Pesq. Vet. Bras. 38(1):154-166, janeiro 2018 DOI: 10.1590/1678-5150-PVB-5310 Morphogenesis of the rhea (Rhea americana) respiratory system in different embryonic and foetal stages1 Renata P. Sousa2, Hatawa M. de A. Monteiro2, Dayseanny de O. Bezerra2, Leticya L. da S. Soares2 3, Rose E.G. Rici3 4 2* , Antônio C. Assis Neto , Aírton M. Conde Júnior ABSTRACT.- and Maria A.M. de Carvalho Morphogenesis of the rhea (Rhea americana) respiratorySousa R.P., Monteiro system in H.M.A., different Bezerra embryonic D.O., Soares and foetalL.L.S., stages.Assis Neto Pesquisa A.C., RiciVet- erináriaR.E.G., Conde Brasileira Junior 38(1):154-166 A.M. & Carvalho M.A.M. 201,8. - . [email protected] de Morfofisiologia Veterinária, Centro de Ciências Agrícolas,Rhea Universidadeamericana Federal do Piauí, Campus Ministro Petronio Portela, Inin ga, Teresina, PI 64049-550, Brazil. E-mail: - The rhea ( ) is an important wild species that has been highlighted in- national and international livestock. This research aims to analyse embryo-foetal develop ment in different phases of the respiratory system of rheas. Twenty-three embryos and foe tuses were euthanized, fixed and dissected. Fragments of the respiratory system, including the nasal cavity, larynx, trachea, syrinx, bronchi and lungs, were collected and processed- for studies using light and scanning electron microscopy. The nasal cavity presented cubic- epithelium in the early stages of development. The larynx exhibited typical respiratory epi thelium between 27 and 31 days. The trachea showed early formation of hyaline cartila ge after 15 days. Syrinx in the mucous membrane of 18-day foetuses consisted of ciliated- epithelium in the bronchial region. The main bronchi had ciliated epithelium with goblet cells in the syringeal region. In the lung, the parabronchial stage presented numerous pa rabronchi between 15 and 21 days. This study allowed the identification of normal events that occur during the development of the rhea respiratory system, an important model productionthat has not systems. previously been described. The information generated here will be useful for the diagnosis of pathologiesRhea Americana, that affect this organic system, aimed at improving captive- INDEX TERMS: Rhea, respiratory system, embryonic stage, foetal stage, avian, em RESUMO.- [Morfogênesebryonic development, do sistema histology, respiratório organogenesis. da ema nacional e internacional. Esta pesquisa objetiva analisar o (Rhea americana) em diferentes estágios embrioná- desenvolvimento embrionário-fetal, em diferentes fases, do rios e fetais.] A ema (Rhea americana) representa impor- sistema respiratório de emas. Vinte e três embriões e fetos tante espécie silvestre que vem se destacando na pecuaria - 1 foram eutanasiados, fixados e dissecados. Fragmentos do parasistema estudos respiratório: por meio cavidade de microscopia nasal, laringe,de luz e microscopiatraqueia, si 2 Received on February 25, 2017. - ringe, brônquios e pulmões, foram coletados e processados Accepted for publication on June 30, 2017. Departamento de Morfofisiologia Veterinária, Centro de Ciências Agrí eletrônica de varredura. A cavidade nasal apresentou, nas [email protected], Universidade rFederal do Piauí (UFPI), Campus Ministro Petronio primeiras fases de desenvolvimento, epitélio estratificado- Portela,3 Ininga, Teresina, PI 64049-550, Brazil. *Corresponding Author: cúbico. A laringe exibiu epitélio respiratório típico entre 27 Departamento de Cirurgia, Setor de Anatomina de Animais Domésticos e 31 dias. A traqueia aos 15 dias apresentou início de for SPe Selvagens, 05508-270, Faculdade Brazil. de Medicina Veterinária e Zootecnia, Universidade mação da cartilagem hialina. Na siringe a túnica mucosa de- de4 São Paulo (USP), Av. Prof. Dr. Orlando Marques de Paiva 87, São Paulo, fetos de 18 dias e formada por epitélio estratificado ciliado na região bronquial. Os brônquios principais apresenta Departamento de Morfologia, Centro de Ciências da Saúde, UFPI, Av. vam epitélio estratificado ciliado com células caliciformes Frei Serafim 2280, Teresina, PI 64001-020, Brazil. na região siringeal. No pulmão, o estágio parabronquial 154 Morphogenesis of the rhea (Rhea americana) respiratory system in different embryonic and foetal stages 155 queapresentou ocorrem numerosos durante o parabrônquios desenvolvimento entre do 15sistema a 21 dias.res- incubation.are formed by disorganized and undifferentiated tissue, piratórioEste estudo de emas,permitiu importante a identificação modelo de ainda eventos não descrito.normais with complete differentiation observed after 10 days of- Some studies have beenGallus performed gallus domesticus to describe the mor- As informações geradas serão úteis para o diagnóstico de phological characteristics of the respiratory organs, mainly patologias que acometem este sistema orgânico, visando a using domestic chicken as an ex- Rhea ame- melhoria dos sistemas de produção em cativeiro. perimental model (Alcântara et al. 2013, Kang et al. 2013, ricana, Struthio camelus (Abi- TERMOS DE INDEXAÇÃO: Sistema respiratório, ema, Lopez et al. 2000, Maina 2003a). In addition to this, oth estágio embrionário, estágio fetal, aves, desenvolvimento er species of birds, likeMelopsittacus the ostrich undulatus embrionário, histologia,INTRODUCTION organogenese. du-Figueiredo etCoturnix al. 2012, coturnix Makanyaa japonicum et al. 2012, Yildiz et al.- 2003), the parakeet (Smith et al. 1987), the quail Pelicanus conspicillatus(Cevik-Demir (Runci- Rhea americana) kan et al. 2007), the Meleagris gallopavo turkey (Khaksar Brazil has the world’s largest biodiversity and one of the area.et al. 2012) and the pelican richest avifaunas in the world. The rhea ( man et al. 2005) have served as models for studies in this is among the oldest birds on the South American continent,- inhabiting the countryside areas and savannas (Sick 2001). The lack of more detailed data on the morphogenesis of It is a large, wild bird, of the order Rheiforme, family Rhe- 2003a).the respiratory system of birds has undoubtedly hindered idae, genus Rhea, belonging to the group of ratites birds, the decisive perception of its functional structure (Maina which includes the ostriches, emus, rheas, cassowaries, ki Rhea amer- (Sickwis (Dani 2001). 1993, Sigrist 2009) and the present-day ratites, icanaThe aim of this study was to analyse the microscopic- the most primitive birds from a phylogenetic point of view aspects of the respiratory system of the rhea ( ), a model that has not yet been described at differ- In general, the respiratory system of birds, as well as ent stages of embryo-foetal development. The information that of other vertebrates, has the importante function of- generated here will be of great importance for the identifi capturing oxygen and releasing carbon dioxide, providing cation of the ontogenetic pattern of the respiratory system the gas exchange that is fundamental to cellular metabo captiveand will production allow other systems. investigations related to conditions lism. This system is also responsible for the elimination of that can generally occur in this system, aimed at improving heat, detoxification metabolism, production of chemical - MATERIALS AND METHODS messengers and vocalization (Macari 1994). Understanding the morphological aspects of embry - - onic and foetal development in rheas is important for the- We used 23 rhea embryos and foetuses from the Study and Con calbreeding potential of thisfor nationalspecies andin captivity, international given livestock that this (Dani wild servation of Wild Animals, NEPAS (Registration Brazilian Institu 1993).bird is representative of the large species with zootechni te of Environment and Renewable Natural Resources, IBAMA, no. 02/08-618, CTF no. 474064, SISBIO no. 35374-1) of the Federal- Rhea americana) at diferente incuba- University of Piauí. The methodology of these research protocols Studies on the external morphology of embryos and were approved by the Ethics Committee on Animal Experimenta foetuses of rheas ( tion (CEEA), UFPI, no. 029/12. tion times in addition to the histological features during- The feeding of breedstock was based on commercial feed the development of the birds’ digestive tract were made (crude protein min - 160g, ether extract min - 25g, max mineral- termaterial ad libitum - 120g,. fibrous matter max - 160g, calcium max - 25g, by Monteiro (2014). However, there is still a lack of infor phosphorus min - 8g), grass Brachiaria, fruit all the time and wa mation about the morphology of the respiratory system of this species during embryonic and foetal development, The eggs were collected daily from July 2012 to September- a study of great importance, considering that they are the 2013, from different nests, always at dawn and transported to the- economiccomponents losses of this to producers. system frequently affected by diseases Integrated Center of Morphology and Research Stem Cell (NUP that often cause heavy reproductive losses, also resulting in- Celt) of the Federal University of Piauí, where they were disin Gallus gallus fected with sodium hypochlorite solution at 0.1% and incubated domesticusThe first morphological sign of respiratory tract de identified at an adjustable temperature of 37.5°C and average velopment observed in chicken embryos ( placedrelative in humidity incubation. of 45%. Embryos and foetuses were collected from ) is the emergence of the laryngeotracheal Age “0” was defined as the time at which the eggs were groove, which becomes