Choosy cannibals: Targeted consumption of conspecific hatchlings by larval cane toads is triggered by species-specific defensive toxins

Abstract

In many species, cannibalism is uncommon and involves nonselective consumption of conspecifics as well as heterospecifics. However, within their invasive Australian range, cane toad larvae (Rhinella marina) specifically target and voraciously consume the eggs and hatchlings of conspecifics, often extirpating entire clutches. In contrast, toad larvae rarely consume the eggs and hatchlings of native frogs. Here, we use laboratory studies to demonstrate that this selective consumption is triggered by species-specific chemical cues: maternally-invested bufadienolide toxins that otherwise defend cane toad eggs and hatchlings against predators. We find that these cues stimulate feeding behaviors in toad tadpoles, such that the addition of bufadienolide toxins to the water column increases predation on eggs, not only of conspecifics, but also of native anuran species that are otherwise usually ignored. In contrast, we find that cannibalism rates on conspecific hatchlings are high and unaffected by the addition of bufadienolide cues. The maternally-invested toxins present in conspecific eggs may therefore be more easily detected post-hatching, at which point tadpole feeding behaviors are induced whether or not additional toxin cues are present. As bufadienolide cues have previously been found to attract toad tadpoles to vulnerable hatchlings, our present findings demonstrate that the same toxin cues that attract cannibalistic tadpoles also induce them to feed, thereby facilitating cannibalism through multiple behavioral effects. Because native fauna do not produce bufadienolide toxins, the species specificity of these chemical cues in the Australian landscape may have facilitated the evolution of targeted (species-specific) cannibalism in invasive cane toad populations. Thus, these bufadienolide toxins confer cost (increased vulnerability to cannibalism in early life-stages) as well as benefit (reduced vulnerability to predation by other taxa).

Keywords: Anura; Bufo marinus; behavior; chemical communication; embryonic development; intraspecific predation; ovivory; pheromone.

FIGURE 1

Comparison of cane toad tadpoles as predators of native frog eggs/hatchlings versus conspecific eggs/hatchlings under standardized experimental conditions. Ten individuals were exposed to predation by a single toad tadpole for each trial (for 10 replicate trials per species); data depict the proportion of individuals eaten before they could develop into free‐swimming tadpoles (Gosner (1960) stage 25), at which point they are no longer vulnerable to predation by cane toad tadpoles. Data on native frogs were extracted from Crossland (1998)

FIGURE 2

The proportion of 10 cane toad embryos or hatchlings exposed to a single cane toad tadpole that had been cannibalized at each monitoring period. Cannibalism rates were measured in the presence of a ceramic ring that either contained 2 mg of bufadienolide toxins (treatment: toxin present, N = 7) or did not contain toxins (treatment: toxin absent, N = 7). The numbers associated with each period indicate the mean developmental stage (Gosner, 1960) of the monitored individuals. In panel a experimental exposure to the cannibal tadpole began at Gosner stage 5–6 and hatching occurred late in stage 17; egg stages are shown in the gray section and hatchling stages in the white section. In panel b exposure to a cannibal tadpole began at hatchling stage 18. Monitoring in both experiments ended at stage 25; at this point, hatchlings have become free‐swimming tadpoles and can no longer be cannibalized. Asterisks indicate stages at which significantly more individuals had been cannibalized in the toxin treatment (p < .05). In the absence of a cannibalistic cane toad tadpole, survival to Gosner stage 25 was 100% (data not shown)

FIGURE 3

Predation by a cane toad tadpole on 10 unhatched heterospecific or conspecific embryos (Litoria tornieri or Rhinella marina) in the absence or presence of additional toxin cues (bufadienolides). Toxin treatments were either toxin freshly squeezed from adult toad parotoid glands (~1 mg bufadienolides) or toxin extracted from adult toad parotoid gland secretions and loaded onto ceramic rings (2 mg bufadienolides). Control (toxin absent) treatments contained a blank, biologically inert ceramic ring that contained no toxins. Embryo predation is depicted immediately prior to hatching (i.e., Gosner stage 23 for L. tornieri [63 h exposure] and Gosner stage 17 for R. marina [36 h exposure; see Figure 2]). In the absence of a predatory cane toad tadpole, mean survival for L. tornieri was 98% (range: 90% to 100%; data not shown)