Studies on the biology of some parasites of the three-spined stickleback, Gasterosteus aculeatus L. with special reference to myxosporea

Abstract

A population of three-spined stickleback, Gasterosteus aculeatus L., was sampled every two weeks for 14 months from Airthrey Loch on the campus of the University of Stirling. A total of 857 fish were collected and three species of parasites were studied. The monogenean Gyrodactylus gasterostei was found on the skin and fins and two myxosporean parasites, Sphaerospora elegans and Myxobilatus gasterostei, were present in the kidney. All parasite species were present throughout the year but abundance was correlated with the yearly life cycle of the host fish. Lower prevalence and intensity were observed in summer due to the large number of young fish in the samples. The comparative ultrastructure and development of the two myxosporeans was studied by light and transmission and scanning electron microscopy. Both myxosporeans followed the general pattern of myxosporean development but showed some novel features. Sphaerospora e/egans had two distinct developmental cycles. A proliferative cycle involving extrasporogonic stages occurred in the blood whereas spore production occurred in the kidney. Light microscopy of Giemsa stained blood smears suggested proliferation of extra-sporogonic stages by external budding or plasmotomy. Structural similarities between extra-sporogonic blood stages and sporogonic kidney stages are discussed. Although S. elegans mostly formed disporous plasmodia, monosporous plasmodia were also occasionally observed. Before the appearance of sporogonic cells within the early pseudoplasmodia, certain areas of pseudoplasmodial cytoplasm became electron lucent, eventually acquired cell organeUes and later appeared as sporogonic cells. Developing valvogenic cells contained protuberances at the posterolateral side of spores which disappeared in mature spores. Characteristic lipid bodies were seen in developing capsulogenic cells and developing uninucleated sporoplasmic cells contained abundant glycogen granules. The sporoplasmic cells were devoid of sporoplasmosomes. Plasmodia of M. gasterostei were mono, di or polysporous and showed features of both coelozoic and histozoic myxosporeans, including a unit surface membrane, simple pinocytosis aanand presence of a number of vegetative nuclei and generative cells, the latter which formed pansporoblasts before the initiation of sporogenesis. A membrane bound tubular structure and some electron dense fibrillar bundles are previously undiscovered cytoplasmic organelles of the plasmodia. Developing capsulogenic cells contained characteristic membrane bound vacuoles filled with electron dense (glycogen) material. Myxobilatus gasterostel attached to the epithelial cells by plasmodial surface projections and there were electron dense areas at the point of attachment. Sphaerospora elegans showed occasional hairlike processes projecting from the pseudoplasmodial surface to the microvillous brush border of the epithelial cells. There were no electron dense areas at the point of attachment to the epithelial cells of the kidney tubules. Early undifferentiated pre-sporogonic stages of both parasites were occasionally present intracellularly in the tubular epithelium suggesting this is a route of entry into the tubular lumen. Early stages of S. elegans were also seen in the capillary lumen of the glomerulus. Intracellular and intraluminal stages of S. elegans and M. gasterostel caused pathological changes in different ways. Histopathological changes associated with S. elegans included vacuolation and accumulation of electron dense material in the epithelium whereas M. gasterostei caused large vacuolation with necrosis of the epithelial layer. Both parasites caused destruction of glomerular tufts in heavy infections and an increased number of rodlet cells in the epithelial layer were common in both cases. The two myxosporean species were most abundant during the winter and spring. Extra-sporogonic stages of S. elegans were found only in January and June in the rete-mirabile of the eye, circulating blood and kidney. In infections with S. elegans sex of the host fish was apparently of no significance, whereas significantly lower infestations occurred in male sticklebacks infected with M. gasterostei compared with females. Host size was important in determining the prevalence and intensity of both myxosporean species. Older fish were less heavily infected, possibly due to an acquired immunity or pathogenic effects on the host. A high number of mixed infections indicated that there was no interspeciflc competition between the two parasites. There appeared to be a continuous recruitment of myxosporeans throughout the year. Studies on myxosporean spore shedding suggested that spore production and shedding was continuous throughout the year and was uninfluenced by temperature or season. Gyrodactylus gasterostel was generally more abundant in winter and spring than in summer and autumn, reflecting the greater numbers of small young of the year fish at these times. The age of the host fish was a significant factor influencing the prevalence and intensity of infestation with G. gasterostei. Sex of the host had no apparent influence on infestation. The parasite was highly overdispersed within the host population and its distribution was best fitted by the negative