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Amphibian Species Responds to Offspring’s Demands for Milk

    Siphonops-annulatus, or S. annulatus

    Written by: Alla Katsnelson, Ph.D | Issue # 120 | 2024

    • Siphonops annulatus, a type of egg-laying amphibian called a caecilian, produces milk for its young on demand, a parental care and feeding system that’s not shared by its closest relatives.
    • Many animals besides mammals produce milk for their young, but this caecilian is the first amphibian found to do so in response to signals from its young. 
    • This discovery enables researchers to study the traits and evolutionary significance of different parental feeding and care strategies.

    A worm-like, egg-laying amphibian is the latest addition to the list of animals that produce milk to feed their young, according to a new study in Science [1]. The researchers observed that in the two months after hatching, the young of this species, Siphonops annulatus, crowded around the mother, consuming a secretion produced from her body. The hatchlings also emitted sounds that appeared to act as signals to elicit its production.

    “What seems quite spectacular about this paper is that the young are signaling for the parents to release the milk,” says Katie Hinde, an evolutionary biologist who studies lactation at Arizona State University and who was not involved in the work.

    S. annulatus is the first egg-laying amphibian observed to produce milk for its young on demand—that is, in response to cues from infants—begging the fascinating question of this why this arrangement for feeding and parental care evolved in this species and not other, closely related ones, Hinde says.

    Mammals may be the animals most famous for producing milk for their young, but many other animals do so, including some spiders [2], cockroaches [3], fish [4] and birds [5].  Members of the worm-like group of amphibians called caecilians, to which S. annulatus belongs, are among the least-studied vertebrates. They are known to exhibit another type of parental feeding behaviors, called skin-feeding [6]. In these caecilian species, maternal skin changes consistency and becomes enriched with lipids, and offspring feed on this substance during their first two months of life. Unlike S. annulatus, most caecilian species are viviparous – that is, females give birth to live young. Viviparous caecilians – and other amphibians – are thought to produce milk that is consumed by embryos in the oviducts – the tubes in which embryos develop [7].

    S. annulatus is known to engage in skin feeding. But researchers led by Carlos Jared at the Butantan Institute in Sao Paulo, Brazil, were studying the species’ reproductive biology, they noticed that offspring also consumed a viscous substance secreted from a slit near the mother’s tail. They also saw that the hatchlings were getting nourishment from this substance, which they then referred to as milk.

    The researchers then observed the feeding dynamics of 16 adult females and their offspring in detail. Several times a day, the hatchlings nibbled at the mother’s tail area while moving their bodies and producing high-pitched sounds. These actions seemed to stimulate the release of milk from the mothers’ vents. The researchers aligned video and recordings of hatchlings feeding and determined that their vocalizations were strongest in the minute before the mother’s milk was released. This suggested that the vocalizations act as a biological signal that acts on the mother’s body, much like the sounds of mammalian infants stimulate maternal milk let-down

    Additionally, when S. annulatus hatchlings stopped consuming milk, the mothers seemed to stop producing it, Jared and his colleagues found.  “That lets us know that it is costly, to some extent, for her to be producing this fluid for them,” says Hinde. The energetic cost suggests that the system confers an evolutionary advantage, she says. 

    An analysis of the composition of S. annulatus milk revealed it to be rich in lipids and carbohydrates. The lipid portion contained long-chain fatty acids – primarily palmitic acid and stearic acid. “Lipids are such a rich fuel that it makes sense as a key nutrient for energy for the young,” says Hinde. 

    “We demonstrate that the secretion from the oviducts released through the vent is an important food source provided in response to hatchlings’ signaling,” the researchers write in the paper. “This context can explain why the mother remains entirely dedicated to the hatchlings during the 2 months of parental care, not leaving them even to feed herself.” 

    The study raises a host of fascinating questions, says Hinde. Millions of years ago, there were lots of mammal-like animals that did not produce milk, but we milk-producers outcompeted them during the course of evolution, she says. 

    References

    1. Mailho-Fontana PL, Antoniazzi MM, Coelho GR, Pimenta DC, Fernandes LP, Kupfer
      A, Brodie ED Jr, Jared C. Milk provisioning in oviparous caecilian amphibians. Science. 2024 Mar ;383(6687):1092-1095.
    2. Chen Z, Corlett RT, Jiao X, Liu SJ, Charles-Dominique T, Zhang S, Li H, Lai R, Long C, Quan RC. Prolonged milk provisioning in a jumping spider. Science. 2018 Nov ;362(6418):1052-1055.
    3. Stay B., Coop A.C. “Milk” secretion for embryogenesis in a viviparous cockroach. Tissue and Cell.1974; 6: 669–693.
    4. Sato K, Nakamura M, Tomita T, Toda M, Miyamoto K, Nozu R. How great white
      sharks nourish their embryos to a large size: evidence of lipid histotrophy in
      lamnoid shark reproduction. Biol Open. 2016 Sep ;5(9):1211-1215.
    5. Wang L, Zhu J, Xie P, Gong D. Pigeon during the Breeding Cycle: Behaviors,
      Composition and Formation of Crop Milk, and Physiological Adaptation. Life
      (Basel). 2023 Sep ;13(9):1866.
    6. Kupfer A, Müller H, Antoniazzi MM, Jared C, Greven H, Nussbaum RA, Wilkinson
      M. Parental investment by skin feeding in a caecilian amphibian. Nature. 2006
      Apr ;440(7086):926-929.
    7. Jared C, Mailho-Fontana PL, Jared SGS, Kupfer A, Delabie JHC, Wilkinson M, Antoniazzi MM. Life history and reproduction of the neotropical caecilian Siphonops annulatus (Amphibia, Gymnophiona, Siphonopidae), with special emphasis on parental care. Acta Zoologica. 2019 July;100(3): 292-302.