. The trophozoite gradually fills with spores of various stages of development. The parasite within the fiber is sufficiently isolated from the host to prevent its immediate defen­ sive reaction. At this stage the term "pseudocyst" is properly applied to the infected fiber, to distinguish this condition from the true cysts which Figure 2. - Transverse section through musculature of hake, showing uninfected fibers (N); young, white pseudocysts (W); and old, black are much more disruptive to the pseudocysts (B). tissues and are surrounded by connec­ tive tissue capsules deposited by the host. Each pseudocyst is a cylindrical, elongated structure, often apparent to the naked eye as a streak of color, distinguishing it from the surround­ gram of muscle tissue have been As demonstrated by Patashnik et al. ing, uninfected muscle fibers. The col­ found (Kabata and Whitaker, un­ (1982), the substances in question are or of pseudocysts varies with the age pub!. data). The infected fibers ob­ proteolytic enzymes. During the life of the infection. At the relatively early viously lose their contractility and can of the fish, the excretory system is ef­ stage, when the trophozoite is still no longer participate in the locomo­ ficient enough to prevent the ac­ growing and filling with spores, the tion of the fish. The fact that the fish, cumulation of the enzyme in quan­ color of the fiber is opaque white. As even when heavily infected, can still tities sufficient to result in serious the villosities of the trophozoites ap­ continue its locomotory activities, is damage to the muscle tissue. The proach the sarcolemma of the muscle understandable, when one takes into death of the host has a twofold effect: fiber, the enzymes produced by the account that the white muscle, which It terminates the functioning of the parasite leak out and are detected by constitutes the substrate of the excretory mechanisms, while, at the the host; the host's reaction becomes parasite, is not extensively involved in same time, the production of the en­ histologically evident. It consists of the normal cruising movements. zyme continues unabated. Facing surrounding the infected fiber with Kudoa has not been found in the dark biochemical changes induced by the histiocytes. Within the coating of muscle, the main natatory effector. death of the host, the parasite brings these cells, the infected fiber gradually The infected fillet is streaked with its development to the final process of assumes a yellowish hue, passing into distended, white or black (or both) sporulation, and formation of protec­ brown and eventually black. By a fibers, depending on the intensity and tive spores, over a period of 8-12 process as yet unknown the parasite is age of the infection. Not unnaturally, hours (Willis, 1949). No longer compressed, the spores progressively its appearance markedly lowers the removed from the site, the enzyme ac­ crumpled, and, in the end, destroyed. acceptance ofthe product by potential cumulates there, with consequences (Work on the reaction of whiting to customers, even if infected fish is sup­ discussed by Nelson et aI. (1985). K. thyrsitis is in progress.) plied to them in otherwise satisfactory Tsuyuki et al. (1982) discovered The three stages, from uninfected condition. From the point of view of two temperature optima for the pro­ (N), through young, white pseudocyst the fishing industry, however, much teolytic activity of the enzyme pro­ (W), to old, black ones (B) are shown more important than any mechanical duced by Kudoa, one at 35-40o e (pH in Figure 2. In particularly heavy in­ damage is the effect of the chemical 3.8), the other at 55-60 o e (pH 6.7). It fections nearly 1,000 pseudocysts per substances produced by the parasite. is possible that these optima corre-

47(2),1985 57 spond to the actIvItIes of two en­ data) from examination of a small elapse between the time of entry of zymes, produced by the two species of sample (35 fish) collected off the the parasite and the formation of Kudoa examined. There are strong in­ mouth of Columbia River in June these aggregates of spores. That dications that the efffects these species 1982. The overall prevalence was 94.3 period must be characterized by the exert on whiting differ in their percent with K. thyrsitis present in intensive activity of the parasite, pass­ magnitude. Although more work is 42.9 percent of the sample, K. ing through its successive stages of required to arrive at definitive conclu­ panijormis in 17 percent, and mixed development. The existence of a "hid­ sions, it appears, in light of present infection in 34.3 percent. den increment" of infection can be evidence, that K. thyrsitis is less The estimate of intensity of proto­ confidently postulated. The size of damaging to whiting flesh than K. zoan infections is notoriously dif­ that increment cannot be assessed on panijormis. Some speculations on the ficult, exact counts being impossible the basis of data available. Its assess­ reason for this difference are included for obvious reasons. It is fairly ment is, however, necessary, if the below. generally accepted that categorizing true effects of Kudoa on the flesh are of infection into light, medium, and to be correctly understood. Some am­ Prevalence and Intensity heavy is sufficient to express intensity. biguous results of investigation of of Infection Kabata and Whitaker (1981) used this these effects are almost certainly due In spite of its acknowledged impor­ scale, having arbitrarily defined light to the fact that of any two apparently tance to the fishing industry, the as the presence of < 20 pseudocysts, uninfected fish one might harbour prevalence of the Kudoa infection of medium as 21-100, and heavy as Kudoa in its "hidden" stage. Proposed whiting has never been subjected to > 100 per area. Counts of future studies of the Kudoa problem an adequate parasitological investiga­ pseudocysts were made under a dis­ must, therefore, include investigation tion. The work of Patashnik et a!. section microscope, the entire fillet of the origin and early stage of infec­ (1982) is an example of the difficulties being macerated in the process. A tion. facing workers investigating a fillet was divided into six areas, The distribution of the two Kudoa parasitological problem without ap­ horizontally by the lateral line and species and their effects offer grounds propriate input from parasitologists. vertically by two lines marking off for some interesting speculations. K. Although Patashnik and his col­ three parts of equal length. Patashnik thyrsitis, the less harmful species, is leagues were aware of the existence of et al. (1982) estimated the intensity of also the more widespread. It has been two species of Kudoa (which were infection by "visual observation," reported from several species of fish referred to as "small" and "large" presumably without any optical aids. as far from the American Pacific as Kudoa), the infection was treated as a Their scale of intensity was 0-5, with 0 Australia and South Africa. In the single phenomenon. Having exam­ denoting absence of observable para­ latter part of the world it was record­ ined samples of 10-15 fish, they found sites. It was based "on the percent of ed in Merluccius capensis by Priebe that the combined prevalence ranged the area affected," I '" trace (up to 5 (1967). In the area inhabited by the from 20 to 40 percent. These figures percent); 2 '" slight (5-20 percent); 3 Pacific whiting it has been found also are at odds with those obtained by '" moderate (20-30 percent); 4 '" in walleye pollock, Theragra Kabata and Whitaker (1981), who severe (30-50 percent); 5 '" excessive chalcogramma, and some flatfish found much higher prevalence of (> 50 percent). The precise definition species. Both the distribution and the Kudoa. In a sample of 322 fish taken of the "area affected" was not provid­ host range .suggest an "old" species, in a single haul off the southwest ed. The present authors, in work now well adjusted to its hosts and, conse­ coast of Vancouver 1. in September in progress, have resorted to a more quently, not excessively harmful. In 1980, the prevalence of infection was quantitative determination of the in­ contrast, K. panijormis, widespread 89.5 percent. K. thyrsitis was found in tensity of infection. They are using a in the offshore whiting population, 32.2 percent and K. panijormis in number of pseudocysts (nearly or appears to be a relative newcomer. It 38.8 percent of the fish examined. A completely equivalent to the number does not occur in the Georgia Strait further 18.3 percent were infected of trophozoites) per gram of muscle whiting stock or in a small inshore with both species. In the Strait of tissue in six areas defined above. stock on the west coast of Vancouver Georgia, where 100 fish were exam­ Neither of the two sets of observa­ I., both isolated from the main off­ ined, only K. thyrsitis was found, tions described above can be said to shore population. It has not been parasitizing 99 percent of the sample. reflect the true prevalence and intensi­ found in any other fish species. These It is possible that a systematic survey ty of Kudoa in whiting flesh. As men­ facts suggest that K. panijormis in­ will discover a middle ground between tioned, the presence of this parasite in fected whiting subsequent to the these two sets of data. However, the the fish is not easily detectable until separation of these stocks. As a "new" prevalence figures of Patashnik et a!. the development of pseudocysts. parasite, it has not yet attained a (1982) are probably too low. This is (Stages prior to cyst formation have stable equilibrium with its host and is, suggested by the data obtained recent­ not yet been detected.) Some period, therefore, much more virulent in its ly (Kabata and Whitaker, unpub!. of still unknown duration, must effects.

58 Marine Fisheries Review Literature Cited Yakovlev. 1979. Miksosporidii roda Sankurathri, C. S. 1977. Conispora renalis Kudoa (Myxosporidia, Multivalvulea) bas­ gen. nov. et sp. nov. (Myxosporida: War­ seyna Atlanaticheskogo Okeena. [Myx­ diidae) from the kidney tubules of Pacific osporidia (Multivalvulea) of the genus Kudoa hake, Merluccius productus, (Ayres, 1855), in Evdokimova, E. B. 1977. Miksosporidii in the basin of the Atlantic Ocean.] Trudy coastal waters of British Columbia. Can. J. kostinykh ryb patagonskogo shelfa (Atlan­ Zoo!. Ins!. Akad. Nauk SSSR, 87:42-90. Zoo!. 55(7): 1147-1150. ticheskoe poberezhe Argentiny). [Myx­ Margolis, L., and J. R. Arthur. \979. ____, Z. Kabata, and D. J. Whitaker. osporidia of the teleost fishes of Patagonian Synopsis of the parasites of fishes of Canada. (In press). Parasites of the Pacific hake, shelf (Atlantic coast of Argentia).] Bul!. Fish. Res. Board Can. 199,269 p. Merluccius productus, (Ayres, 1855) in the Parazitologiya, II (2): 166-178. Nelson, R. W., H. J. Barnett, and G. Kudo. Strait of Georgia, in 1974-/975. Syesis. Grabda, E., and J. Grabda. 1975. Prelimin­ 1985. Preservation and processing charac­ Tsuyuki, H., S. N. Williscroft, Z. Kabata, and ary note on some protozoan species of the teristics of Pacific whiting, Merluccius pro­ D. J. Whitaker. 1982. The relationship genus Kudoa (Myxosporidia) parasitizing ductus, Mar. Fish. Rev. 47(2):60-74. between acid and neutral protease activities codfishes (Gadidae) muscles. Summaries, 2nd Patashnik, M., H. S. Groninger, Jr., H. Bar­ and the incidence of soft cooked texture in European Multicolloquim of Parasitology. nett, G. Kudo, and B. Koury. 1982. the muscle tissue of Pacific hake (Merluccius Drustvo Parazitologa Jugoslavije, Beograd, Pacific whiting Merluccius productus: I. Ab­ productus) infected with Kudoa panijormis p.89-90. normal muscle texture caused by and/or K. thyrsitis, held for varying times Kabata, Z., and D. J. Whitaker. 1981. Two myxosporidian-induced proteolysis. Mar. under different pre-freeze chilled storage con­ species of Kudoa (Myxosporea: Fish. Rev. 44(5):1-12. ditions. Fish. Aqua!. Sci. Can. Tech. Rep. Multivalvulida) parasitic in the flesh of Priebe, K., 1967. Ober das Vorkommen von 1130,39 p. Merluccius productus, (Ayres, 1855) Pisces: Myxosporidien-pseudocysten in der Willis, A. G. 1949. On the vegetative forms Teleostei) in the Canadian Pacific. Can. J. Muskulatur von siidatlantischen Seehecht and life history of Chloromyxum thyrsitis Zoo!., 59(11):2085-2091. (Merluccius capensis). Arch. Lebensmit­ Gilchrist and its doubtful systematic position. Kovaleva, A. A., S. S. Shulman, and V. N. telhyg. Hannover 18:202-204. Aus!. J. Sci. Res. (Ser.B), 2(4):379-398.

47(2),1985 59