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

Abstract

Parental care in salamanders is thought to be simple and typically limited to female egg attendance. No elaborate preoviposition parental care had been described from salamanders. Recent studies revealed complex care behaviours by male Japanese giant salamanders (Andrias japonicus), a fully aquatic, secretive species with external fertilization. These studies emphasize behavioural convergence in paternal care between some of the fish species and the giant salamanders. The fish examples further imply the possibility that males of A. japonicus provide preoviposition parental care in the form of nest cleaning and building. We tested this possibility and also predicted that cleaning effort by a male salamander, if exists, would increase as it approaches the spawning event. Prior to the breeding season, large males (i.e. den masters) of A. japonicus occupy and guard suitable burrows well-hidden along the stream bank. In the falls of 2012, 2013 and 2015, we videotaped and examined a single den master's pre-and postoviposition behaviours at Asa Zoological Park in Hiroshima, Japan. The den master repeatedly exhibited vigorous movements of front and hind limbs in a paddling motion at the bottom of the nest every day for the three separate years. The cleaning effort by the den master lineally increased as the spawning event approached, after which the den master completely ceased cleaning. With the cleaning behaviour, the den master made the den filled with debris including leaves and twigs buried in the sand. The floating debris was subsequently removed by the water current flowing through the nest. Water mould infection is a major cause of offspring mortality of aquatic amphibians including A. japonicus. By reducing the amount of organic matter that provides food sources for water mould, the nest cleaning likely reduces the risk of water mould infection among the offspring, serving as an important preoviposition parental care.

Freshwater megafauna shape ecosystems and facilitate restoration

“…When large semi‐aquatic megafauna, such as marsh deer ( Blastocerus dichotomus ) and southern lechwe ( Kobus leche ), feed in floodplains and wetlands, their trampling imposes strong disturbances on the substratum. Although the two amphibian megafauna Chinese giant salamander ( Andrias davidianus ) and Japanese giant salamander ( A. japonicus ) do not tend to excavate nests from scratch, male giant salamanders modify existing dens by pushing sand and gravel out to create nest depressions (Luo et al ., 2018; Terry et al ., 2019). As the population density of giant salamanders can be quite high in suitable environments [e.g.…”

Ethogram of the Chinese Giant Salamander during the Breeding Period Based on the PAE Coding System

“…The male modifies the cave's bottom, creating a larger space for spawning, and increases the water depth inside the cave to create an excellent environment for fertilization and incubation [28,29]. This behavior may eliminate organic matter in the cave and improve the water quality to attract females; the depression in the cave also reduces the risk of the eggs being washed away by flowing water [34]. The showering behavior is predominantly observed in males, which probably promotes the development of the testis and is beneficial to the natural reproduction of adult A. davidianus [35].…”

“…We incorporated them into the environmental coding framework (Table 3), which more accurately expresses the environmental conditions and thresholds required during the reproductive period and is an exploration of a quantitative research model of animal behavior. The family of Cryptobranchidae can successfully breed in a simulated natural environment [6,29,34], and a suitable space can improve the reproductive success rate of C. alleganiensis. The confined and narrow environment inhibits the development of the gonads of A. davidianus, resulting in a decline in the quality of sperm and eggs [42].…”

Egg predators improve the hatching success of salamander eggs

“…Oviparous animals often suffer high mortality during the embryonic stage through predation, infection, and changes in abiotic factors such as temperature and moisture (Begon & Townsend, 2021 ; Davidson et al, 2022 ; Kuris, 1990 ; Stearns, 2000 ; Wilbur, 1980 ). In order to improve early‐life survivorship, various modes of parental investment into egg defenses have evolved across taxa, including oviposition site selection, preparation of nesting sites, and egg attendance (Mainwaring & Hartley, 2013 ; Mitchell et al, 2015 ; Okada et al, 2015 ; Resetarits & Wilbur, 1989 ; Scott, 1990 ; Terry et al, 2019 ). Parental investment can also take the form of providing physical structures protecting embryos; eggshells and extraembryonic membranes of avian and reptilian amniotic eggs serve as well‐known examples (D'Alba et al, 2021 ; Starck et al, 2021 ).…”