For those of you that know me personally you’ll understand how I’ve always had a fascination with Herpetology, so when perusing the literature I couldn’t help but read the newly published study by Ringler et al. (2017). The paper broadens our ever-changing understanding of parental care in animals specifically the roles of complex behaviours such as infanticide and the care of non-related offspring. These behaviours are well documented in so called ‘higher’ vertebrates such as birds and mammals but until now nobody has taken a dive into the world of amphibians when evaluating these traits.
Infanticide is the intentional killing of infants often those that are related to the killer. This process is often deemed to be a sexually selected for trait and as a way of males to gain increased access to female mating partners. However males that have this cannibalistic streak must take great care in avoiding their own offspring in the process. Ringler et al. (2017), shows that male brilliant-thighed poison frogs Allobates femoralis (Dendrobatidae, Aromobatinae) adjust their parental responses for care and infanticide towards unrelated clutches based upon their territorial statuses. Males were immediately switching to cannibalism upon relocation. Could this mean care and cannibalism are antagonistically linked? Glad I’m not a frog to be honest!
So what even is an Allobates femoralis?
Well it’s a small colourful frog from the Dendrobatidae family that includes a number of toxic frogs originating in South America. Parental care by one or both sexes is considered a synapomorphy of this entire family. Allobates femoralis males are highly territorial despite only being the size of a two pence piece. Males advertise via calls to make females aware of their territory and to ward off other potential intruders, who are physically attacked by the territory holder (Narins et al., 2003). In what can only be described as miniature wrestling matches that can last up to 15 minutes. Females however are highly promiscuous moving between male territories and providing no parental care, merely just their eggs to be fertilised in ephemeral pools.
After three weeks of development the male will transport newly hatched tadpoles on his back to water bodies often outside his territory. Some males have been recorded to travel up to 100m, which is approximately 5000 times the length of their bodies! Quite a feat while carrying your offspring on your back (Pašukonis et al., 2014). Courtship, mating, and terrestrial oviposition take place in the leaf litter inside the male’s territory. It is therefore a prerequisite for male reproductive success. This explains the strong competition for territory but not the need for infanticide.
So what did the study entail?
The study is based on manipulation of territorial status of males to induce ‘takeover’ behaviour and ‘resident’ behaviour. These experiments took place ex- situ in a lab-based study using a total of 20 males that were known to have sired offspring. Takeover males (N=10) were transferred from their home terraria into novel empty terraria. Resident males (N=10) were then captured and returned to their home terraria after the same handling procedure given to the takeover group. This helped to eliminate any effects of being handled. In both trials unrelated clutches of developing conspecifics were places in the terraria before the males were released (Fig 1). All trials were then filmed and the occurrence and frequency of cannibalism along with tadpole transport to pools was recorded.
What did they find out?
Well it appeared that significantly more takeover males than residents were cannibalistic to unrelated clutches. In fact all 10 males that took new territory consumed the developing embryos of unrelated conspecifics compared with only 2 resident males (Fig 2A). Takeover males also fed more often and consumed more tadpoles (Fig 2B + 2C). Resident males however transported more tadpoles to water bodies with 8 out of 10 males transporting tadpoles compared to only 2 takeover males (Fig 2A). All these results point to a common trend that there are strongly differing parental decisions linked directly to an individual’s territory status.
It seems that A. femoralis territory holders follow a very simple decision-making rule ‘care for any clutch inside my territory’, but ‘cannibalism’ is the way to go when taking over a new territory. This suggests that this context-dependent behavioural switch between infanticide and parental care is likely to be adaptive. It effectively allocates parental effort while minimising the risk for parental errors at a very low cognitive cost. To put it very simply the frog thinks ‘why not eat your neighbours babies because it’s too much effort to look after them and your own at the same time’. Plus it’s a good source of nutrients compared to eating insects all day.
It can also act as an antagonistic backup strategy as it is difficult for a frog to tell if the embryos are his or not and can only decide through memory. This is supported by similar behaviour in a species of harvestman and recently also for the plainfin midshipman fish which cannibalises foreign eggs after nest takeover (Bose et al., 2014) In A. femoralis the likelihood for males to encounter foreign clutches naturally inside their own territory is very uncommon due to their defensive nature. It is therefore logical for resident males to take care of all offspring in their patch.
These findings demonstrate that parental decision-making incorporating an adaptable shift between care and infanticide to avoid misdirected care can evolve in the absence of group living. This behaviour can also clearly evolve in species with comparatively simple brain organisations.
But how is this beneficial for Science?
Ringler et al.’s (2017) results should now prompt a reconsideration of evolutionary and causal aspects of parental decision making, as we currently understand it. The study is suggesting that selective infanticide of unrelated young may generally become adaptive when the risks and costs of misdirected care are high. This seems very reasonable in my eyes and further consideration should be taken to address these predictions. This could be achieved by further assessments between diverse animal taxa, with different social structures and parental systems. It would help us further understand how different parental strategies are promoted and maintained over evolutionary time.
Coupled with recent research on mice it has emphasised that feeding and parental behaviours might be regulated antagonistically via a common physiological pathway (O’Rourke and Renn, 2015). This fascinating paper has sparked many ideas into investigating the links between neuronal and hormonal activity in territoriality, mating, feeding, and parental care.
All of this because of one little frog! Sit back and think about that for a second!
By Joe Gilmour
Bose, A., Cogliati, K., Howe, H. and Balshine, S. (2014). Factors influencing cannibalism in the plainfin midshipman fish. Animal Behaviour, 96, pp.159-166.
Narins, P., Hodl, W. and Grabul, D. (2003). Bimodal signal requisite for agonistic behavior in a dart-poison frog, Epipedobates femoralis. Proceedings of the National Academy of Sciences, 100(2), pp.577-580.
O’Rourke, C. and Renn, S. (2015). Integrating adaptive trade-offs between parental care and feeding regulation. Current Opinion in Behavioral Sciences, 6, pp.160-167.
Pasukonis, A., Warrington, I., Ringler, M. and Hodl, W. (2014). Poison frogs rely on experience to find the way home in the rainforest. Biology Letters, 10(11), pp.20140642-20140642.
Ringler, E., Barbara Beck, K., Weinlein, S., Huber, L. and Ringler, M. (2017). Adopt, ignore, or kill? Male poison frogs adjust parental decisions according to their territorial status. Scientific Reports, 7, p.43544.