Brood-partitioning behaviour in unpredictable environments: hedging the bets?

Abstract

Spreading reproduction across time or space can optimize fitness by minimizing the risks for offspring survival in varying and unpredictable environments. Poison frogs (Dendrobatidae) are characterized by complex spatial and reproductive behaviour, such as territoriality, prolonged courtship and parental care. The partitioning of larvae from terrestrial clutches across several water bodies is mainly known from species with carnivorous tadpoles that allocate their tadpoles in very small pools, where limited food availability is accompanied by an increased risk of cannibalism. However, little is known about the deposition behaviour of non-carnivorous species that use medium-sized to large pools. In the present study, we investigated whether the Neotropical poison frog Allobates femoralis exhibits brood-partitioning behaviour when males transport tadpoles 3 weeks after oviposition. We sampled 30 artificial water bodies for tadpoles, which we genotyped at seven highly polymorphic microsatellite loci. Based on the reconstructed pedigree, we show that A. femoralis males distribute larvae of single and of successive clutches across several water bodies. The number of pools used was significantly associated with the number of clutches per male. Ninety-three percent of the males that were assigned to more than one clutch spread their tadpoles across several water bodies. Given the highly variable and unpredictable biotic and abiotic conditions in tropical rainforest, at the spatial scale of the study species’ behaviour, we interpret this behaviour as bet-hedging to improve offspring survival.

Hierarchical decision‐making balances current and future reproductive success

“…Drop‐off likelihood significantly decreased in the presence of predators, suggesting that adult males do actively avoid pools that contain dragonfly larvae, corroborating the findings of Erich et al. (), that also identified a negative relationship between dragonfly larvae and number of tadpoles inside pools. Theoretically, such a negative relationship could also result from a high predation rate on deposited tadpoles rather than from males choosing not to deposit within pools that contain dragonfly larvae.…”

“…Ringler et al., ). As males were previously shown to also disperse their clutches (even within a single clutch) across multiple water bodies (Erich et al., ), we included clutch identity in our analyses to account for temporal and spatial autocorrelation of these data points. In previous studies, it was further shown that occasionally female A. femoralis will perform the tadpole transport in those cases where the respective fathers go missing during the period of clutch development (Ringler et al., ; Ringler, Pašukonis, et al., ; Ringler, Hödl, et al., ).…”

“…Tadpoles are deposited in a variety of medium‐sized terrestrial water bodies, such as floodplains, water‐filled depressions, palm fronds and holes in fallen trees. Males have been observed to distribute tadpoles across several water bodies, which likely acts as a bet‐hedging strategy against total offspring loss (Erich, Ringler, Hödl, & Ringler, ), and do not provide any further care after tadpole deposition. Recent studies have shown that suitable water sites for tadpole deposition seem to be a limiting resource in A. femoralis (Ringler, Hödl, et al., ) and that spatial memory plays an important role in the reproductive behaviour of this species (Beck et al., ; Pašukonis, Warrington, Ringler, & Hödl, ; Pašukonis et al., ).…”

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

“…Several studies in poison frogs have shown that adults avoid depositing tadpoles in pools with predators (conspecific and heterospecific), competitors, and cannibalistic tadpoles (Brown et al, 2008;Summers, 1999;Summers & Symula, 2001). Nonetheless, clutch-partitioning behavior observed here may be advantageous if males maximize their fitness by depositing small numbers of tadpoles in different deposition sites, thereby minimizing risks associated with particular pools or "hedging" bets across variation in biotic and abiotic pool characteristics (Erich, Ringler, Hödl, & Ringler, 2015). However, in our study, males of L. palavanensis did not avoid pools with conspecific tadpoles or predatory dragonfly larvae and often split their clutches between the two available artificial pools.…”

“…As such, whether males split clutches may depend on pool availability and awareness of the location of neighboring pools. Nonetheless, clutch-partitioning behavior observed here may be advantageous if males maximize their fitness by depositing small numbers of tadpoles in different deposition sites, thereby minimizing risks associated with particular pools or "hedging" bets across variation in biotic and abiotic pool characteristics (Erich, Ringler, Hödl, & Ringler, 2015).…”