Approximately 100 years ago, about 400 fingerling striped bass (Morone saxatilis) were introduced from the Navesink River, N.J., into San Francisco Bay. For many years, fishermen noticed red "strawberry" marks, or open lesions, on the right side of the fish. Past explanations have included lamprey bites, copepod heads, gaff scars, embedded red algae and pollution. We showed that the lesions are the results of an infection by the trypanorhynchan metacestode, Lacistorhynchus dollfusi (= tenuis).1
In San Francisco Bay striped bass, the metacestodes penetrate the intestinal wall and die soon after becoming embedded in mesentery and Muscle. Other infected species of fish from this area have viable metacestodes. If many of these dead parasites in striped bass are in close proximity to each other, they will become encapsulated with fibrous tissue and form a 'raft' in the mesentery. When this 'raft' touches the peritoneum, an inflammatory response produces reddening on the external right flank of the fish. Lymphocytes and collagen-producing fibroblasts begin to appear at the edge of the 'raft'. As encapsulation continues, the 'raft' becomes embedded in the flesh and the first signs of a lesion develop on the skin. If the 'raft' is small, scar tissue will form behind it as it passes through the Muscle. In time, the 'raft' is expelled through the open lesion on the side of the fish. Removal of the 'raft' can result in a wound which exposes the coelomic cavity. Healed wounds often produce irregularly arranged replacement scales and indentations in the body wall. Laboratory studies showed that it takes at least two months for the wound to heal, is detectable for at least 22 months and probably the life of the fish. Degenerated individual metacestodes are found embedded in the muscle, however, they do not produce external surface lesions.
Lesions are usually found on the right side of the fish because of the fish's internal anatomy. The intestinal mesentery touches the right side of the body wall, hence when individual metacestodes emerge from the intestine on the right side and rafts are formed, they come in contact with the peritoneum. On the left side, the liver and stomach are between the mesenteries and the peritoneum. Dorsally-emerging parasites are blocked by the swimbladder.
The metacestode of Lacistorhynchus has been reported in over 60 species of fishes worldwide, including other fishes from San Francisco bay, with little or no pathological effect on the host.2 In addition, Lacistorhynchus is sympatric with striped bass on the cast coast of the U.S., but no lesions have been reported from these fish.
The purposes of this study were: to complete the life cycle the parasite and to produce these lesions in striped bass in the laboratory; to determine why the striped bass on the east coast do riot have lesions; and to assess what, if any, evolutionary adjustments the west coast stripers have mace as result of the presence of the parasite.
The presumptive life cycle of Lacistorhynchus was that the eggs passed out with the feces of elasmobranchs and product ciliated larvae (coracidia) which were eaten by microcrustaceans The microcrustaceans infected with procercoids in turn were ingested by fish, and the metacestode stage developed. The infected fish were then eaten by the elasmobranchs and the adult cestode developed in the spiral valve. This life cycle, however, had never been confirmed. Our study showed Lacistorhynchus eggs collected from the leopard shark hatched in 5 to 7 days3 at room temperature but were not viable at salinities of 8.5 or 17.0 ppt.4 The ciliated coracidia remained viable for two weeks at salinities greater than 50% seawater. The coracidia were fed to the marine copepod Tigriopus californicus. Procercoids developed, and remained infective up to four weeks. High temperature (19°C) shortened caracidia hatching times and survivorship, increased sizes of procercoids, and decreased prevalence of infection in the copepod. The procercoids cause copepod mortality, regardless of the intensity of the infection. As the intensities increased, the mean individual area (size) of procercoids decreased, suggesting a crowding effect. Infected copepods were fed to mosquitofish, Gambusia affinis. Metacestodes developed and were viable for up to six months. The infected fish were force-fed to uninfected leopard sharks . Adult cestodes were recovered one and a half years later.
To produce the lesions in the laboratory, infected copepods were fed to hatchery-raised striped bass. Histological sections indicated that a cellular host response was mounted early in the infection period, and that despite the leucocytic infiltration, the parasites continued to develop. However, at 3 months post-infection, some of the plerocercoids began to degenerate, and lesions formed at this time and continued 14 months post-infection.
The most probable reason that lesions have not been reported from the east coast is that the life history and geographic distribution of the East Coast stripers prevents them from coming in contact with the parasite at the time the striper would be feeding on the appropriate intermediate host. The east coast has a much more extensive river system than California. The young stripers spend their first year or more in freshwater. They are therefore, not exposed to the infected crustaceans. By the time that they enter the higher salinity waters, where sharks are found, they are feeding on fish. Hence, they do not become infected.
We conducted a series of reciprocal laboratory inflections between East and West Coast stripers and larval Lacistorhynchus6 to determine if: West Coast stripers are becoming resistant to the cestode infections; West Coast stripers would also react to a sibling species (L. tenuis) from the east coast; and infected East Coast stripers form lesions. The results showed that East Coast stripers will develop lesions when infected. In fact, they react more strongly to the larvae than do the West Coast stripers.
The East Coast fish had a greater percentage of degenerate larvae and a higher intensity of infection than West Coast stripers. We believe that the difference in the reactions to the larvae between the two stocks indicates that during the 100 years that the West Coast stripers have been exposed to the tapeworm, they have adapted to the parasite. The ancestral, naive East Coast stock has not encountered the parasite. Therefore, to its own detriment, it has a strong cellular response. Of interest, both East and West Coast stripers reacted more strongly to the West Coast population of Lacistorhynchus. This supports the suggestion that the two populations of Lacistorhynchus are different species (Beveridge and Sakanari, submitted).
We believe that the host-parasite relationship on the west coast has evolved towards a more compatible association as a result of selective mortality caused by the pathogenic parasite.6
To establish parasite-induced host mortality, we determined, over a four year period, the number of fish that had parasite induced lesions and scars resulting from the lesions. As mentioned earlier, these scars are probably detectable for the life of the fish. Therefore, we were able to predict the percentage of fish (cohorts) that would be expected to have scars the following year based on the previous year of sampling. The expected frequencies were compared and the results showed that there were significantly lower numbers of fish with scars than would be expected had the fish survived to the following year, suggesting that the lesions cause mortality. Selection may be favoring those fish that can maintain a more compatible host-parasite relationship, i.e. striped bass that do not respond pathologically to the infection.
References
1. Moser, M., and J. Sakanari, S. Wellings and K. Lindstrom. 1984. Incompatibility between San Francisco striped bass, Morone saxatills Walbaum) and the metacestode, Lacistorhynchus tenuis (Beneden, 1858). J. Fish Disease . 7 : 397-400.
2. Moser, M. 1983. Parasitological survey of San Francisco Bay - Delta area striped bass and other select species. Rept. to California State Water Res. Control Bd.
3. Sakanari J., and M. Moser. 1985. Infectivity of, and laboratory infection with, an elasmobranch cestode, Lacistorhynchus tenuis. (Van Beneden, 1858). J. Parasitol. 7 1 : 788-91.
4. Sakanari, J. and Moser, M. 1985. Salinity aria temperature effects on eggs, coracidia, and procercoids of Lacistorhynchus tenuis (Cestoda: Trypanornyncha) and induced mortality in first intermediate host. J. Parasitol. 71: 583 - 587.
5. Sakanari, J. A. and M. Moser. 1986. Lesion induction by the plercoceroid Lacistorhynchus tenuis (Cestoda) and wound healing in the striped bass Morone saxatilis (Walbaum) J. Fish. Biol. 28: 289-296.
6. Sakanari, J. and M. Moser. Evolutionary adjustments of a host species following its introduction. (Submitted)