Holliday, C.M., Ridgely, R.C., Balanoff, A.M. and L.M. Witmer. 2006. Cephalic vascular anatomy in flamingos (Phoenicopterus ruber) based on novel vascular injection and computed tomographic imaging analyses. Anatomical Record 288A:1031-1041.

The Caribbean flamingo, Phoenicopterus ruber, is one of five species of extant Phoenicopteridae, an avian group probably most closely related to Ciconiiformes (Livezey, 1997; Mayr and Clarke, 2003) although phylogenetic relationships with Anseriformes (Feduccia, 1976, 1978; Olsen and Feduccia 1980) and Podicipedidae (van Tuinen et al., 2001; Mayr, 2004) have also been proposed based on morphological and molecular analyses. Flamingos are easily distinguishable by their rosy or pink feathers (due to the ingestion of carotenoids in their diets), elongate necks and legs, and a conspicuously ventroflexed bill. Flamingos are highly social birds generally found in subtropical and tropical estuarine and briny bodies of water across Latin America, Africa, and India, in addition to numerous front lawns.

Perhaps the most intriguing aspect of flamingo natural history is their feeding behavior, during which they invert their heads and hold their bills nearly horizontal. During these maneuvers, they strain shallow waters for a variety of food items including algae, small invertebrates, and small fish; P. ruber predominately feeds on brine flies and shrimp. Flamingo mouths are peculiarly built to dexterously separate water and unwanted particles from food items using a large, fatty, highly sensitive tongue with numerous fleshy spines complemented by a keeled, lamellate bill. In general, the tongue is used as a rostrocaudally-oriented pump that quickly (5-20 beats/minute) sucks in particulate-laden water and expels unwanted items via a complex set of movements (Jenkin, 1957; Zweers et al., 1995). Food is then ingested using the typical "throw and catch" behavior of most birds. Whereas P. ruber has a rather small maxillary keel, lesser flamingos, James' flamingos, and Andean flamingos have more heavily keeled maxillae (Mascitti and Kravetz, 2002). This keel aids in the mediolateral movement of water and solutes towards the lamellate margins of the tongue and bill. Despite these studies of feeding function, little is known about flamingo head anatomy in general.

Labeled Volumetric Renderings and Three-dimensional Anaglyphic Stereo Images

Labeled volumetric renderings and anaglyphic (red/cyan) images of flamingo cephalic vasculature. View with standard "3D movie" glasses. For best results view in a dark area.

3D anaglyphic glasses (red/cyan) can be purchased from http://www.berezin.com/3d/3dglasses.htm.

Vascular nomenclature from Sedlmayr (2002). See Sedlmayr (2002) for an analysis of head vasculature in other birds and crocodilians.

Anatomical views:

Left Lateral Labeled 3D stereo	Right Medial Labeled 3D stereo	Caudal Labeled 3D stereo
Dorsal Labeled 3D stereo	Ventral Labeled 3D stereo	Ventral Oblique Labeled 3D stereo

Labeled Slices

Labeled coronal, sagittal, and horizontal slices of flamingo head. Scout image depicts location of slice.

Vascular nomenclature from Sedlmayr (2002). See Sedlmayr (2002) for an analysis of head vasculature in other birds and crocodilians.

Click for a larger image.

Coronal Slices
Horizontal Slices
Sagittal Slices

See 'Additional Imagery' page for animations.

The specimen of Phoenicopterus ruber (Ohio University Vertebrate Collections [OUVC] 9756) was donated to Ohio University from the Brevard Zoo, Florida, USA (http://www.brevardzoo.org/ ). The specimen was frozen, subsequently thawed, injected, scanned and dissected.

The common carotid artery and jugular anastomosis were separately cannulated, and the vessels were flushed with tap water for 10 minutes. Separate 60cc volumes of both blue and red Ward’s latex injection solution were each mixed with E-Z-M barium sulfate suspension to an approximately 30% solution for arteries and 40% for veins (See Sedlmayr and Witmer, 2002, for a more complete vascular injection technique). Differential barium concentrations were used to provide contrast between arteries and veins in radiographic analyses. About 30cc each of the barium-latex solutions were successfully injected into their respective vessels (red for arteries, blue for veins).

Lateral view of head	Specimen cannulated for vascular injection

Injected vessels

Funding for the anatomical preparation and study and for the 3D visualization was provided by NSF (IBN-0343744 to LMW) and Ohio University. Funding for scanning was provided by an National Science Foundation Digital Libraries Initiative grant to Dr. Timothy Rowe of The University of Texas at Austin.

The specimen was scanned at the University of Texas High-Resolution X-ray Computed Tomography Facility at 180kV, 0.2mA. Field of view was 73.0mm across 1024 x 1024 pixels, and slice thickness and spacing were 0.264mm (yielding a voxel size of 0.0713 x 0.713 x 0.264 mm). The data were imported into a Dell Precision 360 workstation and analyzed with Amira 3.1 (TGS software, San Francisco) software. To ease in handling of the large size of the data set, the 16-bit data were converted to 8-bit, and cropped to eliminate the extraneous data (e.g. air, uninjected area of the specimen). The data were then resampled to yield a voxel size of 0.12 x 0.12 x 0.18mm. To provide topographic references, the cranial endocast and inner ear labyrinths were segmented and rendered in 3D.

Literature

Arad, Z., U. Mitgard, and M. H. Bernstein. 1989. Thermoregulation in turkey vultures: vascular anatomy, arteriovenous heat exchange, and behavior. Condor 91:505-514.

* Baumel, J. J. 1993. Systema Cardiovasculare; pp. 407-476 in J. J. Baumel (ed.), Handbook of Avian Anatomy: Nomina Anatomica Avium. Nuttal Ornithological Club, Cambridge, Massachusetts.

Baumel, J. J., A. F. Dalley, and T. H. Quinn. 1983. The collar plexus of subcutaneous thermoregulatory veins in the Pigeon, Columba livia: its association with esophageal pulsation and gular flutter. Zoomorphology 102:215-239.

Ericson, P. G. P. 1999. New material of Juncitarsus (Phoenicopteriformes), with a guide for differentiating that genus from the Presbyornithidae (Anseriformes). Smithithsonian Contributions to Zoology 89:245-251.

Feduccia, A. 1976. Osteological evidence for shorebird affinities of the flamingos. Auk 93:587-601.

Feduccia, A. 1978. Presbyornis and the evolution of ducks and flamingos. American Scientist 66:298-304.

Holliday, C. M., R. C. Ridgely, A. M. Balanoff, L. M. Witmer. 2006. Cephalic vascular anatomy in flamingos (Phoenicopterus ruber) based on novel vascular injection and computed tomographic imaging analyses. Anatomical Record 288A:1031-1041.

Homberger, D. G. 1988. Comparative morphology of the avian tongue; pp. 2427-2435 in H. Oeullet (ed.), Acta XIX Congressus Internationalis Ornithologici Vol 2. University of Ottawa Press, Ottawa.

* Jenkin, P. M. 1957. The filter-feeding and food of flamingoes (Phoenicopteri). Philosophical Transactions of the Royal Society B, Biological Sciences 240:401-493.

Livezey, B. C. 1997. A phylogenetic analysis of basal Anseriformes, the fossil Presbyornis, and the interordinal relationships of waterfowl. Zoological Journal of the Linnean Society, London 121:361-428.

* Mascitti, V., F. O. Kravetz. 2002. Bill morphology of South American flamingos. Condor 104:73-83.

Mayr, G. 2004. Morphological evidence for sister group relationship between flamingos (Aves: Phoenicopteridae) and grebes (Podicipedidae). Zoological Journal of the Linnean Society, London 140:157-169.

Mayr, G., and J. Clarke. 2003. The deep divergences of neornithine birds: a phylogenetic analysis of morphological characters. Cladistics 19:527-553.

Mitgard, U. 1984. Blood vessels and the occurrence of arteriovenous anastomoses in cephalic heat loss areas of mallards, Anas platyrynchos, Aves. Zoomorphology 104:323-335.

Olsen, S. L., A. Feduccia. 1980. Relationships and evolution of flamingos (Aves: Phoenicopteridae). Smithsonian Contributions to Zoology 316:1-73.

Rich, P. V., and C. A. Walker. 1983. A new genus of Miocene flamingo from East Africa. Ostrich 54:95-104.

Rich, P. V., G. F. van Tets, T. H. V. Rich, and A. R. McEvey. 1987. The Pliocene and Quaternary flamingoes of Australia. Memoirs of the Queensland Museum 25:207-226.

* Sedlmayr, J. C. 2002. Anatomy, evolution, and functional significance of cephalic vasculature in Archosauria. Ph.D. dissertation, Ohio University, 398 pp.

Sedlmayr, J. C., and L. M. Witmer. 2002. Rapid technique for imaging the blood vascular system using stereoangiography. Anatomical Record 267:330-336.

van Tuinen, M. D., B. Butvill, J. A. W. Kirsch, and S. B. Hedges. 2001. Convergence and divergence in the evolution of aquatic birds. Proceedings of the Royal Society of London B, Biological Sciences 268:1345-1350.

Vanden Berge, J. C., and G. A. Zweers. 1993. Myologia; pp. 189-247 in Baumel J. J. (ed.), Handbook of Avian Anatomy: Nomina Anatomica Avium. Nuttal Ornithological Club, Cambridge, Massachusetts.

Zweers, G. F., H. Berkhoudt, and J. C. Vanden Berge. 1994. Behavioral mechanisms of avian feeding; pp. 241-279 in V. L. Bels, M. Chardon, P. Vandewalle (eds.), Biomechanics of Feeding in Vertebrates. Advances in Comparative and Enviromental Physiology, Vol. 18. Springer-Verlag, Berlin.

* Zweers, G. F., F. de Jong, and H. Berkhoudt. 1995. Filter feeding in flamingos (Phoenicopterus ruber). Condor 97:297-324.

Asterisks (*) denote anatomical literature

Links

Audubon Institute

www.lawnflamingo.com

Phoenicopterus ruber on the Animal Diversity Web (Univ. of Michigan Museum of Zoology).

3D glasses to view stereo images www.berezin.com

Three-dimensional Reconstructions

Movies of segmented and reconstructed vessels, brain endocast, and semicircular canals. Arteries are colored red; veins are colored blue.

Roll Spin (4.5mb)	Yaw Spin (3.8mb)	Yaw spin - translucent head (3mb)

Animations of segmented and reconstructed otic region.

Inner ear (osseous labyrinth) (2mb)	Otic region (3.8mb)

Three-dimensional Volume Renderings

Grayscale animations of injected vessels (right side) in a sagittally sectioned volume

Roll Spin (4.5mb)	Yaw Spin (4.5mb)

Three-dimensional color animations of cephalic vascular system

Roll Spin (4mb)	Yaw Spin (3.5mb)