RESUMO
Anuran amphibians (frogs and toads) typically have a complex life cycle, involving aquatic larvae that metamorphose to semi-terrestrial juveniles and adults. However, the anuran olfactory system is best known in Xenopus laevis, an animal with secondarily aquatic adults. The larval olfactory organ contains two distinct sensory epithelia: the olfactory epithelium (OE) and vomeronasal organ (VNO). The adult organ contains three: the OE, the VNO, and a "middle cavity" epithelium (MCE), each in its own chamber. The sensory epithelia of Xenopus larvae have overlapping sensory neuron morphology (ciliated or microvillus) and olfactory receptor gene expression. The MCE of adults closely resembles the OE of larvae, and senses waterborne odorants; the adult OE is distinct and senses airborne odorants. Olfactory subsystems in other (non-pipid) anurans are diverse. Many anuran larvae show a patch of olfactory epithelium exposed in the buccal cavity (bOE), associated with a grazing feeding mode. And other anuran adults do not have a sensory MCE, but many have a distinct patch of epithelium adjacent to the OE, the recessus olfactorius (RO), which senses waterborne odorants. Olfaction plays a wide variety of roles in the life of larval and adult anurans, and some progress has been made in identifying relevant odorants, including pheromones and feeding cues. Increased knowledge of the diversity of olfactory structure, of odorant receptor expression patterns, and of factors that affect the access of odorants to sensory epithelia will enable us to better understand the adaptation of the anuran olfactory system to aquatic and terrestrial environments.
Assuntos
Neurônios Receptores Olfatórios/fisiologia , Anfíbios , AnimaisRESUMO
The aquatic-to-terrestrial shift in the life cycle of most anurans suggests that the differences between the larval and adult morphology of the nose are required for sensory function in two media with different physical characteristics. However, a better controlled test of specialization to medium is to compare adult stages of terrestrial frogs with those that remain fully aquatic as adults. The Ceratophryidae is a monophyletic group of neotropical frogs whose diversification from a common terrestrial ancestor gave rise to both terrestrial (Ceratophrys, Chacophrys) and aquatic (Lepidobatrachus) adults. So, ceratophryids represent an excellent model to analyze the morphology and possible changes related to a secondary aquatic life. We describe the histomorphology of the nose during the ontogeny of the Ceratophryidae, paying particular attention to the condition in adult stages of the recessus olfactorius (a small area of olfactory epithelium that appears to be used for aquatic olfaction) and the eminentia olfactoria (a raised ridge on the floor of the principal cavity correlated with terrestrial olfaction). The species examined (Ceratophrys cranwelli, Chacophrys pierottii, Lepidobatrachus laevis, and L. llanensis) share a common larval olfactory organ composed by the principal cavity, the vomeronasal organ and the lateral appendix. At postmetamorphic stages, ceratophryids present a common morphology of the nose with the principal, middle, and inferior cavities with characteristics similar to other neobatrachians at the end of metamorphosis. However, in advanced adult stages, Lepidobatrachus laevis presents a recessus olfactorius with a heightened (peramorphic) development and a rudimentary (paedomorphic) eminentia olfactoria. Thus, the adult nose in Lepidobatrachus laevis arises from a common developmental 'terrestrial' pathway up to postmetamorphic stages, when its ontogeny leads to a distinctive morphology related to the evolutionarily derived, secondarily aquatic life of adults of this lineage.
Assuntos
Anuros/anatomia & histologia , Anuros/crescimento & desenvolvimento , Evolução Biológica , Mucosa Olfatória/anatomia & histologia , Mucosa Olfatória/crescimento & desenvolvimento , Animais , Larva/anatomia & histologia , Larva/crescimento & desenvolvimento , Órgão Vomeronasal/anatomia & histologia , Órgão Vomeronasal/crescimento & desenvolvimentoRESUMO
The anuran peripheral olfactory system is composed of a number of subsystems, represented by distinct neuroepithelia. These include the main olfactory epithelium and vomeronasal organ (found in most tetrapods) and three specialized epithelia of anurans: the buccal-exposed olfactory epithelium of larvae, and the olfactory recess and middle chamber epithelium of postmetamorphic animals. To better characterize the developmental changes in these subsystems across the life cycle, morphometric changes of the nasal chemosensory organs during larval development and metamorphosis were analyzed in three different anuran species (Rhinella arenarum, Hypsiboas pulchellus, and Xenopus laevis). We calculated the volume of the nasal chemosensory organs by measuring the neuroepithelial area from serial histological sections at four different stages. In larvae, the vomeronasal organ was relatively reduced in R. arenarum compared with the other two species; the buccal-exposed olfactory epithelium was absent in X. laevis, and best developed in H. pulchellus. In postmetamorphic animals, the olfactory epithelium (air-sensitive organ) was relatively bigger in terrestrial species (R. arenarum and H. pulchellus), whereas the vomeronasal and the middle chamber epithelia (water-sensitive organs) was best developed in X. laevis. A small olfactory recess (likely homologous with the middle chamber epithelium) was found in R. arenarum juveniles, but not in H. pulchellus. These results support the association of the vomeronasal and middle chamber epithelia with aquatic olfaction, as seen by their enhanced development in the secondarily aquatic juveniles of X. laevis. They also support a role for the larval buccal-exposed olfactory epithelium in assessment of oral contents: it was absent in X. laevis, an obligate suspension feeder, while present in the two grazing species. These initial quantitative results give, for the first time, insight into the functional importance of the peripheral olfactory subsystems across the anuran life cycle.