Abstract
Multiple pathogens coexist in nature, and hence, host species often encounter several pathogens simultaneously. The sequence in which the host encounters the parasites influences interactions between parasites and host pathology. Here, the effects of infection by two cercaria (larvae of trematodes) types, pleurolophocercous cercaria of Acanthostomum burminis and a furcocercous cercaria, on the tadpoles of common hourglass tree frog (Polypedates cruciger) were examined. Ten days posthatch, tadpoles (Gosner stage 27/28) were used for infection exposures. First, in a single infection each cercaria type was introduced to the tadpoles separately. Second, coinfection of the two cercaria was carried out by alternating the sequences of exposure. For all the experiments, appropriate controls were instituted. Tadpoles of all groups exposed to parasites had lower survival levels compared to controls. Among the four groups exposed, the highest survival was observed in the coinfection when furcocercous was introduced first (82.5%). The lowest survival was observed in the coinfection when the A. burminis cercaria was introduced first (65.0%). In the coinfections, when A. burminis was introduced prior to furcocercous, survival of the tadpoles was reduced by 17.0% compared to the exposures of furcocercous prior to A. burminis. Prior infection with A. burminis induced negative effect on the host with an increased infection severity, while prior infection with furcocercous had reduced infection severity than lone exposures. These results suggest that furcocercous infections can be beneficial for hosts challenged with A. burminis provided that A. burminis exposure occurs second. None of the treatments had an effect on the growth of the tadpoles, but lengthening of developmental period was observed in some exposures. All exposed tadpoles developed malformations which were exclusively axial—kyphosis and scoliosis. However, there was no difference in the number of malformed individuals in the single infection (19.0%–25.0%) compared to coinfection (20.0%–22.5%) or between coinfections. The results suggest that the sequence of parasite exposure affects host–parasite interactions and hence the disease outcomes. Understanding the effects of coinfection on disease outcomes for hosts provides insight into disease dynamics.
Highlights
Hosts encounter multiple pathogens in nature, increasing the likeli‐ hood of coinfection, a condition where two pathogens exploit a host species one after the other (Hoverman, Mihaljevic, Richgels, Kerby, & Johnson, 2012; Pedersen & Babayan, 2011)
Exposure sig‐ nificantly reduced the survival in both groups (A. burminis = 67.5%, binomial generalized linear model (GLM), F = 9.47, p = 0.003, furcocercous = 75.0%, binomial GLM, F = 5.38, p = 0.023) compared to the control (95%)
A significant reduction of survival was observed when the tadpoles were exposed to cercaria of A. burminis prior to furcocercous but not vice versa
Summary
Hosts encounter multiple pathogens in nature, increasing the likeli‐ hood of coinfection, a condition where two pathogens exploit a host species one after the other (Hoverman, Mihaljevic, Richgels, Kerby, & Johnson, 2012; Pedersen & Babayan, 2011). The sequence in which hosts encounter parasites influences the interactions between parasites, and these priority effects have been identified in many systems (Alford & Wilbur, 1985; Connell & Slatyer, 1977; Hoverman, Hoye, & Johnson, 2013). The effect of Ribeiroia infection was reduced when the frogs were al‐ ready infected with Echinostoma, but the reverse sequences had no effect (Hoverman et al, 2013) This is the only study where sequen‐ tial exposure effects of trematode parasites have been shown for a frog species. Pleurolophocercous cercaria of Acanthostomum burminis, a trem‐ atode that infects water snakes, induces malformations, reduces mortality, and affects the growth in the tadpoles of the common hourglass tree frog, Polypedates cruciger (Jayawardena, Rajakaruna, Navaratne, & Amerasinghe, 2010b). We investigated the differential infection sever‐ ity, in terms of survival and malformations associated with sequence of exposure of tadpoles to the two parasites
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