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26 September 2018 A striking, critically endangered, new species of hillstar (Trochilidae: Oreotrochilus) from the southwestern Andes of Ecuador
Francisco Sornoza-Molina, Juan F. Freile, Jonas Nilsson, Niels Krabbe, Elisa Bonaccorso
Author Affiliations +
Abstract

We describe a new species of the genus Oreotrochilus from the southwestern Andes of Ecuador. The new species is most similar in adult male plumage to O. stolzmanni and O. chimborazo. However, male and female show unique combinations of plumage characters that are likely to act as social signals. Phylogenetic analyses based on mitochondrial DNA indicate that this new taxon is closely related to O. stolzmanni and O. melanogaster, whereas genetic distances and preliminary comparisons of vocalizations suggest a sister relationship with O. stolzmanni. The geographic distribution of the new species seems to be restricted to cordillera Chilla-Tioloma-Fierro Urcu, in the southwestern highlands of Ecuador, an area historically poorly explored by ornithologists. Thus, based on its restricted distribution, apparently low population size, and lack of protection of its habitat, we evaluate it as critically endangered.

INTRODUCTION

Hummingbirds represent one of the most spectacular avian radiations of the New World. With more than 340 species (Clements et al. 2017), they occur from sea level up to 5,000 m a.s.l. in a range of habitats as different as tropical rain, deciduous, and cloud forests, Andean shrub, puna, paramo, mangrove, and desert oasis (Schuchmann and Bonan 2017). Hillstars of the genus Oreotrochilus are peculiar among hummingbirds because of their preference for high-elevation habitats along the Andes, among the highest in the Trochilidae, which is accompanied by behavioral (Pearson 1953, Carpenter 1976) and physiological (French and Hodges 1959, Carpenter 1974) adaptations to low temperatures. Their geographic range spans from extreme southern Colombia to southern Chile and Argentina, occupying paramo environments near the equator, and puna and arid plateaus southwards (Schuchmann and Bonan 2017).

According to Remsen et al. (2018), the genus Oreotrochilus includes 5 species: O. chimborazo (extreme southern Colombia to south central Ecuador); O. estella (extreme southern Ecuador to northern and central Peru, and southern Peru to northern Chile, Bolivia, and northern Argentina); O. melanogaster (south central Peru); O. adela (Bolivia to extreme northern Argentina); and O. leucopleurus (extreme southern Bolivia, Argentina, and Chile) (Schuchmann and Bonan 2017). The monophyly of the genus is well established but the status and validity of some taxa have been debated. Fjeldså and Boesman (2017) consider the northern populations of O. estella (O. estella stolzmanni) from Ecuador, northern and central Peru as a separate species, based on plumage differences. This proposal has been considered as potentially valid by Clements et al. (2017) and Remsen et al. (2018), based on molecular evidence showing that O. estella stolzmanni is more closely related to O. melanogaster than to O. estella estella (McGuire et al. 2014). Further, O. chimborazo and O. leucopleurus have been regarded as subspecies of O. estella (Zimmer 1951), whereas O. estella bolivianus has also been ranked as full species (Peters 1945). Here, we adopt the classification of Remsen et al. (2018), but recognize O. stolzmanni as a valid species (as per Fjeldså and Boesman 2017).

Recent fieldwork in the highlands at the border of El Oro and Loja provinces, southwest Ecuador, revealed the presence of an undescribed taxon of Oreotrochilus. Herein, we describe this new taxon, assess its evolutionary relationships with other species of Oreotrochilus, and discuss potential scenarios that led to the evolutionary origin of this species. Finally, we assess its conservation status following UICN (2012) criteria.

METHODS

Following the conceptual framework developed by Simpson (1951), Wiley (1978), and de Queiroz (2007), species are defined as segments of separately evolving metapopulation lineages. As operational criteria for delimiting species (de Queiroz 2007), we assess the morphological diagnosability of the new taxon and revise other lines of evidence (i.e. genetic, vocal, ecological) that may indicate evolutionary independence and reproductive isolation from other taxa. Specific details of our methods are provided below.

Fieldwork

On April 12, 2017, during a brief visit to the paramos of Cerro de Arcos, El Oro province, southwest Ecuador (see coordinates below), F.S.M. observed and photographed what seemed to be an immature male of an Oreotrochilus hummingbird, apparently different from other Oreotrochilus described to date. Further photographs taken on May 7, 2017, by F.S.M. confirmed that this Oreotrochilus was not assignable to any known taxon in the genus. Later, on May 22–26, 2017, F.S.M., J.F.F., and J.N. visited the same locality with the aim to collect specimens of this unique population. Capturing effort consisted of 9 mist nets (6 × 3 m and 9 × 3 m; 2 mm mesh) opened during 3 full days, 0630 hours through 1730 hours. A second expedition to the area was undertaken on July 10–13, 2017, by F.S.M. and J.N. Field observations were made in the northern part of Cordillera de Chilla (July 10), as well as west of Guanazán, in Cordillera de Tioloma (July 11). On July 13, F.S.M. and J.N. visited a Chuquiraga jussieui stand 3.9 km E of Refugio de Cerro de Arcos, setting up 5 mist nets (12 × 3 m, 2 mm mesh) that were opened from 1000 hours through 1600 hours. Additionally, on June 5–9, 2017, J.N. visited the east-central region of the Cordillera de Tioloma, making field observations only, and F.S.M. visited 5 localities along the paramos of Lagunillas-Piura-Podocarpus (along the continental divide of the Andes) and one at the Cuenca-Oña road (between the Girón and León rivers) in search of the new taxon. Finally, on April 7–9, 2018, F.S.M. and N.K. obtained sound recordings and photographs of the new taxon in and near Cerro de Arcos (including the second collecting locality), and of O. stolzmanni above Jimbura, in Zamora-Chinchipe province. Here, we also present observations from 2 localities along the paramos of Azuay-Morona-Zamora, gathered by Carlos A. Rodríguez-Saltos.

Before preparing the captured individuals as study skins, we preserved tissue from the pectoral muscle and liver in 95% ethanol, and preserved the stomach contents in 70% ethanol. To obtain behavioral data, 3 camera traps (Plotwatcher Pro, Columbus, Georgia, USA) were installed in front of flowering patches of Chuquiraga jussieui—the preferred plant of Oreotrochilus in Ecuador (Ortiz-Crespo and Bleiweiss 1982)—and other plant species. Cameras captured shooting records every 1 s and footage was analyzed using Motion Meerkat software (Weinstein 2015). Additional photographs were secured, as well as sound recordings, field observations on behavior, descriptions of habitats, and a collection of plants for identification at local herbaria.

Morphological Data

Specimens of the new taxon were compared to specimens of all taxa in the genus Oreotrochilus, with emphasis on O. stolzmanni, O. estella, and O. chimborazo deposited at Museo Ecuatoriano de Ciencias Naturales (MECN), Museo de Zoología, Pontificia Universidad Católica del Ecuador (QCAZ), Natural History Museum, Tring (NHM), and Senckenberg Natural History Museum, Frankfurt (SNM). Additional comparisons were performed with series of photographs taken from specimens of O. estella and O. stolzmanni deposited at Academy of Natural Sciences of Philadelphia (ANSP) and Natural History Museum of Denmark, University of Copenhagen (NHMD). Original descriptions of Oreotrochilus were reviewed, when relevant (Gould 1847), as well as species accounts and illustrations (Fjeldså and Krabbe 1990, Ridgely and Greenfield 2001, Schulenberg et al. 2007, McMullan 2016, Schuchmann and Bonan 2017) and online photographs ( www.hbw.com;  neotropical.birds.cornell.edu). Specimens were photographed individually and in species series, and photographs of outer tail feathers were taken of specimens whose preparation permitted harmless manipulation. Specimens studied are listed in Appendix A.

We made quantitative morphometric comparisons with all known species of Oreotrochilus. Analyses were based on measurements of bill length from base of feathers, wing chord, tail length, and width of the 2 outermost rectrices. Additionally, information of sex, age, and weight was recorded, based on field notes and specimen labels. Before performing statistical comparisons, we applied the Shapiro–Wilk statistic test to evaluate the normality of individual measurements (i.e. wing, bill, tail, rectrices 1 and 2) on species with more than 12 specimens per sex, separating specimens by species and by sex. We then performed 2-tailed Student's t-tests to compare measurements between sexes within each species. To explore potential morphometric differences between species, we applied a principal component analysis (PCA) on the correlation matrix of all 5 measurements. We could not control for body weight, since this measurement was missing from most specimen labels, especially those of historical specimens. All statistical analyses were performed in STATISTICA 8.0 (StatSoft Inc. 2007).

Evolutionary Relationships

We used samples of pectoral tissue from 4 individuals of the new taxon for molecular phylogenetic analyses. We sequenced the mitochondrial gene NADH dehydrogenase subunit 2 (ND2), which has been widely used on molecular studies of hummingbirds in general (McGuire et al. 2008) and Oreotrochilus, in particular (Rodríguez-Saltos and Bonaccorso 2016). Genomic DNA extraction, amplification, sequencing, and sequence edition protocols follow Rodríguez-Saltos and Bonaccorso (2016). Obtained sequences were compared with those available on GenBank ( https://www.ncbi.nlm.nih.gov/genbank/) of all other Oreotrochilus except O. adela. Based on the most recent hypothesis of hummingbird relationships (McGuire et al. 2008), we selected Ramphomicron microrhynchum and Chalcostigma herrani as outgroup species. Sequences were aligned in Clustal X2 (Larkin et al. 2007) and translated into amino acids in Mesquite 3.2 (Maddison and Maddison 2017) to verify the absence of stop codons. We used PartitionFinder2 (Lanfear et al. 2016) to determine the most appropriate partition scheme for the dataset—which turned out to be HKY + G, HKY, and GTR for the first, second, and third codon positions, respectively. Phylogenetic trees were obtained using maximum likelihood (ML) and Bayesian analyses. ML trees were estimated using GARLI 2.0 (Zwickl 2006), running 20 independent analyses with default settings, and selecting the tree with the maximum value of log likelihood. Bootstrap support (1,000 pseudoreplicates) was assessed running one replicate per search. Bayesian analyses were conducted in MrBayes 3.2 (Ronquist and Huelsenbeck 2003) using a random starting tree, 4 simultaneous Markov chains run for 1,000,000 generations, sampling every 1,000 trees, discarding the first 20% of trees as burn-in, and combining the remaining into a 50% majority-rule consensus tree. We also obtained a statistical parsimony network in TCS 1.21 (Clement et al. 2000) among the new taxon and its more closely related species. Finally, uncorrected genetic pairwise distances were calculated in PAUP v.4.0a109 (Swofford 2009) in order to provide a framework for comparisons of genetic differences among species of Oreotrochilus.

Potential Distribution

As a preliminary exploration of the potential distributional range of the new taxon, we obtained an Ecological Niche Model (ENM). For this analysis we used the coordinates of 5 known occurrence localities (all separated by at least 4 km) and the 19 WorldClim 1.4 variables ( www.worldclim.org; Hijmans et al. 2005) at 30 s resolution (∼ 1 × 1 km pixel size in Ecuador). Model estimation was achieved with Maxent 3.3.3k (Phillips et al. 2006) using default settings and logistic output. As background, we used 10,000 random points taken from the portion of the Andes above 1,000 m a.s.l., between the Jubones and Catamayo rivers. Significance of model predictions was assessed with the Pearson et al. (2007) jackknife validation approach, which is particularly suited for models derived from small numbers of occurrence records. Model predictions were projected to encompass areas between southern Ecuador and northern Peru, in order to explore the extent of the potential distribution of the species in a broader geographical region.

Bioacoustics

Pitch, duration, relative volume, note shape, and cadence of vocalizations were determined and compared among most Oreotrochilus taxa, depending on availability of audio recordings, and oscillograms and sonograms prepared with the sound-editing program CoolEditPro (Syntrillium Software, Scottsdale, Arizona, USA). The recordings analyzed are listed in Appendix B.

RESULTS

Fieldwork resulted in the collection of 5 specimens at 1 km W of Refugio de Cerro de Arcos (2 adult males, 3 females) and 2 adult males 3.9 km E of Refugio de Cerro de Arcos (see below). A combination of unique plumage characters studied in collected specimens and live individuals distinguish the Oreotrochilus population from Cerro de Arcos and vicinities as a new taxon, for which we provide the following description:

Oreotrochilus cyanolaemus sp. nov.
Blue-throated Hillstar
Estrella de Garganta Azul (Spanish).

  • Holotype

    Study skin MECN-9614 (Figure 1A); adult male (testes 3.7 × 3 mm, no bursa fabricii), 1 km W of Cerro de Arcos, El Oro province (3.5662°S, 79.4580°W; Figure 2A); 3,648 m a.s.l.; collected on May 23, 2017, by F. Sornoza-Molina, J. Freile, and J. Nilsson; prepared by F. Sornoza-Molina; field catalogue number AVES-0319; GenBank accession number MH543324.

    FIGURE 1.

    Series of Oreotrochilus cyanolaemus species nova collected at Cerro de Arcos, El Oro province, southwest Ecuador, May 23, 2017: (A) holotype, (B) paratopotype male, (C) paratopotype females, (D) paratype males.

    i0004-8038-135-4-1146-f01.tif

    FIGURE 2.

    Distribution of Oreotrochilus cyanolaemus species nova in southwest Ecuador. (A) Occurrence localities: (1) Cerro Arcos, El Oro province; (2) base of Cerro de Arcos on the road to Celén, 3.9 km E of Cerro de Arcos, Loja province; (3) La Capilla, near laguna de Chinchilla, Loja province; (4) 7.5 km S of Guanazán, El Oro province; (5) Fierrourco, Loja province. (B) Potential distribution; warmer colors indicate higher probability of presence. (C) Presence (black circles) and absence (white circles) localities identified to date.

    i0004-8038-135-4-1146-f02.tif

    Generic Placement

    The new species is placed in the genus Oreotrochilus Gould 1847, on the basis of morphological and molecular data. The main diagnostic morphological traits of Oreotrochilus, as originally described (Gould 1847:10), are shared by the new species. Analyses of ND2 place it as a close relative to other Oreotrochilus, making generic placement unambiguous (Figure 3).

    FIGURE 3.

    Phylogenetic tree of species in Oreotrochilus based on maximum likelihood (ML support and Bayesian posterior probabilities shown on major nodes) and haplotype network for O. cyanolaemus and closely related species.

    i0004-8038-135-4-1146-f03.tif

    Diagnosis

    The following combination of characters are diagnostic for male Oreotrochilus cyanolaemus from other Oreotrochilus species (Figure 4): (1) ultramarine blue throat, (2) emerald green head with blue green terminal tips, (3) emerald green upperparts with blue green terminal tips, (4) narrow and faint emerald green terminal tips to throat feathers. Females are distinguished by the following characters: (1) dusky grayish chin and upper throat contrasting with whitish lower throat, (2) emerald green head with blue green terminal tips, (3) emerald green upperparts with faint blue green shine, especially on the rump.

    FIGURE 4.

    Adult male (above left, center right), adult female (below), and immature male (above right) Oreotrochilus cyanolaemus species nova at the type locality, El Oro province, southwest Ecuador. Illustration courtesy of Paul Greenfield (2017).

    i0004-8038-135-4-1146-f04.tif

    Comparisons with Similar Taxa

    The new species is most similar in male plumage to Oreotrochilus stolzmanni and O. chimborazo, with which it shares a black throat collar, white breast to vent, narrow black longitudinal mid stripe in belly that does not reach the collar, greenish to buffy gray flanks to crissum, and metallic blue to greenish blue upper surface of tail. However, it differs from O. chimborazo in the absence of deep purple hood (O. c. jamesonii) or purple hood and turquoise green throat patch (O. c. chimborazo); the new species also has greener to blue-green dorsal parts, not as dull olive green as both subspecies of O. chimborazo.

    The most similar Oreotrochilus taxon is O. stolzmanni, with which it shares an overall pattern of emerald green crown, shining throat, and other characters aforementioned for O. stolzmanni and O. chimborazo. However, throat patch in O. stolzmanni is shining green with narrow bronzy tips in a few feathers, and a slight bluish sheen on the sides at certain angles. Entire upperparts of O. cyanolaemus are emerald green to emerald blue green, greener and brighter than in O. stolzmanni; O. cyanolaemus also lacks the bronzy sheen on the upperparts of O. stolzmanni, and the crown is greener, not bronze green as in O. stolzmanni.

    Oreotrochilus stolzmanni and O. cyanolaemus have similar shape of the outermost rectrices, which are broader-based, with very narrow outer web from mid part towards tip, and blunt tip. Outermost rectrices in O. chimborazo also have very narrow outer web, but are narrower and straighter throughout than in O. cyanolaemus and O. stolzmanni, whilst in the remaining species the outer rectrices have outer webs of uniform width and less blunt-shaped tips. Outer rectrices in some specimens of O. adela and especially O. leucopleurus are more curved. Intraspecific and interspecific variation in shape of outer rectrices needs further study of a larger sample size, especially in O. cyanolaemus, O. stolzmanni, O. melanogaster, and O. estella.

    Differences from the remaining Oreotrochilus species are more marked, with ultramarine blue throat and emerald to blue green upperparts being the most remarkable in male plumage. Besides throat color, O. cyanolaemus differs from O. estella by a black mid-belly stripe (brownish in O. estella) and green upperparts (dull bronzy olive in O. estella). In O. leucopleurus, the black mid-belly stripe is much broader than in O. cyanolaemus, throat is shining lime green, the upperparts are duller bronzy green, and the outermost tail feathers more arched. Oreotrochilus cyanolaemus is strikingly different from O. melanogaster, which has green throat, velvet black lower underparts, with orange buff flanks, and all rectrices greenish black. Oreotrochilus adela has chestnut flanks and breast sides, black central stripe that extends from lime green gorget to crissum, and all rectrices are blackish and buff. Characters like color of upperside of tail (steel blue to metallic greenish blue), color of glossy feathers in black throat collar and mid-belly stripe (bright green to bright blue), and extent of white on base of throat feathers are rather variable within the genus and need further attention.

    Female Oreotrochilus cyanolaemus is the only Oreotrochilus with dark grayish chin and throat with sparse metallic green spots; females of all other species in the genus have whitish chins. The amount and pattern of green spots in throat is variable across the genus, but O. cyanolaemus has bluer green spots in throat sides than all other Oreotrochilus taxa. Lower underparts in O. cyanolaemus are duller and darker grayish buff than in O. stolzmanni, O. estella, O. melanogaster, and O. leucopleurus, being closer to both subspecies of O. chimborazo. Upperparts are emerald green, greener than most congeners, with much less bronzy shine than O. chimborazo and lacking the dull bronzy tone of O. estella, O. leucopleurus, and O. adela. It is closer in tone to O. stolzmanni and O. melanogaster, but bluer green overall, with less bronzy forecrown and less bronzy shine overall.

    Comparative photographs of museum specimens of all Oreotrochilus species are found in Appendix Figures 712; Appendix Figure 13 compares O. cyanolaemus and its putative closest relative: O. stolzmanni. Living individuals photographed at the type locality are presented in Appendix Figure 14.

    Description of the Holotype

    Color nomenclature (capitalized colors) follow Ridgway (1912). Forehead to hindcrown glittering emerald green (between Killarney and Motmot Green), with blue-green reflections (approaching Methyl Blue). Nape, mantle, lower back, upperwing coverts, and rump glittering emerald green (approaching Killarney, Motmot Green, and Vivid Green), with narrow blue-green edges in several feathers (between Leitch's and Paris Blue) and some bronzy green reflections; uppertail coverts emerald blue-green (between Leitch's and Paris Blue). Dorsal surface of central rectrices steely (blackish) blue (Dusky Dull Violet-Blue to Bluish Black) with little glitter. All remiges and greater upperwing coverts dull blackish, with a faint steely blue sheen in some angles (Dusky Dull Violet-Blue to Bluish Black); outer web of outermost primaries with a very narrow whitish edge.

    Chin and throat feathers glittering ultramarine blue (approaching Lyons Blue), with broad, pure white bases and a narrow blackish line separating ultramarine blue from white; throat feathers have narrow and faint emerald green terminal tips (between Peacock Green and Killarney Green). Feathers in throat sides are longer than in central throat and chin. Velvet black throat collar (Black), feathers with shinier blue-green mid portion that provides a blue sheen in some angles, and narrow white bases. Breast to belly sides dull white, feathers with blackish bases. Narrow longitudinal stripe in mid belly is velvet black (Black), some feathers with shinier blue-green mid portion that provide a blue-green sheen; bases of feathers forming the central stripe are dull white. Breast sides to flanks greenish gray (between Grass Green, Cress Green, and Deep Dull Yellow-Green 1), with green sheen in some angles. Undertail coverts dull grayish buff (between Warbler Green and Yellowish Oil Green). Ventral surface of tail dull white in rectrices 3 and 4, both with narrow, dull blackish blue edges to outer webs (Dusky Dull Violet-Blue to Bluish Black); rectrices 2 with dull blackish blue tip and most outer webs, rectrices 1 with entire outer half dull blackish blue. Central rectrices entirely blackish blue.

    Bill is black with yellowish tomia, legs and claws also black, eyes are dark brown. Measurements are as follows: culmen = 18.3 mm; wing chord = 70 mm; tail = 49.4 mm; right rectrix 1 (outer) = 7.6 mm; right rectrix 2 = 8 mm; weight = 8.15 g.

    Paratopotypes

    Study skin MECN-9615 (Figure 1B); adult male (testes 4.5 × 3.2 mm, no bursa fabricii); collected May 24, 2017, by F. Sornoza-Molina, J. Freile, and J. Nilsson; prepared by F. Sornoza-Molina; field catalogue number AVES 0323; GenBank accession number MH543326.

    Study skin MECN 9616 (Figure 1B); adult female (ovum 5.4 × 2.7 mm, no bursa fabricii). Collected on May 25, 2017, by J. Nilsson, J. Freile, and F. Sornoza-Molina; prepared by F. Sornoza-Molina; field catalogue number AVES 0324; GenBank accession number MH543327.

    Study skin MECN 9617 (Figure 1C); presumed immature female (ovum 3.7 × 2.1 mm, no bursa fabricii). Collected on May 25, 2017, by J. Nilsson, J. Freile, and F. Sornoza-Molina; prepared by F. Sornoza-Molina; field catalogue number AVES 0325; GenBank accession number MH543325.

    Study skin MECN 9618 (Figure 1C); adult female (ovum 5.2 × 3.8 mm, 30 follicles smaller than 1 mm, no bursa fabricii). Collected on May 25, 2017, by J. Nilsson, J. Freile, and F. Sornoza-Molina; prepared by F. Sornoza-Molina; field catalogue number AVES 0326 (Figure 1C).

    Photographs of live individuals secured at the collection localities are archived at Macaulay Library, Cornell University (ML105920601, ML105921501, ML105921711, ML105922381), and the Internet Bird Collection (IBC 1502180, 1502183–1502186, 1502189, 1502192, 1502193). Audio recordings archived at Macaulay Library (104901281, 104901351, 104901391) and Xeno-Canto (419234, 419237, 419240, 419247).

    Paratypes

    Study skins MECN-9619 and 9620; adult males (testes 1.75 × 1.75 mm and 1.82 × 1.82 mm, respectively, no bursa fabricii; Figure 1D); 3.9 km E of Refugio de Cerro de Arcos, Loja province (3.5567°S, 79.4213°W; Figure 2A); 3,374 m a.s.l.; collected July 13, 2017, by J. Nilsson and F. Sornoza-Molina; prepared by F. Sornoza-Molina; field catalogue numbers FS-2377 and FS-2378. Audio recordings archived at Macaulay Library (104900761, 104900901, 104900971) and Xeno-Canto (419214, 419224, 419229).

    Plumage Variation

    Dorsal parts in male plumage are emerald green, varying in reflections from emerald bronzy green to blue-green (approaching Rood's Blue and Hortense Blue) in one specimen (MECN 9615), which has the largest gonads. Dorsal surface of rectrices is steely (blackish) blue with little glitter in 2 specimens, including the holotype, but metallic blue green in 2 specimens (approaching Dusky Greenish Blue, Dusky Green Blue 2, and Dusky Dull Bluish Green), recalling female's tail (see below).

    Extent of narrow emerald green tips to feathers of throat varies from extensive edges on throat sides and even chin in one specimen (MECN 9615) to fewer and fainter edges limited to throat. Amount of green sheen in flanks varies little, but in 2 specimens greenish gray extends more onto belly sides, leaving a narrower white portion between flanks and mid-belly stripe. Mid-belly stripe has variable amounts of blue-green feathers that provide a bright sheen. Specimen MECN 9615 has bluer and more extensive shining feathers, whereas others have faint green sheen. Undertail coverts are dull grayish buff with greener sheen in 2 specimens. There is little variation in tail pattern, resulting from narrower blackish edges of outer webs of inner rectrices, excepting central pair.

    Color of dorsal parts in female plumage is glittering emerald green (between Killarney and Motmot Green), duskier on forehead, sheen varies from bluish emerald green to bronzy emerald green; uppertail coverts are bluer and brighter (between Benzol Green and Prussian Green), and dorsal surface of central rectrices has a metallic blue-green sheen (approaching Dusky Greenish Blue, Dusky Green Blue 2, and Dusky Dull Bluish Green). Remiges and greater wing coverts are dusky, with a slight bluish sheen in some angles; outer web of outermost primaries has a very narrow whitish edge.

    Chin and mid-throat feathers have grayish olive outer halves, blackish bases, whitish central portion, and a dark green distal spot, providing a dusky background (between Dark Grayish Olive and Dark Olive) to dark green spots (between Duck Green and Dark Green); throat sides are whiter. Extent of dusky in chin and throat presents some variation, with dusky extending down to lower throat and connecting with grayish buff breast in one specimen (MECN 9618), down to mid throat in specimen MECN 9617, and limited to chin and upper throat in specimen MECN 9616. Extent of grayish on chin and throat results in varying amounts of white on lower throat, more noticeable white in those specimens with less extensive dusky. Amount, extent, size, and tone of green dots in throat and malar region vary from large, blue-green dots in conspicuous rows in 2 specimens, to smaller, sparser, and greener dots in one specimen. The former 2 specimens have larger ova, suggesting that variation in size and color of throat dots is related to reproductive status. Breast, breast sides, belly, flanks, and undertail coverts are dull grayish buff (Grayish Olive to Mouse Gray), with a few brighter olive green feathers on flanks and a slight green sheen on undertail coverts; ventral parts show little variation from breast to undertail coverts, and in amount of olive green in flanks. Rectrices are metallic bluish green (Dusky Greenish Blue 2 to Dusky Dull Green) with dull white bases in all but central pair, and dull white, round-shaped panels towards feather tips, variable in size and shape among feathers, but larger on outer rectrices. Tail pattern varies individually in size and shape of dull white patches.

    Measurements

    The Shapiro–Wilk test could not reject normality of the data for species with more than 12 samples per sex (all P > 0.05). In applying the Student's t-tests, we found no statistical differences in bill size between males and females of any species (Table 1). For all species, except O. adela, wings of males were always longer than in females, and were significantly longer in O. chimborazo, O. estella, and O. leucopleurus (all P < 0.001). Difference in length of tail between males and females varied, and was significant in O. chimborazo (P < 0.01). Rectrix 1 was always wider in females than in males, and significantly wider in females of O. chimborazo and O. estella (both P < 0.01). Finally, for all species except O. leucopleurus, rectrix 2 was wider in females than in males, and significantly wider in O. chimborazo (P < 0.01).

    TABLE 1.

    Summary of measurements (mm) of species in the genus Oreotrochilus. We also show the results of 2-tailed Student's t-tests of differences between males and females for species with more than 12 samples for each sex.

    i0004-8038-135-4-1146-t01.tif

    Because of differences detected between sexes, PCA comparisons were performed separately in males and females (Figure 5). For males, the first 3 PCAs accounted for 87% of variation in the correlation matrix. The PC1 explained 38% of the total variation, and was negatively and significantly correlated with width of rectrix 2 (r = −0.84; t = −16.88, P < 0.001), width of rectrix 1 (r = −0.71; t = −10.87, P < 0.001), and wing length (r = −0.59; t = −7.78, P < 0.001). The PC2 explained 27% of the variance, and was negatively and significantly correlated with tail length (r = −0.73; t = −11.49, P < 0.001) and bill length (r = −0.61; t = 9.10, P < 0.001). The analysis placed samples of O. cyanolaemus within the variation of O. stolzmanni, close to O. chimborazo and O. melanogaster, and one individual of O. estella. However, small sample size for O. cyanolaemus could be masking a greater variation in measurements. Samples of O. leucopleurus and O. adela clearly separated from samples of all other species. Overall, both species had narrower rectrices 1 and 2 and longer wings than the other species (PC1), but O. leucopleurus had shorter tails and bills than O. adela (PC2).

    FIGURE 5.

    Principal component analysis of morphological measurements in males (A) and females (B) of Oreotrochilus species. PC1 and PC2, principal component 1 and 2, respectively.

    i0004-8038-135-4-1146-f05.tif

    For females, the first 3 PCAs accounted for 86% of variation in the correlation matrix. The PC1 explained 39% of the total variation, and was negatively and significantly correlated with length of rectrix 2 (r = −0.81; t = −10.24, P < 0.001), wing length (r = −0.74; t = −8.03, P < 0.001), and tail length (r = −0.70; t = −7.27, P < 0.0001). The PC2 explained 25% of the variation, and was positively and significantly correlated with bill length (r = 0.77; t = 8.95, P < 0.001). Samples of O. cyanolaemus group closer to samples of O. melanogaster and O. chimborazo, and within the variation of O. stolzmanni. Here again, samples of O. leucopleurus and O. adela separate from samples of all other species, but show more dispersion than in males. Overall, bills in O. adela are longer than in the other species (see Table S1 for raw data used in morphometrics comparisons).

    Vocalizations

    Judging from the limited material at hand (listed in Appendix B), the vocalizations of O. cyanolaemus do not differ appreciably from those of O. stolzmanni. Playback of song of the latter elicited strong response from 3 different individuals of O. cyanolaemus. A territorial song (chase call) from a male O. cyanolaemus (Figure 6) illustrates the large number of different notes found in chase calls in the genus, which makes it hard to establish homologies with small sample sizes. In all Oreotrochilus species, chase calls are given by both sexes and are rapid twitters of rising and falling series interspersed with rattles and a variety of different notes highly changeable in composition.

    FIGURE 6.

    Oscillograms and sonograms of territorial song (chase call) and single-noted call of Oreotrochilus taxa. Upper panel: territorial song of male O. cyanolaemus (XC419229). Fairly similar songs are given by all other members of the genus. Lower panel: single-noted calls presumed to be homologous (except possibly G): (A) chimborazo chimborazo (OCHIMB02); (B) chimborazo jamesonii (COTOPX_0116); (C) cyanolaemus (XC419214); (D) stolzmanni (XC414298); (E) estella estella (ML33865); (F) estella bolivianus (XC95442); (G) leucopleurus (XC95441); (H) adela (XC146834). In all taxa, the call is composed of a single up–downstroke. Note the relative volume of the downstroke and the short and high-pitched peak frequency in chimborazo and jamesonii (AB). No homologous call of melanogaster was available.

    i0004-8038-135-4-1146-f06.tif

    As in other Oreotrochilus species, both sexes of O. cyanolaemus also frequently give a short, single-noted call composed of an up–down stroke. This call differs between at least some of the taxa (Figure 6). In one individual of O. chimborazo chimborazo (n = 2) and in 6 individuals from 4 different localities of O. chimborazo jamesonii (n = 20), it has a short and high-pitched peak frequency (13.8 ± 1.1 kHz; range: 11.5–16.7; n = 22) and most volume is invariably on the downstroke (Figure 6A, 6B). No similar single calls were found in any other Oreotrochilus recording. In calls from 2 individuals of O. cyanolaemus the peak frequency is lower (11.1 ± 0.6 kHz; range: 9.9–11.6; n = 17) and of much longer duration than in O. chimborazo, and most volume is invariably on the upstroke. In all 3 respects, they are similar to calls of 2 individuals of O. stolzmanni (peak frequency: 10.3 ± 0.3 kHz; range: 9.9–10.7; n = 6) and to calls of 4 individuals from 3 localities of O. estella (10.0 ± 0.7 kHz; range: 8.2–11.0; n = 43). Recordings from more individuals and localities are needed to prove constancy of possible difference in duration of the call between O. cyanolaemus and O. stolzmanni (78 ± 15 ms; range: 60–122; n = 23) and O. estella (46 ± 7 ms; range: 33–56; n = 43).

    Habitat and Ecology

    At the type locality, Oreotrochilus cyanolaemus occurs in patches of shrubs characterized by numerous stands of Chuquiraga and dominated by shrubs in the families Asteraceae, Polygalaceae, Melastomataceae, Hypericaceae, Rubiaceae, Rosaceae, and Clethraceae (D. Fernández, personal communication). Shrub patches ranged from 0.5–1.5 ha to a few square meters, had a dense understory, and canopy reached 3–4 m in height, with a few emergent shrubs up to 7–8 m. Open grassy paramo, meadows, and cultivated/grazed paramo surrounded shrub patches. The species was also observed in stands of Chuquiraga isolated from shrubby patches, ranging from <10 m2 to 1 ha, and reaching 2 m in height.

    Up to 2 males and 4 females were observed in a small creek with sparse shrubs, which apparently provided shelter from windy and foggy weather. Other small creeks facing westwards were also occupied by at least one or two females, which perched low and flew up and down the creek. Also found in open, dry paramo with scarce remnant vegetation and few stands of Chuquiraga at Fierro Urcu, marginally in introduced stands of Pinus radiata at the type locality, and once in a 0.6 ha woodland patch dominated by Polylepis sp. and Gynoxys sp. at Laguna de Chinchilla. Topography of areas occupied by O. cyanolaemus was hilly terrain, steep hills, rocky outcrops, and creeks with gentle slopes.

    Oreotrochilus cyanolaemus fed mostly by clinging sideways and upside down, but also perching next to flowers. It was observed once hovering in front of flowers (B. Vásquez et al., personal communication). Often, it perched a few seconds in the flowering shrub before visiting flowers. Main feeding plant is Chuquiraga jussieui (Asteraceae), but it was also observed feeding on the shrubs Macleania rupestris (Ericaceae) and Lleresia hypoleuca (Asteraceae). Four morphotypes of flies were found in stomach contents of collected male specimens.

    Adult male and female-plumaged individuals of Oreotrochilus cyanolaemus were seen perching on lichen-laden rocks and boulders, often near ground. Also perched on exposed stumps of Puya hamata (Bromeliaceae) up to 4 m above ground, and in living or dead (burnt) Puya leaves a few centimeters from ground level. They regularly perched atop Chuquiraga jussieui, Macleania rupestris, Monnina sp., and other shrubs up to 5 m from ground, as well as on fence posts, barbwire, and in introduced pine trees up to 12 m high. Females were observed perching and even disputing one perch next to a small rushing strea