The Adhesive Glands during Embryogenesis in Some Species of Phyllomedusinae (Anura: Hylidae)
Among anuran embryonic structures, the adhesive (cement) glands appear posterolaterally to the stomodeum and produce a mucous secretion that adheres embryos to surfaces in and out of the egg. In this paper, we study the ontogeny of the adhesive glands in five species of Phyllomedusa representing the two main clades recognized in the genus, plus embryos of Agalychnis aspera and Phasmahyla cochranae. Clutches were collected in the field, and embryos were periodically fixed to obtain complete developmental series and then studied with a stereomicroscope, scanning electron microscopy and routine histological techniques. Structural variations include glands absent (in P. cochranae and Phyllomedusa boliviana), functional club-shaped glands (morphogenetic Type C in Phyllomedusa sauvagii, Phyllomedusa iheringii, and Phyllomedusa tetraploidea), and an unusual Type C-like pattern in Phyllomedusa azurea, characterized by large, oblong glands in a horseshoe-like disposition around the oral disc. This latter gland configuration is similar to that of A. aspera. Interspecific variations also include the arrangement and regression pattern of the secretory region, which are in turn different from those of Type C glands in other clades. To interpret the origin and evolution of gland developmental patterns in the group, we still need information on gland occurrence and development in the basal genera of Phyllomedusinae (Phrynomedusa and Cruziohyla) and in the basal taxa of the two major clades of Phyllomedusa. Entre las estructuras embrionarias de los anuros, las glándulas adhesivas (o de cemento) aparecen posterolaterales al estomodeo y producen una secreción mucosa que adhiere los embriones a las superficies dentro y fuera del huevo. En este trabajo estudiamos la ontogenia de las glándulas adhesivas de cinco especies de Phyllomedusa, representantes de los dos principales clados reconocidos en el género, y de embriones de Agalychnis aspera y Phasmahyla cochranae. Las puestas se colectaron en el campo, los embriones fueron fijados periódicamente para obtener series de desarrollo completas y luego estudiados con lupa estereoscópica, microscopía electrónica de barrido y técnicas histológicas de rutina. Las variaciones estructurales incluyen glándulas ausentes (en P. cochranae y Phyllomedusa boliviana), glándulas cónicas funcionales (Tipo morfogenético C, en Phyllomedusa sauvagii, Phyllomedusa iheringii y Phyllomedusa tetraploidea), y un patrón similar al Tipo C inusual en P. azurea, caracterizado por ser glándulas grandes, oblongas, con una disposición en herradura en torno al disco oral. Este último patrón es comparable al observado en A. aspera. Las variaciones interespecíficas también conciernen al arreglo y patrón de regresión de la región secretora, a su vez diferentes del de glándulas Tipo C de otros clados. Aún se requiere información sobre la ocurrencia y desarrollo de las glándulas en géneros basales de Phyllomedusinae (Phrynomedusa y Cruziohyla), y en los taxones basales de los dos clados principales de Phyllomedusa, a fin de interpretar el origen y evolución de los patrones morfogenéticos de las glándulas adhesivas en el grupo.Abstract
Resumen
Adhesive glands in embryos of Phyllomedusa, showing their placement lateral to the oral disc (arrows in A,C,E), and details of the superficial cell types. (A, B) Phyllomedusa sauvagii K22; the inset shows a more advanced, regressing gland at K24. (C, D) Phyllomedusa iheringii K22. (E, F) Phyllomedusa tetraploidea K21/22. Note the bordering cells (bc) and the secretory cells (sc) and the discontinuous arrangement of the secretory cells in the regressing gland of P. sauvagii and in the fully developed gland of P. iheringii. Scale lines = 100 μm (A, C, E) and 10 μm (B, D, F).
Histological features of glands in embryos of Phyllomedusa at K23 (Alcian Blue-PAS), showing transverse, topographic views at the level of eyes, and details of secretory (sc) and bordering (bc) cells. (A, B) Phyllomedusa sauvagii. (C, D) Phyllomedusa iheringii. Note the patches of free apices of secretory cells (arrow tips), two in P. iheringii. Scale lines = 50 μm (A, C) and 2 μm (B, D).
Development of the adhesive glands of Phyllomedusa azurea. (A) K19/20. (B) K22. (C) K23. (D) K > 23. (E–G) Details of superficial cell types at K > 23. bc, bordering cells; mr, microridges; sc, secretory cells; mv, microvilli. Scale lines = 100 μm (A–D) and 1 μm (E–G).
Histological features of Phyllomedusa azurea glands at K23 (Alcian Blue-PAS). (A) Transverse, topographic view at the level of eyes. (B) details of secretory and bordering cells. Note the apical free extreme of PAS positive secretory cells (arrow tip). (C) Detail of an AB positive cell in an area adjacent to the adhesive gland (black arrow). Scale lines = 50 μm (A), 2 μm (B), and 20 μm (C).
Oral region in other phyllomedusines. (A, B) Agalychnis aspera K22, distribution of secretory patches (arrow tips) lateral and posterolateral to the oral disc, and detail of secretory cells. (C, D) Phyllomedusa boliviana K21/22 and K23. (E, F) Phasmahyla cochranae K22. Note the absent glands in these two latter species. Scale lines = 2 μm (B) and 100 μm in the others.
Regression patterns of glands in phyllomedusine and dendropsophini hylids. Regressing glands are evident as patches of secretory cells (arrow tips) anterolateral to the oral disc in: (A) Phyllomedusa sauvagii K24. (B) Phyllomedusa iheringii K24. (C) Phyllomedusa tetraploidea K24. (D) Phyllomedusa azurea K24. (E) Pseudis minuta Gosner Stage >25. Regressing glands at the commissures of the oral disc: (F) Dendropsophus minutus Gosner Stage >25. Regressing glands posterolateral to the oral disc: (G) Scinax uruguayus Gosner Stage 25. Regressing glands anterolateral, lateral and posterior to the oral disc: (H) Agalycnhis aspera K24. Scale lines = 100 μm.
Oral region in pre-hatching embryos of Phyllomedusa tetraploidea (A–C) and Agalychnis aspera (D–F), showing topographic distribution of secretory patches of adhesive glands (white arrow tips), details of hatching gland cells between the oral disc and nares (asterisks in B and E), and oral neuromasts (black arrows in C and F). Scale lines = 100 μm (A,D), 10 μm (C,E,F), and 1μm (B).
Contributor Notes
