Taxonomy, Phylogeny, and Biogeography of the Andean Hummingbird Genera Coeligena LESSON, 1832; Pterophanes GOULD, 1849; Ensifera LESSON 1843; and Patagona GRAY, 1840 (Aves: Trochiliformes) Dissertation zur Erlangung des Doktorgrades (Dr. rer. nat.) der Mathematisch-Naturwissenschaftlichen Fakultät der Rheinischen Friedrich-Wilhelms-Universität Bonn vorgelegt von Carlos Sánchez Osés aus Valencia, Venezuela Bonn, August 2003 Angefertigt mit Genehmigung der Mathematisch-Naturwissenschaftlichen Fakultät der Rheinischen Friedrich-Wilhelms-Universität Bonn 1. Referent: Prof. Dr. K.-L. Schuchmann 2. Referent: Prof. Dr. W. Böhme Tag der Promotion: 26. September 2003 Contents Introduction 1 Materials and Methods 6 1. Specimens Data 6 2. Mapping 11 3. Geographic Pools and Statistical Analysis 11 4. Phylogenetic Analysis 12 5. Biogeographic Analysis 14 Species Accounts: Discussion on the Taxomomy and the Geographic Variation of the Morphometric and Coloration Characters 17 1. Genus Coeligena Lesson, 1832 17 1.1 Coeligena coeligena (Lesson, 1832) 20 1.2 Coeligena phalerata (Bangs, 1898) 35 1.3 Coeligena torquata (Boissonneau, 1840) 41 1.4 Coeligena bonapartei (Boissonneau, 1840) 55 1.5 Coeligena eos (Gould, 1848) 64 1.6 Coeligena helianthea (Lesson, 1838) 69 1.7 Coeligena prunellei (Bourcier, 1843) 75 1.8 Coeligena lutetiae (DeLattre & Bourcier, 1846) 81 1.9 Coeligena wilsoni (DeLattre & Bourcier, 1846) 89 1.10 Coeligena violifer (Gould, 1846) 96 1.11 Coeligena iris (Gould, 1853) 106 1.12 Coeligena inca (Gould, 1852) 119 2. Genus Pterophanes Gould, 1849 128 2.1 Pterophanes cyanopterus (Fraser, 1840) 128 3. Genus Ensifera Lesson, 1843 138 3.1 Ensifera ensifera (Boissoneau, 1839) 138 4. Genus Patagona Gray, 1840 146 4.1 Patagona gigas (Viellot, 1834) 146 Phylogenetic Relationships, Biogeography and Taxonomic Conclusions 155 1. Phylogenetic Relationships 155 2. Biogeography and Radiation Scenarios 165 3. Taxonomic Conclusions 178 Summary 185 Zusammenfassung 187 References 189 Acknowledgements 201 Appendix Erklärung Introduction The phylogeny and biogeography of tropical birds has been, and still is an important theme during the past two decades, retaining its validity partially thanks to the continuing discovery of new taxa. Unfortunately the taxa discovery rate is not coupled to the gain in knowledge in the fields of phylogeny and biogeography. This is especially true in the Neotropical region, so the design and elaboration of studies on such themes becomes especially relevant. The long and complex geological history of the South American continent has led to the formation of a great variety of habitats, resulting in a proliferation of plant and animal species, putting this zone in the category of “the region with the highest diversity on the planet” ( e.g., c. 3300 bird species have been documented for the Neotropics, in contrast with 1600 within the Afrotropis, 961 in the Oriental Region, and 906 in the Australasian, Schuchmann 1990). One of the Neotropical groups which responded rapidly and spectacularly to the high number of available habitats was the birds, which can be found in an enormous number of forms (highly specialised or generalists) occupying almost every available niche. To understand the history of the Andean biota it is necessary to review the general historical background of the South American continent. Geological data show that high-Andean habitats have been available for plant colonisation only since the end of the Tertiary (late Miocene – Pliocene, c. 11.2 Ma). Although the uplift of the Andes began in the late Cretaceous (c. 70 Ma), the final uplift throughout the range took place at the end of the Pliocene and the beginning of the Pleistocene (c. 2.6 Ma), ending with the uplift of the northern Andes (Simpson 1975, Van der Hammen 1989). Thus the current evidence indicates a recent south- to-north pattern of Andean uplift (Doan 2003). Based on this south-to-north progression, it is likely that high-elevation habitats were available for colonisation first in the south, then more recently (Pleistocene) in the north. The action of erosion and high-energy streams and rivers, together with water accumulation in the highlands, resulted in the excavation of major canyons, increasing the effectiveness of barriers to dispersal of the species that colonised the high-Andean habitats (Johnson 2002). Many hypotheses explaining the origin of the Andean avifauna have been based mainly on the effects of Pleistocene climatic fluctuations on speciation processes (e.g., Avise & Walker 1998, Vuilleumier 1968). However, other authors propose that many Andean genera and species have had a much longer occupancy in the region and an autochthonous origin (before 1 the Pleistocene). The possibility that ancient groups of birds responded directly to the orogenic activity in their habitat could be a consequence of this proposal (Graves 1985). In many cases, the Refugia Theory (Haffer 1969), together with palaeoclimatological data, have been employed in order to explain Andean bird speciation patterns. These hypotheses present a notable incoherence: the palaeoclimates are documented for the highlands but the supposed refugia are documented for the lowlands (Shapiro 1989). From this perspective it is logical to propose an early origin for high-Andean taxa. Three different kinds of processes modify the geographical spatial arrangement of organisms: extinction, dispersal and vicariance (Crisci 2001). The latter has been considered an alternative method of understanding the historical biogeography of Andean biota; in many taxa vicariance is seen as the cause of biota differentiation (vicariant biogeography), implying the occurrence of parapatric or allopatric speciation. This approach does not exclude the effect of climatic or other factors in the formation of new taxa, but the driving force is always vicariance. It is now generally acknowledged, since Nelson’s (1969) contributions on cladistical biogeography, that the interdependence between geographical distribution and phylogeny is fundamental to biogeographic analyses. Based on this relationship, several methods have been proposed to investigate the origin of extant taxa and the presence and localisation of ancestral areas (Bremer 1992; Ronquist 1994, 1995; Sober 1988; Wiley 1988; and recently van Veller et al. 1999, 2002). The presence of bird species before the Pleistocene strongly supports the use of vicariance hypotheses in order to explain the differentiation patterns observed in the Andes, patterns that would be directly related to the geological history of the region. This approach is known as the South-to-North Speciation Hypothesis (SNSH), which proposes that speciation of high- Andean taxa followed a south-to-north pattern, generally coinciding with the progression of uplift of the Andes (Doan 2003). The same process has been proposed by García-Moreno & Fjeldså (2000) to explain the radiation of the Andean avifauna. For several genera from the non-hermits hummingbirds lineage, a speciation model that coincids with the SNSH’s south-to-north radiation general statement has been proposed, This conclusion has been achieved in biogeographic studies made on Aglaiocercus (Schuchmann & Duffner 1993), member of the Andean ‘coquettes’ lineage (sensu Bleiweiss et al. 1997), and on other related Andean genera as Chalcostigma (Schuchmann & Heindl 1997) and Metallura (Heindl & Schuchmann 1998). In these studies the radiation scenario is placed basically in the Pleistocene, the center of origin for the taxa is supposed to be in south of the 2 equator (somewhere in southeastern Peru and northeastern Bolivia), and a northward direction for the speciation process is proposed. In these mentioned studies, the location of the centre of origin is explained by the presence of plesiomorphic characters in the southern taxa populations. The direction of dispersal is justified with the observed northward gradual progression of apomorphic characters. Coeligena species (Aves: Trochiliformes) were probably one of those ancestral bird groups that radiated into high-Andean habitats during the orogenic formation activity, making it a good group to study in an approach to the general biogeographic history of the Andes. The current taxonomy of the genus Coeligena was established by Peters (1945), and the most recent taxonomic arrangement, presented by Schuchmann (1999), includes 12 species, all distributed on the Andean slopes and adjacent mountain ranges, from the north-eastern Venezuelan Cordillera de la Costa to northern Argentina, including the isolated Sierra de Santa Marta in north-eastern Colombia (Fjeldså & Krabbe 1990, Schuchmann 1999, Sibley & Monroe 1990). There are numerous studies on the systematic and geographic variation of Andean hummingbird genera other than Coeligena (e.g., Graves 1980). Specific studies on Coeligena species are limited to hybrid forms (Graves 2001), nest descriptions (Ortiz-Crespo 2000, Schuchmann 1978, Wiedenfeld 1985), or ethology (Schuchmann 1975). No studies exist on the phylogeny of Coeligena and its relationship to other Trochilinae lineages. There is some evidence (based mainly on plumage coloration) indicating possible phylogenetic relationships between the well-established genus Coeligena and the genera Pterophanes, Ensifera (Berlioz 1936), and possibly Patagona (Schuchmann, pers. comm.). Within the last few decades, there has been an increase in the number of studies using phylogenies to address a wide range of issues (especially biogeography), but even with the advances