Can predators stabilize host-parasite interactions? Changes in aquatic predator identity alter amphibian responses and parasite abundance across life stages

Abstract

The role of parasites can change depending on the food web community. Predators, for instance, can amplify or dilute parasite effects on their hosts. Likewise, exposure to parasites or predators at one life stage can have long-term consequences on individual performance and survival, which can influence population and disease dynamics. To understand how predators affect amphibian parasite infections across life stages, we manipulated exposure of northern leopard frog (Rana pipiens) tadpoles to three predators (crayfish [Orconectes rusticus], bluegill [Lepomis macrochirus], or mosquitofish [Gambusia affinis]) and to trematode parasites (Echinostoma spp.) in mesocosms and followed juveniles in outdoor terrestrial enclosures through overwintering. Parasites and predators both had strong impacts on metamorphosis with bluegill and parasites individually reducing metamorph survival. However, when fish were present, the negative effects of parasites on survival was not apparent, likely because fish altered community composition via increased algal food resources. Bluegill also reduced snail abundance, which could explain reduced abundance of parasites in surviving metamorphs. Bluegill and parasite exposure increased mass at metamorphosis, which increased metamorph jumping, swimming, and feeding performance, suggesting that larger frogs would experience better terrestrial survival. Effects on size at metamorphosis persisted in the terrestrial environment but did not influence overwintering survival. Based on our results, we constructed stage-structured population models to evaluate the lethal and sublethal effects of bluegill and parasites on population dynamics. Our models suggested that positive effects of bluegill and parasites on body size may have greater effects on population growth than the direct effects of mortality. This study illustrates how predators can alter the outcome of parasitic infections and highlights the need for long-term experiments that investigate how changes in host-parasite systems alter population dynamics. We show that some predators reduce parasite effects and have indirect positive effects on surviving individuals potentially increasing host population persistence.

Keywords: anurans; carryover effects; host–parasite interactions; predator–prey interactions; trematodes.

FIGURE 1

Adult northern leopard frog (Rana pipiens). Photo by Mike Wilhelm.

FIGURE 2

Influence of treatment on survival in the aquatic environment. (a) Proportion of leopard frog tadpoles exposed to predator treatments (none, bluegill, crayfish, or mosquitofish) and parasite treatments (absent, present) that survived to metamorphosis. (b) Proportion of individuals exposed to predator treatments that died in mesocosms after reaching metamorphosis. Plotted values are means ±1 SE. Asterisks indicate differences from the no predator treatment based on Dunnett's pairwise comparisons.

FIGURE 3

Mass at metamorphosis and larval period for leopard frogs exposed to (a) different predator treatments (none, bluegill, crayfish, or mosquitofish) and to (b) different parasite treatments (absent, present). Plotted values are means ±1 SE.

FIGURE 4

The average proportion of leopard frog tadpoles moving in each mesocosms exposed to (a) different parasite treatments (absent, present); and to (b) different predator treatments (none, bluegill, crayfish, or mosquitofish) for 7 weeks. Plotted values are means ±1 SE.

FIGURE 5

Average parasite load of frogs exposed to predator treatments (none, bluegill, crayfish, or mosquitofish) (a) at metamorphosis or (b) after overwintering. Plotted values are means of right kidneys only ±1 SE. Asterisks indicate differences from the no predator treatment based on Dunnett's pairwise comparisons.

FIGURE 6

Average number of original snails visible in mesocosms exposed to predator treatments (none, bluegill, crayfish, or mosquitofish). Plotted values are means ±1 SE. Asterisks indicate differences from the no predator treatment based on Dunnett's pairwise comparisons.

FIGURE 7

Influence of predator (none, bluegill, crayfish, or mosquitofish) and parasite treatment (absent, present) on (a) mass at metamorphosis, (b) average jumping distance, (c) maximum jumping distance, (d) swimming speed, and (e) number of crickets consumed by leopard frog metamorphs. Figure 7a Only shows the mass at metamorphosis for individuals that were used in the behavioral trials. Plotted values are means ±1 SE.

FIGURE 8

Relationship between mass at metamorphosis and (a) average jumping distance, (b) maximum jumping distance, (c) swimming speed, and (d) number of crickets consumed within 15 h. X‐axis is log transformed. Linear regression lines of best fit show the nature of relationship.

FIGURE 9

Mean λ (the finite rate of increase of population growth) values with 95% confidence intervals under experimental conditions. Parasite, bluegill, and their combined exposure represent scenarios where population growth is influenced by treatment effects on metamorph survival (i.e., lethal effects). The fast maturity scenario represents an earlier time to first reproduction resulting from the effects of parasites and bluegill on body condition (i.e., sublethal effects).