The Condor 86:48-52 0 The CooperOrnithological Society 1984

THE RELATIONSHIPS OF THE (OXYRUNCUS CRISTATUS)

CHARLES G. SIBLEY SCOTT M. LANYON

AND JON E. AHLQUIST

ABSTRACT. -The Sharpbill (Oxvruncus cristatus) is a Neotropical suboscine passerinewhose affinities have been unclear. The tyrant flycatchers,, and of the superfamily Tyrannoidea have been suggestedas the closest relatives of the Sharpbill. DNA-DNA hybridization comparisons between the radioiodine-labeled single-copy DNA of the Sharpbill and the DNAs of cotingas, manakins, tyrant flycatchers, and representativesof the other Neotropical super- family, the Furnarioidea, indicate that Oxyruncus is a . We place it in the subfamily Cotinginae, family Tyrannidae.

The Sharpbill (Oxyruncus cristatus) is a me- (1972:605) saw “four or five” together in Pan- dium-sized (ca. 16 cm) suboscine ama and recorded spiders,ants, and seedsfrom with a straight, pointed bill and short rictal stomach contents. bristles. In the adult male the crested crown Brooke et al. (1983) found the first recorded hasa crimson center bordered by olive feathers nest of the Sharpbill near the top of a 30-m tipped with black. The back is bright olive- tree in the montane forest of the Serra do Tin- green,wings and tail blackish,underparts white gua, 50 km north of Rio de Janeiro, Brazil. with black spots,and the flanks pale greenish- The nest, which was built by the female, was yellow. The plumage colors of the adult female “saddled onto a slender (ca. 3 cm) horizontal are lessintense than those of the male and the branch” and was a “simple . . . shallow cup coronal stripe is inconspicuous. . . . composed of roughly interlaced legumi- The Sharpbill apparently has a discontin- nous petioles . . . and a very few dry leaves.” uous range in the humid montane forests of The outer surface “was a thin coat of mosses, Costa Rica, Panama, southeasternVenezuela, liverworts, and spider’s web. . . with a texture southern Guyana and Surinam, northeastern akin to thin cardboard, possibly resultingfrom and southeastern Brazil, southern Paraguay, the application and subsequentdrying of sa- and central Peru (Mees 1974, Traylor, 1979). liva.” The female fed the young by regurgita- Extensive field observationsof the Sharpbill tion, as do cotingas,rather than as in insectiv- have not been recorded but Sick (197 1) re- orous tyrannids. Brooke et al. (1983) observed viewed the sparse literature and reported on adult Sharpbills feeding in the ways described his encounterswith the speciesduring his many by Sick (1971). years of field studies in Brazil. He found that Sharpbills tend to occur most often in dense TAXONOMIC HISTORY tall forest, although they sometimes feed on The genus Oxyruncuswas described by Tem- fruits at the forest edge or in solitary trees. minck (1820) who placed it in his VI, Fruits are the principal food but insects have the “Anisodactyli.” Bonaparte (1850) and been found in the stomachsof specimensand Cabanis (18 59) included it in the family “An- Sick observed Sharpbills hangingupside down abatidae” (=Furnariidae) but Godman and from twigs to capture insect larvae. The vocal- Salvin (1888) placed it in a monotypic family. izations are relatively simple and similar to Most subsequentauthors have also given the those of certain cotingas. Sharpbill family status, including Sclater Sick found the most often in pairs and (1888) Sharpe (I 90 l), Ridgway (1907) Hell- in mixed flocks of , furnariids, trou- mayr (1929), Wetmore (1930, 1960, 1972), pials, cotingas, , etc. feeding on Ames (1971) Storer (1971) Mees (1974), fruiting trees.A captive Sharpbill ate fruits and Traylor (1977, 1979), Wolters (1977) and cast hard pellets composed of the skins. Bangs Meyer de Schauenseeand Phelps (1978). All and Barbour (1922) also observed Sharpbills of these authors have placed the Oxyruncidae feeding in fruiting trees with cotingas; Mees near the Tyrannidae, the Cotingidae, the Pip- (1974) found them solitary, in pairs, and in ridae, and the Phytotomidae, often with state- mixed swarms in Surinam. Wetmore ments reflecting uncertainty about the rela-

[481 THE RELATIONSHIPS OF THE SHARPBILL 49

tionships of the Sharpbill. For example, sion of the Sharpbill in life asresembling “ some Ridgway (1907:332-335) consideredthe Oxy- of the medium-sized of Cotingidae” runcidae to be most closely related to the Ty- and Sick (197 1:260) concluded that some of rannidae but “readily distinguishedfrom other the facts he recorded seemed“ to indicate more Mesomyodian groupsby the. . . sharp-pointed, affinity to the cotingas than to the tyrant-fly- wedge-shapedbill and exaspideantarsi. ” catchers which are generally supposed to be The exaspidean tarsal envelope in the ty- the nearest relatives.” rants, manakins, and Oxyruncus was used by In this paper we addressone principal ques- Sclater (1888) as evidence that the Sharpbill tion: namely, to which other group of the tyr- should not be placed with the pycnaspidean annoid suboscine passerinesis the Sharpbill cotingas. Ridgway (1907) noted considerable most closely related, the tyrant flycatchers,the variation in the tarsal scutellation types and cotingas, or the manakins? Pycraft (1906) Blaszyk (1935) Plotnick and Pergolani de Costa (1955) and Ames et al. METHODS (1968) have shown that this character has little Sibley and Ahlquist have published moder- or no value as evidence of family-level rela- ately detailed descriptions (198 1, 1983) and tionships. synoptic accounts (1982a+l), of the DNA- Hellmayr (1929: 1) placed the Oxyruncidae DNA hybridization procedures used to pro- between the Tyrannidae and Pipridae, but duce the data in Table 1. The delta T,,H values commented in a footnote that “the affinities are measuresof the average rate of nucleotide of this family are not satisfactorilydetermined, substitution,i.e., DNA , and the same and it may become necessaryto merge it with averagerate occurs in all avian lineages. The the Cotingidae.” delta T,,H values are therefore measures of Chapman (1939) declared that Oxyruncus the relative times of divergence between the “has no close relatives and its exact position lineagesrepresented by the two specieswhose in our system of classificationhas never been DNAs were combined to producea DNA-DNA satisfactorily determined.” After “consider- hybrid. A preliminary calibration of delta T,,H ation of the factual evidence” Chapman de- values in absolutetime indicatesthat each 1“C cided that “Oxyruncus is a relict speciesap- delta T,,H equals 4 to 5 million years since proaching extinction.” the time when the two lineages diverged, at Wetmore (1960: 17) noted that “if the sharp- leastfor delta valuesgreater than ca. 6.0 (Sibley bills have other affinities it is doubtful that they and Ahlquist 198 1, 1982a; Sibley et al. 1982). are within the family Tyrannidae, where some have placed them.” The latter reference was RESULTS AND DISCUSSION to Gadow (1893), Clark (19 13) and Mayr and Table 1 presentsthe delta T,,H values for 23 Amadon (19 5 1) who had included Oxyruncus DNA-DNA hybrids between the single-copy in the Tyrannidae. tracer DNA of the Sharpbill and the driver Warter (1965) studied the cranial osteology DNAs of 11 cotingas,two manakins, eight ty- of the Tyrannoidea and concluded that “the rant flycatchers, and two species of the Fur- highly specialized skull [of Oxyruncus] argues narioidea as defined by Sibley and Ahlquist (in against the inclusion of the genus in an oth- pressa). erwise so relatively homogeneousa family as The cotingas in Table 1 range from 4.6 to the Tyrannidae.” 7.6 delta T,,H from Oxyruncus. These rela- Ames (1971:163) concluded that “the pe- tively low values, and the wide range of 3.0, culiar sharpbill . . . has a basically tyrannid indicate (1) that the Sharpbill is a member of , . . . but I cannot agreewith Clark ( 19 13) the cotinga cluster, and (2) that, as expected, that its syrinx bears a “striking resemblance” the other cotingas branched at various times to that of any particular genusof tyrannid, least from the lineage leading to the Sharpbill. We of all to Tyrannus and Sayornis. The syringeal estimate that the divergences between the musculature of the sharpbill is strikingly like Sharpbill lineage and the other cotingasin Ta- that of the becards (Pachyramphus) but there ble 1 occurred between ca. 35 and 20 million are substantial differences in the supporting years ago (MYA), from the early Oligocene to cartilages. The type of musculature found in the mid-Miocene. However, the Sharpbill is the sharpbill and the becardsoccurs elsewhere probably even more closely related to some among the Tyrannidae, so the similarity should cotinganot representedin Table 1. Also, single not be given too much weight.” delta T,,H values may have an experimental The arguments of Warter and Ames con- error of as much as * 1.0. Thus Querula and vinced Traylor (1977: 133-l 34) that Oxyrun- Procnias are not necessarily more closely re- cus should be kept in a separate family. lated to Oxyruncusthan are some other cotin- Wetmore (1972:602) recorded his impres- gas.To determine the actual closestrelative of 50 C. G. SIBLEY, S. M. LANYON AND J. E. AHLQUIST

TABLE 1. DNA-DNA hybridization values between the radioiodine-labeled single-copyDNA of the Sharpbill (Oxy- runcuscristatus) and the DNAs of other members of the Infraorder . Under “Group Index” the C = cotinga, M = , Ti = tityrine, T = , Mio = mionectid, F = furnarioid, Th = thamnophilid.

English name Scientific name Delta T,,H Group Index

Sharpbill Oxyruncuscristatus 0.0 C Purple-throated Fruitcrow Querula purpurata 4.6 C Bare-throated Bellbird Procniasnudicollis 5.4 C Bare-neckedFruitcrow Gymnoderusfoetidus 6.2 C Ornate Umbrellabird Cephalopterusornatus 6.3 C Barred Fruiteater arcuata 6.4 C Andean Cock-of-the-Rock Rupicolaperuviana 6.5 C Black-tailed Tityra cayana 6.6 Ti Masked Tityra Tityra semifasciata 6.6 Ti Red-crested Cotinga Ampelion rubrocristatus 6.9 C Pink-throated Becard Platypsarisminor 1.4 Ti Barred Becard Pachyramphusversicolor 7.6 Ti Golden-headed Manakin Pipra erythrocephala 8.7 M Green Manakin Chlorouivoholochroa 8.7 M Whiskered Flycatcher Myiob& barbatus 8.8 T White-crested Elaenia Elaenia albiceps 8.8 T Brown-backed Chat-tyrant Ochthoecafumicolor 9.2 T Wied’s Flycatcher Myiarchus tyrannulus 9.4 T StreakedAttila Attila spadiceus 9.6 T Grayish Mourner Rhytipternasimplex 9.6 T Slaty-cappedFlycatcher Leptopogonsuperciliaris 10.0 Mio Olive-striped Flycatcher Mionectesolivaceus 10.5 Mio Rufous Homer0 Furnarius rufus 14.0 F Black-cappedAntshrike Thamnophilusschistaceus 14.4 Th

Oxyruncuswould require several comparisons imental error, not to variable rates of nucleo- with each of the generaof cotingas,but we lack tide substitution. See Sibley and Ahlquist DNAs of all but those in Table 1. Thus, al- (1983) and Sibley et al. (1982) for additional though the DNA data show that Oxyruncus is information concerning the measurement and a cotinga, they do not reveal to which other magnitude of experimental error. cotingine genus it is most closely related. For the branch betweenthe Tyrannoidea and The manakins Pipra and Chloropipo,at del- the Furnarioidea we have a total of 65 delta ta T,,H 8.7 from Oxyruncus, indicate that the T,,H values which average 14.2 + 0.1, +- 1.0. cotinga and manakin lineagesdiverged ca. 35- Sibley and Ahlquist (in press b) present the 40 MYA, in the late Eocene. This is supported complete data. by 21 DNA hybrids between cotingas and The tyrannoid-furnarioid dichotomy oc- manakins, which have an average delta T,,H curred in the Paleocene, ca. 60-65 MYA. All of 8.8 +- 0.1 standard error (SE) and kO.4 divergence datings are subject to revision as standard deviation (SD) (Sibley and Ahlquist, the calibration between delta values and ab- in press b). solute time is improved and corrected. The eight delta T,,H values between Oxy- We conclude that Oxyruncus cristatus is a runcus and the tyrant flycatchers range from cotinga and that it should be included in the 8.8 to 10.5, a spread of 1.7. They average Subfamily Cotinginae, Family Tyrannidae, 9.5 + 0.2 SE, kO.6 SD. A set of 62 DNA hy- Superfamily Tyrannoidea, Parvorder , brids between cotingas plus manakins vs. ty- Infraorder Tyrannides. The Subfamily Pipri- rants has an average delta T,,H of 9.0 * 0.1, nae is the sister group of the Cotinginae. This t-0.5. When the eight Oxyruncus x tyrant hy- assignment of categories follows Sibley and brids are added, making a total of 70, the av- Ahlquist (in press a) and is based upon the erage = 9.1 ? 0.1, kO.6. These data are in- delta T,,H averagevalues for divergencenodes cluded in Sibley and Ahlquist (in pressb). becausethey are measuresof the agesof origin, The average delta T,,H of 9.1 indicates that as proposed by Hennig (1966). The scaleis as the cotinga-manakin lineageand the tyrant fly- follows: up to delta T,,H 4 = members of the catcher lineage diverged in the late Eocene, ca. same genus,or closely related genera; delta 4- 40 MYA. 7 = members of the same Tribe; 7-9 = The 70 DNA hybrids used in the above cal- Subfamily; 9-l 1 = Family; 1 l-l 3 = Super- culations range from 8.6 to 10.5, a spread of family; 13-15 = Parvorder; 15-18 = Infraor- 1.9. We believe this variation is due to exper- der; 18-20 = Suborder; 20-22 = Order. It has THE RELATIONSHIPS OF THE SHARPBILL 5 1

been necessaryto allow some flexibility in these Family Furnariidae boundaries to avoid excessiveproliferation of Subfamily Furnariinae, oven- categoriesand to accommodate the uncertain- birds ties in the time calibration. Subfamily Dendrocolaptinae, The inclusion of the Sharpbill in the Cotin- ginae may be unacceptableto some avian sys- Superfamily Formicarioidea tematists who prefer a classificationin which Family , ground ant- specialized “grades” of morphologically dis- birds tinctive taxa are recognized as separate cate- Family Rhinocryptidae, gories above the generic level. We reject this Family Conopophagidae, gnateat- procedure as subjective and leading to the rec- ers ognition of arbitrary groupingsthat do not re- Parvorder Thamnophili flect degreesof genetic similarity. If the Sharp- Family Thamnophilidae, typical bill is placed in a separatesubfamily or family, in spite of its close genetic relationship to the Suborder Passeres cotingas, then such morphologically distinc- tive genera as Cephalopterus, Procnias, and ACKNOWLEDGMENTS Rupicola should be treated likewise. However, Snow (1973, 1979, 1982), the most recent stu- We thank L. Wallace, E. Nowicki, and F. C. Sibley for laboratory assistance.For other help we are indebted to dent of the cotingas,has included these genera S. Allen-Stotz, D. Braun, P. Galindo, E. Mkndez, J. S. in his concept of the Cotingidae and the DNA McIlhenny, B. Odum, J. O’Neill, M. Robbins, H. I. and data support his arrangement. We have re- L. Schweppe,R. Semba, D. W. Snow, M. A. Traylor, Jr., duced the cotingas to a subfamily in the Ty- R. H. Watten, N. and E. Wheelwright, and D. Wysham. rannidae to reflect the branching pattern of the The GorgasMemorial Laboratory, Panama City, Panama, and the Museum of Natural Sciencesof Louisiana State phylogeny and to bring categorical levels into University provided assistancefor the field work. Yale equivalencethroughout the Passeriformes.The University and the National ScienceFoundation (DEB 79- following classification of the Suborder Oli- 26746) supportedthe laboratory studies. gomyodi is that of Sibley and Ahlquist (in press a, b), which is based solely on the phylogeny LITERATURE CITED derived from extensive DNA-DNA compari- sons among all of the traditional families of AMES,P. L. 1971. The morphology of the syrinx in pas- serine birds. Peabody Mus. Nat. Hist. Yale Univ. suboscinesexcept the Philepittidae. Bull. 37:1-194. AMES, P. L., M. A. HEIMERDINGER,AND S. L. WARTER. Order Passeriformes 1968. The and systematic position of the Suborder Oligomyodi antpipits Conopophaguand Corythopis. Postilla 114: l-32. Infraorder Acanthisittides BANGS,O., AND T. BARBOUR.1922. Birds from Darien. Family Acanthisittidae, New Zea- Mus. Comp. Zool. Harvard Univ. Bull. 65: 19l-229. land wrens BLASZYK,P. 1935. Untersuchungeniiber die Stammes- Infraorder Eurylaimides geschichteder Vogelschuppenund Fedem und Bber Abhangigkeitihrer Ausbildungam Vogelfussvon der Superfamily Pittoidea Funktion. GegenbaursMorphol. Jahrb. 75~483-567. Family Pittidae, BONAPARTE,C. L. 1850. Conspectusgenerum avium. Family , broadbills Vol. 1. Lugduni Batavorum. E. J. Brill, Leiden. (Family inc. sedisPhilepittidae, as- BROOKE,M. DE L., D. A. SCOTT,AND D. M. TEIXEIRA. ities) 1983. Some observationsmade at the first recorded nest of the Sharpbill Oxyruncus cristatus. Ibis 125: Infraorder Tyrannides 259-261. Parvorder Tyranni CABANIS,J. 1859. Museum Heineanum. Vol. 1, part 2. Superfamily Tyrannoidea Halberstadt. Family Tyrannidae CHAPMAN,F. M. 1939. The riddle of Oxyruncus. Am. Subfamily Tyranninae, tyrant Mus. Nat. Hist. Novit. 1047:l-4. CLARK,H.L. 1913. Anatomical notes on Todus, Oxy- flycatchers runcus, and Spindalis. Auk 30:402-406. Subfamily Tityrinae GADOW,H. 1893. V6gel. II. SystematischerTheil. Vol. Tribe Schiffornini, Schi#brnis 6, part 4. In H. G. Bronn, Klassen und Ordnungen Tribe Tityrini, , becards des Thier-Reichs. C. F. Winter, Leipzig. GODMAN,F. D., AND0. SALVIN. 1888. BiologiaCentrali- Subfamily Cotinginae, cotingas, Americana. Aves, Vol. 2. Taylor & Francis, London. plantcutters, Sharpbill HELLMAYR,C. E. 1929. Catalogueof birds of the Amer- Subfamily Piprinae, manakins icas. Part 6. Field Mus. Nat. Hist. Zool. Ser. 13:l- Family Mionectidae, mionectid 258. HENNIG, W. 1966. Phylogenetic systematics.Univ. of flycatchers Illinois Press, Urbana. Parvorder Furnarii MAYR, E., AND D. AMADON. 1951. A classification of Superfamily Furnarioidea Recent birds. Am. Mus. Nat. Hist. Novit. 1496:1-42. 52 C. G. SIBLEY, S. M. LANYON AND J. E. AHLQUIST

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