Toxin depletion has no effect on antipredator responses in common toad (<i>Bufo bufo</i>) tadpoles

Kurali, Anikó; Pásztor, Katalin; Hettyey, Attila; Tóth, Zoltán

doi:10.1111/bij.12864

Cited by 10 publications

(11 citation statements)

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“…This result, combined with the fact that toxin content was not related to body mass, corroborates our earlier finding that the energetic costs of toxin production in toad larvae may be low [71]. It seems contradictory that an inducible defence may be cheap to produce, but detecting associated costs of expressed plastic traits may be problematic in species with a complex life-history, such as anurans, because costs may not appear synchronously with the displayed trait [74–77].…”

Section: Discussionsupporting

confidence: 91%

Age- and environment-dependent changes in chemical defences of larval and post-metamorphic toads

et al. 2017

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BackgroundChemical defences are widespread in animals, but how their production is adjusted to ecological conditions is poorly known. Optimal defence theory predicts that inducible defences are favoured over constitutive defences when toxin production is costly and the need for it varies across environments. However, if some environmental changes occur predictably (e.g. coupled to transitions during ontogeny), whereas others are unpredictable (e.g. predation, food availability), changes in defences may have constitutive as well as plastic elements. To investigate this phenomenon, we raised common toad (Bufo bufo) tadpoles with ad libitum or limited food and in the presence or absence of chemical cues on predation risk, and measured their toxin content on 5 occasions during early ontogeny.ResultsThe number of compounds showed limited variation with age in tadpoles and was unaffected by food limitation and predator cues. The total amount of bufadienolides first increased and later decreased during development, and it was elevated in young and mid-aged tadpoles with limited food availability compared to their ad libitum fed conspecifics, whereas it did not change in response to cues on predation risk. We provide the first evidence for the active synthesis of defensive toxin compounds this early during ontogeny in amphibians. Furthermore, the observation of increased quantities of bufadienolides in food-restricted tadpoles is the first experimental demonstration of resource-dependent induction of elevated de novo toxin production, suggesting a role for bufadienolides in allelopathy.ConclusionsOur study shows that the evolution of phenotypic plasticity in chemical defences may depend on the ecological context (i.e. predation vs. competition). Our results furthermore suggest that the age-dependent changes in the diversity of toxin compounds in developing toads may be fixed (i.e., constitutive), timed for the developmental stages in which they are most reliant on their chemical arsenal, whereas inducible plasticity may prevail in the amount of synthesized compounds.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-017-0956-5) contains supplementary material, which is available to authorized users.

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Section: Discussionsupporting

confidence: 91%

Age- and environment-dependent changes in chemical defences of larval and post-metamorphic toads

et al. 2017

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“…In both of our experiments, tadpoles reared in more competitive environments attained smaller body mass, but in spite of this inhibited growth, their total bufadienolide levels were at least as high or even higher compared to tadpoles reared in less competitive environments (Üveges et al., ; figure e,f in the present study). This suggests that competing tadpoles invested their resources into toxin production at the expense of growth; or alternatively, they may have been able to maintain or even increase their bufadienolide levels despite food limitation because the costs of bufadienolide synthesis may be low in terms of dietary resources (Kurali, Pásztor, Hettyey, & Tóth, ; Üveges et al., ). It is possible, however, that induced bufadienolide synthesis is traded off against long‐term investment into critical life‐history traits, as suggested by earlier studies (Benard & Fordyce, ; Hagman et al., ).…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2017

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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.

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“…Recent studies investigating various aspects of B. bufo tadpoles’ bufadienolide production have also revealed that individuals can respond plastically in the amount of produced bufadienolides to the perceived intensity of competition (Bókony et al 2018 ) and to the presence of a glyphosate-based herbicide (Bókony et al 2017 ). Moreover, experimentally induced toxin release was found not to be associated with high costs measured in several fitness-related traits (Kurali et al 2016 ).…”

Section: Methodsmentioning

confidence: 99%

“…To induce the depletion of bufadienolide stores in the tadpoles’ skin, we applied in vivo stimulation via hormonal treatment (administration of norepinephrine). Tadpoles in the norepinephrine treatment group were placed into a 3-ml, 100-μM norepinephrine-bitartrate (CAS 3414-63-9, Sigma-Aldrich, USA) solution for 15 min (Kurali et al 2016 ; Maag et al 2012 ). To facilitate the washing of norepinephrine and any toxins that had been released from the skin, we subsequently transferred individuals into a box filled with 700 ml RSW for one minute and finally placed them back into their rearing containers.…”

Section: Methodsmentioning

confidence: 99%

“…Norepinephrine has been successfully applied in previous studies to induce toxin release from skin glands in tadpoles of several species (e.g. Calhoun et al 2016 ), including the common toad (Kurali et al 2016 ). We predicted that immersion into norepinephrine solution would lead to a decrease in the amount of bufadienolides in tadpoles’ toxin reserves due to enforced excretion, but expected bufadienolide reserves to become similar to that of untreated individuals within five days.…”

Section: Introductionmentioning

confidence: 99%

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Changes in Toxin Quantities Following Experimental Manipulation of Toxin Reserves in Bufo bufo Tadpoles

et al. 2019

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Possessing toxins can contribute to an efficient defence against various threats in nature. However, we generally know little about the energy- and time-demands of developing toxicity in animals, which determines the efficiency of chemical defence and its trade-off with other risk-induced phenotypic responses. In this study we examined how immersion into norepinephrine solution inducing the release of stored toxins, administration of mild stress mimicking predator attack or simple handling during experimental procedure affected the quantity and number of toxin compounds present in common toad ( Bufo bufo ) tadpoles as compared to undisturbed control individuals, and investigated how fast toxin reserves were restored. We found that total bufadienolide quantity (TBQ) significantly decreased only in the norepinephrine treatment group immediately after treatment compared to the control, but this difference disappeared after 12 h; there were no consistent differences in TBQ between treatments at later samplings. Interestingly, in the norepinephrine treatment approximately half of the compounds characterized by >700 m/z values showed the same changes in time as TBQ, but several bufadienolides characterized by <600 m/z values showed the opposite pattern: they were present in higher quantities immediately after treatment. The number of bufadienolide compounds was not affected by any treatments, but was positively related to TBQ. Our study represents the first experimental evidence that toxin quantities returned to the original level following induced toxin release within a very short period of time in common toad tadpoles and provide additional insights into the physiological background of chemical defence in this model vertebrate species. Electronic supplementary material The online version of this article (10.1007/s10886-019-01045-9) contains supplementary material, which is available to authorized users.

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Toxin depletion has no effect on antipredator responses in common toad (Bufo bufo) tadpoles

Cited by 10 publications

References 93 publications

Age- and environment-dependent changes in chemical defences of larval and post-metamorphic toads

Age- and environment-dependent changes in chemical defences of larval and post-metamorphic toads

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

Changes in Toxin Quantities Following Experimental Manipulation of Toxin Reserves in Bufo bufo Tadpoles

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