The Impact of Detoxification Costs and Predation Risk on Foraging: Implications for Mimicry Dynamics

Abstract

Prey often evolve defences to deter predators, such as noxious chemicals including toxins. Toxic species often advertise their defence to potential predators by distinctive sensory signals. Predators learn to associate toxicity with the signals of these so-called aposematic prey, and may avoid them in future. In turn, this selects for mildly toxic prey to mimic the appearance of more toxic prey. Empirical evidence shows that mimicry could be either beneficial ('Mullerian') or detrimental ('quasi-Batesian') to the highly toxic prey, but the factors determining which are unknown. Here, we use state-dependent models to explore how tri-trophic interactions could influence the evolution of prey defences. We consider how predation risk affects predators' optimal foraging strategies on aposematic prey, and explore the resultant impact this has on mimicry dynamics between unequally defended species. In addition, we also investigate how the potential energetic cost of metabolising a toxin can alter the benefits to eating toxic prey and thus impact on predators' foraging decisions. Our model predicts that both how predators perceive their own predation risk, and the cost of detoxification, can have significant, sometimes counterintuitive, effects on the foraging decisions of predators. For example, in some conditions predators should: (i) avoid prey they know to be undefended, (ii) eat more mildly toxic prey as detoxification costs increase, (iii) increase their intake of highly toxic prey as the abundance of undefended prey increases. These effects mean that the relationship between a mimic and its model can qualitatively depend on the density of alternative prey and the cost of metabolising toxins. In addition, these effects are mediated by the predators' own predation risk, which demonstrates that, higher trophic levels than previously considered can have fundamental impacts on interactions among aposematic prey species.

Fig 1. Optimal foraging strategies when detoxification is not costly.

Optimal foraging strategy for predators, shown as which prey types are rejected as a function of energy reserves R and toxin burden D for the four treatments: (a) mildly defended prey, α alone; (b) highly defended prey, β alone; (c) α and β both present and visually distinguishable; (d) α and β both present and perfect mimics. Here, there is no detoxification cost (κ = 0) and alternative prey are at intermediate availability (γ = 0.2). The shaded areas show the states where: the predators reject all prey including alternative prey (black); reject only the mildly defended prey (pale grey); reject only the highly defended prey (intermediate grey) reject both defended prey (dark grey). In the white areas, all prey are accepted.

Fig 2. Optimal foraging strategies when detoxification is costly.

Optimal foraging strategy for predators, shown as which prey types are rejected as a function of energy reserves R and toxin burden D for the four treatments: (a) mildly defended prey, α alone; (b) highly defended prey, β alone; (c) α and β both present and visually distinguishable; (d) α and β both present and perfect mimics. Here, there is a detoxification cost (κ = 1) and alternative prey are at intermediate availability (γ = 0.2). The shaded areas show the states where: the predators reject all prey including alternative prey (black); reject only the mildly defended prey (pale grey); reject only the highly defended prey (intermediate grey) reject both defended prey (dark grey). In the white areas, all prey are accepted.

Fig 3. Mortality of mildly and highly defended prey types.

Proportion of mildly defended α and highly defended β prey consumed by predators in the four experimental treatments (Mildly defended prey α alone; Highly defended prey β alone; α and β both present but distinguishably coloured; α and β both present and perfect mimics) for three values of the availability of alternative prey fγ (a, b) fγ = 0.1, (c, d) fγ = 0.2, (e, f) fγ = 0.3, and for whether detoxification is (a, c, e) cost-free (κ = 0) or (b, d, f) costly (κ = 1).

Fig 4. Impact of alternative prey on predator strategy and -state when defended prey are non-mimetic.

Effect of availability of alternative prey (fγ) on predator strategy (a, c, e) and stationary distribution of predator state (b, d, f) in the non-mimetic treatment. Results are shown for three values of availability of alternative prey (a, b) γ = 0.1, (c, d) γ = 0.2, (e, f) γ = 0.3. The shaded areas show the states where: the predators reject all prey including alternative prey (black); reject only the mildly defended prey (pale grey); reject only the highly defended prey (intermediate grey) reject both defended prey (dark grey) (a, c, e). In the white areas, all prey are accepted. Distribution of predator states are shown from high (white) to zero (black) (b, d, f).