ORNITOWGIA NEOTROPICAL 7: 119-148, @ The Neotropical Oroithologi<2! Society

SYSTEMATICS ANO GEOGRAPHIC VARIATION IN LONG-TAILEO HERMIT HUMMINGBIROS, THE PHAETHORNIS SUPERCIL/OSUS- MALARIS-LONGIROSTRIS SPECIES GROUP (TROCHILIOAE), WITH NOTES ON THEIR BIOGEOGRAPHY

Christoph Hinkelmann*

Alexander Koenig Zoological Research Institute and Zoological Museum, Ornithology, Group: Biology and Phylogeny of Tropical Birds, Adenauerallee 160, D-53113 Bonn 1, Germany.

Resumen. El grupo de Phaethornis superciliosus y especies relacionadas se compone de tres especies de orígen probablemente monofilético: R superciliosus, R malaris y R longirostris. R longirostris está limitado a América Central y Sudamérica al oeste de los Andes. Existen 6 subespeciesválidas; una de estas, R I. baroni, posiblemente ya ha alcanzado aislamiento reproductivo. Las poblaciones distribuidas entre Guatemala y Costa Rica representan una wna extensa de introgresi6n de caracteres morfol6gicos entre dos subespecies,R I. cephalUsy R I. longirostris. En Sudamérica al este de los Andes, similitudes y introgresi6n de caracteres morfol6gicos indican que 6 subespecies válidas pueden ser asignados a R malaris mientras que R superciliosus incluye dos subespeciesválidas en los dos margenes del Río Amawnas en su curso inferior. En el Perú, caracteres de coloraci6n de R malaris moorei y R m. bolivianUs se mezclan en una zdna de introgresi6n aparentemente en correlaci6n con la distribuci6n altitudinal. Sin embargo, no se puede definir con certeza la posici6n taxon6mica de R malaris ochraceiventris; posiblemente, este taxon ya ha alcanzado el estado de especies.Mientras R tongirostris está completamente aislado geograficámente de R malaris y R superciliosus, las subespeciesde estas dos actuan como paraespecieso alloespecies en varias partes de sus áreas de distribuci6n. Solamente R m. malaris occurre en simpatría con un otro taxon de este grupo de especiesrelacionadas, con R s. superciliosus, en la entera área de distribuci6n de R m. malaris. Las dos especies habitan el mismo espacio vital. Probablemente, evitan competencia directa utilizando diferentes recursos de alimentaci6n cual es indicado por diferencias en sus masas corporales y longitudes del pico. La validez de ambas especies está corroborada por el descubrimiento de s6lo un especimen híbrido. Areas de distribuci6n de estas tres especies de colibnes ermitaños indican que los procesos de especiaci6n probablemente fueron facilitados por eventos paleoclimáticos y vegetacionales como postulados del modelo biol6gico de diversificaci6n (teona de refugios). Abstract. Long-tailed Hermit hummingbirds can be assigned to three closely related, probably monophyletic species: Phaethomis superciliosUs,R malaris, and R longirostris. R longirostris is limited to Central America and W Andean South America. There are 6 valid subspecies; one of these, R I. baroni, may al¡-eady have achieved repro- ductive isolation. Populations occurring between Guatemala and Costa Rica represent an extensive wne of character introgression between two subspecies, R I. longirostris and R I. cephalus. In E Andean South America, morphological similarity and character introgression indicate that 6 valid subspeciescan b~ assigned to R malaris, whereas R superciliosus is composed of 2 valid subspecies, one on each side of the lower Amazon river. In Peru, coloration characters of R malaris moorei and R m. bolivianus intergrade along an apparently altitude-based intro- gression wne. However, the taxonomic position of R malaris ochraceiventris cannot be defined with certainty yet; this taxon may have achieved species status. Whereas R longirostris is completely isolated from R malaris and R superciliosus, subspecies of both cis-Andean species behave like para- or allospecies in severa! parts of their distribution ranges. Only R m. malaris occurs sympatrically with another taxon of this species group, R s. super- ciliosus, over its whole distribution range. Both species inhabit the same habitat, and probably avoid direct competition by depending on different food niches as indicated by differences in their body masses and bill lengths. The validity of both species is corroborated by the discovery of only one hybrid specimen. Recent distribution patterns within Long-tailed Hermit hummingbirds indicate that speciation processesmay have been facilitated by paleoclimatic-vegetational events that are postulated by the biological model of diversification (refuge theory). Acceptai 17 July 1996. Key words: Systematics,geographic variation, Phaethornis, hermit hummingbirds, biogeography.

Present address: Timelostr. 38, D-2140l Deutsch Evern, Germany.

119 HINKELMANN

1979, Snow 1981) of wng-tailed Hermit INTRODUCTION hummingbirds, and also in regionallists. Within Long-tailed Hermit hummingbirds (Phaethornis the genus Phaethornis, wng-tailed Hermit superr:iliosus-malaris-longirostrisspecies group) in- hummingbirds form a monophyletic unit. They habit lowland rain forest of the terra firme, are most closely related to Phaethornis syrmato- humid secondary growth, lower montane forests, phorus, P. koepckeae,P. philippii, and P. bourcieri. and may be found even in gallery forests, planta- Recent taxonomic studies in the P. super- tions, wooded pastures, and mangroves, from S ciliosus-malaris.longirostris speciesgroup in Ama- Mexico to N Argentina. They are non-territorial zonian Peru ( Capparella 1987), Brazil (Grantsau trap-liners, the males gather at leks during 1988) and Central America (Banks, unpubl. ms.) certain periods of the year where they utter a have cast doubt on the validity of Peters' (1945) simple song to attract females. Nesting, display, classification. Therefore, the objective of this and general behavior do not differ significantly paper is to clarify the relationships between the from other members of the Phaethornithinae or taxa within the Phaethornis superciliosus-mala. hermit subfamily (Nicholson 1931, Davis 1958, ris-longirostris species group which I arrange in Snow 1973, Stiles & Wolf 1979), Long-tailed three species. Hermit hummingbirds belong to one of the largest hummingbird genera, Phaethornis. Species of this genus may be distiguished by their body MATERIAl.S AND METHODS masses,and can thus be united in two body mass This study is based on the examination of 1.065 categories: 2-4 and 4-8 g. Of all Phaethornis, museum skins representing a1l taxa of Long-tai- only two members of the superriliosus-mala- led Hermit hummingbirds, and probably ris-longirostris speciesgroup regularly exceed 8 g. including the majority of study skins of this These are birds occurring in SW Mexico (states group preserved in scientific collections. A list of of Michoacán, Guerrero, Oaxaca) and Surinam, the institutions providing specimens is given in French Guiana as well as in the Brazilian state of Appendix I.I examined 13 type specimens of 19 Amapá, respectively. In general, Long-tailed preserved. Hermit hummingbirds can be assigned to the For almost all specimens I measured 3 linear body mass category of 4-8 9 (Hinkelmann characters to the nearest 0.5 mm with a conven- tiona1 scale (Fig. 1): bill length including the 1988a). For many decades,the taxonomic treatment operculum (BL), chord length of the unflattened of the Phaethornis superciliosus-malaris-longi- wing (wing length, WL), and the shortest rostris species group was a topic of intensive distance between tips of the outermost (V) and discussion. Taxa were assigned to two species by centra1 (1), i. e., longest feathers of the rectrices Salvin & Elliot (1873) and Simon (1897), whereas ("taillength" as used in this study, TL; in caseof later the same author (Simon 1921), as well as differences between left and right ha1f, the left Boucard (1895) and Hartert (1900) considered side [dorsal] was taken for ca1culations). I did not them to belong to 6 species; others accepted 3 measure immature birds (indicated by light (e.g., Cory 1918) and 5 species (e.g., Gould feather margins on hind-crown, nape, and back) 1861), respectively. The discussion was almost as well as those with obviously molting rectrices. finished by Peters (1945) who grouped the taxa Differences in linear measurements between into 2 species,P. malaris and P. superciliosus.Zim- respective groups (sexes,taxa, geographica1units) mer (1950) prepared the most recent taxonomic were examined by t-test and Mann-Whitney-U analysis and accomplished a general shift of sub- test. Significance levels were fixed at P<0.05 and speciesfrom P. superr:iliosusto P. malaris but con- P<0.01, respectively. tinued to recogriize only 2 species.Peters' (1945) Though O' and 9 are alike in coloration, treatment was generally followed in subsequent sexing specimens proved only a minor problem. studies on the bchavior (e. g., Davis 1958, Skutch Recently collected skins from several institutions 1964, Snow 1973, Stiles & Wolf 1979), general include gonad data on their labels. Besides, O' biology (e.g., Skutch 1964, Young 1971), or differ from 9 by significantly longer wings and ecology (e.g., Stiles 1975, 1980, Stiles & Wolf usua1ly less curved bills (Table 1). Only a very

120 LONG'fAILED HERMIT HUMMINGBIRD!

limited number of specimens (n = 11) could not be sexed with certainty and was thus excluded from calculations. At the Zoological ResearchInstitute and Zoo- logical Museum Alexander Koenig (ZFMK), Bonn, I united 302 study skins belonging to the scientific collection of the ZFMK and to several of the museums listed in Appendix I, sent on loan to Bonn. These birds originated from almost all regions in which Long-tailed Hermit hummi~gbirds are distributed. This total of 302 members of the Phaethornis superciliosus-mala- ris-longirostris species group enabled a careful examination of character variation depending on age, sex, and geographical distribution by direct comparisons of all specimens, providing a gene- ral survey of variability. With this experience, and many color slides portraying series of birds from the same locality ( or limited area), I ex- amined the collections of almost all institutions listed in Appendix I. There I investigated all specimens of the species group, took measure- ments and noticed plumage variation, and could extend the data basis to 1,065 specimens from which the analysis of character variation was drawn. For the determination of distribution ranges, locality data from the specimens' labels were plotted with the aid of ornithological gazetteers (Paynter 1982, Paynter & Traylor 1977, 1981, Paynter et al. 1975, Stephens & Traylor 1983, 1985), regional ornithological monographs in- cluding gazetteers (e.g., Griscom 1932b, Slud FIG. 1. Linear character measurements taken for this 1964, Monroe 1968, Haffer 1974, Novaes 1974, study. Binford 1989) and atlases (e.g., Scobel1912, Bar- tholomew etal. 1985). I follow Haffer (1974) in the use of terms "cis-Andean" ( = South Ameri- detail while presenting geographical variation can E of the Andes) and "trans-Andean" ( = Cen- and zones of character introgression. In case of tral American and South American W of the small numbers of measurements within a certain Andes). sample (n<4), neighbouring PG were united to Pooling of geographical units (population permit statistical comparisons. In the presenta- groups, PG) for the analysis of geographic varia- tion of results, this treatment is indicated by a tion was facilitated by physical borders and con- "+", e.g.: 4+5>6, P2, P2, P2, P2, P

121 HINKELMANN

Bill Length (BL) [mm] wiseoventer 0" 15 44.20 1.33 42 48 0.092 9 4 42.00 2.16 40 45 0.131 'mexícanus 0" 13 46.62 1.21 44 48.5 <0.01 ++ 9 17 42.65 1.47 39 45 0 ++ longirostris 0" 82 40.87 1.53 38 46 <0.01 ++ 9 46 38.76 1.21 36 42 0 ++ cephalus 0" 74 39.28 1.45 37 43 <0.01 ++ 9 70 37.20 1.21 35 40 0 ++ susurrus 0" 44 42.24 0.93 40 44 <0.01 ++ 9 6 40.08 0.97 39 43.5 <0.01 ++ baroni 0" 23 41.46 1.39 39 43.5 <0.01 ++ 9 8 39.06 1.50 37 41.5 0 ++ 0" 29 47.21 1.01 44 49 <0.01 ++ 9 17 44.08 1.15 42 46 0 ++ insotitu~ 0" 13 41.88 2.25 38 45.5 <0.01 ++ 9 5 38.10 1.14 37 39.5 0 ++ 0" 80 41.78 1.94 37 46 <0.01 ++ 9 53 38.44 1.52 35 41 0 ++ Peruvian zone of 0" 48 41.26 1.45 38 44 character introgression 9 44 38.69 1.59 35 42 o bolivianus 0" 62 37.98 1.36 35.5 41 <0.01 9 60 35.88 0.98 34 38 0 maTKarettae 0" (37) 9 (35.5) ochraceiventris 0" 16 43.97 1.47 41.5 46 <0.01 ++ 9 9 41.39 0.65 40.5 42.5 0 ++ muelleri 0" 25 37.64 0.84 36 39 <0.01 ++ 9 29 35.97 1.11 34.5 38 0 ++ superciliosus 0" 60 38.50 1.43 35 42 <0.01 ++ 9 38 36.03 1.40 33 39 0 ++ Wing length (WL) [m m] griseoventer (1 15 66.87 0.67 66 68 <0.01 ++ 9 4 63.50 0.58 63 64 0 ++ mex¡canuJ (1 14 68.64 1.08 67 70 <0.01 ++ 9 19 66.11 1.24 64 68 0 ++ longirostris (1 86 63.98 1.05 61.5 66 0 ++ 9 48 60.94 1.28 59 64 0 ++ cephalus (1 79 62.24 1.55 59 68 0 ++ 9 74 59.26 1.54 55 63 0 ++ SUSUrntS (1 48 65.73 1.25 64 69 <0.01 ++ 9 7 61.71 1.60 59 64 0 ++ baroni (1 24 61.67 1.63 59 65 <0.01 ++ 9 10 58.50 1.65 56 61 0 ++ malaris (1 32 67.61 1.42 64 70 <0.01 ++ 9 16 64.53 1.39 62 66.5 0 ++ insolitus (1 14 63.96 1.08 62.5 66 <0.01 ++ 9 5 60.40 1.14 59 62 0 ++ moorei (1 83 62.57 1.42 59 66 0 ++ n 9 54 58.97 1.48 56 63 Peruvian zone of (1 49 62.07 1.62 58 65 character introgression 9 45 58.58 1.56 56 62 o bOlivianus (1 65 60.06 1.08 58 63 o 9 69 56.77 1.13 54 59 o

122 WNG-TAILED HERMIT HUMMINGBIRDS

TABLE 1. (continued)

Subspecies Sex mean s. d. Min Max p Si.

Wing length (WL) [mm] margarettae O' 1 (60) 9 1 (58) ochraceiventris O' 15 64.50 1.24 62.5 67 <0.01 ++ 9 10 61.05 1.38 59 63 0 ++ muelleri O' 25 60.52 0.95 59 62 <0.01 ++ 9 30 57.90 0.96 56 60 0 ++ superciliosus O' 64 59.48 1.09 57 62 <0.01 ++ 9 42 56.79 1.01 55 58 0 ++

Tail measurement used in this study (TL) [mm] griseoventer O' 13 56.08 1.66 54 59 0.772 9 4 56.25 2.06 54 58 0.885 mexicanus O' 14 57.93 2.37 56 61 0.956 9 19 57.08 4.45 47 62 0.485 longirostris O' 81 44.78 2.42 40 57 0.189 9 45 45.36 2.81 38 52 0.255 cephalus O' 68 42.16 2.66 38 49 0.101 9 59 42.86 2.73 37 49 0.150 susurrus O' 45 47.84 2.15 44 53 0.425 9 7 46.57 3.36 41 50 0.364 baroni O' 20 44.23 2.53 41 49 0.298 9 10 45.10 2.08 41 48 0.324 malaris O' 32 48.23 2.66 42 52 0.010 + 9 16 51.13 3.16 45 56 0.004 ++ insolitus O' 10 43.10 1.79 40 46 1.000 9 4 43.00 2.94 41 46 0.953 moorei O' 72 40.28 2.33 34 46 0.663 9 42 40.52 2.68 35 47 0.621 Peruvian zone of O' 41 41.50 2.07 38 46 character introgression 9 36 42.03 2.75 32 47 0.341 bolivianus O' 37 40.14 2.56 36 46 <0.01 ++ 9 28 42.25 2.65 36 48 0.002 ++ margarettae O' 1 (42) 9 1 (46) ochraceiventris O' 16 42.25 2.11 39 47 0.122 9 9 43.50 1.62 41 46.5 0.113 muelleri O' 24 41.58 3.35 34 48 0.030 + 9 24 44.63 3.19 37 51 0.002 ++ superciliosus O' 60 42.68 2.21 37.5 47 <0.01 ++ 9 40 44.20 2.14 39 48 0.001 ++

occur on throat, breast, belly, under tail-coverts, subspecies' morphological characters and dif- and rectrical margins; coloration of crown, nape, ferential diagnostic aids to distinguish them from upperparts, wings, and primary coloration of the another are given in Appendix II. rectrices varied individually, if at all. Geographi- After having grouped specimens of all pOpU- cal variation in plumage coloration, however, lations, the linear measurements BL, WL, and proved to be limited to clearly definable geogra- TL were tested in the resulting subspeciesand the phical areasin most cases;exceptions are discus- populations of the Peruvian zone of character sed in detail in the text. Thus, I took these PG introgression by a one-way analysis of variance, of distinctly reduced color variation as the basic ANOVA. Significances found by ANOVA were taxonomic entities that were later united to sub- confirmed by the Scheffe test with significance species and species.Detailed descriptions of the level fixed at P

123 HINKELMANN

analysis was performed on the specieslevel using Linear me1SUrements,BL, WL, and TL (as the three variables BL, WL, and TL in common. used in this study), of all subspeciesare presented Speciesas applied in this study are considered in Table 1. Comparisons between the sexes as biological species (sensu Mayr 1963, 1969, revealed that O' have longer bills and wings than 1982). Geographically representative taxa whose 9 , confirmed by both statistical tests. To the close relationship is indicated by either wnes of contrary, the shortest distance between the tips character introgression or limited, though obli- of rectrices I and V (TL) do either not exhibit gate morphological distinctness are considered as significal differences, or, in 4 taxa, these are larger subspecies of a biological species. The latter are in females. Fig. 2 demonstrates BL and WL .separatedby at least one apomorphy from other me1SUrementsfor both sexes. such units (i. e., other biological species). Intra- Performance of ANOVA resulted in the indi- specific entities regarded as valid taxa in this cation of several significant differences in all 3 study represent morphologically well-characte- linear measurements between the taxa, and in rized subspecies that could be considered full both sexes.These were exarnined in detail by the species under a phylogenetical species concept Scheffe test, and are presented in Table 2. (sensu Cracraft 1983, McKitrick & Zink 1988). Severallevels of differentiation, obviously repre- Specieslimits within the Long-tailed Hermit hum- senting different periods in the evolutionary mingbird group. Distributed in Central America history of the Long-tailed Hermit humming- and South America W of the Andes ( = trans-An- birds, are easier to portray applying the hierarchy dean) (Figs. 3, 4), griseovente1; mexicanus, of speciesand subspeciesprovided by the biologi- longirostris, cephalus, susurrus, and baroni all cal species concept than by the phylogenetic agree in having three light ochraceous bands species concept because the latter decreasesthe separated by two blackish bands on the outer- information value by "lumping of two categorial most, longest feathers of the upper tail-coverts, levels" (Fjelds;1.1985). different from that of their cis-Andean relatives, and I consider them to represent a distinct RESULTS species, R longirostris. All remaining taxa (Nos. Specimens pertaining to the Phaethornis super- 7-14 in the above list) have two light ochraceous ciliosus-malans-longirostris species group can be and two blackish bands. Whereas the apomor- assigned to 14 different taxonornic entities, or phic band pattern confirms the monophyly of valid subspecies, based on morphological dif- R longirostris, only some of them, griseovente1; ferences (for details of their plumage colorations, mexicanus, baroni and longirostris (with the measurements and geographic distributions, see exception of some ochraceous at the inner edges Appendix II and Table 1): of rectrices IV and V), exhibit white rectrical margins; susurrus and cephalus, however, bear 1. griseoventer ochraceous margins (with the exception of 2. mexicanus whitish tips of rectrix II) similar to their cis-An- 3. longirostris (incl. veraecrucis) dean relatives; the central pair is completely whi- 4. cephalus (incl. cassinii, panamensis) 5. susurrus te-tipped in all Long-tailed Hermit humming- 6. baroni birds. 7. malaris Most cis-Andean members of the R super- 8. insolitus ciliosus-malaris-longirostris species group have 9. moorei (incl. consobrinus, var. nigella, relatively broad ochraceous rectrical margins of ucayalii in part) varying (color ) tone. Only superciliosusand muel- 10. bolivianus (incl. insignis, ucayalii in part) leri have narrow and pale ochraceous, rather 11. margarettae (incl. camargoi) light brownish rectrical margins. A synapo- 12. ochraceiventris morphy of these taxa is provided by their 13: superciliosus (incl. fraterculus, guianensis, whitish under tail-coverts with dark rachises. saturatior) Both superciliosus and muelleri bear distinct 14. muelleri midthroat streakings in both sexes similar to

124 WNG-TAILED HERMIT HUMMINGBIRDS

those of the trans-Andean Long-tailed Hermit TABLE 2. Results of a one-way ANOVA, Scheffetests hummingbirds. (P

125 :ELMANN

male 50

female 48

46

44 T~

42 g; . ~ ~ 40 T eR r:Jn ! 38 YQ ~ Uí~! @.36 lT 1~R. 8~ ~ 34 ~ :c 32 , , , , , .. N = 4 17 46 70 6 8 17 5 53 44 60 1 9 29 38

FIG. 2. a) Billlengths (BL) of O'; b) Billlengths (BL) of 9; c) Wing lengths (WL) of O'; d) Wing lengths (WL) of 9 .Dots and circles including asterisks indicate measurements outside the regular range. PERUVIAN means specimens from the zone of character introgression in Peru (c.f. Fig. 8).

126 WNG-TAILED HERMIT HUMMINGBIRDS

male

female 70

661

127 HINKELMANN

the majority of specimens was grouped to the P. l. baroni represents a well-distinguished "correct" species: O' = 69.5 %, 9 = 63.5 %. De- form isolated in the trans-Andean lowlands of tails of the discriminant analysis' classification Ecuador and NW Peru. There is only very are presented in Table 3. limited, and no geographical, variation in colora- tion and linear measurements (Fig. 5). Geographic variation and zones of character intro. The populations distributed between S Mexi- gression in PhaethorlÍis longirostris. Four sub- co and N Colombia, considered here as sub- species, griseovente1; mexicanus, susurrus, and species longirostris (NW) and cephalus (SE), ex- baroni inhabit relatively small areas (Fig. 4). hibit an extensive zone of character introgression These populations appear to be quite uniform in , both coloration and linear measurements. Excep- between Guatemala and Costa Rica. Several mor- phological characters exhibit gradual change, and tions are observable only in those areas where differences in some casescan be separated clear- their respective ranges are close to each other or to those of the remaining subspecies,longirostris ly only if specimens from the northern- or and cephalus.P. I. griseoventer and P. I. mexicanus southernmost distribution limits are compared. approach each other in S Michoacán, Mexico, These characters are: and apparently hybridize. A specimen from 22 (1) barred throat markings: regularly developed km S Arteaga (DMNH 18892) exhibits inter- in Colombia and Panama, less regularly in Costa mediate colorntion and size. P. I. mexicanus and Rica and Nicaragua, seldom in Honduras and P. I. longirostris meet each other in the state of Guatemala, and lacking in S Mexico. Oaxaca, Mexico. There are only few specimens (2) under tail-coverts: increasing intensity of collected along the SE margins of the Sierra ochraceous coloration from N to S; cephalushave Madre mountains where the subspeciescould get these more ochraceous than longirostris. in contact with each other, and some of them (3) rectrical margins: increasing amounts of (e.g., USNM 477532, DMNH 18657, AMNH ochraceous coloration from N to S. In S Mexican 778267) link both taxa by intermediate colora- populations almost completely white, only the tion and linear measurements. outermost rectrices (IV and V) usually have some

~ p, malaris malaris

-/

.. ... ~:::. P.longirostris Brazil

SOUTH AMERICA

FIG. 3. Distribution and geographical replacement of the species of the Phaethornis superciliosus-malaris- longirostris species group.

128 WNG-TAILED HERMITHUMMINGBIRDS

TABLE 3. Classification results of a discriminant analysis. Only data from specimens with indications for all three linear measurements were processed.

Grouping to

longirostris superciliosus

Males

Po longirostris 227 150 {66.1 %) 46 {20.3 %) 31 {13.7 %) Po malaris 193 29 {15.0 %) 129 {66.8 %) 35 {18.1 %) Po superciliosus 78 5 { 6.4 %) 6 { 7.7 %) 67 {85.9 %)

Females

Po longirostris 133 82 (61.7 %) 33 (24.8 "lo) 18 {13.5 %) Po malaris 127 25 (19.7 %) 73 (57.5 "lo) 29 {22.8 %) Po superciliosus 58 2 ( 3.4 %) 9 (15.5 "lo) 47 {81.0 %)

ochraceous at their inner edges. In populations in O' BL and WL as well as in 9 TL are distinct, from Panama and Colombia these are almost but not significant; Fig. 5), whereas all remaining completely ochraceous with whitish tips of the PG exhibit merely slight differences (unique rectrices (II) next to the central, i. e., longest pair; exception: 9 WL: 6>4+5, P4+5, P4+5, variation was observed. However, a unique speci- P4, P

129 !lNKELMANN

Serra do Navio, ZFMK 89.031) has the shortest bill moorei, but are clearly separated from the varia- of all malaris investigated in this study. tion found within malaris. This, however, may Due to litcle collecting within its distribution be explained by the geographic proximity to range, P. m. insolitus is known from only few moorei, whereas there is a distinct separation localities and specimens (Fig. 6). This limited from malaris. Most probably, insolitus merely number, however, exhibits a certain color varia- represents populations of P. malaris (secondarily) tion: birds from the type locality and its vicinity intergrading between moorei and the nominate closely approach the dark brownish coloration subspeciesbut the probably once existing, exten- of nominate malaris and in some cases are sive zone of character introgression was recently .merely distinguishable by their smaller size. On interrupted by the advance of the closely related the contrary, specimens from E Colombia are P. superciliosus(Figs. 3, 6, 9). Both P. m. insolitus lighter, inore greyish and resemble P. m. moorei. and P. s. superciliosus replace each other at the Thus, insolitus "links" the geographically clearly opposite banks of the lower Negro river and separated subspecies malaris and moorei by co- meet each other, obviously to a certain degree loration. This connection is corroborated only parapatrically, at the upper Negro in the Colom- to a certain degree by linear measurements. BL, bian/Venezuelan border area. In spite of inten- WL, and TL variations of insolitus specimens are sive field work (summarized in Phelps & Phelps ranked within the upper levels of those within 1958, Meyer de Schauensee& Phelps 1978), inso-

Á P. 1, longirostris

@ P. 1. griseoventer

.P, 1. mexicanus .P. 1. cephalus

~ P, 1. susurrus -/ ~ P. 1. baroni

Mexico

Guatemala I, Panama

Rica / /

: ~ ,~;-~ ~

..:.$¡:~:,. ;~ Ecuador ,,' ~ ,o-o.,...,. : ¡ t~~irJ~~~:::, mountain ridges with elevations

.~.t5%~¡~¡¡::~~.exceeding 2.000 m 'Peru 0000'--

( ,~~( Brazil

c c '-.l .character introgression between !--\ f : mexicanus and longirostris , \. ,

FIG. 4. Distribution range of Phaethomis longirostris.

130 WNG-TAILED HERMIT HUMMINGBIRDS

barom ~~( longiros~ cephalus PG 1 I 2 I 3 -¡-r-s-- 6 I 7 I 8 10

n 0"9 12318115714220 ~ 91817201126 ,M 167 ~ 45 -

[mm] : 18 40- r I~~I =I~ 81 8 35 n d'QI2319~ 168145201 72 142221 920182311371 62 1168

,WL

65 e I ¡mm]

60 =I~ 819 I~ 81

- 55

PG population group BL billlength WL wing length

FIG. 5. Geographic variation of linear measurements in Phaethomis longirostris longirostris, p I. cephalus, and p I. baroni. Presented are mean, standard deviation, minimal and maximal values of billlength (BL) and wing length (WL).

litu5 was never found in inner Venezuela where least in centfal Peru, color introgression seemsto it is (ecologically) replaced by R 5upercilio5U5as be influenced by topography. Whereas the grey- well. Thus, only a recent interruption of a N ish, less ochraceous moorei plumage is mainly Amazonian zone of character introgression be- confined to the Andean foothills and adjacent tween malaris and moorei by R 5upercilio5U5 lowlands S to the dept. of Pando, Bolivia (12 km justifies the maintenance of R m. in5olitu5, which S Cobija, 1109S/6851W; LSUMNS specimens) is darker than moorei. and the Shintuya area, Peru (around 1250S/ Except for variation in the color (light 7116W; FMNH specimens), the darker, intensely brownish, whitish, or light ochraceous in ochraceous bolivianus plumage prevails in variable amounts) of the rectrical margins (1 forested areasalong the E Andes slopes north to found no correlations to geographic distribution, Pomará (Dept. of Amazonas, 7823W/0523S; age or sex) R m. moorei is rather uniform in AMNH 185593). Between the areas inhabited plumage. In contrast, some linear measurements only by individuals of moorei or bolivianus vary geographically. Northernmost populations colorations, there is a character introgression of moorei (PG 1 in Fig. 7) exhibit significantly zone of more than 1000 km length observable. shorter bills than the remaining ones ( O' : 2, 3, Specimen series from various localities exhibit 5>1, P1, P1, variable amounts of general moorei or genefal P3, P3, P

131 HINKELMANN

3. 59 km W Pucallpa -AMNH; 4. Hacienda or ochraceous); this variation does not correlate Flor, Puerto Victoria (350 m) -ZFMK; 5. with that of the underparts' coloration. In gene- Lagarto (type locality of R m. ucayalii Zimmer, ral, whitish or light brownish rectrical margins 1950); Santa Rosa, Boca Río Urubamba - as well as whitish under tail-coverts prevail in N AMNH; 6. Balta (300 m) -LSUMNS; 7. Río Peru whereas ochraceous rectrical margins and Mapitunuari (930 m) and E Luisiana (890 m), under tail-coverts are predominantly found in S Cordillera Vilcabamba -AMNH; 8. Cerro de Peru. Pantiacolla (460-1350 m); Pantiacolla (430 m); Almost continuous variation is observed in Hacienda Amazonia, Shintuya (500-830 m); some linear measurements. BL and WL in both Río Palotoa (490 m) -FMNH; Cosñipata (700 sexes decreaseslightly from N to S independent m) -AMNH; S Cobija (325 m) -LSUMNS. of the apparently altitude-related variability in However, note that some bird specimens col- coloration. Careful comparison of all measure- lected by the Olallas along the upper Ucayali ments within 21 geographical units (adjoining river (Lagarto, Santa Rosa) may in fact originate localities) revealed that variation is limited to from the lower Ucayali river (Haffer 1978, p. 43). larger areas,and populations could be grouped to There is also some variability in the color of S PG (Nos. 3-7 in Fig. 7). Some BL and WL the rectrical margins and under tail-coverts. display significant differences (Fig. 7 and Table These areas are always orange-ochraceously in 4). Some PG, however, do not reflect the slight bolivianus, but variable in moorei (rectrical southward decrease of the WL but have larger margins: whitish, light brownish, or ochraceous wings than the neighbouring ones in the N in variable amounts; under tail-coverts: whitish (wing: O': 6>3, S, p3, p

132 IRDS

TABLE 4. Significant differences in bill (BL) and wing lengths (WL) between various poulation groups in the Phaethomis malaris moorei / R m. bolivianus zone of character introgression (numbers of population groups, PG, correspond with those in Fig. 7).

BL: O': 3, 5,6 > 7, p < 0.01;6, 7 > 8,9, p < 0.01; 9 : 6 > 7, 8, 9, p < 0.01;7 > 8, 9, p < 0.01; WL: O': S > 7, p < 0.01;6 > 7,8,9, p < 0.01;7 > 8, p < 0.05;7 > 9, p < 0.01 9: S, 6 > 7, p < 0.05;6, 7 > 8, 9, p < 0.01.

Populations of P. m. bolivianus from extreme occurring between the lower rivers Madeira and SE Peru and Bolivia do not show any appreciable Tapaj6s show almost no differences in either variation in either coloration or linear measure- coloration or linear measurements from Andean- ments. This srems to be the same over the entire based bolivianus. Possibly, Brazilian birds have range of the subspecies, although present infor- slightly more intensely colored rectrical margins. mation indicates an interruption of about 850 However, due to the small number of specimens km between the Bolivian and the Brazilian popu- examined, this character as well as the possibility lations (Fig. 6). This "distribution gap" is more that males more regularly show a well-marked likely due to the lack of ornithological explora- midthroat streaking than males of .true" bolivia- tion than to the absence of suitable habitat. nus cannot be confirmed. Linear measurements There is only one, still unpublished note indi- of the two are similar (exception: TL in O' : cating the occurrence of " Phaethomis supercilio- 8>10, P<0.05; Fig. 7). I do not consider the sus" in the Parque Nacional Noel Kempff Merca- slight character variation sufficient to maintain a do, Bolivia (? in Fig. 6; LSUMNS, unpubl. list) valid subspecies "insignis". that can be referred to P. malaris bolivianus. Geographically well separated from its Ama- Formerly separated as "insignis", populations zonian relatives, margarettae inhabits some

FIG. 7. Geographic variation of linear measurements in Phaethornis malaris moorei and 1?m. bolivianus. Presented are mean, standard deviation, minimal and maximal values of billlength (BL) and wing length (WL).

133 HINKELMANN

134 )NG-TAILED HERMIT HUMMINGBIRDS

remnants of the highly endangered Atlantic not hybridize where they meet. Specimens avai- forests of SE Brazil (Fig. 6). According to Hueck lable in museum collections are from the S bank & Seibert (1972), the intervening area is covered of the Amazon (Solim8es) and from a relatively by unsuitable habitat for at least 2000 km small area between the lower rivers Purús aríd distance. However, bolivianus and margarettae Madeira, and represent only a small portion of are surprisingly similar in all morphological its probable large range. I found no color diffe- characters. Perhaps margarettae has paler under- rences among these PG. Linear meas- parts, and males may have more regularly urements as well exhibited little variation (com- distinct midthroat streakings than those of boli. pared to other malaris subspecies);however, the 'vianus (due to a very limited number of speci- limited number (n = 21 and 5, respectively) Ibens examined this has still to be confirmed). In prohibited any test of significance. contrast, there are several morphological dif- ferences (underparts, under tail-coverts, rectrical Geographic variation in Phaethornis supercilio- margins, and bill curvature) between margarettae sus. The norninate subspecies, superciliosus, oc- and R s. muelleri, the geographically closest cupies the largest area of all subspecific taxa treat- member of the speciesgroup, and I thus consider ed in this paper (Fig. 9). However, I found no margarettae a subspecies of R malaris. The very appreciable geographic variation in coloration. narrow linear distribution theoretically facili- Differences in the amount of ochraceous colora- tates the development of clinally varying char- tion in the rectrical margins are apparently age- acters, in particular becausethe distribution strip related; juveniles always have these areas white, crossesthe va1ley of the sao Francisco river. Due while various amounts of ochraceous coloration to the lack of material, however, this possibility are found only in adults. While there is no color cannot be confirmed today. variation, tests between several PG revealed some Although geographically separated by distri- significant differences in linear measurements bution gaps in various regions, all hitherto treat- (Fig. 10 and Table 5). ed subspecies of R malaris appear to be closely Well separated by the lower Amazon, super- related to each other based on morphological ciliosus and muelleri do not exhibit any character similarity or character introgression. Only R m. introgression. Although the muelleri specimens ochraceiventris does not fit easily into this examined represent only the westernmost and assemblage. Its distribution range is clearly easternmost populations (Figs. 9, 10), I found no separated from that of bolivianus by the course geographic variation in either coloration or of the lower Madeira, and from those of insolitus linear measurements between them. and moorei by the Amazon (Solimoes) (Fig. 6). Although the distribution ranges of ochraceiven- Sympatry and hybridization in the Phaethornis tris and moorei may closely approach each other superciliosus-malaris-longirostris species group. in the lower Ucayali river region (Figs. 3, 6), The distribution of Phaethornis longirostris is there is no indication of character introgression. completely limited to trans-Andean, i. e., Central U nfortunately, little or no collecting has been American and west-Andean South American done in the E and SE of this area, along the Peru- lowlands and lower mountain ridges (Figs. 3, 4). vian- Brazilian border where these subspeciespro- At present, the members of this species cannot bably are in contact. It is possible that they do come in contact with R superciliosusor R malaris

TABLE 5. Significant differences in linear measurements (billlength, BL, and shortest distance between tips of rectrices I and V, TL) among population groups (PG) in Phaethornis superr:iliosussuperciliosus (numbers for PG correspond with those in Fig. 10).

BL: O': 3,6 > 4, p < 0.05;5 > 3,4,6, p < 0.01;5 > 7+8, p < 0.05; 9: 6 > 3, p < 0.05;6 > 7+8, p < 0.01. TL: 9: 4+5 > 3, 7+8, p < 0.05;3 > 6, p < 0.05;4+5 > 6, p < 0.01

135 HINKELMANN

due to topographical barriers. Narrow lowlands Surinam, French Guiana, and adjacent Brazil with gallery forests, plantations, wooded pastu- (Novaes 1974, Mees 1977). Data on the habitat res and similar habitats all along and around the requirements of both R m malari5 (Mees 1977, base of the N Andes are inhabited by R anthophi- Dick et al. 1984) and R 5. 5upercilio5U5(Snethlage lus, a speciesof similar body mass and apparently 1913, Nicholson 1931, Davis 1958, Snyder 1966, better adapted to drier, more open habitats than Haverschmidt 1968, Snow 1973, Willis 1977, Long-tailed Hermit hummingbirds. Dick et al. 1984) indicate that they occupy the R superciliosus and R malaris, however, be- same altitudinal and habitat niche. Thus, they have like paraspecies in most areas and replace apparently avoid direct competition by, at least, each other on the opposite banks of some major depending on different food resources, as indi- rivers (Figs. 3, 6, 9); thus, ecologically the species cated by their body masses(R m. malari5: 7.5-10 behave towards each other like several subspecies grams; R 5. 5upercilio5US:4-6.5). This situation is (within both R superciliosus and R malaris) similar to the one found regularly in the Carib- which are separatedby rivers. They replace each bean islands (Lack 1973, Schuchmann 1980). other geographically where they meet. This is Extensive sympatry can occur only in taxa the case along the upper Negro river, the Casi- which are genetically and reproductively iso- quiare junction, and the upper Orinoco river lated. This does not necessarily exclude occasio- where R s. superciliosus and R m. insolitus meet nal hybridizations; however, until today only each other. Because there is no indication either one example could be found. A 9 collected by of character introgression or of broader sympa- S.M. Klages at Pied Saut, French Guiana, is per- try, these taxa probably replace each other para- fectly intermediate in coloration, linear measure- patrically to avoid direct competition. Only one ments, and even in bill curvature (Hinkelmann exception is presented by R m. malaris and R s. 1996). Both malari5 and 5upercilio5U5were record- superciliosus which occur sympatrically in E ed from Pied Saut (Zimmer 1950).

I.

;' .P. s. superciliosus ~ .[t] P. s. mue//eri ~, ..::::::: .:.;" ,,:.:.:.;.. F hG . ~~.:;;~~.~.::;..--renc ulana

\\¡¡¡¡\¡¡\f..-/ .8 ~~~~:::Colombia .:. :/ --J 7 > \ .

)'\. v )

) / Brazil ~~ ~1

FIG. 9. Distribution range of Phaethornis superciliosus.

136

~ WNG-TAILED HERMIT HUMMINGBIRDS

FIG. 10. Geographic variation of linear measurements in Phaethomis superciliosus. Presented are mean, standard deviation, minimal and maximal values of billlength (BL) and wing length (WL).

Biogeo.graphical remarks. Phaethornis supercilio- Data on the habitat requirements of R longi- sus/R rnalaris and R longirostris represent a cis-/ rostris griseoventer (Phillips 1962, Schaldach trans.Andean relationship as it is known from 1963), R I. mexicanus (Binford 1968, 1989), and severa1 bird species, superspecies and species R I. baroni (Oberholser 1902, Wiedenfeld et al. groups (e.g., Haffer 1967, 1975). It is obvious 1985) indicate that these subspecies at the that lowland biota of both W and E Andean northern- and southernmost limits of the area~were once in contact. Warm, humid condi- species' distribution are adapted to less humid tions probably permitted the predecessors of R forest types than are the remaining subspecies. longirostris to cross the northern Andean ridges This may, at least in part, explain why there is a that act as an almost insuperable barrier to distribution gap between the ranges of R I. cepha- species adapted to humid lowland forests today. Ius and R I. baroni: Phaethomis yaruqui, a con- The crossing may have occurred at lower eleva- generic species of similar body mass, appears to tions of the Coastal Cordillera along the Colom- be better adapted to extremely humid conditions bian/Venezuelan border and between the ex- and replaces R longirostris in the lowland forests treme northern foothills of the East Cordillera of trans-Andean Colombia and Ecuador. Haffer and the isolated massif of the Sierra Nevada de (1975) already presumed that the lack of seasonal Santa Marta in N Colombia. In trans-Andean forests in W Colombia may be responsible for South America and Centra1 America, the an- the absence of Long-tailed Hermit humming- cestors of R longirostris probably spread out and birds in this area. However, F. Gary Stiles ob- colonized all suitable habitats. Subsequent clima- served R longirostris in Bahia Solano, north-cen- tological and geological events temporarily inter- tral dept. Chocó, Colombia, and expects its oc- rupted the probably once continuous distribu- currence even farther to the S in adequate tion range. According to Haffer' s ( 1967, 1969, habitats (Stiles, in litt.). 1975, 1982) model of biological diversification Within the cis-Andean South American taxa, (refuge theory), several populations may have the history of distribution ranges still provides survived geographically and genetically isolated some problems. Subspeciesof R malaris in most from one another resulting in the evolution of cases inhabit areas that are in accordance with several morphologically differentiated popula- the location of forest refuges postulated by Haf- tions. Zones of character introgression between fer (1969, 1974, 1978) for drier periods in the the most of the adjoining PG and subspecies past. (Only the distribution of R m. ochraceiven- indicate that the isolation period was not suf. tris does not include any forest refuge.) In some ficient to obtain reproductive isolation. cases,subspecies' distributions are separatedfrom

137 another by major rivers (Amazon [Solim6es], Previous attempts at classifying the Phaethornis lower Madeira and lower Tapaj6s) that probably superciliosus-malaris-longirostris species group. facilitated the morphological differentiation of The classification of the Long-tailed Hermit several taxa. E superciliosusmuelleri and R mala- hummingbirds in three species,R superciliosus,R ris bolivianus, which are separated by the lower malaris, and R longirostris was already presented Tapaj6s river, may be in parapatric contact in by Cabanis & Heine (1860) and Cory (1918). All southern Pará, Brazil, but no specimens are remaining authors accepted a larger number of available from this area. Separation of the sub- species(e.g., Gould 1861, Boucard 1895, Hartert 1900, Simon 1921) or limited their number to species' distribution ranges by major rivers is two. Salvin & Elliot (1873) accepted R supercilio- especially important in R malaris because this sUSand R longiro5tri5, Simon (1897) R supercilio- species is limited to the forests of the terra firme sUsand R bolivianu5, whereas Peters (1945) and whereas the várzea and other river-created forest Zimmer (1950) assigned the taxa to R supercilio- types in W Amazonia are inhabited by Phaethor- sUs and R malaris. nis hispidus, another closely-related species of In R longirostris, several taxa were regarded as similar body mass (Remsen & Parker 1983). separate speciesby some authors (Boucard 1895, Thus, the riverine barriers between the respec- Hartert 1900, Simon 1921), whereas they were tive ranges are not only represented by the width treated as subspecies of R longirostri5 by Cory of the rivers but, along their lower courses, also (1918) and Todd (1942), as subspeciesof R 5Uper- enlarged by a river-created vegetation of variable cilio5U5by Peters (1945) and as those of R malaris extension. by Zimmer (1950). Heretofore, specimens The subspecies of Phaethomis superciliosus belonging to the Central American populations "interrupt" the distribution ranges of closely linked by an almost clinal relationship (con- related subspeciesof R malaris by inhabiting the sidered here as R I. longiro5tri5 and R I. cephalu5) intervening areas. As already mentioned earlier, were assigned to four subspecies (from NW to R s. superciliosus occurs between the areas in- SE): veraecrucis,longiro5tris, cephalu5,and cassinii habited by I! m. insolitus and R m. malaris, (Griscom 1932a, Peters 1945, Zimmer 1950, Wet- whereas R s. muelleri occupies the only region more 1968). Their respective morphological where R m. bolivianus and R m. margarettae differences and distribution limits were repeated- might come in contact with each other during a ly discussed: warmer, more humid period than today. This "veraecruci5" -longirostris: Austin 1929, Peters assumption would reproduce the probable situa- 1945, Brodkorb 1943, Friedmann et al. 1950, tion that enabled the ancestors of R m. marga- Paynter 1957; rettae to colonize the Atlantic forests of SE longiro5tri5 -cephalu5: Hartert 1897a, Peters Brazil. The most likely connection between the 1929, Griscom 1932a, Todd 1942, Monroe 1968; lowland rain forests of Amazonia and SE Brazil cephalu5 -"ca5sinii": Bangs & Barbour 1922, would be established along the southern bank of Griscom 1932a, Zimmer 1950, Wetmore 1968. the Amazon and north of the Brazilian high- However, these studies did not reveal the lands in the statesof Maranhao, Piauí, Ceará, Rio gradual character introgressions among the trans- Grande do Norte, and Paraiba (T. A. Parker, Andean populations. pers. comm.). Another alternative, a forest con- R I. baroni was described as a separate species (Hartert 1897a) with closer affinities to " R super- tact via the Brazilian states of sao Paulo and Para- ná, and across Paraguay to Bolivia, however, is cilio5U5moorei" than to R longirostris. Isolated in unlikely due to the presence of Phaethomis eury- t.rans-Andean lowlands, it may have achieved nome, an endemic species of similar body mass reproductive isolation and, if so, may thus be replacing R malaris margarettae in the S and sw. considered a separate species, as the only taxon In the southern parts of its range, R m. marga- within the trans-Andean Long-tailed Hermit rettae inhabits the lowland forests whereas R Hummingbirds. However, this possibility can- eurynome is limited to mountain forests (Hinkel- not be verified on morphological characters mann 1988b). alone.

138 IONG:rAlLED HERMlT HUMMINGBIRDS

Relationships of the cis-Andean South Ame- forms of a 'ring species'...". Consequently, he rican taxa have always provided some taxonomi- emphasized some intermediate morphological cal difficulties. First, there has been confusion characters in populations geographically linking r regarding the identity of Trochilus superciliosus the ranges of morphologically well-differentiated Linnaeus, 1766. Gould (1861) applied it to the subspecies. He pointed to the intermediate larger and darker speciesfrom "Cayenne and the coloration and size of some populations from adjacent countries" (Trochilus malaris Nord- the Venezuelan/Colombian border area (that he mann, 1835) and was followed by Boucard (1895) described as R malaris insolitus) between nomi- and Hellmayr (1906). As a consequence, the nate malaris and moorei, later confirmed by , misnaming resulted in the descriptions of two Blake (1962). Zimmer (1950) also recognized that synonyms: Phaethornis fraterculus Gould, 1861, Peruvian birds inhabiting the area between the S and Pháethornis guianensis Boucard, 1891 to bank of the Amazon and the Chanchamayo separate the smaller and lighter species. Others, Valley (Dpto. Junín) differed from moorei, ochra- e.g., Hartert 1897a, Salvin & Elliot 1873, Salvin ceiventris, and bolivianus. Thus, he described 1892, Penard & Penard 1910, treated both species these as a new subspecies, R malaris ucayalii occurring in French Guiana as synonyms. which he considered to be intermediate between Finally, Pelzeln (1871), Berlepsch (1887, 1888, ochraceiventris and bolivianus. Zimmer (1950) 1908), Hartert (1897b, 1900) and Hellmayr determined SE Peruvian birds as intermediate be- (1912) presented the correct taxonomical treat- tween ucayalii and bolivianus but did not dis- ment of both nominate subspecies. cover the introgression of characters between Another problem has been how to assign the bolivianus and moorei along the E Andean slopes various cis-Andean subspeciesto either R superci- in Central Peru leaving "ucayalii" as an inter- liosus or R malaris. Several taxa were regarded as grade, or invalid taxon. Interestingly, a "transitio- separate species,e.g., R m moorei (as "Phaethor- nal" relationship between moorei and bolivianus nis consobrinus" [Reichenbach, 1854, nomen nu- was already emphasized by Seilern (1934) who dum] by Gould 1861, Eudes-Deslongchamps investigated SE Peruvian birds. 1881, and Boucard 1895) and R m. bolivianus Due to its morphological similarity to R (Gould 1861; Boucard 1895; Simon 1897, 1921; longirostris, typical bolivianus was considered to and Hartert 1900). Todd (1942), however, con- be of mislabeled origin by Salvin & Elliot (1873)j sidered all cis-Andean taxa known at that time as later authors regarded it as a subspecies of R valid species.Peters (1945) assigned all subspecies longirostris (Oberholser 1902, Cory 1918) or to Phaethornis superciliosus in contrast to a mo- preferred to treat it as a separatespecies" ...unless notypical R malaris. This treatment was accepted future explorations show that it occurs in the by Eisenmann (in Meyer de Schauensee 1966), long stretch of intervening countries ..." (Har- whereas Zimmer (1950) assigned all subspecies tert 1897a). Populations occurring S of the Ama- with the exception of saturatior to R malaris. zon between the lower rivers Madeira and Tapa- Recently, Grantsau (1988) separatedthe Brazilian jós, formerly separated as "insignis", hitherto taxa occurring S of the Amazon river as a were not carefully compared with bolivianus distinct species, R ochraceiventris, assigning to it from Bolivia, but considered as a valid subspecies muelleri, insignis, camargoi, margarettae, and of R superciliosus (Todd 1937) or even a species ochraceiventris. R ochraceiventris is said to be (Todd 1942). Peters (1945) and Pinto (1978) again distinguishable from R superciliosus(sensu Peters regarded them as subspecies of R superciliosus. 1945) ofN Amazonian Brazil by mandible color, The occurrence of Phaethornis malaris in SE song, and nest structure, but, unfortunately, Brazil has been known for a relatively short time Grantsau (1988) neither specifies these differen- (reviewed by Hinkelmann 1988b, 1989b). Ruschi ces nor discussesthe relationships to bolivianus (1972) described birds of a population inhabiting and its character introgression with moorei. remnant forest in Espirito Santo as Phaethornis Zimmer (1950) was the first to examine the margarettae after having compared these with all relationships within the cis-Andean taxa and subspecies of R malaris (sensu Zi!11mer 1950). stated: "It appeared even that it might be possible U nfortunately, he did not provide sufficient to consider malaris and superciliosus as terminal~ diagnostical characters to separate this "species"

139 HINKELMANN from R malaris (R superciliosussensu Peters 1945); DISCUSSION thus, the specieswas considered doubtful (Mayr Unfortunately, the continuously increasing for- & Vuilleumier 1983, Collar 1987) or even invalid est destruction in Central and South America (Grantsau [in Vuilleumier & Mayr 1987], 1988, has devastated many localities treated as in- Teixeira et al. 1987, Hinkelmann 1988b). Sick habited by Long-tailed Hermit hummingbirds in (1985) considered margarettae as the sister species this paper. Thus, distribution ranges given of the Amazonian superciliosus (sensu Peters should be considered as referring to the situation 1945). Recently, Grantsau (1988) separated birds prior to the large-scalehabitat alteration of this from Pernambuco as" Phaethornis ochraceiven- century. .tris camargoi", considering these as geographical- ly well-isolated from " R o. margarettae". How- Long-tailed Hermit hummingbirds form a species group. At first sight, they seem to repre- ever, he neither provided definite morphological sent a situation similar to those of many other characters not due to individual variation nor did tropical American superspecies distributed in he discuss the probably uninterrupted distribu- both cis- and trans-Andean lowlands, e.g., Pio- tion range of margarettae before the Europeans nopsitta caica ( 6 species), Pipra erythrocephala ( 5 arrived in SE Brazil. According to Hueck & species),P. se1r?na(6 species)(Haffer 1970), Cotin- Seibert (1972), a homogeneous kind of rain forest ga maynana (6 species), Psarocolius bifasciatus ( 4 covered the coastallowlands between the states species),Ramphastos dicolorus (4 species) or Sele- of Paraiba and Espirito Santo. A summary of nidera maculirostris (6 species) (Haffer 1974). locality data for R m. margarettae is provided by Many taxa of the Phaethornis supe1t'iliosus-mala- Hinkelmann (1989b). ris-Iongirostris species group are parapatric or R m. ochraceiventris was considered a sub- even allopatric and most of them probably species of "R boliviana" (Simon 1921, Hartert occupy a single ecological niche. However, the 1922), of R malaris (Zimmer 1950), of R super- sympatric occurrence of P. malaris malaris and P. ciliosus (Hellmayr 1912, Peters 1945, Pinto 1978), superciliosus supe1t'iliosusin French Guiana, E and a separate,monotypic speciesR ochraceiven- Surinam and adjacent Brazil indicates that at tris (Hellmayr 1907b, Todd 1942, Gyldenstolpe least two taxa successfully established sympatry 1950). Zimmer (1950) detected some morpholo- which is probably supported by significant diffe- gical approaches to neighbouring "insignis" and rences in body mass and bill size. There are 3 bio- "ucayalii" which he concluded to be ". ..inter- logical species united in the Long-tailed Hermit mediate between R m. moorei ...and R m. ochra- hummingbird species group: P. malaris, P. super- ceiventris ...". Probably, ochraceiventris does not ciliosus and P. longirostris. Two taxa, P. m. ochra- have regular contact with the taxa occupying the ceiventris and P. 1. baroni, may also turn out to opposite banks of the rivers Amazon and Madei- be separate species. ra. It has perhaps achieved reproductive isolation Plumage coloration in Long-tailed Hermit and may thus be regarded as a distinct species, hummingbirds appears to be very conservative. but its affinities to moorei are still obscure. As a consequence, this overall similarity caused Several authors tried to assign different pOpU- many authors to treat the birds as belonging to lations within Phaethornis superciliosussupercilio- no more than two species.Unfortunately, there sus to separate additional subspecies, in particu- are no studies on the systematics of the P. supe1t'i- lar, those of S Venezuela (e.g., Hartert 1900, liosus-malaris-Iongirostris species group based on Simon 1921, Zimmer 1950, Phelps & Phelps non-morphological methods that treat a number 1958, Grantsau 1988). Peters (1945), however, of taxa. Based on electrophoretic analyses of en- considered Phaethornis superciliosa saturatior zymes, Capparella ( 1987) investigated the genetic Simon, 1921, as "doubtfully distinct from R s. differentiation of Long-tailed Hermit humming- superciliosus" and Todd (1942) found "no birds from opposite river banks in Amazonian grounds for the distinction" of "saturatior". The Peru and concluded that " Phaethomis supe1t'ilio- sus moorei" (N of the Amazon) and " Phaethornis affinities between superciliosus and muelleri, resulting in the assignment of muelleri as the superciliosus ucayalii" ( = P. malaris ochraceiven- only valid subspecies of R superciliosus in this tris; S of the Amazon) "are different species if paper, have not been discovered previously. one compares those levels to allozyme analyses~

140 WNG-TAILED HERMIT HUMMINGBIRDS

of temperate zone birds" (Capparella, in litt.). several plumage characters differ simultaneously Gill & Gerwin (1989) examined the protein between Guatemala and NW Honduras as well relationship of 12 Phaethornis species including as between SE Honduras and Costa Rica. Similar Long-tailed Hermit hummingbirds from the to longirostris and cephalus, there is an obvious Peruvian departments of Pasco, Loreto, and San distributional break in Honduras between two Martín (R malaris bolivianus, R m moorei) but closely related Ortalis species, O. vetula (NW) did not investigate possible intraspecific diffe- and 0. garrula (SE). Whereas these differ in their rences. habitat preferences (Vaurie 1968), however, there There are also few studies on behavioral is apparently no such separation between P. l. , characters in members of the R superciliosus-ma- longirostris and P.l. cephalus(according to habitat laris-Iongirostris speciesgroup that may contribu- data from RusseII1964, Skutch 1964, Slud 1964, te to the systematic relationship among the taxa. Monroe 1968, Wetmore 1968, Stiles & Wolf Snow (1973) reported a R s. superciliosus a to in- 1979, Binford 1989). Stiles (in litt.) pointed to trude into the lek territory of another a (of R clearly geographical-based differences in P. l. s. superciliosus): "the owning a opened his beak cephalusfrom Costa Rica; birds from the SW are and displayed his orange-red gape. The visitor significantly larger than those of the Caribbean then touched the inside of the displayed gape eit- her with its tongue or the tip of its beak." A very slope. In cis-Andean South America, contacts of similar, probably homologous behavior was re- several Long-tailed Hermit hummingbird sub- ported for R s. muelleri (Hellmayr 1912) and may species are inhibited by the courses of large support the affiliation to the same species.Stiles rivers. Consequently, there are no zones of & Wolf (1979), however, indicate that they could character introgression along the rivers even never observe a corresponding behavior in R lon- when taxa of opposite banks are considered to girostris cephalus,a taxon still regarded as conspe- cific. Unfortunately, there are no similar descrip- belong to the same species and might interbreed tions or detailed informations of lek behavior in freely where they get in contact without physical any subspecies of R malaris published. barriers. Zimmer (1950) discovered character Zones of character introgression between the introgression and intermediate plumage charac- core areas of the ranges of several taxa point to ters between most Amazonian taxa and regarded the lack of genetical barriers. In R longirostris, P. m. malaris and P. s. superciliosusas the terminal these are barely evident (few collecting localities) forms of a "ring species". There is a remarkable between griseoventer and mexicanus as well as plumage similarity between malaris and insoli- between mexicanus and longirostris. As a con- tus, an obvious zone of character introgression sequence,Banks (MS) prefers to treat griseoventer (though few collecting localities) between insoli- and mexicanus as separate species,and Howell & tus and moorei, and an extensive zone of charac- Webb (1995) recently included both taxa in a ter introgression between moorei and bolivianus. distinct species, R mexicanus. There is probably Regarding the distributions of these taxa, there is no zone of character introgression between an almost continuous area -N of the Amazon cephalusand susurrus today, and baroni is geogra- from French Guiana (interrupted in Venezuela phically clearly separated from the remaining and Guyana) to Colombia, Ecuador, Peru, and subspecies. However, there is an extensive Bolivia, and S of the Amazon to the W bank of hybridization zone between longirostris and the Tapajós river -inhabited by a single species. cephalus. Due to the relatively narrow distribu- In contrast to a "ring species", however, there is tions of both subspecies in Central America, no indication of a continuing genetical relation- their secondary contact area (Guatemala - ship between bolivianus and the remaining E Costa Rica) exhibits a situation very similar to a Amazonian taxa, muelleri and superciliosus.If P. phenocline. In contrast to clinal variation, how- superciliosus muelleri and P. malaris bolivianus ever, character variation in Central American should get in contact in the headwater region, Long-tailed Hermit hummingbirds is highest in most likely they would remain in parapatry or the (N)W and in the (S)E of Honduras where one taxon would replace the other on a long- both subspecies may approach each other, and~ term basis; they are of equal body mass (4-7 g).

141 ~LMANN

Haffer (1970, 1974) provided examples for REFEREN CES speciescrossing the Tapajós S of its lower course Austin, O.L., Jr. 1929. Birds of the Cayo District, (Pipra nattereri, Pteroglossusbeauharnaesii) that British Honduras. Bull. Mus. Comp. Zool. 69: obviously remain in parapatry with their con- 361-394. geners of the opposite bank. Xipholena punicea Bangs, O., & T. Barbour. 1922. Birds from Darien. of N and W Amazonia also crosses the Tapajós Bull. Mus. Comp. Zool. 65: 191-229. in the headwater region whereas the SE Amazo- Banks, R. C. (Unpubl. MS). Comments on the syste- nian X. lamellipennis was able to colonize the W matics of some Central American hermit hum- bank of the lower Tapajós (Haffer 1970). mingbirds. Bartholomew, J. C., Christie, J. H., Ewington, A., The close relationship between superciliosus Geelan, P. J. M., Lewis, H. A. G., Middleton, P., & and muelleri indicates that even broad rivers need B. Winkleman. 1985. The Times atlas of the world. not rep~esent an important barrier for the range 7th ed., London. expansion of terra firme birds. There are several Berlepsch, H. von. 1887. Kritische Übersicht der in species of Amazonian birds limited to the lower den sogenannten Bogota-Collectionen (S. 0. Co- Amazon region but inhabiting both the N and lombia) vorkommenden Colibri-Arten. J. Orn. 35: S banks of the Amazon, e. g., Ortalis motmot 313-336. (Vaurie 1968), Phoenicircus carnifex, Euphonia Berlepsch, H. von. 1888. Notes on some Neotropical cayennensis(Haffer 1970), Pteroglossusaracari, or birds belonging to the United States National Museum. Proc. U. S. Nat. Mus. 11: 559-566. Brachygalba lugubris (Haffer 1974). Besides, the Berlepsch, H. von. 1908. On the bin:ls of Cayenne. closely related Phaethornis bourcieri was able to Novit. Zool. 15: 261-324. cross the lower Amazon as well, and like R super- Binford, L. C. 1968. A preliminary survey of the avi- ciliosus, different subspeciesinhabit the opposite fauna of the Mexican state of Oaxaca. Ph. D. diss. banks (Hinkelmann 1989a). Major rivers are able Louisiana State University, Baton Rouge. to prevent an extensive gene flow and may sup- Binford, L. C. 1989. A distributional survey of the port the differentiation of taxa. However, it is birds of the Mexican state of Oaxaca. Orn. still unproven that riverine barriers cause specia- Monogr., No.43. tion as emphasized by, e.g., Sick 1976, Connor Blake, E. R. 1962. Birds of the Sierra Macarena, eastern Colombia. Fieldiana (Zool.) 44: 69-112. 1986, Salo et al. 1986, and Capparella 1987. It is Boucard, A. 1891. Notes on rare species of Humming unlikely in long-tailed Hermit hummingbirds Birds and descriptions of several supposed new becausesome taxa occur on both banks of major species in Boucard's Museum. Humming Bird 1: rivers (Purús, Juruá: ochraceiventris; Xingú, 17-18. Tocantins: muelleri; Marañon, Napo: moorei), Boucard, A. 1892. A complete list up to date of the although other rivers (Amazon, Negro, Madeira, Humming birds found in Colombia, with descrip- Tapajós) delimit the range of taxa. tions of several supposed new species. Humming Bird 2: 73-87. Boucard, A. 1895. Genera of Humming Birds. Hum- A CKN OWLEDG EMENTS ming Bird 5: 1-402. Brisson, M. J. 1760. Ornithologia sive synopsis metho- This paper profited from valuable comments by dica ...Paris. Robert Bleiweiss, Jürgen Haffer, F. Gary Stiles, Brodkorb, P. 1943. Birds of the gulf lowlands of and Fran~ois Vuilleumier; I also thank Karl-L. southern Mexico. Misc. Publ. Mus. Zool. Univ. Schuchmann for many discussions on the topic, Mich., No.55. and all curators of bird collections for enabling Cabanis, J., & F. Heine. 1860. Museum Heineanum. me to study specimens in their care (museum Verzeichnis der omithologischen Sammlung des acronyms are presented in Appendix 1). The Oberamtmanns Ferdinand Heine auf Gut St. Deutscher Akademischer Austauschdienst pro- Burchard vor Halberstadt., Volume 3. Halberstadt. Capparella, A. P. 1987. Effects of riverine barriers on vided a study grant to examine hummingbird genetic differentiation of Amazonian forest under- specimens in the United States of America. growth birds. Ph. D. diss. Louisiana State Universi- Martha Monroy de Hinkelmann kindly edited ty, Baton Rouge. the Spanish summary and Hermann Müller Collar, N. J. 1987. Red data bin:l Hook-billed Hermit. helped with the statistics. World Birdwatch, 9/1, p. 5.

142 WNG-TAILED HERMIT HUMMINGBIRDS

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Scobel, A. 1912. Andrees Allgerneiner Handatlas. 5th Stiles, F. G. 1980. The annual cycle in a tropical wet ed. Bielefeld and Leipzig. forest hummingbird community. Ibis 122: 322- Seilern,. J. 1934. Ornithologische Miszellen. Ann. 343. Naturhist. Mus. Wien 47: 33-41. Stiles, F. G., & L L. Wolf. 1979. Ecology and evolution Sick, H. 1967. Rios e enchentes na AmazOnia corno of lek mating behavior in the Long-tailed Hermit obstáculo para a avifauna. In Lent, H. (ed.). Atas Hummingbird. Orn. Monogr., No.27.. do sirnp6sio sobre a biota arnazOnic, Volurne 5 Teixeira, D. M., Nacinovic, J. B., & F. B. Pontual. 1987. (Zool.). Rio de Janeiro. Notes on some birds of northeastern Brazil (2). Sick, H. 1985. Ornitologia brasileira. Urna introdu~ao, Bull. Brit. Orn. Club 107: 151-157. Volurne 1. Brasilia. Todd, W E. C. 1937. New South American birds. Ann. Sirnon, E. 1897. Catalogue des especes actuellernent Carn. Mus. 25: 24>-255. , connues de la farnille des Trochilidae. Paris. Todd, W E. C. 1942. List of the hummingbirds in the Sirnon, E. 1921. Histoire naturelle des Trochilidae collection of the Carnegie Museum. Ann. Carn. (Synopsis et catalogue). Paris. Mus. 29: 271-370. Skutch, A. F. 1964. Life histories of herrnit hurnrning- Vaurie, C. 1968. Taxonomy of the Cracidae (Aves). birds. Auk 81: 5-25. Bull. Amer. Mus. Nat. Hist. 138: 131-260. Slud, P. 1964. The birds of Costa Rica. Distribution Vuilleumier, F., & E. Mayr. 1987. New species of birds and ecology. Bull. Arner. Mus. Nat. Hist. 128: describedfrom 1976to 1980.J. Orn.128: 137-150. 1-430. Wetmore, A. 1%8. The birds of the Republic of Pana- Snethlage, E. 1913. Über die Verbreitung der Vogel- ma, Volume 2. Columbidae (Pigeons) to Picidae arten in Unterarnawnien. J. Orn. 61: 469-539. (Woodpeckers). Smithson. Misc. Coll. 150, 2. Snow, B. K. 1973. The behavior and ecology of herrnit Wiedenfeld, D. A., Schulenberg, T. S., & M. B. Rob- hurnrningbirds in the Kanaku Mountains, Guyana. bins. 1985. Birds of a tropical deciduous forest in Wilson Bull 85: 163-177. extreme northwestern Peru. Pp. 305-315 in Buck- Snow, B. K. 1981. Relationships between herrnit hurn- ley, P. A., Foster, M S., Morton, E. S., Ridgely, R. rningbirds and their food plants in eastern Ecuador. S., & F. G. Buckley (eds.). Neotropical ornitholo- Bull. Brit. Orn. Club 101: 387-396. gy. Orn. Monogr., No.36: 305-315. Snyder, D. E. 1966. The birds of Guyana (forrnerly Willis, E. O. 1977. Lista preliminar das aves da parte British Guiana). Salern. noroeste e áreas vizinhas da Reserva Ducke, Ama- Stephens, L., & M. A. Traylor, Jr. 1983. Ornithological zonas, Brasil. Rev. brasil. Biol. 37: 585-601. gazetteer of Peru. Carnbridge. Young, M. A. 1971. Foraging for insects by a tropical Stephens, L., & M. A. Traylor, Jr. 1985. Ornithological hummingbird. Condor 73: 36-45. gazetteer of the Guianas. Carnbridge. Zimmer, J. T. 1950. Studies of Peruvian birds No.55. Stiles, F. G. 1975. Ecology, flowering phenology, and The hummingbird genera Doryfera, Glaucis, Thre- hurnrningbird pollination of sorne Costa Rican netes, and Phaethornis. Amer. Mus. Novit., No. Heliconia species. Ecology 56: 285-301. 1449.

APPENDIX I Museums, with their aconyms, providing specimens for this study AMNH American Museum of Natural History, New York ANSP The Academy of Natural Sciences of Philadelphia BMNH British Museum (Natural History), Tring CMNH Carnegie Museum of Natural History, Pittsburgh DMNH Delaware Museum of Natural History, Greenville FMNH Field Museum of Natural History, Chicago IVIC Instituto Vallecaucano de Investigaciones Cient¡ficas, Cali LACM Natural History Museum of Los Angeles County, Los Angeles LSUMNS Louisiana State University, Museum of Zoology, Baton Rouge MBPML Museu de Biologia "Prof. Mello-Leitao., Santa Teresa MCZ Museum of Comparative Zoology, Harvard University, Cambridge MNHB Museum für Naturkunde der Humboldt-Universitat zu Berlin MNHN Muséum National d'Histoire Naturelle, Paris MZUSP Museu de Zoologia da Universidade de sao Paulo HINKELMANN

NHMW Naturhistorisches Museum Wien NMFS Naturmuseum und Forschungsinstitut Senckenberg, Frankfurt/M. PMNH Peabody Museum of Natural History, Yale University, New Haven RNHL Rijksmuseum van Natuurlijke Historie, Leiden ROM Royal Ontario Museum, Toronto SMNS Staatliches Museum für Naturkunde in Stuttgart SMTD Staatliches Museum für Tierkunde, Dresden UCB Museum of Vertebrate Zoology, University of California, Berkeley ÜMB Überseemuseum Bremen UNCB Instituto de Ciencias Naturales, Museo de Historia Natural, Universidad Nacional de Colombi; Bogotá T.JMMZ Museum of Zoology, University of Michigan, Ann Arbor USNM National Museum of Natural History, Smithsonian Institution, Washington, D. C. WFLA Westem Foundation of Vertebrate Zoology, Los Angeles ZFMK Zoologisches Forschungsinstitut und Museum Alexander Koenig, Bonn ZMUC Zoologisk Museum Copenhagen ZMUH Zoologisches Institut und Zoologisches Museum, Universitat Hamburg ZSM Zoologische Staatssammlung, München

APPENDIX II

Taxonomy, type localities, distributions and characters Characters: Sma1ler and more curved-billed than R I. of all taxa in the Phaethomis superciliosus-malaris-longi- griseoventer and R I. mexicanus. Birds of the northern- rostris species group most populations tend to have large amounts of white in their rectrical margins while there is an increasing Phaethomis longirostris amount of ochraceous coloration from Guatemala R longirostris griseoventer southward. Throat on both sides of the midthroat Phaethomis superciliosus griseoventer Phillips, 1962. streaking more uniform, less barred than in R I. cepha- Type specimen: no type specimen designated; a type Ius and R I. susurrus. series of 9 specimens is preserved in the DMNH. Type Distribution: S Mexico, states of Veracruz, Oaxaca, locality: "Arroyo de la Cordoncillera, al sur de Puerto Tabasco, and Chiapas; N Guatemala; Belize; NW Hon- Vallarta, Jalisco" (Mexico; Phillips 1962). duras (Fig. 4). Characters: Smaller, underparts more greyish, under tail-coverts and midthroat strming paler than in R I. R longirostris cephalus mexicanus. Larger than remaining subspecies. Bill Trochilus cephalus Bourcier and Mulsant, 1848. Type curvature less pronounced than in R I. longirostris. specimen: location unknown; there are no indications Rectrical margins pure white. in either Eudes-Deslongchamps 1881 or Jouanin 1950. Distribution: W Mexico, states of Colima, Jalisco, and Type locality: ". ..'l'Amerique centrale' = Rio San Nayarit (Fig. 4). Juan, Nicaragua" (Bangs and Barbour 1922). Synonyms: Phaethornis cassinii Lawrence, 1866 (Type R longirostris mexicanus specimen: USNM; type locality: "New Granada, Phaethomis mexicanus Hartert, 1897. Type specimen: Carthagena", Colombia, Lawrence 1866) AMNH. Type locality: "Dos Arroyos in Chilpancin- Phaethornis panamensis Boucard, 1892 (Type specimen: go" (Mexico; Hartert 1897a). Characters: Larger than MNHN; type locality: "Panama and Veragua, Colum- other subspecies.Underparts darkerand more brown- bia", Boucard 1892). ish than in R I. griseoventer and R I. baroni; the re- Characters: Similar to R I. longirostris, but larger maining subspocies lack pure white rectrical margins. amounts of ochraceous coloration in the rectrical Distribution: SW Mexico, states of Michoacán, Guerre- margins (in particular SE of Costa Rica), less uniform, ro, and Oaxaca (Fig. 4). more barred throat, less distinct bill curvature and R longirostris longirostris more ochraceous coloration of the underparts. Smaller Ornismya longirostris DeLattre, 1843. Type specimen: than R I. SUSUmts. "Location of type material unknown" (Dickerman Distribution: E Honduras; Nicaragua; Costa Rica; 1987). Type location: "Guatimala" (Hartert 1897a). Panama; NW Colombia, Depts. of Choc6, Antioquia, Synonym: Phaethomis longirostris veraecrucis Ridgway, Bolívar, and Santander (Fig. 4). Recently, F. Gary Stiles 1910 (Type spocimen: USNM; type locality: "Buena became aware of Colombian specimens distributed S to Vista, Veracruz, southeastern Mexico", Ridgway 1910). Caldas (Stiles, in litt.).

146 cRMIT HUMMINGBIRDS

R longirvstris susurrus (Type specimen: private collection Simon-Berlioz, Phaethornis longirvstris susurrus Bangs, 1901. Type Paris; typelocality: "Bogota", Colombia, Simon 1921) specimen: MCZ. Type locality: .Chirua, Sierra Nevada Phaethornis malaris ucayalii Zimmer, 1950 (Type speci- de Santa Marta, Colombia» (Bangs 1901). men: AMNH; type locality: "Lagarto, right bank of Characters: Almost completely ochraceous rectrical the upper Río Ucayali, Peru", Zimmer 1950). margins (feather tips and inner webs may be whitish). Characters: Distinctly more greyish underparts than Larger than R I. cephalus. all other subspecies: P. m. malaris and P. m. insolitus Distribution: Sierra Nevada de Santa Marta area, N have darker, more brownish underparts, P. m. bolivia- Colombia; adjacent Venezuela, W Zulia (Fig. 4). nus, P. m margarettae, and P. m. ochraceiventris have R longirvstris ktrvni distinctly more ochraceous-colored bellies. Phaethornis barvni Hartert, 1897. Type specimen: Distribution: East-Andean Colombia, Depts. (and AMNH, Type locality: .Naranjal, near the Rio Pesca- other political entities) of Meta, Caquetá, Putumayo, do, in Western Ecuador» (Hartert 1897a). Characters: and Amazonas; E Ecuador; N Peru, north of rivers Barred appearance of the throat feathers on both sides Marañon and Amazonas, probably in the lower Ucaya- of the midthroat streaking similar to R I. cephalus and li region (Fig. 6). Adjoining populations south of N R I. susurrus; different from these taxa by pure white Peru exhibit characters of P. m. bolivianus as well (Fig. rectrical margins. Smaller than R I. mexicanus and R I. 8). griseoventer. More greyish underparts than R I. longi. P. malaris bolivianus rvstris. Phaethornis boliviana Gould, 1861. Type specimen: Distribution: W Ecuador; adjacent NW Peru, Dept. of Tumbes (Fig. 4). BMNH. Type locality: "Bolivia" (Gou!d 1861). Synonyms: Phaethornis superciliosus insignis Todd, Phaethornis malaris 1937 (Type specimen: CMNH; type locality: "Itaituba, R malaris malaris Rio Tapaj6z, Brazil", Todd 1937) Trvchilus malaris Nordmann, 1835. Type specimen: Phaethornis malaris uca)Ulii Zimmer, 1950 (Type speci- before 1945 in MNHB, now obviously lost. Type local- men: AMNH; type locality: .Lagarto, right bank of ity: .No type locality = Cayenne» (French Guiana; the upper Río Ucayali, Peru", Zimmer 1950). Peters 1945). Characters: Smaller than P. m. malaris, P. m insolitus, Characters: Distinctly larger and with darker brownish P. m. ochraceiventris, and P. m. moorei. Darkish brown underparts than all remaining subspecies. Only R m. throat and breast as well as ochraceous belly are addi- insolitus may closely approach the coloration charac- tional characteIO to distinguish bolivianus from ochra- ters which distinguish malaris from the other sub- ceiventris and moorei. P. m. margarettae appears to be Specles. paler below and might have a distinct midthroat Distribution: Surinam; French Guiana; adjacent Bra- streaking in males as well. zil, territory of Amapá (Fig. 6). Distribution: SE Peru, Depts. of Cuzco, Puno, and R malaris insolitus Madre de Dios; Bolivia, Depts. of La Paz, Beni, Cocha- Phaethornis malaris insolitus Zimmer, 1950. Type speci- bamba, Santa Cruz; Brnzil, between lower rivers Ma- men: AMNH. Type locality: .Río Huaynia, junction deira and Tapaj6s (Fig. 6). Populations north of Peru- with Río Casiquiare, right bank, (. ..), Venezuela» vian Depts. of Cuzco and Madre de Dios exhibit (Zimmer 1950). characters of P. m. moorei as well (Fig. 8). Characters: Smaller than R m. malaris, larger than R m. P. malaris mar~rettae bolivianus and (probably) R m. margarettae. Distinctly Phaethornis margarettae Ruschi, 1972. Type specimen: more brownish underparts than R m. moorei and R m. MBPML. Type locality: "Rio Agua Preta, Fazenda ochraceiventris. Distribution: E Colombia, intendencias of Vaupés and Klabin, Município de Concei!riio da Barra, Estado do E. Santo, Brasil" (Ruschi 1972). Guainia; adjacent Venezuela, territory of Amazonas; adjacent Brazil, state of Amazonas (Fig. 6). Synonym: Phaethornis ochraceiventris camargoi Grant- sau, 1988 (Type specimen: MZUSP; type locality: R malaris moorei "Agua Azul, Vicencia, Pernambuco, Brasil", Grantsau Phaethornis moorei Lawrence, 1858. Type specimen. 1988). AMNH. Type locality: .Ecuador» (Lawrence 1858), Characters: Very similar to P. m. bolivianus, but ap- .Napo» (specimen's label). parently somewhat paler below. Males may have Synonyms: Trochilus consobrinus Bourcier, MS; Rei- distinct midthroat streakings, like females. ch~nbach, 1854 (nomen nudum) (Type specimen: Distribution: Brazil, close to the Atlantic coast destroyed in 1944; Jouanin, in litt.) between the states of Pernambuco and Espirito Santo Phaethornis superciliosa moorei var. nigella Simon, 1921 (Fig.6).

147 R malaris ochraceiventris Phaethomis superciliosa saturatior Simon, 1921 (Type Phoethornis (sic) affinis ochraceiventris Hellmayr,1907. specimen: private collection Simon-Berlioz, Paris; type Type specimen: AMNH. Type locality: .Humaytha, locality: .Guyane fran~aise: Maroni, Vénézuela E.: on the left bank of the Rio Madeira, Brazil. (Hellmayr bassin de l'Orenoque et de la Caura. -? Brésil nord: 1907a). sur le haut rio Branco", Simon 1921). Characters: Differing from all remaining subspecies of Characters: Like R s. muelleri, superciliosus has white R malaris by the orange-ochraceous coloration on under tail-coverts' feathers with dark coloration along breast, belly, and under tail-coverts. Larger than boli. the rachis. Throat and breast lighter, more ochraceous, vianus and margarettae. and bill more intensively curved than in muelleri. Distribution: W Brazil, state of Amazonas, S of the Distribution: Venezuela, S and E of the Orinoco; N Amazon river between the confluence of the rivers Brazil, N of the rivers Negro and Amawn; Guyana; Marañon and Napo and the W bank of the lower Surinam; French Guiana (Fig. 9). Madeira (Fig. 6). R superciliosus muelleri Phaethornis superciliosus Phaethomis superciliosusmuelleri Hellmayr, 1911. Type R superciliosus superciliosus specimen: ZSM Type locality: .North-eastern Brazil, Trochilus superciliosus Linnaeus, 1766. Type specimen: State of Pará: San Antonio do Prata (. ..), Peixe-Boi (...), not existent; description is based on a bird named Ipitinga, on the R. Acará (. ..)" (Hellmayr 1911); .Pei- .Polytmus cayanensis longicaudus. and portrayed by xe-Boi, Pará" (specimen's label). Brisson (1760). Type locality: .Cayenne. (Peters 1945). Characters: Throat and breast on both sides of the Synonyms: Phaethornis fraterculus Gould, 1861 (nom. midthroat streaking darker, more brownish, and bill nov.) distinctly less curved than in R s. superciliosus. Phaethornis guianensis Boucard, 1891 (Type specimen: Distribution: Brazil, State of Pará S of the Amawn MNHN; type locality: .Demerara., Guyana, Boucard between the lower Tapajós river and the Gurupí river 1891) as well as adjacent Maranhao (Fig. 9).

148