A nestling bird from the Lower Cretaceous of Spain: Implications for avian skull and neck evolution

Science

Volumn 276, Issue 5318, 1997, Pages 1543-1546

  Sanz, José L ^a   Chiappe, Luis M ^b   Pérez Moreno, Bernardino P ^a   Moratalla, José J ^a   Hernández Carrasquilla, Francisco ^a   Buscalioni, Angela D ^a   Ortega, Francisco ^a   Poyato Ariza, Francisco J ^a   Rasskin Gutman, Diego ^c   Martínez Delclòs, Xavier ^d  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b DIVISION OF INVERTEBRATE ZOOLOGY   (United States)

^c DEPARTMENT OF PALEOBIOLOGY   (United States)

^d UNIVERSITY OF BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHEOLOGY; ARTICLE; BIRD; EVOLUTION; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; SKULL; SPAIN;

BIRD; CRETACEOUS; ENANTIORNITHINE; SKULL;

SPAIN, LLEIDA, SERRA DE EL MONTSEC;

EID: 0030617999     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.276.5318.1543     Document Type: Article

References (58)

1. L. M. Chiappe, Nature 378, 349 (1995); C. A. Forster, L. M. Chiappe, D. W. Krause, S. D. Sampson, ibid. 382, 532 (1996); J. L. Sanz et al., ibid., p. 442; P. Wellnhofer, C. R Acad. Sci. Paris Ser. 2 319, 299 (1994); L. Hou, L. D. Martin, Z. Zhou, A. Feduccia, Science 274, 1164 (1996).
2. L. M. Chiappe, Nature 378, 349 (1995); C. A. Forster, L. M. Chiappe, D. W. Krause, S. D. Sampson, ibid. 382, 532 (1996); J. L. Sanz et al., ibid., p. 442; P. Wellnhofer, C. R Acad. Sci. Paris Ser. 2 319, 299 (1994); L. Hou, L. D. Martin, Z. Zhou, A. Feduccia, Science 274, 1164 (1996).
3. L. M. Chiappe, Nature 378, 349 (1995); C. A. Forster, L. M. Chiappe, D. W. Krause, S. D. Sampson, ibid. 382, 532 (1996); J. L. Sanz et al., ibid., p. 442; P. Wellnhofer, C. R Acad. Sci. Paris Ser. 2 319, 299 (1994); L. Hou, L. D. Martin, Z. Zhou, A. Feduccia, Science 274, 1164 (1996).
4. L. M. Chiappe, Nature 378, 349 (1995); C. A. Forster, L. M. Chiappe, D. W. Krause, S. D. Sampson, ibid. 382, 532 (1996); J. L. Sanz et al., ibid., p. 442; P. Wellnhofer, C. R Acad. Sci. Paris Ser. 2 319, 299 (1994); L. Hou, L. D. Martin, Z. Zhou, A. Feduccia, Science 274, 1164 (1996).
5. L. M. Chiappe, Nature 378, 349 (1995); C. A. Forster, L. M. Chiappe, D. W. Krause, S. D. Sampson, ibid. 382, 532 (1996); J. L. Sanz et al., ibid., p. 442; P. Wellnhofer, C. R Acad. Sci. Paris Ser. 2 319, 299 (1994); L. Hou, L. D. Martin, Z. Zhou, A. Feduccia, Science 274, 1164 (1996).
6. J. L. Sanz, L. M. Chiappe, A. D. Buscalioni, Am. Mus. Novit. 3133 (1995).
7. E. N. Kurochkin, Archaeopteryx 13, 47 (1995).
8. B. Peybernès, thesis, Université de Paul Sabatier, Toulouse (1976). Rocks at La Pedrera are rhythmically laminated, lithographic limestones deposited in the distal areas of a large, shallow Lower Cretaceous (Upper Berriasian-Lower Barremian) (36) coastal lake. The subtropical, semiarid environment at La Pedrera supported a diverse biota, including plants, mollusks, arthropods, and a variety of vertebrates (37). Before this discovery, the Lower Cretaceous birds from the lithographic limestones of El Montsec were represented by several isolated feathers and the single, fragmentary specimen of Noguerornis (38), a basal bird of uncertain affinities.
9. The two slabs were prepared with formic acid after being embedded in a frame of transparent polyester resin [J. G. Maisey, I. Rutzky, S. Blum, W. Elvers, in Santana Fossils: An Illustrated Guide, J. G. Maisey, Ed. (T. F. H. Publ., New York, 1991), pp. 98-105].
10. The fossil displays characters unknown in any other enantiornithine bird. For example, the dorsal coracoidal fossa approaches the humeral articular facet, and the ventral condyle of the humerus is strongly projected distally. Although these characters may be autapomorphies and thus justify the erection of a new taxon, the fact that the specimen is of an early ontogenetic age clouds the determination of these unique characters as true autapomorphies. Further studies or findings may prove that this specimen belongs to a species as yet unknown.
11. M. K. Hecht, J. H. Ostrom, G. Viohl, P. Wellnhofer, Eds., The Beginnings of Birds (Freunde des Jura-Museums, Eichstätt, Germany, 1985).
12. L. M. Witmer, Zool. J. Linn. Soc, 100, 327 (1990).
13. L. D. Martin, in Origins of the Higher Groups of Tetrapods, H.-P. Schultze and L. Trueb, Eds. (Cornstock, London, 1991), pp. 485-540.
14. Z. Zhou, F. Jin, J. Zhang, Chin. Sci. Bull. 37, 1365 (1992); Z. Zhou, Cour. Forschungsinst. Senckenb. 181, 9 (1995).
15. Z. Zhou, F. Jin, J. Zhang, Chin. Sci. Bull. 37, 1365 (1992); Z. Zhou, Cour. Forschungsinst. Senckenb. 181, 9 (1995).
16. O. C. Marsh, Mem. Peabody Mus. Yale College 1, 1 (1880).
17. 39Ar dates [P. Smith et al., Can. J. Earth Sci. 32, 1426 (1995)]. Both lines of evidence support a Lower Cretaceous age for the fossil-bearing deposits.
18. 39Ar dates [P. Smith et al., Can. J. Earth Sci. 32, 1426 (1995)]. Both lines of evidence support a Lower Cretaceous age for the fossil-bearing deposits.
19. 39Ar dates [P. Smith et al., Can. J. Earth Sci. 32, 1426 (1995)]. Both lines of evidence support a Lower Cretaceous age for the fossil-bearing deposits.
20. A. Elzanowski, Palaeontol. Pol. 37, 153 (1977).
21. _, Cour. Forschungsinst. Senckenb. 181, 37 (1995).
22. P. Wellnhofer, Palaeontogr. Abt. A 147, 169 (1974); P. Buhler, in (7), pp. 135-140.
23. P. Wellnhofer, Palaeontogr. Abt. A 147, 169 (1974); P. Buhler, in (7), pp. 135-140.
24. A. Elzanowski and P. Wellnhofer, J. Vertebr. Paleontol. 16, 81 (1996).
25. A. Walker, in (7), pp. 123-134.
26. L. M. Chiappe, in Contributions of Southern South America to Vertebrate Paleontology, G. Arratia, Ed. [Münchner Geowissenschaftliche Abhandlungen (A) 30, Verlag Dr. Friedrich Pfeil, München, 1996], pp. 203-244.
27. D. B. Weishampel, P. Dodson, H. Osmólska, Eds., The Dinosauria (Univ. of California Press, Berkeley, 1990).
28. We regard the pterygoid flange of the quadrate of nonavian theropods as homologous to the orbital process of the avian quadrate.
29. The presence of a bifurcated terminal facet in the rostral process of the squamosal of the seventh Archaeopteryx specimen, a condition virtually identical to that of the new fossil, also supports the presence of a postorbital in Archaeopteryx.
30. J. J. Baumel and L. Witmer, in Handbook of Avian Anatomy: Nomina Anatomica Avium, J. J. Baumel, Ed. (Publ. 23, Nuttall Ornithology Club, ed. 2, 1993), pp. 45-132.
31. P. Wellnhofer, Archaeopteryx 11, 1 (1993).
32. Except for a tiny foramen piercing the lateral surface of the surangular, the mandible of the Eichstätt specimen of Archaeopteryx appears to lack any other fenestra. Wellnhofer (23) showed that the jaw of the Solenhofer Aktien-Verein specimen has a well-developed medial fossa aditus, but this fossa does not appear to open laterally, corroborating the information available in the Eichstätt specimen. See also (9).
33. J. H. Ostrom, Biol. J. Linn. Soc. 8, 91 (1976).
34. On the basis of the presence of slightly opisthocoelous vertebrae in the Enantiornithes (presumably referring to the anterior dorsals), Kurochkin (3) has claimed that the Enantiornithes could not have evolved heterocoelous vertebrae. The new fossil, along with the material from El Brete (18), indicates that this is incorrect. The cervicals of Enantiornithes present an incipient degree of heterocoely. Likewise, claims that the ancestral condition for heterocoelic vertebrae is the procoelic (3) are incongruent with evidence from basal birds and nonavian theropods. In the Upper Cretaceous bird Patagopteryx, for example, the anterior opisthocoelic dorsals gradually change into heterocoelic cervicals (18). Furthermore, an opisthocoelic condition is typical of those theropods close to the origin of birds.
35. J. H. Ostrom, Bull. Peabody Mus. Nat. Hist. 30, 1 (1969).
36. L. M. Chiappe and J. O. Calvo, J. Vertebr. Paleontol. 14, 230 (1994); L. D. Martin, Cour. Forschungsinst. Senckenb. 181, 23 (1995).
37. L. M. Chiappe and J. O. Calvo, J. Vertebr. Paleontol. 14, 230 (1994); L. D. Martin, Cour. Forschungsinst. Senckenb. 181, 23 (1995).
38. Skeletal characters of the bird were scored in the data matrix provided by Sanz, Chiappe, and Buscalioni (2). Several modifications to this matrix were introduced: (i) Dromaeosauridae was used as single outgroup; (ii) for simplicity, Patagopteryx was excluded from the analysis because it introduces no relevant information; (iii) Concornis was included within Enantiornithes; and (iv) in Enantiornithes, character states of characters 2 and 5 were rescored as "0" (primitive state), on the basis of new data (J. L. Sanz et al., in preparation). Eight additional characters were also added to the data matrix: (i) jugal-postorbital contact (present = 0, absent = 1); (ii) quadratojugal-squamosal contact (present = 0, absent = 1); (iii) squamosal incorporated to the braincase and lacking contact to the postorbital (absent = 0, present = 1); (iv) postorbital (present = 0, absent = 1); (v) caudal end of dentary forming most of the ventral margin of the caudal mandibular fenestra (absent = 0, present = 1); (vi) epipophyses [large, projecting caudally beyond the postzygapophysial facet throughout the cervical series (0); large, but restricted to the anterior portion of the cervical series (1), or small, not projecting beyond the postzygapophysial facet (2)]; (vii) dorsal fossa on the coracoid (absent = 0, present = 1); and (viii) metacarpal III longer than metacarpal II (absent = 0, present = 1). The parsimony analysis was conducted using the Hennig 86 software (39). This analysis resulted in a single, most parsimonious tree (length, 109 steps; Cl, 0.86; Rl, 0.87). The nodes of this cladogram are diagnosed by the following unambiguous synapomorphies: (i) Aves: contact between jugal and postorbital absent; contact between the quadratojugal and squamosal absent, (ii) Ornithothoraces: prominent ventral processes on cervicodorsal vertebrae; dorsal vertebral count less than 13 to 14 elements; presence of pygostyle; strutlike coracoid; scapula with sharp caudal end; humerus shorter than or nearly equivalent to ulna; shaft of radius considerably thinner than that of ulna (ratio of diameter of radius to that of ulna less than 0.70). (iii) Ornithurae: premaxillary teeth absent; orbital process of quadrate sharp and pointed; quadratojugal cotyle in lateral face of the mandibular process of quadrate; pneumatic articular; ossified uncinate processes; procoracoid process; sagitally curved scapular shaft; craniocaudally convex, spherical head of humerus; acetabulum small, ratio of acetabulum to ilium less than or equal to 0.11; iliac fossa for M. cuppedicus (equivalent to M. iliofemoralis internus); apices of pubis not in contact; shaft of pubis laterally compressed throughout its length; femur with a deep patellar groove; posterior trochanter of femur absent; cranial cnemial crest of tibiotarsus; extensor canal on tibiotarsus; distal tarsals and metatarsals fused completely to form a tarsometatarsus; metatarsal fusion starting distally; proximal end of metatarsal III plantarly displaced with respect to metatarsal II and IV; intercondylar eminence of tarsometatarsus well developed; distal vascular foramen in metatarsus; squamosal incorporated to the braincase and lacking contact to the postorbital; absence of postorbital; small epipophyses, not projecting beyond the postzygapophysial facet. The new El Montsec bird is clustered with other enantiomithine birds by the following unambiguous synapomorphies: prominent bicipital crest of humerus, cranioventrally projected; convex lateral margin of the coracoid; supracoracoid nerve foramen of coracoid opening into an elongate furrow medially and separated from the medial margin by a thick bony bar; dorsal fossa on the coracoid; metacarpal III longer than metacarpal II.
39. E. N. Kurochkin, Russ. Acad. Sci. Paleontol. Inst. (special issue) (1996); L. D. Martin, in Perspectives in Ornithology, A. H. Brush and G. A. Clark Jr., Eds. (Cambridge Univ. Press, Cambridge, 1983), pp. 291-338; in L'Evolution des Oiseaux d'Après te Témoignage des Fossiles, C. Mourer-Chauviré, Ed. (Doc. 99, Laboratoires de Geologie, Lyon, France, 1987), pp. 9-19.
40. E. N. Kurochkin, Russ. Acad. Sci. Paleontol. Inst. (special issue) (1996); L. D. Martin, in Perspectives in Ornithology, A. H. Brush and G. A. Clark Jr., Eds. (Cambridge Univ. Press, Cambridge, 1983), pp. 291-338; in L'Evolution des Oiseaux d'Après te Témoignage des Fossiles, C. Mourer-Chauviré, Ed. (Doc. 99, Laboratoires de Geologie, Lyon, France, 1987), pp. 9-19.
41. E. N. Kurochkin, Russ. Acad. Sci. Paleontol. Inst. (special issue) (1996); L. D. Martin, in Perspectives in Ornithology, A. H. Brush and G. A. Clark Jr., Eds. (Cambridge Univ. Press, Cambridge, 1983), pp. 291-338; in L'Evolution des Oiseaux d'Après te Témoignage des Fossiles, C. Mourer-Chauviré, Ed. (Doc. 99, Laboratoires de Geologie, Lyon, France, 1987), pp. 9-19.
42. L. M. Chiappe, Cour. Forschungsinst. Senckenb. 181, 55 (1995); S. L. Olson, in Avian Biology, D. Famer, J. King, K. C. Parkes, Eds. (Academic Press, New York, 1985), vol. 8; A. Feduccia [Science 267, 637 (1995)] used the paraphyletic "Sauriurae," although in his phylogenetic diagram he clearly specified that Enantiornithes are closer to modern birds than to Archaeopteryx.
43. L. M. Chiappe, Cour. Forschungsinst. Senckenb. 181, 55 (1995); S. L. Olson, in Avian Biology, D. Famer, J. King, K. C. Parkes, Eds. (Academic Press, New York, 1985), vol. 8; A. Feduccia [Science 267, 637 (1995)] used the paraphyletic "Sauriurae," although in his phylogenetic diagram he clearly specified that Enantiornithes are closer to modern birds than to Archaeopteryx.
44. L. M. Chiappe, Cour. Forschungsinst. Senckenb. 181, 55 (1995); S. L. Olson, in Avian Biology, D. Famer, J. King, K. C. Parkes, Eds. (Academic Press, New York, 1985), vol. 8; A. Feduccia [Science 267, 637 (1995)] used the paraphyletic "Sauriurae," although in his phylogenetic diagram he clearly specified that Enantiornithes are closer to modern birds than to Archaeopteryx.
45. J. L. Sanz and J. F. Bonaparte, in Papers in Avian Paleontology Honoring Pierce Brodkorb, K. E. Campbell, Ed. (Sci. Ser. 36, Natural History Museum of Los Angeles County, Los Angeles, 1992), pp. 39-49.
46. A. Elzanowski, Palaeontol. Pol. 42, 147 (1981).
47. L. D. Martin and O. Bonner, Auk 94, 787 (1977).
48. A. Chinsamy, L. M. Chiappe, P. Dodson, Nature 368, 196 (1994); Paleobiology 21, 561 (1995).
49. A. Chinsamy, L. M. Chiappe, P. Dodson, Nature 368, 196 (1994); Paleobiology 21, 561 (1995).
50. The age of the La Pedrera de Rúbies Lithographic Limestones Formation is regarded as Upper Berriasian-Lower Valanginian on the basis of ostracods [P. Brenner, W. Geldmacher, R. Schroeder, Neues Jahrb. Geol. Palaeontol. Monatsh. 9, 513 (1974)]. Nevertheless, it could be somewhat younger (Upper Hauterivian-Lower Barremian), on the basis of a work in progress on its charophytes [C. Martín-Closas and N. López-Morón, in (37), pp. 29-31].
51. The age of the La Pedrera de Rúbies Lithographic Limestones Formation is regarded as Upper Berriasian-Lower Valanginian on the basis of ostracods [P. Brenner, W. Geldmacher, R. Schroeder, Neues Jahrb. Geol. Palaeontol. Monatsh. 9, 513 (1974)]. Nevertheless, it could be somewhat younger (Upper Hauterivian-Lower Barremian), on the basis of a work in progress on its charophytes [C. Martín-Closas and N. López-Morón, in (37), pp. 29-31].
52. X. Martínez-Delclòs, Ed., Montsec and Montral-Alcover, Two Konservat-Lagerstätten (Catalonia, Spain), Field Trip Guide Book (Institut d'Estudis Ilerdencs, Lleida, Spain, 1995).
53. A. Lacasa-Ruíz, Terra Nova (UK) 1, 45 (1989); A. Lacasa-Ruíz, Estud. Geol. (Madrid) 45, 417 (1989). The new El Montsec bird is not considered cogeneric with Noguerornis on the basis of differences in the furcula and humerus, aside from the size (Noguerornis is an adult, being smaller than the nestling specimen). In addition to W. gonzalezi, Ilerdopteryx viai was based on an isolated feather [A. Lacasa, in Les Calcàries Litogràfiques del Cretaci Inferior del Montsec, Deu Anys de Campanyes Paleontològiques, X. Martínez-Delclòs, Ed. (Institut d'Estudis Ilerdencs, Lleida, Spain, 1991), pp. 147-150]. We believe, however, that the holotype of Ilerdopteryx viai is not diagnostic for a specific status and regard this taxon as a nomen dubium.
54. A. Lacasa-Ruíz, Terra Nova (UK) 1, 45 (1989); A. Lacasa-Ruíz, Estud. Geol. (Madrid) 45, 417 (1989). The new El Montsec bird is not considered cogeneric with Noguerornis on the basis of differences in the furcula and humerus, aside from the size (Noguerornis is an adult, being smaller than the nestling specimen). In addition to W. gonzalezi, Ilerdopteryx viai was based on an isolated feather [A. Lacasa, in Les Calcàries Litogràfiques del Cretaci Inferior del Montsec, Deu Anys de Campanyes Paleontològiques, X. Martínez-Delclòs, Ed. (Institut d'Estudis Ilerdencs, Lleida, Spain, 1991), pp. 147-150]. We believe, however, that the holotype of Ilerdopteryx viai is not diagnostic for a specific status and regard this taxon as a nomen dubium.
55. A. Lacasa-Ruíz, Terra Nova (UK) 1, 45 (1989); A. Lacasa-Ruíz, Estud. Geol. (Madrid) 45, 417 (1989). The new El Montsec bird is not considered cogeneric with Noguerornis on the basis of differences in the furcula and humerus, aside from the size (Noguerornis is an adult, being smaller than the nestling specimen). In addition to W. gonzalezi, Ilerdopteryx viai was based on an isolated feather [A. Lacasa, in Les Calcàries Litogràfiques del Cretaci Inferior del Montsec, Deu Anys de Campanyes Paleontològiques, X. Martínez-Delclòs, Ed. (Institut d'Estudis Ilerdencs, Lleida, Spain, 1991), pp. 147-150]. We believe, however, that the holotype of Ilerdopteryx viai is not diagnostic for a specific status and regard this taxon as a nomen dubium.
56. J. Farris, Hennig 86 References: Documentation for Version 1.5 (privately published, 1988).
57. Sixteen neonate specimens of the following taxa were examined: Burhinus oecdinemus (Charadriiformes, three specimens), Ciconia ciconia (Ciconiformes, two specimens), Columba palumbus (Columbiformes, two specimens), Clamator glandarius (Cuculiformes, one specimen), Alectoris rufa (Galliformes, two specimens), Picus viridis (Piciformes, two specimens), Pica pica (Passeriformes, two specimens), and Athene noctua (Strigiformes, two specimens). These specimens belong to the skeletal collection of the Unidad de Arqueozoología from the Universidad Autónoma de Madrid. All examined specimens presented the pattern of foramina or grooves discussed in Fig. 4.
58. We thank J. I. González, who found the specimen and kindly made it available for study; L. Witmer for comments on an early version of the manuscript; and S. Copeland, P. Dandonoli, and D. Treon for general editorial suggestions. Photographs used for Figs. 1 and 2 were taken by G. F. Kurtz and those for Fig. 4 by M. Bautista. This research was supported by the Institut d'Estudis Ilerdencs, the Junta de Comunidades de Castilla-La Mancha, DGICYT (Promoción General del Conocimiento, PB93-0284), the European Union (Human Capital and Mobility Program, CHRXCT930164), and grants to L.M.C. from NSF (DEB-9407999), J. S. Guggenheim Foundation, The Dinosaur Society, and the Frank M. Chapman Memorial Fund (American Museum of Natural History).