Numbers, neighbors, and hungry predators: What makes chemically defended aposematic prey susceptible to predation?

Abstract

Many chemically defended aposematic species are characterized by relatively low toxin levels, which enables predators to include them in their diets under certain circumstances. Knowledge of the conditions governing the survival of such prey animals-especially in the context of the co-occurrence of similar but undefended prey, which may result in mimicry-like interactions-is crucial for understanding the initial evolution of aposematism. In a one-month outdoor experiment using fish (the common carp Cyprinus carpio) as predators, we examined the survival of moderately defended aposematic tadpole prey (the European common toad Bufo bufo) with varying absolute densities in single-species prey systems or varying relative densities in two-species prey systems containing morphologically similar but undefended prey (the European common frog Rana temporaria). The density effects were investigated in conjunction with the hunger levels of the predator, which were manipulated by means of the addition of alternative (nontadpole) food. The survival of the B. bufo tadpoles was promoted by increasing their absolute density in the single-species prey systems, increasing their relative density in the two-species prey systems, and providing ample alternative food for the predator. Hungry predators eliminated all R. temporaria individuals regardless of their proportion in the prey community; in treatments with ample alternative food, high relative B. bufo density supported R. temporaria survival. The results demonstrated that moderately defended prey did benefit from high population densities (both absolute and relative), even under long-term predation pressure. However, the physiological state of the predator was a crucial factor in the survival of moderately defended prey. While the availability of alternative prey in general should promote the spread and maintenance of aposematism, the results indicated that the resemblance between the co-occurring defended and undefended prey may impose mortality costs on the defended model species, even in the absence of actual mimicry.

Keywords: amphibian; aposematism; associational effects; mimicry; predator hunger; tadpole.

Figure 1

Species used in the study: (a) common toad Bufo bufo (early tadpole stage, chemically defended prey); (b) common frog Rana temporaria (early tadpole stage, undefended prey); (c) common carp Cyprinus carpio (predator). The images are not to scale

Figure 2

Survival to metamorphosis of moderately chemically defended B. bufo tadpoles along the gradient of the initial absolute densities of conspecifics in experimental enclosures with fish predators. Data points are individual replicates. Circles indicate enclosures with low (empty circles) or high (filled circles) levels of alternative non‐tadpole food (fish feed pellets) for the predator. The overlapping data points have been jittered. The graph is based on raw data; the line showing the effect of prey density is fitted using binomial regression

Figure 3

Survival to metamorphosis of moderately chemically defended B. bufo tadpoles along the gradient of their initial relative density in two‐species tadpole communities containing undefended, morphologically similar R. temporaria tadpoles, in experimental enclosures with a fish predator. Initial relative density is expressed as the proportion of B. bufo tadpoles to the total initial number of tadpoles. The initial absolute density of B. bufo was fixed across all treatments (30 tadpoles/enclosure). Data points are individual replicates. Circles indicate enclosures with low (empty circles) or high (filled circles) levels of alternative nontadpole food for the predator (fish feed pellets). The overlapping data points have been jittered. The graph was based on raw data; the line showing the effect of the relative density of the chemically defended species was fitted using binomial regression

Figure 4

Metamorph mass (mean ± SE) of B. bufo (N = 436) specimens along the gradient of their initial absolute density in experimental enclosures with common carp C. carpio. Lightly‐shaded bars indicate treatments with low levels of alternative (non‐tadpole) food for fish, dark shaded bars indicate treatments with high levels of alternative food. Particular combinations of treatments are not represented because either some enclosures were excluded from the experiment, or very few tadpoles survived to metamorphosis (<3 metamorphs)

Figure 5

Metamorph mass (mean ± SE) of B. bufo (N = 166) specimens along the gradient of their initial relative density in experimental tadpole communities with R. temporaria under predation pressure from the common carp C. carpio. Lightly‐shaded bars indicate treatments with low levels of alternative (non‐tadpole) food for fish, dark shaded bars indicate treatments with high levels of alternative food. Particular combinations of treatments are not represented because either some enclosures were excluded from the experiment, or very few tadpoles survived to metamorphosis (<3 metamorphs)