Pathogens and predators: examining the separate and combined effects of natural enemies on assemblage structure

Abstract

Natural enemy ecology strives to unify predator–prey and host–pathogen interactions under a common framework to gain insights into community- and ecosystem-level processes. To address this goal, ecologists need a greater emphasis on: (1) quantifying pathogen-mediated effects on community structure to enable comparisons with predator-mediated effects and (2) determining the interactive effects of combined natural enemies on communities. We conducted a mesocosm experiment to assess the individual and combined effects of predators (dragonfly larvae and adult water bugs) and a pathogen (ranavirus) on the abundance and composition of a larval amphibian assemblage. We found that our three natural enemies structured victim assemblages in unique ways, producing distinct assemblages. Additionally, we found that in combination treatments, predators mainly drove assemblage structure such that the assemblages most closely resembled their respective predator treatments. We also found that predators reduced infection prevalence in combination treatments, and that the magnitude of this effect was dependent on predator identity. Compared to virus-alone treatments, the presence of dragonflies and water bugs reduced infection prevalence by 79% and 63%, respectively. Additionally, the presence of dragonflies eliminated ranavirus infection in two species, which demonstrates the prominent role of predators in disease dynamics in this system. Overall, this work demonstrates the importance of considering natural enemies in community ecology, as each enemy can elicit a unique structural change. Additionally, this study provides a unique empirical test of the healthy herds hypothesis for multi-species assemblages and underscores the importance of advancing our understanding of multi-enemy interactions within communities.

Appendix

See Tables 4, 5, 6, 7, 8 and Figs. 3, 4, 5 and 6.

Table 4 Initial mass and stage data for each species added to the mesocosm experiment

Table 5 Summary of linear discriminant analysis for differences in amphibian abundances across natural enemy treatments

Table 6 Results of one-way ANOVA analyses of mass data for each species, and one-way Kruskal-Wallis tests for each species stage data.

Table 7 Results of pairwise contrasts using Wilcoxon rank-sum tests run subsequent to a significant Kruskal-Wallis rank sum test (${\chi }^{2}=11.8, P=0.008$) on tadpole viral load in response to enemy presence and density

Table 8 Results of PERMANOVA examining the interactive effects of predators, virus, density, a virus-by-predator interaction and a predator-by-density interaction on the tadpole assemblage

Fig. 3

Species-level abundance across treatments at the end of the experiment. Data are means ± 1 SE

Fig. 4

Mean mass for each of our focal species at the end of the experiment. Letters represent differences between group means determined using Tukey post-hoc tests. Error bars are ± 1 SE

Fig. 5

Mean Gosner stage for each of our focal species at the end of the experiment. Error bars are ± 1 SE

Fig. 6

Overall log-transformed viral load (solid circles) and species-level log-transformed viral load (bars) in the four treatments containing virus at the end of the experiment. Data for overall viral load are means ± SE