A new species of skin-feeding amphibian has been discovered in French Guiana. Named Microcaecilia dermatophaga, it joins just three other caecilian species whose young have been observed to regularly feed on their mother's skin.
Amphibians can be pretty good parents, committing themselves to various guarding, transporting and feeding behaviours to foster their offspring. The Surinam toad from French Guiana has her fertilised eggs implanted into her skin by the male as a protective measure, while the gastric brooding frog of Queensland, Australia, swallows her eggs so her tadpoles can develop in her stomach. Another type of amphibian, the legless, wormlike caecilian, has evolved a unique, and apparently quite effective, parenting technique that has only recently been observed.
Caecilians are found in Central and South America, Subsaharan Africa, India, South-east Asia and the Seychelles. They live mostly in tropical soils but a few aquatic and semi-aquatic species can be found in freshwater systems around the world. They can grow to almost 1.5 m in length and breed through internal copulation, which can last between 45 minutes and three hours. Unlike any other type of amphibian, male caecilians mate using a phallic organ that folds out from inside its cloaca.
The caecilian order (Gymnophiona) can be classified into three different groups depending on how their young develop: there are those whose eggs hatch in the water, where the young will live until they have metamorphised into their final, adult form, just like frogs; there are those whose young hatch from eggs and develop into the adult form without having to metamorphose, known as direct-developing; and there are those that retain their eggs internally and give birth to live young, known as viviparity. Because almost all species of caecilian spend their lives in underground burrows, their natural behaviour can be very difficult to study - they have to be disturbed before they can be observed.
In the 1990s, Mark Wilkinson from the Department of Zoology at the London Natural History Museum and Ron Nussbaum from the University of Michigan discovered unique baby teeth in hatchlings of the South American direct-developing caecilian, Siphonops annulatus. Together with observations that the young remained with their mother until they had grown a great deal and that mothers tending to a brood had different, much paler skin than adult females without dependant young, the team suggested that the S. annulatus young could be feeding on the mother's skin secretions, sort of like mammalian lactation, using specialised teeth.
They were almost right, because 16 years later, Alexander Kupfer from the London Museum of Natural History and Wilkinson watched as the young of an East African species called Boulengerula taitanus fed on their mother's skin, which was the first ever observation of this behaviour, known as maternal dermatophagy. "Rather than scraping up skin secretions, the young of B. taitanus use their teeth to peel and eat the specially modified skin of their mothers," they reported in Nature.
Two years later, Kupfer and Wilkinson also confirmed the behaviour in S. annulatus, and described it all of its grossness in Biology Letters:
Feeding behaviour is quite frenetic with the young frequently tearing pieces of skin by spinning along their long axes and sometimes struggling over the same piece of skin. The mother remains calm during this activity. When the mother has been peeled, the young continue to search for and eat fragments of skin on the substrate. Feeding bouts are short: just seven minutes for the only complete bout observed and interspersed with long periods of quiescence. Skin feeding was seen twice in one family group separated by approximately 64 hours.
They concluded that while the behaviour had only been observed in a handful of caecilians from two species, there was reason to believe that skin-feeding was a widespread phenomenon in the Siphonopidae family of direct-developing caecilians. "Biogeographic considerations, the separation of Africa and South American land masses, and inferred timescales of amphibian diversification all suggest that skin-feeding is an ancient form of parental care in caecilians, which has probably persisted in multiple lineages for more than 100Myr [million years]."
The team also discovered that young S. annulatus individuals would congregate around their mother's cloacal opening to drink the clear fluid that would flow from within.
Now, Wilkinson and Emma Sherratt from the London Natural History Museum have discovered a new species of direct-devloping, skin-feeding caecilian, M. dermatophaga - the first new caecilian species to be discovered in French Guiana in more than 150 years. "The forest was very full of mosquitos, making for uncomfortable digging - that is how we find caecilians, using a bladed hoe to turn over rotten logs and dig in the soil," says Sherratt. "I was systematically breaking down a rotten log, when I came across this pink wiggling animal, about 15cm long. I grabbed at it and instantly screamed with delight - A CAECILIAN! We found several more that day, breaking through mounds of rather orange, clay like soil. We found juveniles and adults. Subsequent trips by my colleagues a few years later have found even more."
Publishing last month in PLoS One, the team describes M. dermatophaga as a new species due to the number and type of rings that run around its segmented body. They maintained live individuals in captivity with an artificial night and day cycle and a 'nest' constructed from compressed soil covered with clear plastic. A piece of wood was placed over the top, and removed at 'daytime' and 'nighttime' intervals so the caecilians could be observed with as little disturbance as possible. After about a month of incubation, the eggs hatched, and their mother curled around them. The body length and mass of both parent and offspring were recorded periodically as the skin-feeding behaviour was observed.
"The altricial hatchlings (newly-hatched young that are relatively immobile, unable to burrow) peel off, remove and ingest the outer layer skin of the mother, which she [the mother] is shedding. The skin is very fatty, and she is not hurt in the process, although her body weight decreases over the time because she herself is presumably not feeding," says Sherratt. "The mother's skin changes when the eggs hatch, it becomes quite pale, a bit like when snakes are close to shedding their skin. The young of these species have distinctive multicasted teeth - good for scraping - that are shed when the young start their independent existence. The feeding happens periodically over one month, although we don't know just how frequently each day."
According to Sherratt, the skin-feeding behaviour occurs in quick, 30-second bursts. During the month after hatching, the young caecilians grow in mass considerably so they are strong enough to burrow, so it looks their skin-feeding behaviour is giving them a good start in life.
Because the behaviour has been found in two of M. dermatophaga's distant relatives, from two different families, the team suggests that this could mean that it evolved independently in the ancestors of each of these families, or it could support Wilkinson and Kupfer's earlier suggestion that skin-feeding is a widespread behaviour in direct-developing caecilians. Variations on the theme could also be common in the other types of caecilians - offspring of the viviparous Scolecomorphidae family are known to feed on the lining of their mother's uterus before birth. Further observations in other caecilian species are needed to better understand the origin of this behaviour.
"My gut feeling is this is a widespread trait in direct-developing caecilians (more than half of the known species), but I'm not speaking for my colleagues, this is my opinion," says Sherratt. "We need to continue studying the reproductive biology of caecilians - there are so many species for which we just don't know anything about their biology. It is a very exciting time of discovery! If this is so, this trait evolved at least 100 million years ago and has obviously been beneficial for caecilians."
Here's footage David Attenborough filmed with some of the team the first caecilian skin-feeding behaviour was reported:
Wilkinson, M., & Nussbaum, R. (1998). Caecilian viviparity and amniote origins Journal of Natural History, 32 (9), 1403-1409 DOI: 10.1080/00222939800770701
Kupfer, A., Müller, H., Antoniazzi, M., Jared, C., Greven, H., Nussbaum, R., & Wilkinson, M. (2006). Parental investment by skin feeding in a caecilian amphibian Nature, 440 (7086), 926-929 DOI: 10.1038/nature04403
Wilkinson, M., Kupfer, A., Marques-Porto, R., Jeffkins, H., Antoniazzi, M., & Jared, C. (2008). One hundred million years of skin feeding? Extended parental care in a Neotropical caecilian (Amphibia: Gymnophiona) Biology Letters, 4 (4), 358-361 DOI: 10.1098/rsbl.2008.0217
Wilkinson, M., Sherratt, E., Starace, F., & Gower, D. (2013). A New Species of Skin-Feeding Caecilian and the First Report of Reproductive Mode in Microcaecilia (Amphibia: Gymnophiona: Siphonopidae) PLoS ONE, 8 (3) DOI: 10.1371/journal.pone.0057756
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