Abstract
BackgroundFish are common intermediate hosts of trematode cercariae and their gills can potentially serve as important sites of penetration by these larval stages. We experimentally tested the hypothesis that volume of ventilation flow across the gills contributes to acquisition of these parasites by fish. We manipulated the intensity of ventilation by using different oxygen concentrations.MethodsJuvenile Oncorhynchus mykiss were individually exposed for 10 minutes to a standard dose of Diplostomum pseudospathaceum cercariae at three levels of oxygen concentration, 30, 60 and 90%. Ventilation amplitude (measured as a distance between left and right operculum), operculum beat rate, and the number of cercariae established in the eyes of fish were recorded.ResultsFish reacted to low oxygen concentration with wider expansion of opercula (but not with increasing beat rate), leading to an increase in ventilation volume. As expected, the intensity of infection increased with decreasing oxygen saturation—probably due to a higher exposure to cercariae caused by increased ventilation under low oxygen concentrations. The number of cercariae acquired by an individual fish was positively correlated with ventilation amplitude and with ventilation volume, but not with operculum beat rate. However, even though the infection rate increased under these circumstances, the proportion of larval trematodes successfully establishing in fish eyes decreased with increasing ventilation volume, suggesting that the high flow velocity, although increasing host exposure to cercarial parasites, may interfere with the ability of these parasites to penetrate their hosts. There was no difference in the behaviour of trematode cercariae exposed to low and high oxygen concentrations.ConclusionA reduction in oxygen saturation resulted in an increase in ventilation volume across the gills and in doing so an increase in the exposure of fish to cercariae. A significant correlation between ventilation volume and parasitism represents the first experimental evidence that this physiological mechanism generates variation in transmission of parasites to fish hosts. Other factors that modify ventilation flow, e.g. physiological or social stressors, are expected to produce similar effects on the transmission success of the parasites penetrating fish hosts using the gills.
Highlights
Fish are common intermediate hosts of trematode cercariae and their gills can potentially serve as important sites of penetration by these larval stages
Behaviour of cercariae To check whether the activity of D. pseudospathaceum cercariae was influenced by water oxygen content, we examined the behaviour of individual parasites at 90 and 30% oxygen saturation
The present results show that most rapid increase in ventilation and subsequent acquisition of D. pseudospathaceum cercariae occurred with a moderate reduction of oxygen concentration
Summary
Fish are common intermediate hosts of trematode cercariae and their gills can potentially serve as important sites of penetration by these larval stages. Respiration among most teleost fishes is based on pumping large volumes of water through the buccal and pharyngeal cavities and across the gills. This ventilation flow provides necessary dissolved oxygen, but contains various suspended particles including free living stages of parasites. Flow of the ventilation water in fish is regulated by two variables: ventilation frequency and the volume of each pump stroke [4]. Both parameters vary over a broad range [5]. Could intensity of infection by gill-penetrating parasites vary depending on ventilation rate and be influenced by the internal and external factors affecting ventilation rate? How costly could increased ventilation be in terms of elevated parasite burden? To answer these questions, infection success of gill penetrating parasites should be examined while manipulating the ventilation activity
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