When I saw my first poison frog in the amazing surroundings of the Bocas del Toro archipelago in Panama, I knew that the course of my life was forever changed. Enchanted by their bright colors and astonished by their small body size, this epiphany entirely altered my perception of frog behavior and ecology.
Poison frogs (Dendrobatidae) belong to a neotropical frog family of some 300 different species that differ vastly from the stereotypical frog. They are active throughout the day, exhibit strong territoriality, and lay their clutches on land. Many of them are brightly coloued, which indicates high levels of toxicity to potential predators. The dilemma of terrestrial clutches that will develop into aquatic tadpoles –- able to breath in water only through gills -– has been “solved” in these frogs via parental behaviours. Adult frogs take their hatched tadpoles piggy-back across the rainforest to water bodies, and sometimes they have to cross quite large distances to accomplish this duty.
Why to not study poison in poison frogs
Initially, poison frogs started to attract the attention of both scientists and hobbyists due to the highly conspicuous appearance and associated high toxicity of several species within this group. Even a common name of this frog family, “poison dart frogs”, is derived from the practice of some native tribes that rubbed the secretions of highly toxic species onto their hunting weapons.
However, neither all dendrobatid frogs feature high levels of toxicity, nor is this a commonly shared feature of the entire family. It is rather the case that all species of poison frogs are characterized by complex social and reproductive behaviour, involving territoriality, mate choice, prolonged courtship, and parental care –- and these amazing social behaviours are also what attracted me to become a scientist in the field of behavioural ecology.
I conducted most of my research on the dendrobatid frog Allobates femoralis, which is non-toxic with a rather cryptic coloration, but has proven to be an optimal model for studying mating and parental behaviour. During the breeding season, males are highly territorial and broadcast territory occupancy with a prominent advertisement call that is aimed at both attracting nearby females and also warning male competitors not to come closer. Females decide when and with whom they want to mate. They approach calling males and thereby initiate a very extended and complex courtship behaviour.
Observing an entire courtship in the field can be quite challenging, as the full sequence can last several hours, and even be interrupted overnight before prolonged resumption the next morning. However, if you are lucky to detect and follow a breeding pair, you will be rewarded with close views of the stunning reproductive behaviour of these rainforest frogs.
During courtship, the male guides the female across his territory and presents her with various possible egg deposition spots in the leaf litter –- a process that can take many hours! After a clutch has been deposited, the female leaves the male’s territory and goes back to her resting site outside the male’s territory. The male remains in his territory and will transport the clutch to widely distributed water bodies as soon as tadpoles hatch about three weeks later.
The island of frogs
In 2012, my husband Max Ringler and I established an experimental population of A. femoralis on a river island by the controlled introduction of 1,800 morphologically measured and genetically sampled tadpoles. Surprisingly, although A. femoralis populations exist on both sides of the river surrounding the island, the species was not present on the small river island itself. This lucky coincidence allowed us to establish this experimental frog population within the species’ natural habitat. The possibility to study these frogs in a naturally isolated habitat within the rainforest allows us to address a wide array of research questions, ranging from animal cognition to population ecology and evolution.
A few weeks after the start of this colonization event, we witnessed the first tiny froglets emerging out of the water buckets we provided. Since then, a stable population of about 150 adult frogs per year has settled.
The controlled introduction of tadpoles further allowed us to evaluate the use of genetic fingerprinting for population studies in amphibians. Reliable tracking of individual amphibians throughout different lifecycle stages has been a long-standing problem in amphibian population research. Any conventional marking or tag is usually lost during the course of metamorphosis, the full reorganisation of the body from a tadpole to an adult frog. We could demonstrate that microsatellite markers are a highly powerful tool to track individual tadpoles throughout metamorphosis until adulthood, which should be of substantial value for future studies on amphibian population ecology and conservation.
The Frog Lab
In 2012 we also established a captive breeding colony, currently based at the University of Vienna. We started out with 30 adult frogs that immediately started to successfully reproduce. This completely controlled indoor setup allows us to tackle questions that cannot be easily addressed under natural conditions.
Dedicated fathers and attentive mothers
These little forest frogs are very thoughtful parents and exhibit behavioral flexibility across various contexts. Males of A. femoralis are responsible for guarding, hydrating and transporting the hatched tadpoles to suitable water bodies. When doing so, they distribute their clutches into several water bodies, to minimize the risk of total offspring loss if they accidentally choose a bad-quality pool.
Tadpole pick up and transport in the field. Video by Andrius Pašukonis.
Females in general do not engage in any brood care activities. Still, we occasionally discovered females with tadpoles on their backs. Genetic parentage analyses then confirmed that these females were indeed the biological mothers of these tadpoles.
This finding really captured my attention. Now I wanted to know more about the motivation of those females. Why did they take over their partners’ job?
To answer this question, we conducted a behavioral experiment in the Frog Lab: We allowed male and female frogs to produce a clutch and afterwards removed the male partner in half of the trials. What we found was really exciting: Females transported the tadpoles to water, but only in cases where the father had been removed. This was a very spectacular finding, since such compensatory behaviour was previously known mainly from species in which both males and females are generally involved in brood care.
Based on these findings, I was wondering if males and females are able to differentiate between their own and other individuals’ offspring. We therefore conducted a clutch exchange experiment, to see if individual frogs were willing to pick up and transport “foster” offspring. Surprisingly, males transported any clutch that we placed inside their territories. Females in turn showed highly spatial selectivity and picked up and transported only clutches, their own and unrelated ones, that were placed at locations where they themselves recently produced a clutch. This shows that males and females use quite different rules when it comes to clutch recognition and discrimination.
When one of my students tried to experimentally initiate female tadpole transport in the field by removing individual males from their territory, he made an exciting observation: a neighbouring male entered the territory of a removed male and fed on the “abandoned” clutch.
Via behavioural experiments in the laboratory we then could verify the underlying motivational pattern of this observation: Male frogs follow the simple rule “care for any clutch inside my territory”, but switch to cannibalism when taking over a new territory. This finding demonstrates that male poison frogs adjust their parental responses – care or cannibalism – towards unrelated clutches according to their territorial status.
Male cannibalism in the field. Video by Steffen Weinlein.
Together with my colleagues Andrius Pašukonis and Kristina Beck, we recently discovered that tadpole transport behaviour can also be experimentally induced in both males and females of A. femoralis, by simply transferring tadpoles to the backs of adult frogs.
The ability to experimentally induce tadpole transport behavior has the potential to be a highly powerful tool for future experiments, that shall investigate the role of chemical and visual cues for navigation, predator-avoidance behaviours, and spatial cognition in poison frogs.
But this is part of another exciting story … stay tuned!
Translocated tadpoles spontaneously induce parental behaviours in foster parents. Video by Andrius Pašukonis.
Ringler E, Mangione R, Ringler M (2014) Where have all the tadpoles gone? Individual genetic tracking of amphibian larvae until adulthood. Molecular Ecology Resources 15: 737-746. DOI: 10.1111/1755-0998.12345
Erich M, Ringler M, Hödl W, Ringler E (2015) Brood-partitioning behaviour in unpredictable environments: hedging the bets? Behavioural Ecology and Sociobiology 69: 1011-1017. DOI: 10.1007/s00265-015-1913-1
Ringler E, Pašukonis A, Fitch WT, Huber L, Hödl W, Ringler M (2015) Flexible compensation of lost uniparental care in a poison frog. Behavioral Ecology 26: 1219-1225. DOI: 10.1093/beheco/arv069
Ringler E, Pašukonis A, Ringler M, Huber L (2016) Sex-specific offspring discrimination reflects respective risks and costs of misdirected care in a poison frog. Animal Behaviour 114: 173-179. DOI http://dx.doi.org/10.1016/j.anbehav.2016.02.008
Ringler E, Beck KB, Weinlein S, Huber L, Ringler M. Adopt, ignore or kill? Parental decision making by male poison frogs. Scientific Reports 7: 43544. doi:10.1038/srep43544
Pašukonis A, Beck KB, Fischer M-T, Weinlein S, Stückler S, Ringler E (2017) Induced parental care in a poison frog: a tadpole cross-fostering experiment. Journal of Experimental Biology. 220: 3949-3954. doi: 10.1242/jeb.165126