Bálint Üveges: Toad poison is a Swiss army knife against multiple enemies

In this post Bàlint Uvëges, postdoc at Bangor University, present his latest work ‘Chemical defence effective against multiple enemies: Does the response to conspecifics alleviate the response to predators?’, discuss the multiple ways animals have to avoid predation and shares his passion for venomous creatures.

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About the paper

Bálint Üveges
Bálint Üveges

Predation is commonplace in nature, so prey animals need to continuously survey their environment and respond to the presence of predators and predation attempts. Two example strategies to avoid being eaten are: preparing for an attack by altering ones phenotype, and forming groups. The former means that prey sense the presence of predators (or any other adverse environmental factor) in their surroundings, which triggers changes in their behaviour, physiology, life-history or even morphology. This is commonly known as phenotypic plasticity and is a near-ubiquitous trait in organisms. Forming groups is another effective way to decrease the chance of being a meal because living in a group decreases the per capita chance of predation simply by a dilution effect, by allowing for a more effective monitoring of the environment (increased vigilance) or by confusing predators. Since living in a group in itself decreases predation chance on group members and altering phenotype is usually costly, individuals tend to respond less intensely to predator cues as the size of the group increases.

However, group living also comes with its own unique challenges, including the easier and faster spread of pathogens (e.g. think COVID-19), increased competition for food or other resources (e.g. toilet paper, hand sanitizer), and cannibalism (fortunately we’re not there yet). Combating these negative consequences of group living can weaken anti-predatory responses by energetic trade-offs and also because phenotypes providing fitness benefits against competitors or diseases are often disadvantageous against predators. But what if organisms have a single multi-tool which is effective against various foes? Chemical defence, i.e. the use of repellent and toxic compounds against enemies, may be such a multifunctional trait, but how the intensity of toxin production changes with increasing group size in response to the presence of predators has not been investigated in animals so far. We hypothesised that, contrary to phenotypes which are beneficial against one, but disadvantageous against another environmental factor (Panel A in Fig 1), both predator presence and increasing group size would induce the synthesis of toxins. At least until it reaches a point where a further increase in toxin production is either not necessary, because it would not provide any additional fitness benefits, or not possible due to physiological limits (Panel B in Fig 1).                 

Both defensive traits (A, B) provide anti-predatory protection, and their expression level increases with increasing predation risk. However, ‘A’ represents an anti-predatory defence that is disadvantageous in competition whereas ‘B’ is effective against both predators and conspecifics (B).
Both defensive traits (A, B) provide anti-predatory protection, and their expression level increases with increasing predation risk. However, ‘A’ represents an anti-predatory defence that is disadvantageous in competition whereas ‘B’ is effective against both predators and conspecifics (B).

To test this hypothesis, we reared tadpoles of the common toad (Bufo bufo, Fig 2-3) in outdoor mesocosms (Fig 4). Toad tadpoles synthesise toxins called bufadienolides from early life stages. These compounds are cardiotoxic steroids, which are distasteful, poisonous or even deadly to certain predators, but they also have anti-bacterial, anti-fungal (including against the amphibian chytrid fungus, Batrachochytrium dendrobatidis) and anti-parasitic properties. Furthermore, common toad tadpoles also form huge groups (Fig 2) in ponds which make them ideal model organisms for this study. Mesocosms are self-sustaining semi-natural aquaria containing tree leaves to provide shelter, naturally occurring phytoplankton and bacteria to provide food, as well as zooplankton. During our study we exposed toad tadpoles in each mesocosm to one of six treatment combinations: they were reared either in groups of 6, 12 or 24 and received either no predator cues or water from tadpole-fed European perch regularly. After two weeks, we preserved 6 tadpoles from each mesocosm for the upcoming chemical analysis. We found that tadpoles produced more toxins with increasing group size and also when fish cues were present (at least at lower densities). This means that toad tadpoles respond to the presence of other toad tadpoles and predators similarly, which confirmed our hypothesis.

About the research

Mesocosms in the experiment.
Mesocosms in the experiment.

I believe, our study is the first to show that conspecific density and predation can simultaneously and similarly induce toxin synthesis in animals. This means that toad poison may function as a multi-purpose tool, similar to a Swiss army knife, by providing fitness benefits both when encountering predators and when facing facilitated spread of pathogens as a consequence of living in a large group. However, functional studies, i.e. investigating the survival and condition of tadpoles in the actual presence of predators and pathogenes across different densities would be needed to test this. In addition, we only studied common toads in this regard, but it would be beneficial to include other species that use chemical defence, to see how widespread the patterns observed in our study are.

Our results may even have implications for conservation biology. There are currently two toad species which were introduced far away from their native range and wreak havoc on the predator fauna in their new-found home: the cane toad (Rhinella marina) intentionally introduced in Australia to control populations of the sugarcane beetle in the 1930’s and the Asian common toad (Duttaphrynus melanostictus) which was most probably accidentally introduced to Madagascar just recently. Both animals can be quite large, with a lot of toxin reserves to which the native predators do not possess evolutionary adaptations, because before the introductions no native toad species existed at either of these sites for at least millions of years (if ever). This means that Malagasy and Australian predators are generally more vulnerable to toad poison than predators in the native range of these amphibians. If the results of our study are also applicable to these species, then removal of their tadpoles would benefit the native fauna not only by decreasing the number of poisonous toads, but also by decreasing their toxin content (due to lower conspecific density). This latter could help native predators adapting to these toxic invaders, because predators that eat a toad with lesser amount of toxins have a better chance to survive the encounter and learn to avoid this prey in the future.    

About The Author

I‘ve been fascinated with nature since my childhood, so pursuing a career in ecology was a no-brainer. During my first year at the university I became interested in amphibians and reptiles, especially the poisonous/venomous kinds. During my PhD I investigated phenotypic plasticity of chemical defences in animals. Like in the study detailed above, I spent most of my time raising common toad tadpoles and exposing them to environmental cues and measured their toxin content to see how they responded to these stressors. Recently, however, I turned my attention to venomous snakes. I am currently a post-doctoral researcher at Bangor University in the UK, where I investigate how diet and self-defence drive the evolution of snake venoms. I enjoy many aspects of being an ecologist, including the diverse and creative nature of the work and being in the field. In my spare time I like to hike, read fantasy novels, play rugby and pen and paper role-playing games.     

Read the article in full here.

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