The 122(4):1049–1054, 2005 © The American Ornithologists’ Union, 2005. Printed in USA.


PALEOGENE AND THE RADIATION OF MODERN Hq F. Jrx1 Division of Birds, MRC-116, National Museum of Natural History, Smithsonian Institution, Washington, D.C. 20013, USA

M birds arose mainly in 1989, Mayr and Manegold 2004), and others. the Period (1.8–23.8 mya), and mod- fossils also document diverse extinct ern species mainly in the Plio- branches of the neornithine tree, ranging from (0.08–5.3 mya). Neogene birds generally large pseudotoothed to giant fl ightless resemble modern taxa, and those that cannot land birds to small zygodactyl perching birds be a ributed to a modern genus or species (Ballmann 1969, Harrison and Walker 1976, can usually be placed in a modern family with Andors 1992). a fair degree of confi dence (e.g. Becker 1987, Before the Paleogene, fossils of putative neor- Olson and Rasmussen 2001). Fossil birds from nithine birds are sparse and fragmentary (Hope earlier in the can be more challeng- 2002), and their phylogenetic placement is all ing to classify. The fossil birds of the Paleogene the more equivocal. The Paleogene is thus a cru- (23.8–65.5 mya) are clearly a ributable to the cial time period for understanding the history of Neornithes (modern birds), and the earliest diversifi cation of birds, particularly with respect well-established records of most traditional to the deeper branches of the neornithine tree. orders and families of modern birds occur then. But the fossils tend to be primitive and more Eq~ Nnymx Ezu diffi cult to seat phylogenetically within the Neornithes (Dyke and van Tuinen 2004). One ornithologist who has energetically Not a few early Paleogene fossils have been taken up the challenge of Paleogene birds said to exhibit a mosaic of characters associ- is Gerald Mayr of the Forschungsinstitut ated with two or more traditional families or Senckenberg in Frankfurt, Germany. Mayr has orders (e.g. Peters 1992, Feduccia 1999, Mayr published more than 70 papers on Paleogene 2003a). An excellent example is an birds and related topics since 1998 (for a recent referred to the Psi aciformes that lacks summary, see Mayr 2005a). Notably, last the specialized skull of parrots (Mayr 2005a). he described a , Eurotrochilus Paleontologists sometimes resort to describing inexpectatus, from the early of primitive fossils as “petrel-like” or “hoopoe- (Mayr 2004). Fossils with humming- like” (for instance) without referring them to bird-like characters had been known from the corresponding modern families (e.g. Houde the Oligocene of Eurasia, but only from wing and Olson 1992; Feduccia and McPherson 1993; bones that appeared to be very primitive and Mayr 2000a, 2003b). Nevertheless, the primitive perhaps transitional between fossils of the Paleogene provide the earliest fi rm and other apodiform birds (Karhu 1999, Mayr records of such diverse modern radiations as 2003a). Eurotrochilus inexpectatus is based on ratites (Houde 1988), (Mourer-Chauviré a well-preserved fossil skeleton with striking 1987, Peters 1992), waterfowl (Ericson 1997, similarities to modern hummingbirds, includ- Olson 1999, Dyke 2001), ibises (Peters 1983), ing tiny size; long, thin bill; short humerus; and (see Clarke et al. 2003), galliforms deep carina of the sternum. This was a bird that (Mourer-Chauviré 1992, Mayr 2000b, Dyke and hovered to sip nectar from fl owers, and it did Gulas 2002), (Mourer-Chauviré et al. so approximately 30–35 mya in Germany. On page 1055 of this issue of The Auk, Mayr (2005b) introduces a genus and species of tiny 1E-mail: [email protected] barbet-like bird from the near-shore marine 1049 1050 Overview [Auk, Vol. 122 deposits of Frauenwiler, Germany, the same lo- landmasses, particularly for the Eocene and cality where the fossil hummingbird was found. , is a longstanding obstacle to interpre- The new taxon is known from a single associ- tation of the biogeographic history of birds. ated skeleton lacking the skull. The fossil is not suffi ciently well preserved to support a detailed S~xyrynhx Fxxnqx cladistic analysis of its evolutionary relation- ships, though it shows a specialized morphol- Phylogenetic analysis.—Revisionary work in ogy of the distal end of the tarsometatarsus and systematics of fossil birds is now commonly other characters diagnostic of the Pici (wood- based on cladistic character analysis, and taxo- peckers, Picidae; honeyguides, Indicatoridae; nomic descriptions of new taxa are sometimes and barbets and toucans, Rhamphastidae). In accompanied by such analyses (e.g. Bourdon other characters, it appears to be plesiomorphic et al. 2005). Paleontologists prefer to work with with respect to all modern members of the Pici, complete associated skeletons and multiple and Mayr concludes that it is probably outside individuals of each terminal taxon, but oV en the crown group defi ned as the common ances- make do with isolated or fragmentary speci- tor of all modern species and its descendants. mens. To the extent that confi dence is judged by The fossil is thus the oldest substantial record of the quantity of supporting character evidence, the Pici, if the defi nition of Pici is expanded to it follows that confi dence in the phylogenetic accommodate a stem group. Postcranial bones placement is more variable for fossils than for from the of Europe have also been re- modern birds. Interpretations of the fossil re- ferred to the barbets (Ballmann 1969). The fossil cord need to take that variability into account. record thus supports a deep history for the Pici Considerable eff ort is being devoted to re- in the Old World, in consonance with recent solving the deeper branches of phylogeny for molecular evidence (Johansson and Ericson the Neornithes through DNA sequencing and 2003, Moyle 2004). coding of morphological characters in modern The new hummingbird and piciform bird birds (Livezey and Zusi 2001, CracraV et al. are just two recent additions to the very rich 2004). Paleogene fossils appear to represent Paleogene fossil record of Europe (Mlíkovský diverse early stages in the development of 2002, Mayr 2005a). Mayr’s work has empha- those very clades. Consequently, there is great sized the Middle Eocene oil shales of Messel, potential for reciprocal illumination between where complete but oV en crushed skeletons modern and fossil phylogenetic evidence. On represent diverse land and water birds (Peters the other hand, the current lack of consensus on 1988, Mayr 2005a). Other important Paleogene the higher-level relationships of modern birds sites of Europe include the Upper Eocene to is a hindrance to interpretation of the fossil re- Lower Oligocene fi ssure fi lls of Quercy in cord. The polarity and frequency of homoplasy France (Mourer-Chauviré 1982); the Lower for osteological characters of Paleogene fossils Eocene London Clay, especially the exposures could be be er understood in the context of a at Walton-on-the-Naze, United Kingdom robust phylogenetic hypothesis. (Feduccia 1999); and the Upper Paleocene Phylogenetic analyses at lower taxonomic to Lower Eocene marine deposits of the Fur levels (within orders and families) have gener- Formation in Denmark (see Kristoff ersen 2002). ally been more successful for birds. Phylogenetic All told, Europe boasts a richer Paleogene results are always richer when cast in the light of avifauna in terms of number and taphonomic the fossil record, as in the examples of the bar- variety of fossil localities and diversity of avian bets, hummingbirds, and rollers discussed here. taxa compared with other continents. One as- Stem versus crown groups.—Use of fossils to sessment estimated that 55 families of birds calibrate molecular rates has brought to promi- are represented in the major localities of the nence the distinction between crown and stem European Paleogene (Feduccia 1999). Second to group fossils. Crown group fossils can provide Europe is , where the Green River minimum ages of diversifi cation within modern and Willwood formations provide important clades, but stem group fossils may be older than early Eocene records of approximately 25 fami- those clades. In the past, stem group fossils that lies of birds. The dearth of similarly productive are classifi ed in modern orders and families Paleogene localities in and on southern of birds may have been used unwi ingly as October 2005] Overview 1051 calibration points for the corresponding crown with affi nities to the African , groups, providing age estimates that are errone- South American serieamas, and Australian ously too old. Simple misidentifi cation of fossils frogmouths). Avian taxa were probably more can also invalidate calibrations. Therefore, it is widely distributed during the Eocene, when important to begin taking the potential for error global climate was equable. Certainly, there in phylogenetic placement of fossils into ac- was greater faunal similarity between Europe count when performing rate calibrations (Graur and North America, which were connected by and Martin 2004, van Tuinen and Dyke 2004). land in the early Eocene (Blondel and Mourer- An example of reconciliation between Chauviré 1998, Mayr and Weidig 2004). The fossil and molecular evidence is that of the retreat of some taxa to the tropics and sub- Madagascan ground rollers, Brachypteraciidae. tropics is partly explained by climatic cooling Eocene fossils from the Messel oil shales had beginning in the Oligocene. Diff erentiation of been classifi ed as members of the family. the Eurasian and North American avifaunas Kirchman et al. (2001), however, found levels of took place in the Oligocene through Miocene molecular divergence between ground rollers as the continents became isolated (Blondel and and true rollers (Coraciidae) that are too low Mourer-Chauviré 1998). to support an Eocene origin of ground rollers. Debate continues over the biogeographic con- Independently, Mayr and Mourer-Chauviré text of diversifi cation of the Neornithes. The high (2000, 2003) performed a cladistic character number of early Paleogene birds that appear to analysis that supported removing the fossils be basal to modern radiations suggests that the from the Brachypteraciidae and placing them diversifi cation of many crown groups came basal to Brachypteraciidae + Coraciidae. aV er those epochs (Mayr 2005a). Biogeographic analysis of the same crown groups supports the A{nzq D~rnhx alternative hypothesis that they arose earlier in the in Gondwana and were initially radiation.—The weak molecular dispersed by continental driV (CracraV 2001). genetic signal found so far for relationships Questionable molecular-rate calibrations favor among many higher-level taxa of birds could be the la er hypothesis, which is otherwise in explained if there was an early, explosive radia- confl ict with the fossil evidence (Feduccia 2003, tion of birds into diverse ecological niches. Just Mayr 2005a). such an explosion has been hypothesized based Grande Coupure.—The Grande Coupure mark- on the early Paleogene fossil record of Europe ing the Eocene–Oligocene transition (33.7 mya) and North America (Feduccia 1995, 2003). In was a time of great faunal turnover in European Europe, where the record is best, there were , and apparently in birds as well. more family-level taxa of birds in the Eocene Mayr’s (2005a) intensive study of Paleogene birds than at present (Blondel and Mourer-Chauviré has lead him to conclude that there were no neor- 1998). By contrast, the global fossil record for nithines in family-level crown groups in Europe Cretaceous Neornithes is surprisingly slim—49 before the Grande Coupure. Fossils that belong bones that are for the most part too fragmen- within family-level crown groups begin to appear tary for confi dent identifi cation (Hope 2002). in the Oligocene. The implication is that most or Fountaine et al. (2005) studied the quality of the all of the diversity within modern families of fossil record of birds and found that, birds has evolved since the Grande Coupure. when extinct non-neornithine taxa are included, Paleontologists concur that the Passeriformes it has grown to be quite respectable. It is thus originated in the south and invaded the North- uncontroversial that the Neornithes became ern Hemisphere in the late Eocene or early much more diverse and ecologically dominant Oligocene (Olson 1988, Mourer Chauvire 1995). aV er the Cretaceous–Tertiary event, The earliest fossils in Europe are from the Lower but there is still lively debate over just how Oligocene of Frauenwiler and nearby France many lineages originated in the Cretaceous and (Mayr and Manegold 2004). Fossil passerines survived that event (CracraV 2001). do not become prevalent until the Miocene. .—Many Paleogene fossil birds Food competition with passerines is believed to of Europe have their closest modern relatives have been a factor in the extinction of diverse on southern landmasses today (e.g. species small nonpasserine birds that had been present 1052 Overview [Auk, Vol. 122 in the Paleogene of the Northern Hemisphere Lnyyz Cny (Mayr 2005b, c). Ax, A. V. 1992. Reappraisal of the Eocene Szrr~ groundbird Diatryma (Aves: Anserimorphae). Pages 109–126 in Papers in Avian Paleontology We have a picture of the Paleogene of Europe Honoring Pierce Brodkorb (K. E. Campbell, in which fl owers are pollinated by humming- Jr., Ed.). Natural History Museum of Los birds, mosaic psi aciform birds that lack the spe- Angeles County Science , no. 36. cialized heads of parrots fl y about, and what is Bqqr, P. 1969. Die Vögel aus der now the most species-rich order of birds arrives altburdigalen Spaltenfüllung von Wintershof on the scene quite late. The geographic distribu- bei Eichstä in Bayern. Zi eliana 1:5–61. tions and phenotypes of some Paleogene birds Bhp, J. J. 1987. Neogene Avian Localities of would be beyond our capacity to imagine or to North America. Smithsonian Institution reconstruct without the solid evidence of fossils. Press, Washington, D.C. Careful study of the fossils has lead to the Bqq, J., C. Mz-Cmz{n”. 1998. hypothesis that the diversity within traditional Evolution and history of the western modern families of birds arose aV er the Eocene. Palaearctic avifauna. Trends in and Although the record is strongest for Europe, Evolution 13:488–492. the hypothesis also applies to North America, Bz, E., B. B‚n, M. Ihm. 2005. where the Eocene avifauna is very similar. Earliest African neornithine bird: A new Indeed, Mayr indicates that his hypothesis may species of Prophaethontidae (Aves) from the apply globally. This is a signifi cant insight that Paleocene of Morocco. Journal of can be further tested with morphological, mo- Paleontology 25:157–170. lecular, and fossil data. Cqp, J. A., E. B. Oqn{, P. Pzy. 2003. Perhaps the greatest unsolved problem in Description of the earliest fossil avian systematics is the evolutionary relation- from and fi rst Paleogene ships among modern higher-level taxa. Thanks vertebrate locality of Tierra Del Fuego, to collaboration among systematists to resolve Argentina. American Museum Novitates the avian tree of life, large morphological and 3423:1–18. molecular character matrices for neornithine Chy, J. 2001. Avian evolution, Gondwana birds are nearing completion (Livezey and Zusi biogeography and the Cretaceous–Tertiary 2001, CracraV et al. 2004). Smaller molecular mass . Proceedings of the data sets for subclades of Neornithes are appear- Royal Society of London, Series B 268: ing regularly. The resulting trees become much 459–469. more interesting if they can be correlated with a Chy, J., F. K. Bp, M. Bz, J. time scale and a fossil history. Adding osteologi- Hxmr, G. J. D~p, J. Fnxyn, S. cal characters as a data partition in molecular Syq~, A. Cngnx, P. Shmnpq, P. Bx, phylogenetic databases would permit interac- ymx. 2004. Phylogenetic relation- tive analyses of genetic, morphological, and ships among modern birds (Neornithes): fossil evidence. Some of the odd phenotypes of Toward an avian tree of life. Pages 468–489 in the Paleogene might then be placed on the new Assembling the Tree of Life (J. CracraV and phylogenetic trees that are emerging. The rich M. J. Donoghue, Eds.). Oxford University Paleogene fossil record provides a perspective Press, Oxford. on the evolutionary history of birds that cannot D~p, G. J. 2001. The fossil waterfowl (Aves: be reconstructed from studies of modern taxa ) from the Eocene of England. alone. I urge greater eff ort to fully integrate that American Museum Novitates 3354:1–15. record in our modern reassessment of avian D~p, G. J., B. E. Gzqx. 2002. The fossil gal- evolutionary history. liform bird Paraortygoides from the Lower Eocene of the United Kingdom. American Ahp|qryx Museum Novitates 3360:1–14. D~p, G. J., G. M~. 1999. Did parrots ex- I thank G. Mayr and S. L. Olson for comments ist in the Cretaceous period? Nature 399: on the manuscript. 317–318. October 2005] Overview 1053

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