From embryos to larvae: seven‐month‐long paternal care by male Japanese giant salamander

Abstract

Parental care is remarkably diverse in its modes both within and across taxa. Within amphibians, various pre‐ and post‐hatching care behaviours have been described in frogs. In contrast, the current knowledge about salamander parental care is largely limited to pre‐hatching attendance by females. In particular, post‐hatching parental care by male salamanders have never been described and analysed in detail. A recent study revealed various modes of pre‐hatching care provided by male Japanese giant salamanders (Andrias japonicus). Their hatched larvae are known to stay in the nest with the father (i.e. den master) for several months before dispersal, which led to the hypothesis that den masters continue providing care for hatchlings. To test this hypothesis, we videotaped and analysed post‐hatching behaviours of two male A. japonicus that remained in the nests with hatchlings in situ. We also developed and tested several predictions regarding the post‐hatching care behaviours in comparison to the pre‐hatching behaviours. While one male abandoned the nest, the other male remained in the nest and provided care until the larvae dispersed in the following spring. The comparative analyses on three parental care behaviours (tail fanning, agitating/checking and hygienic filial cannibalism) between pre‐ and post‐hatching care suggest their flexible and condition‐dependent nature. Furthermore, the comparison in larval mortality and potential predators between the attended and abandoned nest revealed the crucial role of a den master in improving offspring survivorship. Our observations also disclosed the possibility of leech infection posing a serious threat to larval giant salamanders. The life‐history traits associated with the evolution of such prolonged post‐hatching paternal care in salamanders are fully aquatic life cycle, external fertilization and stream habitat. The rare combination of these traits is unique to the family Cryptobranchidae which consists of the three imperiled and secretive giant salamanders.

Developments in Amphibian Parental Care Research: History, Present Advances, and Future Perspectives

“…Although historical anecdotes described egg fanning and defense, recent field observations and video monitoring have revealed an extended period of pre-and posthatching parental care in the Japanese giant salamander, Andrias japonicus (Okada et al 2015;Takahashi et al 2017). Large males (''den-masters'') occupy nesting burrows along stream banks, performing tail fanning, agitation, filial hygienic cannibalism, and active predator defense (Okada et al 2015), both before hatching (1-2 mo) and with juveniles (up to 5 mo; Takahashi et al 2017). Unfortunately, small sample sizes (n ¼ 2) impede inferences about the causes, correlates, and function(s) of these behaviors.…”

Preoviposition paternal care in a fully aquatic giant salamander: nest cleaning by a den master

“…() and Takahashi et al . () found that male A. japonicus den masters exhibit hygienic filial cannibalism for their embryos and newly hatched larvae; den masters consume eggs and larvae showing signs of maldevelopment, death or water mould infection, which would likely prevent water mould infection from spreading to healthy offspring. Nest cleaning in the form of vigorously stirring the sand throughout the preoviposition period likely reduces the amount of organic matter in the den, such as leaves, twigs, carcasses of small aquatic creatures and waste, which provide food sources for water moulds (Padgett & Heitman, ; Czeczuga, Kozłowska & Godlewska, ; Czeczuga, Godlewska & Kozlowska, ; Czeczuga & Mazalska, ).…”

“…() and Takahashi et al . () recently detailed prolonged and complex postoviposition parental care by male A. japonicus . The present study extended the current knowledge by revealing behavioural convergence in parental care between the fish and the fully aquatic giant salamanders not only in postoviposition but also in preoviposition care by males in the form of nest cleaning.…”

“…Among the 10 extant salamander families, the members of the three families, Cryptobranchidae, Hynobiidae and Sirenidae, perform external fertilization (Reinhard, Voitel & Kupfer, ). Two of these families, Cryptobranchidae and Sirenidae, consist of fully aquatic salamanders, and rare cases of parental care by male salamanders have recently been reported from these families (Reinhard et al ., ; Okada, Fukuda & Takahashi, ; Takahashi, Okada & Fukuda, ). Among cryptobranchid salamanders, Okada et al .…”

“…() and Takahashi et al . () revealed prolonged and complex care behaviours provided for both embryos and hatchlings by male Japanese giant salamanders ( Andrias japonicus ). In contrast, paternal care in the family Sirenidae is relatively simple and short (Reinhard et al ., ).…”