Competition induces increased toxin production in toad larvae without allelopathic effects on heterospecific tadpoles

Abstract

Inducible defences are a form of phenotypic plasticity by which organisms respond to and mitigate the threat posed by predators, parasites and competitors. While anti‐predatory defences are often in trade‐off with anti‐competitor responses, chemicals that deter predators may have negative effects on competitors as well. Allelopathy is well known in plants and plant‐like animals, but whether the toxins of mobile, behaviourally and morphologically complex animals are induced by and exert allelopathic effects on competitors is poorly known. Common toads Bufo bufo synthesize bufadienolides which make them unpalatable or toxic to many predators. However, bufadienolide content of toad tadpoles correlates positively with the density of competitors in natural populations, suggesting that they may upregulate their toxin production to inhibit their competitors, such as heterospecific tadpoles that may be vulnerable to toad toxins. We conducted a microcosm experiment with tadpoles of common toads and agile frogs Rana dalmatina, in which we manipulated the density of conspecific and heterospecific competitors. We measured the bufadienolide content of toad tadpoles to test for competitor‐induced changes in toxin production, and we assessed the growth and development of agile frog tadpoles to test for allelopathy. We found that toad tadpoles contained higher amounts of bufadienolides at higher densities; however, heterospecific competitors did not have a stronger effect than conspecifics. Furthermore, the presence or density of toad tadpoles had no effect on the body mass and development rate of agile frog tadpoles. Our results demonstrate competitor‐induced plasticity in toxin production, but we found no support for an allelopathic function of bufadienolides. Instead, we suggest that inducible changes in bufadienolide production may serve to mitigate risks posed by competitors, including aggression, cannibalism or disease. Therefore, bufadienolides are intriguing candidates for multi‐purpose defences that may provide protection not only against predators but also against competitors. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.12994/suppinfo is available for this article.

Chemical defense of toad tadpoles under risk by four predator species

“…However, previous results reject this explanation by demonstrating plastic adjustment of larval bufadienolide production in response to a variety of environmental factors, such as restricted food levels (Üveges et al, 2017), a herbicide , and competitors (Bókony et al, 2018). Thus, it seems that toad tadpoles are TA B L E 3 Effects of treatment, predator size, and the number of common frog tadpoles eaten on survival of toad tadpoles in the predation trials Note.…”

“…A recent study showed that increased conspecific density can induce elevated bufadienolide synthesis in toad tadpoles (Bókony et al, 2018). A recent study showed that increased conspecific density can induce elevated bufadienolide synthesis in toad tadpoles (Bókony et al, 2018).…”

“…Second, tadpoles raised in the presence of dragonfly larvae enjoyed an enhanced survival probability as compared to their predator-naïve sibs. The lack of increasing toxin content is also unlikely to be an artifact of an insensitivity of our chemical analytical framework, since the same build has proven to be effective in providing evidence for inducible bufadienolide synthesis in the same study species in the past (Bókony et al, , 2018Üveges et al, 2017). These treatment effects together suggest that tadpoles did perceive the presence of predators during their development and were able to respond to them phenotypically; therefore, the lack of responses in chemical defenses was not due to an inability of tadpoles to sense olfactory cues on predation risk.…”

“…This approach yields approximate estimates of bufadienolide quantities and has been used in similar studies (Benard & Fordyce, 2003;Bókony et al, 2016Bókony et al, , 2018Hagman et al, 2009;Üveges et al, 2017). When determining NBC for each animal, we considered a compound to be present when its signal to noise ratio was at least 3 in the HPLC-MS chromatogram.…”

“…However, these former experiments provided inconclusive results. Furthermore, bufadienolide content of common toad (Bufo bufo; Figure 1) tadpoles was not affected by predator cues (Üveges et al, 2017), even though plasticity in toxin production has been documented in the same study system in response to several other environmental stressors (Bókony et al, , 2018Üveges et al, 2017). Furthermore, bufadienolide content of common toad (Bufo bufo; Figure 1) tadpoles was not affected by predator cues (Üveges et al, 2017), even though plasticity in toxin production has been documented in the same study system in response to several other environmental stressors (Bókony et al, , 2018Üveges et al, 2017).…”