Tadpole transport logistics in a Neotropical poison frog: indications for strategic planning and adaptive plasticity in anuran parental care

Abstract

IntroductionIndividuals should aim to adjust their parental behaviours in order to maximize the success of their offspring but minimize associated costs. Plasticity in parental care is well documented from various bird, mammal and fish species, whereas amphibians were traditionally assumed as being highly instinct-bound. Therefore, little is known about ‘higher’ cognitive abilities of amphibians, such as strategic planning and behavioural flexibility. Dendrobatid frogs have evolved a remarkable diversity of parental behaviours. The most noticeable of these behaviours is tadpole transport, which is obligatory in almost all species. Nonetheless, there is limited knowledge about spatial and temporal patterns of tadpole transport and the possible existence of behavioural plasticity on the individual level. In this study, we investigated correlates of tadpole transport behaviour in a natural population of the dendrobatid frog Allobates femoralis during five years.ResultsTadpole transport was predominantly observed during morning hours. Although tadpoles were carried almost exclusively by males (N = 119), we also observed ten females performing this task. The parentage analysis revealed that in all cases females transported their own offspring. In contrast, four tadpole-carrying males were not the genetic fathers of the larvae they were transporting. The average clutch size of 20 eggs and our observation of an average of 8 tadpoles on the back of transporting individuals indicate that frogs do not carry entire clutches at once, and/or that they distribute their larvae across several water bodies. Contrary to the predictions from a hypothetical random search for deposition sites, the number of transported tadpoles was higher in males that travelled over longer distances.ConclusionsOur results suggest a strong selective pressure on males to shift the time invested in tadpole transport to periods of low intra-specific competition. The number of tadpoles on the back of the males significantly correlated with displacement distance from the respective home territories, indicating a strategic non-random tadpole transport rather than random search for suitable tadpole deposition sites during tadpole transport. The observation of females who occasionally transported larvae supports the prevalence of adaptive plasticity in parental behaviours even in a species with a rather low level of parental care.

Adopt, ignore, or kill? Male poison frogs adjust parental decisions according to their territorial status

“…In A. femoralis the likelihood for males to encounter foreign clutches inside their own, established territory can be considered rather low as territories are vigorously defended physically against male intruders41. This notion is further supported by a previous study which reported only four (3%) out of 119 tadpole transporting males carrying unrelated tadpoles (in three cases the tadpoles of neighbouring individuals) on their back45. By following the simple decision rule ‘transport all clutches inside and eat all clutches outside my territory’, male A. femoralis reduce both the risk of accidentally rejecting own offspring at the time a territory has been established as well as the risk of misdirected care at locations where the likelihood of paternity is low.…”

The peculiar breeding biology of the Amazonian frog Allobates subfolionidificans (Aromobatidae)

“…These characteristics are shared with many other Allobates species with exotrophic tadpoles including A. femoralis, the best-studied congeneric species regarding parental care (e.g., Ringler et al 2013Ringler et al , 2015. Male A. subfolionidificans visited egg clutches regularly, probably to hydrate them, and took concomitant care of more than one clutch.…”

“…In addition, in species such as Allobates masniger (Morales 2002) and Allobates nidicola (Caldwell and Lima 2003) eggs hatch into endotrophic tadpoles that complete development in a terrestrial nest. Reproductive modes found in Allobates comprise many behavioral particularities that include 1) the use of a large repertory of visual, acoustic and tactile signals during long interactions for courtship and mating such as in A. caeruleodactylus (Lima et al 2002) and A. femoralis (Boulenger 1884) (Montanarin et al 2011), 2) the use of different oviposition sites such as foam nests constructed by leptodactylids in A. sumtuosus Morales 2002 (Kok and Ernst 2007), fallen leaves on the forest floor by A. marchesianus (Melin 1941) (Lima and Keller 2003) and bromeliads by A. bromelicola (Test 1956), as well as 3) intersexual flexibility in parental care as observed in Allobates femoralis (e.g., Ringler et al 2013Ringler et al , 2015. Many aspects of these behaviors are completely unknown for most species of dendrobatoid (Dendrobatidae + Aromobatidae) frogs, especially due to the high rate of species descriptions within the genus.…”

Factors influencing tadpole deposition site choice in a frog with male parental care: An experimental field study

“…In other taxa with larval transport, larval survivorship is high and parents sometimes carry entire clutches and distribute their offspring in different pools when available, but also travel long distances if suitable sites are rare (Ringler, Pasukonis, Hödl, & Ringler, 2013). Thus, we cannot explain the low number of tadpoles per deposition in L. palavanensis without further studies in offspring survival and larval transport logistics.…”