The phylogenetic relationships of the early Tertiary Primoscenidae and Sylphornithidae and the sister taxon of crown group piciform birds

Abstract

The phylogenetic relationships of the early Tertiary Primoscenidae and Sylphornithidae are, for the first time, evaluated in a cladistic context. Both taxa include small arboreal birds with a permanently (Primoscenidae) or facultatively (Sylphornithidae) retroverted fourth toe. Primoscenidae were hitherto considered to be most closely related to either woodpeckers and allies (Piciformes) or to songbirds (Passeriformes), whereas the Sylphornithidae were classified into the roller-kingfisher-hornbill assemblage (“Coraciiformes”). Analysis of 56 morphological characters supports monophyly of a clade including Sylphornithidae and crown group Piciformes and results in sister group relationship between Passeriformes and a clade including Primoscenidae and the early Miocene Zygodactylidae. However, an analysis in which the search was constrained to trees supporting piciform affinities of the Primoscenidae resulted in trees that were only five steps longer than those from the primary analysis. The character evidence for each hypothesis is discussed. The systematic position of the Primoscenidae appears to be connected to the identity of the sister taxon of crown group Piciformes, as the primary search indicated Upupiformes (hoopoes and wood-hoopoes) and Bucerotiformes (hornbills) as sister taxa of Piciformes, whereas the constrained search resulted in sister group relationship between Coliiformes (mousebirds) and Piciformes. Songbirds do not show the slightest indication of a zygodactyl foot but in these birds the hindtoe is greatly elongated, an alternative strategy to increase the grasping capabilities of the foot. If Passeriformes are indeed the sister group of the clade (Primoscenidae + Zygodactylidae), these birds would be an example that, in closely related taxa, selection towards the same functional demands can result in entirely different morphological specializations.

Appendix I

Character descriptions.

1. Skull, completely ossified septum nasale: absent (0), present (1). The ossified nasal septum of few passerines (e.g., Rupicola sp., Cotingidae) which are deeply nested within Passeriformes (e.g., Barker et al. 2002) is here considered to be an autapomorphy of these taxa.

2. Os lacrimale, descending process greatly enlarged and medially expanded: no (0), yes (1).

3. Os ectethmoidale, greatly expanded, plate-like, with dorsal margin largely fused with frontals: no (0), yes (1).

4. Processus postorbitales strongly elongated, touching (or nearly touching) the jugals: no (0), yes (1).

5. Os palatinum and os pterygoideum fused: yes (0), no (1). Separated palatines and pterygoids are an apomorphy of neognathous birds.

6. Columella with large, hollow, bulbous basal and footplate area which exhibits a large fenestra on one side (Feduccia 1977): no (0), yes (1). The presence of this character in some suboscine Passeriformes (Feduccia 1974) is here considered autapomorphic for these birds (see Mayr et al. 2003).

7. Pygostyle with large, shield-like discus pygostyli with sharply defined, ridge-like lateral margins (Mayr et al. 2003: fig. 3): no (0), yes (1).

8. Number of praesacral vertebrae (all vertebrae cranial to synsacrum): more than 19 (0), 19 (1).

9. Furcula, extremitas omalis: not as follows (0), widened, with blunt or slightly convex end and short processus acrocoracoideus and processus acromialis (1), with processus acrocoracoideus and processus acromialis well-developed and wide, forming a plate-like extremitas omalis of roughly triangular shape (2). The extremitas omalis of the furcula is very similar in Upupiformes, Bucerotiformes, and Galbulae (see Höfling and Alvarenga 2001).

10. Furcula, apophysis furculae: absent (0), present, rod-like (1), well-developed, blade-like (2). Within Galbulae, a blade-like apophysis furculae is present in the Bucconidae but absent in the Galbulidae. The absence of an apophysis furculae in Eurystomus (Coraciidae) is here considered autapomorphic for that taxon, because an apophysis furculae is present in other Coraciidae and in the Brachypteraciidae.

11. Coracoid, processus procoracoideus well-developed, strap-like: no (0), yes (1). There are two types of coracoid as candidates for the coracoid of Sylphornis (Mourer-Chauviré 1988; Mayr 1998) but in both the processus procoracoideus is greatly reduced.

12. Coracoid, extremitas sternalis with notch on margo medialis (Mayr et al. 2003: fig. 4): no (0), yes (1). Mayr et al. (2003) listed the presence of this notch as an apomorphy of the taxon (Galbulae + Pici).

13. Coracoid, facies articularis sternalis dorso-ventrally very wide: no (0), yes (1).

14. Scapula, acromion distinctly bifurcate, i.e. with an additional ventro-medial process (Mayr 1998: fig. 16; Höfling and Alvarenga 2001: fig. 8): no (0), yes (1).

15. Caudal margin of sternum: with four notches (0), with two notches (1). Within Passeriformes, a four-notched sternum occurs in some species of Rhinocryptidae and Formicariidae (e.g., Feduccia and Olson 1982). As these taxa are deeply nested within Suboscines (e.g., Ericson et al. 2003), it is assumed that this condition is derived within Passeriformes and that the stem species of Passeriformes had a two-notched sternum.

16. Humerus, far ventro-distally extending, large fossa musculi brachialis which is situated on the far medial side of the bone and has a weakly developed ventral margin (Fig. 4): no (0), yes (1). Within Galbulae, this character is present in the Galbulidae but absent in the Bucconidae.

17. Ulna distinctly exceeding humerus in length: no (0), yes (1).

18. Ulna, cotyla ventralis greatly enlarged: no (0), yes (1).

19. Ulna, proximal end, olecranon very long, narrow, and pointed (Mayr 1998: fig. 10H): no (0), yes (1).

20. Carpometacarpus, ventral part of trochlea carpalis cranio-caudally narrow and proximo-distally elongate, slanting caudally towards the midline of the caudal side; fovea carpalis caudalis marked: no (0), yes (1).

21. Carpometacarpus, processus dentiformis (Fig. 5): absent (0), present (1). The presence of a well-developed processus dentiformis in Uratelornis (Brachypteraciidae) is here considered autapomorphic for the Brachypteraciidae because a processus dentiformis is absent in Coraciidae and fossil stem group rollers (Mayr and Mourer-Chauviré 2000). Within Galbulae, a processus dentiformis is well-developed in Galbula ruficauda and Monasa nigrifrons but absent in Chelidoptera tenebrosa and Notharchus macrorhynchus.

22. Carpometacarpus, processus intermetacarpalis (Fig. 5): absent or small (0), well-developed, reaching os metacarpale minus (1), well-developed, fused with os metacarpale minus (2). The fusion of the processus intermetacarpalis with the os metacarpale minus in the Brachypteraciidae is here considered to be autapomorphic for that taxon because this feature is absent in the Coraciidae and fossil stem group rollers (Mayr and Mourer-Chauviré 2000). This character was coded as ordered.

23. Carpometacarpus, proximal end of os metacarpale minus with distinct, ventrally protruding tubercle (Mayr and Mourer-Chauviré 2000: fig. 10): no (0), yes (1).

24. Carpometacarpus, os metacarpale minus distally protruding distinctly beyond os metacarpale majus (Fig. 5): no (0), yes (1).

25. Carpometacarpus, distal end of os metacarpale minus strap-like, dorso-ventrally wide, and more or less strongly tilted dorso-ventrally; articulation surface for digitus minor forming a marked knob (Fig. 5): no (0), yes (1).

26. Phalanx proximalis digiti majoris, proximal end with large, proximally directing process on ventral side (Fig. 5): no (0), yes (1).

27. Pelvis, foramen ilioischiadicum caudally closed: no (0), yes (1). A caudally closed foramen ilioischiadicum is an apomorphy of neognathous birds.

28. Pelvis, mid-section of cristae iliacae dorsales greatly reduced: no (0), yes (1).

29. Pelvis, processus terminalis ischii very narrow and slender, touching pubis at an angle of 45°-90°, fenestra ischiopubica very wide: no (0), yes (1).

30. Femur, distal end thickened, tuberculum musculi gastrocnemialis lateralis large: no (0), yes (1).

31. Femur, pneumatic foramen at cranio-lateral side of proximal end: absent (0), present (1).

32. Tibiotarsus, both cristae cnemiales and crista patellaris forming a ridge which circumscribes a groove on the cranial side of the bone: no (0), yes (1). The occurrence of state 1 in the Dendrocolaptidae (Passeriformes) is here considered to be an autapomorphy of this taxon which is deeply nested within Passeriformes (e.g., Ericson et al. 2003).

33. Tibiotarsus, proximal end with ridge opposite crista fibularis: no (0), yes (1).

34. Tarsometatarsus greatly elongated and slender, apart from tibiotarsus longest limb element, exceeding humerus in length: no (0), yes (1). The greatly elongated tarsometatarsus of most Brachypteraciidae is here considered to be derived within rollers because it is absent in Coraciidae and fossil stem group rollers (Mayr and Mourer-Chauviré 2000). No complete humerus of the Sylphornithidae is known, but the preserved remains indicate that it was shorter than the tarsometatarsus.

35. Tarsometatarsus, arcus extensorius (ossified retinaculum extensorium tarsometatarsi): absent (0), present (1).

36. Tarsometatarsus, hypotarsus passing into a well-developed crista medianoplantaris; fossa parahypotarsalis medialis very marked and proximal part of margo medialis forming a sharp ridge: no (0), yes (1).

37. Tarsometatarsus, hypotarsus, ossified canal for tendon of musculus flexor digitorum longus: absent (0), present (1), present, cristae medialis et lateralis delimiting marked sulcus plantar to this canal (2). Within Galbulidae, this canal is open in Galbula ruficauda but closed in G. cyanescens (Simpson and Cracraft 1981: fig. 6B); within Bucconidae, it is open in Chelidoptera tenebrosa and Notharchus macrorhynchus but closed in Monasa nigrifrons.

38. Tarsometatarsus, hypotarsus, tendon of musculus flexor hallucis longus: not as follows (0), situated in a marked sulcus which is medially bordered by a prominent crista lateralis hypotarsi (Fig. 3) (1), enclosed in a bony canal (2). Homology of a hypotarsal canal in the Caprimulgidae is uncertain.

39. Tarsometatarsus, well-developed crista plantaris lateralis: absent (0), present (1).

40. Trochlea metatarsi II, well-developed, plantarly projecting process (Fig. 3): present (0), absent (1).

41. Trochlea metatarsi II much shorter than trochlea metatarsi III: yes (0), no (1).

42. Trochlea metatarsi IV (Fig. 3): not as follows (0), with plantarly projecting wing-like flange (typical of semi-zygodactyl feet) (1), with large trochlea accessoria (typical for fully zygodactyl feet) which is not separated by a furrow from the trochlea metatarsi IV and does not reach beyond the midst of the trochlea metatarsi III (2), with large trochlea accessoria which is separated by a furrow from the trochlea metatarsi IV but does not reach beyond the midst of the trochlea metatarsi III (3), with large, distally elongated trochlea accessoria which is separated by a furrow from the trochlea metatarsi IV and reaches beyond the midst of the trochlea metatarsi III (4). In all known specimens of the Sylphornithidae the trochlea metatarsi IV is damaged but the preserved part indicates that it merely bore a plantarly projecting wing-like flange. Within the Galbulae a furrow between the trochlea accessoria and the trochlea metatarsi IV is present in Galbulidae but absent in Bucconidae. Presence of a furrow between the trochlea accessoria and the trochlea metatarsi IV was listed by Mayr (1998:53 ff.) as synapomorphy of a taxon including Primoscenidae, Zygodactylidae, and Pici; a distally elongated trochlea accessoria was considered to be a synapomorphy of a taxon including Zygodactylidae, and Pici. This character was coded as ordered.

43. Tarsometatarsus, canalis interosseus distalis: present (0), absent (1).

44. Tarsometatarsus facies articularis metatarsalis situated on medial margin of shaft (characteristic of pamprodactyl feet in which the hind toe can be turned forwards): no (0), yes (1).

45. Hallux, proximal phalanx with proximal end greatly widened (Mayr 1998: fig. 20F): no (0), yes (1).

46. Hallux greatly elongated, proximal phalanx about two times longer than proximal phalanx of third toe: no (0), yes (1).

47. Second and third phalanx of fourth toe greatly abbreviated, measuring less than half the length of the fourth phalanx: no (0), yes (1).

48. Third and fourth toe coalescent at least over length of basal phalanx of third toe: no (0), yes (1). Within Bucerotidae this character is absent in Bucorvus but it cannot be conclusively shown a priori whether this absence is plesiomorphic or apomorphic. The presence of this character in few Passeriformes (e.g. Rupicola, Cotingidae), however, unquestionably is a derived condition.

49. Tendon of musculus extensor carpi ulnaris inserting on os metacarpale minus (see Stegmann 1965 - usually this tendon inserts on the os metacarpale majus): no (0), yes (1).

50. Musculus ambiens: present (0), absent (1); (after McKitrick 1991). The musculus ambiens is present in most taxa outside those included in this study.

51. Musculus iliofemoralis externus (“D” muscle in the formula of George and Berger 1966: Tab. IX.1): present (0), absent (1); (after Steinbacher 1937; George and Berger 1966; Maurer and Raikow 1981; Berman and Raikow 1982; McKitrick 1991).

52. Musculus caudofemoralis, pars pelvica (“B” muscle in the formula of George and Berger 1966: Tab. IX.1): present (0), absent (1); (after McKitrick 1991).

53. Musculus flexor hallucis longus: not as follows (0); origin with three heads, iliofibularis tendon passes lateral to lateral head (1) (Swierczewski and Raikow 1981; Raikow and Cracraft 1983). According to Swierczewski and Raikow (1981:473) three heads occur in “most Passerines, but in that case the iliofibularis tendon passes medial to the lateral head, while in Piciformes it passes lateral to the lateral head. The condition in the two orders is therefore probably not homologous.”

54. Musculus flexor hallucis longus: tendon supplying hallux (0), tendon not supplying hallux (1); (after George and Berger 1966; Maurer and Raikow 1981).

55. Tendon of musculus flexor hallucis longus supplies digits I, II, and IV (deep flexor tendons type VI, see George and Berger 1966:448; Simpson and Cracraft 1981): no (0), yes (1).

56. Villi at the bases of the basalmost downy barbules of the breast feathers: absent (0), present (1); (after Brom 1990).