Toxin cues affect cannibalism responses of cane toad tadpoles

In many species cannibalism is uncommon and involves non-selective 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, producing bufadienalide toxins confers a cost (increased vulnerability to cannibalism in early life-stages) as well as a benefit (reduced vulnerability to predation by other taxa). Methods The data are from a series of laboratory experiments conducted in Australia, where eggs/hatchlings of invasive cane toads (Rhinella marina) and a native frog (Litoria tornieri) were exposed to a predatory cane toad tadpole in the absence versus presence of toxin (bufadienolide) cues. The response variable was the number of eggs/hatchlings consumed. Data were analysed as a binomial response to treatment. Usage Notes The data provided are the raw data as collected during the experiments. When we analysed the data, there were several instances where the models failed to reach convergence due to 100% survival in the Control treament. To account for this and obtain a conservative estimate of effect, we allocated one tadpole to have died in the Control treatment. Specifically, we did this for: Experiment 1 C. albogutata (TadPresent versus TadAbsent), P. ornatum (TadPresent versus TadAbsent), R.marina (TadPresent versus TadAbsent) Experiment 2 Egg stage 14 analysis (toxin absent versus present). Details of these adjustments are given in our manuscript and in the attached README file. To follow our analyses in these specific instances, others need to make these adjustments. Also, note that the data sheet "Expt 2 Toad Egg-Hatchling Data" has data for both number of eggs eaten/not eaten and number of hatchlings eaten/not eaten. Thus, while eggs were developing and not yet hatched in this data set, the columns for TotalNSurvivingAtHatching, HatchlingsEaten and HatchlingsNotEaten are not relevant because eggs have yet to reach the hatchling stage (i.e., there are no hatchling data). In these instances, the cells for TotalNSurvivingAtHatching, HatchlingsEaten and HatchlingsNotEaten are filled with "n/a" (not applicable).在多数物种中，同类相食（cannibalism）并不常见，且往往同时涉及同种个体（conspecifics）与异种个体（heterospecifics）的无选择性取食。然而，在入侵至澳大利亚的分布范围内，蔗蟾（cane toad, Rhinella marina）的幼虫会特异性靶向并贪婪取食同种个体的卵与幼体，常常彻底摧毁整批卵块。与之形成鲜明对比的是，蔗蟾幼虫极少取食本土蛙类的卵与幼体。 本研究通过室内实验证实，这种选择性取食行为由物种特异性化学信号（chemical cues）触发：即母体传递的蟾毒内酯类毒素（bufadienolide toxins）——这类毒素原本可保护蔗蟾的卵与幼体免受捕食者侵害。研究发现，此类信号可激发蔗蟾蝌蚪的取食行为：当水体中添加蟾毒内酯类毒素时，不仅同种个体的卵，就连原本常被忽略的本土无尾目（anuran）物种的卵，其被捕食的概率均会上升。与之相反，同种幼体的同类相食率本就较高，且不受添加蟾毒内酯类信号的影响。由此推测，存在于同种卵中的母体传递毒素，在幼体孵化后更易被检测到，此时无论是否存在额外的毒素信号，蝌蚪的取食行为均会被诱导激活。 过往研究已证实，蟾毒内酯类信号可吸引蔗蟾蝌蚪前往易受攻击的幼体所在区域，而本研究结果表明，这类吸引同类相食蝌蚪的毒素信号同时还能诱导其取食行为，从而通过多种行为效应促进同类相食的发生。 由于本土动物群无法产生蟾毒内酯类毒素，在澳大利亚的生态环境中，这类化学信号的物种特异性可能推动了入侵蔗蟾种群中靶向性（物种特异性）同类相食行为的演化。由此可见，合成蟾毒内酯类毒素兼具代价与收益：代价是早期生命阶段的同类相食风险升高，收益则是降低了被其他类群捕食的概率。 ## 研究方法 本数据集源自澳大利亚开展的一系列室内实验：将入侵性蔗蟾（Rhinella marina）以及本土蛙类（Litoria tornieri）的卵/幼体分别置于有无毒素（蟾毒内酯类毒素，bufadienolide）信号的环境中，与捕食性蔗蟾蝌蚪共同培养。响应变量为被取食的卵/幼体数量。数据以处理组的二项分布响应形式进行分析。 ## 使用说明 本数据集提供的是实验过程中直接采集的原始数据。在数据分析阶段，我们遇到多组因对照组（Control）个体全部存活导致模型无法收敛的情况。为修正该问题并得到保守的效应估计值，我们将对照组中1只蝌蚪记为死亡。具体调整情况如下： 实验1：C. albogutata（TadPresent vs TadAbsent）、P. ornatum（TadPresent vs TadAbsent）、R.marina（TadPresent vs TadAbsent） 实验2：卵发育阶段14的分析（toxin absent vs toxin present） 此类调整的详细说明已发表于研究论文及附带的README文件中。若需复现本研究在上述特殊案例中的分析过程，其他研究者需进行相同的调整。 另外请注意，数据表"Expt 2 Toad Egg-Hatchling Data"同时包含“被取食/未被取食的卵数量”与“被取食/未被取食的幼体数量”两类数据。因此，在该数据集内，当卵尚处于发育阶段尚未孵化时，TotalNSurvivingAtHatching、HatchlingsEaten与HatchlingsNotEaten三列均无意义，因为此时尚未有幼体产生（即无幼体相关数据）。此类情况下，上述三列单元格均填充为"n/a"（Not Applicable，不适用）。