Simultaneous infection of Schistosoma mansoni and S. rodhaini in Biomphalaria glabrata: impact on chronobiology and cercarial behaviour

Abstract

Background: The chances of a schistosome cercaria encountering a suitable definitive host may be enhanced by emergence from the molluscan intermediate host with maximal glycogen stores and by an appropriate chronobiological rhythm. This study aimed to identify and characterize the effects of potential competitive interactions in the snail host Biomphalaria glabrata, between the closely-related Schistosoma mansoni and S. rodhaini, on phenotypic behavioural traits. It was predicted that inter-specific competition would affect chronobiological emergence rhythms and reduce the activity of schistosome swimming behavioural traits. Biomphalaria glabrata snails (120) were exposed to either S. mansoni or S. rodhaini single infections, or a mixed infection of both species simultaneously and the resulting cercarial phenotypic traits were characterised. Cercariae were identified from co-exposed snails by amplification and sequencing of the mitochondrial cytochrome oxidase subunit 1 (CO1).

Results: S. mansoni and S. rodhaini largely maintained their distinct chronobiological rhythms after mixed exposures and infections. However, inter-specific competition appeared to result in a restriction of the shedding pattern of S. rodhaini and slight shift in the shedding pattern of S. mansoni. Inter-specific competition also significantly lowered hourly cercarial production for both parasite species in comparison to single exposures and infections and reduced cercarial swimming activity.

Conclusion: Inter-specific competition was shown to influence cercarial production, chronobiology and activity and should therefore be investigated further in field situations to determine the effects of these changes on parasite fitness (incorporating both host finding and infectivity) where these two species overlap. Importantly this competition did not result in a large change in chronobiological emergence of cercariae for either species indicating that it would not have a large influence on the species of hosts available for infection at time of emergence. This study has furthermore demonstrated the potential for phenotypic measures to provide markers for species-specific identification even in conditions of co-infection.

Figure 1

Chronobiology of cercarial emergence. Chronobiology of S. mansoni and S. rodhaini cercarial emergence from snails individually infected with each species (A and B), snails doubly exposed at a dose of 3 miracidia of each species but only patently infected with S. mansoni (C), doubly exposed at a dose of 6 miracidia of each species but with only single patent infections of S. mansoni or S. rodhaini (D) and snails doubly exposed to a dose of 6 miracidia of each species and doubly infected (E) over a 24 hr period (+- SE), ( . . . . = transition from light to dark.)

Figure 2

Cercarial swimming behaviour. Pie charts to show a comparison between the percentage of time unselected S. mansoni and S. rodhaini cercariae spend performing 16 different categories of behaviour (detailed in table 1).