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Structural Biology Journal of Structural Biology 162 (2008) 301–311 www.elsevier.com/locate/yjsbi

Spina cortica and Tapetum spinosus, two new microstructures of flight feathers: Description, function and distribution in modern birds L.C. Straker a,*, M.A. Raposo a, Ma´rcia Attias b a

Setor de Ornitologia, Departamento de Vertebrados, Museu Nacional/UFRJ, Quinta da Boa Vista, Sa˜o Cristo´va˜o, 20940-040 Rio de Janeiro, Brazil b Instituto de Biofı´sica Carlos Chagas Filho, UFRJ, Rio de Janeiro, Brazil Received 31 August 2007; received in revised form 19 January 2008; accepted 23 January 2008 Available online 2 February 2008

Abstract The importance of feathers for the avian group has made them one of the most studied epidermal structures both from the morphological and evolutionary point of view. Surprisingly, our observations by Scanning Electron Microscopy detected the presence of two structures widely distributed within different avian groups and not yet described. In this paper we describe these two new structures (Spina cortica and Tapetum spinosus) and map their distribution within modern birds. The S. cortica is a thorn-like microstructure that grows on the barb cortex and the T. spinosus is the assemblage of these thorns. The distribution of these new structures among birds and their morphological diversity could be of great interest to taxonomists and evolutionary biologists interested in the origin of bird flight. Ó 2008 Elsevier Inc. All rights reserved. Keywords: Neornithes; Primary remex; Barb cortex; Spina cortica; Tapetum spinosus; Scanning Electron Microscopy

1. Introduction The evolution of avian feathers has resulted in the most complex and diverse epidermal appendage within vertebrate animals (Stettenheim, 2000). The study of feather morphology enables us to understand the evolution of this complex structure and of the birds as a group, given the importance of feathers as a taxonomic character. This kind of study can also increase our understanding of the complex system of microstructures that made optimization of flight possible (Prum, 1999). A large part of feather complexity is concentrated in the barbs, perpendicular structures that leave the rachis and form the feather Vexillum (feather sheet). Each barb is comprised of the Ramus (primary branch of the rachis) and the barbules (structures branching from the Ramus and carries the microstructures responsible for the interlocking system of the pennaceous barbs). During feather

*

Corresponding author. Fax: +55 21 22650163. E-mail address: [email protected] (L.C. Straker).

1047-8477/$ - see front matter Ó 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.jsb.2008.01.013

development, cells go through keratinization and differentiation to form the two main Ramus tissues (the Medulla— empty and polyhedral pith cells—and the cortex—firmly compacted squamous cells) and other structures (Strong, 1902; Lucas and Stettenheim, 1972). Morphological studies on the Medulla have shown that its cell organization can be a relevant character for the understanding of bird taxonomy (Mascha, 1905; Auber, 1957) and evolution. Auber and Appleyard (1951) studied the cortex of feather barbs using polyvinyl acetate casts. Their observations showed that surface cells are flattened and present a pattern similar to cuticular scale on mammalian hair. They also showed that these cells have a polygonal shape with the main length running parallel to the length of the Ramus and presenting detailed impressions such as the nucleus, cell boundaries and coarse fibrillary striations. Dyck (1973) studied the cortex using Scanning Electron Microscopy (SEM). In his work he discusses the differences between surface cells of blue and green feathers. His observations show that there are differences in cell shape. He also argues that the coarse fibrillary striation shown by Auber and Appleyard

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(1951) can be a consequence of cell dehydration during the keratinization process. Even though these studies used comparative methods, they did not embrace a broad range of species, nor did they look into the possibility of these characters being important for avian taxonomy as in the Medulla studies. During an exploratory and wider research on the morphology of the microstructures of Neornithes remiges, using SEM, we found two non-described structures on the Ramus’ cortex. In this paper we describe these new structures, mapping their distribution among Neornithes and tentatively discussing some aspects of their evolution. 2. Materials and methods 2.1. Study groups We analyzed remiges from 61 families in 25 orders of birds. According to the specialized literature (e.g., Strong, 1902; Mascha, 1905; Chandler, 1916; Lucas and Stettenheim, 1972) there is little intrafamilial variation within microstructures of a specific type of feather. Therefore, with the exception of Galloanseres Superorder, that was used to verify the above affirmative and to calibrate the methodology, only one feather was collected from all the other groups. All the families (see Appendix A) that were sampled in this work are housed at the Museu Nacional (MNRJ). For a better understanding of the results and discussion, we have adopted the systematic arrangement presented by Livezey and Zusi (2007), which is a very comprehensive paper on bird morphology and phylogeny. 2.2. Sample preparation and nomenclature We chose the 8th or 9th primary remex of the right wing which was generally the second longest. Pennaceous barbs from the mid region of the inner and outer vanes were cut off. Each barb was divided into three regions for more accurate observation: base, mid and apical parts, following Dove (1997). The preparation for SEM was based on Laybourne et al. (1992). First, blown air was used to clean the barbs removing dust and bigger particles. After that they were washed overnight with distilled water and non-ionic detergent, Triton X-100. They were rinsed in distilled water three times to remove all detergent. The barbs were dehydrated with ethanol 70% and ethanol absolute and then air-dried. After this procedure, each barb was cut into the sections as mentioned above. The pieces were mounted on stubs with double-faced carbon cello-tape and received a metal coating of gold for 2 min and 45 s. Our observations were made with a SEM Jeol 5310 at 15 kV and a working distance of 15 mm. For structure descriptions and basic nomenclatural reference we followed George Clark (1993) proposal.

3. Results 3.1. General description of the Ramus cortex The dorsal and ventral ridges of the barb are named Crista dorsalis and Crista ventralis, respectively (Clark, 1993) (Fig. 1C and D). Between the two ridges the barb presents two asymmetrical sides, one facing towards the feather base (proximal) with a convex curvature and supports the proximal barbules (Fig. 1C). The other faces the tip of the feather (distal) with a concave curvature and carries the distal barbules (Fig. 1D). They are called proximal side and distal side, respectively. Each side can then have its cortex surface divided into two regions: (1) dorsal cortex—above the barbules insertion and up to the Crista dorsalis (Fig. 1A and B); and (2) ventral cortex— from the barbules insertion down to the Crista ventralis. Thus, combining these categorical regions we find four regions to explore the surface cells of the Ramus (Fig. 1A–D). The texture of the surface of the Ramus is not equal throughout its parts. The Crista dorsalis is the smoothest part of the surface of the Ramus’ cortex (Fig. 1A). The surface of the dorsal cortex—that starts just below the Crista dorsalis and stops at the barbules insertion—usually presents, a rougher surface than the former structure. The ventral cortex, that is set between the insertion of the barbules and the Crista ventralis, presents a rough surface (Fig. 1C and D). In most of the cases that we examined here, the dorsal and the ventral cortex have a rough surface due to the impressions of the cell nucleus, cell boundaries and coarse fibrillary striations, as previously described by Auber and Appleyard (1951) (Fig. 2E). However, some barbs that we studied did not have any cell impressions whatsoever (e.g., Crotophaga ani, Galbula ruficalda, Momotus momota and Thalurania glaucopis) (Fig. 2F). Despite the fact that the proximal and distal sides of the same barb were quite similar to each other, some differences were found within the ventral and dorsal cortex on each side, especially regarding the new structures here described. 3.2. Description of two new microstructures Unexpected structures projecting from the cortex surface were found in many avian groups. They can be described as thorn-like microstructures growing perpendicularly to the surface of the barbs cuticle (Olson, 1970, formerly called epitrichium by Haecker, 1890). Its widest part is at the base and tapers off along its length. The tip is, in general, slightly bent and pointed. Although this structure generally resembles a small thorn, different shapes were observed varying from a hooked shape structure to a long and straight thorn. It is a very minute structure measuring on average 2 lm, attaining 4.4 lm in Eurypyga helias and less than 1 lm in length in some species. When these minute structures were

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Fig. 1. Mid section cuts of Vexillum internum barbs: asterisk, Crista corsalis; star, proximal ledge (Chandler, 1916); M, Medulla; thin arrows, (short) distal dorsal cortex, (long) proximal dorsal cortex; thick arrows, Crista ventralis; dotted arrows, barbule insertion; VBdist, Vexillum barbae distale; VBprox, Vexillum barbae proximale; DCprox, proximal dorsal cortex; VCprox, proximal ventral cortex; VCdist, distal ventral cortex. (A) Xiphocolaptes albicollis, dorsal view (bar = 50 lm); (B) Capito dayi, dorsal/lateral view (bar = 20 lm); (C) Cathartes aura, lateral view (bar = 100 lm): white arrow head, proximal barbules; (D) Streptoprocne biscutata, lateral view (bar = 50 lm): white arrow head, distal barbule.

abundant it appears as a ‘‘lawn” covering the cortex (see Fig. 2G and H). In some cases, the ‘‘lawn” is so developed and the density of the spines is so great that it becomes impossible to see the cells boundaries, nucleus or the coarse fibrillary striation (see Fig. 2G—able to see; and Fig. 2H— not able to see). Since this structure had no available name we elected the name Spina cortica to designate the individual thorn-like structure and Tapetum spinosus to designate the large assemblage of these minute structures.

3.3. Distribution of S. cortica and T. spinosus The S. cortica and the T. spinosus are not spread equally throughout all families. While they are well developed in some taxa (Livezey and Zusi (2007)) (Tinamiformes, Galliformes, Ardeiformes, Falconiformes, Opisthocomiformes, Psittaciformes, Columbiformes and Caprimulgiformes), some groups showed no sign of these structures (Struthioniformes, Anseres, Podicipediformes, Sphenisciformes, Procellariiformes, Ralliformes, Strigiformes, Cuculiformes,

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Fig. 2. Lateral view of the barb cortex—cells structures and location of Spina cortica and Tapetum spinosus: N, nucleus; M, Medulla; TS, Tapetum spinosus; thin arrow, Spina cortica; thick arrow, coarse fibrillary striation; big arrow head, cell boundary; VC, ventral cortex; VCprox, proximal ventral cortex; VCdist, distal ventral cortex; DCprox, proximal dorsal cortex; (E) Phaeton aethereus, Vexillum externum (bar = 5 lm); (F) Momotus momota, Vexillum externum (bar = 10 lm); (G) Penelope ochrogaster, Vexillum internum (bar = 20 lm); (H) Caprimulgus rufus, Vexillum externum (bar = 20 lm); (I) Nyctibius griseus, Vexillum internum (bar = 2 lm); (J) Opisthocomus hoazin, Vexillum internum (bar = 20 lm): asterisk: barbule insertion and proximal ledge (Chandler, 1916), big arrows: barbula proximalis.

Apodiformes, Trogoniformes and Coraciiformes). Nevertheless, it is worth mentioning that the orders Anseriformes, Pelecaniformes, Ciconiiformes, Gruiformes, Charadriiformes, Caprimulgiformes, Piciformes and Passeriformes include families that present the S. cortica and families where the S. cortica was absent. Table 1 summarizes the distribution of the S. cortica and T. spinosus among the different bird groups. When considering the Ramus cortex, we also found variations in the distribution of the T. spinosus and the S. cortica. We observed the Tapetum on the whole length

of the barb, covering the entire ventral cortex (including the Crista ventralis) and Spina on the dorsal cortex (see Fig. 2I) in Ardea cocoi, Cochlearius cochlearius and Nyctibius griseus. Nevertheless, in most cases, the Tapetum is present only on the ventral cortex (see Figs. 2J and 5B) (e.g., Galliformes, Ciconiiformes, Opisthocomiformes) including, in some cases the Crista ventralis (e.g., Ciconia maguari, Theristicus caudatus) (see Fig. 3K), as mentioned above. The presence or abundance of S. cortica at the most basal region of the Ramus (close to the rachis) does not mean a coating of

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Table 1 Presence and distribution of Tapetum spinosus and Spina cortica (following Livezey and Zusi 2007) Genus

Presence and distribution of Tapeum spinosus and Spina cortica Presence

Tinamus Rhea Penelope Aburria Crax Mitu Collinus Odontophorus Chauna Anhima Dendrocygna Cygnus Anas Cairina Podiceps Spheniscus Oceanodroma Pterodroma Diomedea Phaethon Fregata Sula Phalacrocorax Anhinga Ciconia Phoenicopterus Theristicus Cochlearius Ardea Cariama Eurypyga Psophia Aramus Heliornis Aramides Ventralis Jacana Tringa Charadrius Burhinus Hematopus Chionis Stercorarius Larus Rynchops Cathartes Falco Pandion Buteo Tyto Strix Opisthocomus Crotophaga Ara Columba Caprimulgus Nyctibius Steatornis Streptoprocne Thalurania

Distribution of Spina cortica

Tapetum spinosus

Spina cortica

Dorsal cortex

+

+

+

+ + + + + +

+ + + + + + + ±

+ + + + + + + +

+

+ ±

+ +

+

+ +

+ +

+ + + + + +

+ + + + + +

+ +

Ventral cortex

+ + + + + +

±

+

+

+

±

+

+

+ + ± +

+ + + +

+

+

+

+ + + +

+ + + +

+ + + +

+

+ +

+

Crista Ventralis

+ + +

+

(continued on next page)

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Table 1 (continued) Genus

Presence and distribution of Tapeum spinosus and Spina cortica Presence

Trogon Momotus Megaceryle Galbula Bucco Capito Ramphastos Campephilus Xiphocolaptes Psarocolius +, presence;

Distribution of Spina cortica

Tapetum spinosus

Spina cortica

+ +

+ + ± + +

Dorsal cortex

Ventral cortex

Crista Ventralis

+ + + + +

, absence; ±, present but underdeveloped, with length

Spina cortica and Tapetum spinosus, two new microstructures of flight feathers: description, function and distribution in modern birds

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