Morphology of skin incubation in Pipa carvalhoi (Anura: Pipidae)

Abstract

South American Pipidae show a unique reproductive mode, in which the fertilized eggs develop in temporarily formed brood chambers of the dorsal skin after eggs have been deposited on the back of the female. We studied the skin incubation of Pipa carvalhoi using light microscopy and scanning electron microscopy. The skin consists of a stratified epithelium with a one-layered stratum corneum, and the dermis. The dermis of the dorsal skin of nonreproductive and reproductive females lacks a distinct stratum compactum, which is typical for most anuran skins. The entire dermis shows irregularly arranged collagen bundles like a stratum spongiosum. Before egg laying, the skin swells, primarily by thickening and further by loosening of the middle zone of the dermis. In the epidermis, large furrows develop that are the prospective sites of egg nidation. The epidermis, which forms a brood chamber around the developing egg becomes bi-layered and very thin and lacks a stratum corneum. Further, the dermis loosens and becomes heavily vascularized. Egg carrying females do not have mature oocytes in their ovaries indicating a slow down or interruption of egg maturation during this period. Similarities with the brood pouch of marsupial frogs are discussed.

Carrying Progeny on the Back: Reproduction in the Brazilian Aquatic FrogPipa carvalhoi

“…This modification might be important to make the dermis more malleable and able to better accommodate the eggs and the future embryos. Such characteristic was also noted by Greven and Richter (2009) and, according to them, is present in females of all Pipa species. Through polarized microscopy after picrosirius staining, two types of dermal collagen fibers were distinguished, one more related to the dense regions (Type I collagen, which is thicker and appears in red), and another related to looser regions (Type III collagen, which is thinner and more delicate, appearing in green) (Junqueira et al, 1979).…”

“…We have shown that increase in vascularization is more evident from the 14 th day, when the embryos are in the later developmental stages and no yolk is available inside the egg, although it was seen inside the embryos intestines. This evidence and the close contact between capillaries through a very thin epithelium lead us to suppose that there is some type of interaction between maternal and embryonic tissues in P. carvalhoi (Fernandes, 2007;Fernandes et al, 2007), an observation also made by Greven and Richter (2009). Gas exchange was suggested for the marsupial frog Gastrotheca (Del Pino, 1980).…”

“…Although evolutionarily independent and widely separated in time, egg immersion in pipid skin shows some similarities with egg implantation in the mammal endometrium (Fernandes, 2007;Fernandes et al, 2007;Greven and Richter, 2009) and is a good example of convergent evolution. Both processes seem to be related to the compatibility between egg and maternal tissue.…”

“…In the species of Pipa, this dance results in the deposition of sticky eggs that, with the help of the male, adhere to the dorsum of the female. The eggs rapidly penetrate into the maternal dorsal skin, where the embryos develop into tadpoles (as is the case of Pipa carvalhoi) (Weygoldt, 1976a,b;Greven and Richter, 2009) or into froglets (as occurs in Pipa pipa) (Rabb and Rabb, 1960;Zippel, 2006). Courtship in Pipa has been described Rabb, 1960, 1963;Weygoldt, 1976a;Duellman and Trueb, 1986;Zippel, 2006), but little is known about the formation of the egg chamber in the maternal skin and the development of the egg (Weygoldt, 1976b;Greven and Richter, 2009).…”

A simplified table for staging embryos of the pipid frog Pipa arrabali

“…Fernandes et al (2011) argued in favor of some type of interaction between embryonic and maternal tissues in P. carvalhoi. This suggestion was based on the presence of a large number of blood capillaries in the skin of the embryo, and a thin epidermis lacking a stratum corneum and a heavily vascularized dermis forming the walls of the brood chambers (Greven andRichter 2009, Fernandes et al 2011). A vascularized tail may also suggest a role in gas exchange.…”