A new methodology to use color spectral data for taxonomic, phylogenetic, and biogeographic studies. An example with three genera of lowland hummingbirds: Topaza, Anthracothorax, and Eulampis. Dissertation zur Erlangung des Doktorgrades (Dr. rer. nat.) der Mathematisch-Naturwissenschaftlichen Fakultät der Rheinischen Friedrich-Wilhelms-Universität Bonn vorgelegt von Angela Schmitz Ornés aus München Bonn 2004 ii 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: Diese Dissertation ist auf dem Hochschulschriftenserver der ULB Bonn http://hss.ulb.uni- bonn.de/diss_online elektronisch publiziert iii Dedico este trabajo a mi hija ANDREA CAROLINA por ser mi motor de vida y fuente de inspiración ... iv Contents • Introduction …………………………………………………………………………….1 o Phylogenetic, systematic, and taxonomic bird studies …………………………3 o Hummingbirds: phylogeny and origin ….……………………………………..5 o Characteristics and distribution of the study taxa …...………….……………...7 o Research goals and structure of the study ……………………………………...9 • General methodology …………………………………………………………………13 o Specimens included in the study ……………………………………………...13 o Mappings ……………………………………………………………………...16 o Morphometric data ……………………………………………………………16 o Color measurements (spectral data) …………………………………………..16 o Data analyses …………………………………………………………………19 o Definition of preliminary pools for analysis ………………………………….20 • Methodology to measure and analyze color spectral data ……………………………24 o Theoretical framework on studies of color variation in animals ……………..24 o Color determination on the bird specimens …………………………………..27 o Handling of spectral data ……………………………………………………..29 o Interpretation of the first PCs in coloration data ……………………………...31 o Using color data to determine differences among populations ……………….32 o Phylogenetic analysis on spectral color data …………………………………34 Generalized Frequency Codying (GFC) applied to continuous morphological data …………………………………………...35 • Geographical variation and review of the taxonomy and phylogeny of the genus Topaza GRAY, 1840..........................................................................…............39 o Theoretical background ……………..…..………………………….………...39 v o Preliminary considerations on the validity of Topaza pella pamprepta ……...42 o Taxonomic analysis of the genus Topaza …………………………………….46 o Phylogenetic analysis of the genus Topaza …………………………………..55 Campylopterus as outgroup ……………………………………………….55 Eulampis as outgroup ……………………………………………………..58 o Phylogenetic conclusions for the genus Topaza ……………………………...60 o Further arguments supporting the clinal trend of Topaza …..………………...62 • Geographic variation and review of the taxonomy and phylogeny of the genus Anthracothorax BOIE, 1831 ……………………..…………………………………...69 o Theorethical background………………………..…………………………….69 o Analysis of Anthracothorax at the species level ……………….……………..72 Anthracothorax recurvirostris ………………………….…………….77 Controversies in populations of Anthracothorax nigricollis and Anthracothorax prevostii ……………….…………………………….78 Anthracothorax nigricollis ………………………….………………...86 Anthracothorax prevostii …………………………..……….………...95 Anthracothorax viridigula ……………………….………………….103 Anthracothorax veraguensis ……………………………….………..106 Anthracothorax dominicus and Anthracothorax mango …………….110 Anthracothorax viridis …………………………………….………...115 o Phylogenetic relationships within Anthracothorax ……………….…………120 Species level ……………………………………………….………...121 Subspecies level …………………………………………..…………123 • Geographical variation and review of taxonomy of the genus Eulampis BOIE, 1831 ...…………………………………………………….………………………....127 o Theorethical background …...……….………………………….…………...127 o Taxonomic study of the genus Eulampis ……………………….…………...128 vi • Phylogenetic relationships of the three genera, Topaza, Anthracothorax, and Eulampis .……………………………………………………………………………149 o Descriptive information on Campylopterus (outgroup) ...............……….149 o Phylogenetic analysis ...................................................................……….150 • Historical biogeographical events in the speciation process of the study group ……154 • Concluding remarks …………………………………………………………………161 o On the methodology for plumage color comparison ………………………..161 o Interpretation of spectral color data in terms of real morphological differences …………………...…………………………………………………………..162 o Adapting the methodology for phylogenetic analysis ………………………163 o Taxonomic conclusions and phylogenetic relationships of the genera Topaza, Anthracothorax, and Eulampis ………………………………….…………..164 • Summary …………………………………………………………………………….166 • Bibliographic references …………………………………………………………….167 • Acknowledgments …………………………………………………………………...181 • List and index of plates ……...………………………………………………………187 • List and index of figures …...………………………………………………………..187 • List and index of tables ……………………………………………………………...193 • List of appendices …………………………………………………………………...200 • Compact disc (CD) with appendices ……...………………..………………………..209 • Erklärung …………………………………………………………………….………210 • Curriculum Vitae …..………………………………………………………………..211 1 Introduction Color patterns have long been considered an important component of the evolutionary process in the natural world. This trait can be greatly influenced by predator-prey relationships and sexual selection. Specifically the latter has been frequently studied and assumed to be directly related to speciation (Darwin 1871, Andersson 1994, Townsend Peterson 1996, Moller & Cuervo 1998). Coloration can be highly variable among individuals or groups of individuals and may reflect phylogenetic relationships, mainly at lower-taxa levels, such as species and subspecies. This characteristic has been used to evaluate geographical differences in bird populations, consequently, also being important for identification, taxonomy, systematics, and historical biogeography (e.g., Vuilleumier 1968; Graves 1985, 1997; Marin 2000; Molina et al. 2000). Most taxonomic and evolutionary studies based on coloration have assumed that the human subjective experience of color approximates to that of birds (Bennett et al. 1994). However that may not be the case, since birds have probably the most sophisticated color vision system of all vertebrates (Goldsmith 1990). This means that the inability of humans to perceive the color world of animals applies most dramatically to birds, and consequently to the results of many of the current taxonomic, phylogenetic, and evolutionary studies conducted on this group. Color depends not only on the physical characteristics of the observed object and the sensory system of the receiver, but also on the ambient effect. Endler (1992) has extensively discussed the evolution of coloration, and according to him the evolution of visual signals among animals is a complex process that depends on behavior and microhabitat selection. A specific behavior is required in order to choose the times, seasons, and microhabitats that transmit the signal most efficiently with the minimum degradation and attenuation, the least ambient noise, and the minimum risk of predation. Hence, both breeding behavior and microhabitat selection are likely to coevolve with sensory systems and signals (Endler 1992, Endler & Thery 1996). 2 These factors and interrelationships may have strong implications for geographical differentiation and speciation, since the evolutionary bias of the sensory drive is unlikely to be geographically uniform (Endler 1992). Because signal transmission conditions and background noise also vary with microhabitats, times, and seasons, divergences among populations and species are very likely. Variation in intraspecific signals may not only maintain but also cause differences among populations. Speciation and further divergence can result if populations and species evolve in different directions (Endler 1992). Ideally, color researchers would have knowledge of the visual system of their study organism, including detailed information on cone pigments, spectral sensitivities, etc., as well as data describing attenuation patterns, timing and location of peak animal activity, ambient light levels, etc. (Grill & Rush 2000). However, this information for birds (and other animals) is rarely available. If we assume that differences in reflectance spectra translate to differences in the perceived colors, then approximations still provide useful information about the role of color in biology (Grill & Rush 2000). Moreover, since color patterns are the ultimate consequences of this complex evolutionary process discussed by Endler (1992), the direct, objective measurement of plumage color must be useful for phylogenetic, systematic, and taxonomical studies. A color classification based directly upon the reflectance spectra rather than human perception is a better starting point in studies of animal color patterns (Endler 1990). However, despite its advantages, there are also problems involved with the collection and use of spectral data. Spectrometers generally represent the color of a structure of an organism as the reflectance at a given nanometer value of a large number of arbitrary wavelength points along the electromagnetic spectrum (Thorpe 2002). As color changes, spectra can change in a number of ways, including shifts in curve slopes, amplitude, and number and position of peaks, and these changes are often difficult to quantify. Therefore, a challenge