African amphibians make extreme parental sacrifice: The skin off their backsANN ARBOR, Mich.---Just as baby mammals depend on their mothers' milk, the young of the African amphibian Boulengerula taitanus nourish themselves by stripping off and eating the fat-rich outer layer of their mothers' skin, according to an international team of researchers that includes University of Michigan biologist Ronald Nussbaum.
The findings are reported in today's issue (April 13) of the journal Nature.
Hatchlings of B. taitanus---a legless amphibian that looks something like an earthworm---are born with specialized teeth for peeling and eating skin. Their mothers' skin is specially modified to be particularly nutritious, and the young depend entirely on this food source for perhaps as long as four weeks, Nussbaum said.
"This form of post-hatching parental care, in which the mother provides nutrition to her hatchlings via her skin, has never been seen before in amphibians, and may be unique among vertebrates to this group of amphibians," said Nussbaum, a professor of ecology and evolutionary biology and a curator in the U-M Museum of Zoology. "Some cichlid fishes are known to provide their hatchlings with nutrition through skin secretions, but this does not include skin feeding."
Earlier observations of another species in the same order of amphibians foreshadowed the latest discovery. In the 1990s, the same research team found that newborn Siphonops annulatus had teeth and stayed with their mothers for some time after hatching. Those observations, coupled with the unusually pale skin color of mothers caring for young, led Nussbaum and colleagues to speculate that S. annulatus hatchlings fed on glandular secretions from the mother's skin, but the scientists never observed such behavior.
In the current study, the team collected 21 B. taitanus females along with their broods and put the animals into small, plastic boxes filled with soil to simulate natural nesting conditions. Then they observed and videotaped interactions between young and their mothers.
"We observed eight episodes of skin feeding by different young from five different broods," Nussbaum said. "In each episode, the young moved over and around their mothers' bodies, vigorously pressing their heads against their mothers while repeatedly opening and closing their mouths. They used their lower jaws to lift and peel the outer layer of the mother's skin."
Studies of the females' skin revealed that the outer layer is up to twice as thick in brooding females as in non-brooding females and is full of nutritious fat.
Amphibians are a diverse lot when it comes to parental care, which may include hiding, guarding, carrying and feeding offspring. Among caecilians---the order of amphibians to which B. taitanus and S. annulatus belong---some lay yolky eggs and tend them until they hatch but invest no energy in feeding the young after hatching; others bear live young that fend for themselves after birth.
In those that bear live young, fetuses are equipped with specialized teeth---something like those of B. taitanus and S. annulatus---that are thought to be used for scraping secretions and cellular material from the lining of the mother's oviduct. The skin-feeding behavior seen in B. taitanus may represent an evolutionary intermediate between these two reproductive modes, Nussbaum said.
The discovery of this never-before-seen behavior also highlights the importance of conservation efforts, Nussbaum said. "Concerns have been growing about amphibian populations that appear to be declining worldwide. Our discovery underscores the need for further studies to better document the amazing diversity of amphibian life history strategies and greater efforts to conserve it."
Nussbaum collaborated on the research with Alexander Kupfer and Mark Wilkinson of the Natural History Museum in London, UK; Hendrik Muller of Leiden University in the Netherlands; Marta Antoniazzi and Carlos Jared of Laboratorio de Biologia Celular, Instituto Butantan in Sao Paulo, Brazil; and Hartmut Greven of the Institut fur Zoomorphologie und Zellbiologie der Heinrich-Heine-Universitat Dusseldorf in Dusseldorf, Germany.
The researchers received funding from the European Union and the Natural Environment Research Council.
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