18 December 1992 PROC. BIOL. SOC. WASH. 105(4), 1992, pp. 834-840 DIAGNOSIS OF A HYBRID {PHLEGOPSIS NIGROMACULATA X PHLEGOPSIS ERYTHROPTERA) AND THE RARITY OF HYBRIDIZATION AMONG SUBOSCINES

Gary R. Graves

Abstract. —Phlegopsis barringeri Meyer de Schauensee, 1951, is suggested to be a hybrid between Phlegopsis nigromaculata and P. erythroptera. This rep- resents the first case of hybridity in the large monophyletic assemblage of New World suboscines comprising the woodcreepers, , ovenbirds, and ta- paculos (parvorders Thamnophilida and Furnariida). The rarity of hybridiza- tion among suboscines (Suborder Tyranni) may result from the absence of song learning in this assemblage, resulting in vocal stereotypy within populations and the reduction of mate recognition error by females.

Hybridization in occurs most fre- in zoological nomenclature, the burden of quently in sexually dimorphic with proof rests upon a taxonomist to reject hy- polygynous breeding systems (Sibley 1957). bridity before conferring species status More than half of all known cases of hy- (Graves 1990). Meyer de Schauensee com- bridization in nature occur in four avian pared the specimen of P. barringeri with families or tribes: Anatidae (ducks, geese, three morphologically similar taxa but failed and swans), Phasianidae (grouse and pheas- to address hybridity. That possibility was ants), Trochilidae (hummingbirds), and raised by Willis (1979), who suggested par- Paradisaeini (birds of paradise) (Gray 1958) enthetically that P. barringeri was a hybrid ( of Sibley & Monroe 1990). The between the Black-spotted Bare-eye (P. ni- apparent absence or low frequency of hy- gromaculata) and Red-winged Bare-eye (P. bridization in other lineages may reflect re- erythroptera), which overlap broadly in ality or the failure of biologists to detect it western Amazonia from eastern Colombia (Graves 1990). Only a few cases of hybrid- (Hilty & Brown 1986) south to northern ization have been detected among New Bolivia (Parker & Remsen 1987). World suboscines (e.g., Parkes 1961, Short My analysis of P. barringeri confirmed & Burleigh 1965, Tyler & Parkes 1992), Willis' hunch. The proposed hybrid origin which constitute a quarter (n = 1097) of all of the specimen (P. nigromaculata x p. er- Western Hemisphere species. ythroptera) cannot be rejected. Here I pre- Meyer de Schauensee (1951) described a sent a diagnosis of the hybrid antbird, the relatively large and spectacular species of first known example of hybridity in the antbird, the Argus Bare-eye (Phlegopsis bar- parvorders Thamnophilida and Furnariida ringeri), from a unique specimen collected (Sibley & Monroe 1990), a monophyletic on the Rio Rumiyaco, Department of Na- assemblage representing 131 genera and 560 rino, Colombia. Determining whether a species of woodcreepers, antbirds, oven- unique specimen represents a valid species, birds, and tapaculos. I then briefly discuss a hybrid, or a genetic variant of a previously a correlate of hybridization frequency in described species can be a Herculean task. suboscines (Suborder Tyranni), the absence However, because hybrids have no standing of song learning. VOLUME 105, NUMBER 4 835

Materials and Methods Hypocnemis, Myrmochanes, Sclateria, , Myrmeciza, Pithys, Gymnopi- I compared the holotype of Phlegopsis thys, Myrmornis, Rhegmatorhina, and Hy- barringeri (adult male, Academy of Natural lophylax, that occur in Amazonian forest of Sciences Philadelphia (ANSP), No. 162,675) Colombia and Ecuador. directly with specimens of P. nigromaculata Soft part colors.—The hybrid had bare and P. erythroptera from Ecuador under reddish orbital skin (now faded), an apo- natural light. A complete description of P. morphic character of Phlegopsis among the barringeri, which will not be repeated here, Thamnophilida. The size of the orbital patch can be found in Meyer de Schauensee (1951). in the hybrid is intermediate between that Series of Phlegopsis and nearly all other spe- off. nigromaculata (larger) and P. erythrop- cies of antbirds were examined at the fol- tera (smaller). This character alone suggests lowing institutions: American Museum of that the two species of Phlegopsis were the Natural History; Carnegie Museum of hybrid's parents. Other "bare-eyed" ant- Natural History; Museu Paraense "Emi- birds have smaller patches of bluish-gray or lio Goeldi," Belem; Museum of Natu- bluish-white orbital skin in life, which fades ral Science, Louisiana State University to gray in specimens. Hybrids between a (LSUMNS); Museu de Zoologia, Univer- species of Phlegopsis and a species from an- sidade de Sao Paulo; and the National Mu- other would probably, although not seum of Natural History, Smithsonian In- certainly, have a small orbital patch with stitution. Measurements of wing chord, tail traces of melanization (gray in dried skin). length from point of insertion of central rec- Plumage characters. —Because the hybrid trices to tip of longest rectrix, tarsus length, was male, the plumage diagnosis focused on hallux (plus claw) length, bill length from aspects of male plumage. Meyer de anterior edge of nostril, and bill width at Schauensee (1951:3) noted "this new spe- anterior edge of nostril were made with dig- cies combines in some ways characters found ital calipers to the nearest 0.1 mm. in both P. nigro-maculata and P. erythrop- In order to visualize morphological vari- tera, and has others not found in either." A ation in two dimensions, I used principal careful examination of the hybrid confirms components analysis of log transformed his observation (Fig. 1). No combination of data. Unrotated principal components were potential parental species, except Phlegopsis extracted from covariance matrices (Wil- nigromaculata and P. erythroptera, could kinson 1989). f-values of <0.05 were re- have produced the distinctive characters of garded as significant for two-sample (-tests. the hybrid: (1) unmarked glossy black head, Diagnostic assumptions and methods of throat, and breast; (2) brown mantle with hybrid diagnosis based on plumage char- contrasting spots; and (3) black and rufous- acters and morphology follow Graves cinnamon remiges, rectrices, and upper- and (1990). For brevity, I refer to Phlegopsis undertail coverts. Significantly, the hybrid barringeri as a "hybrid" throughout the text. lacks any trace of pale markings on the head, throat, and breast, or an interscapular patch Results (found in one or more species of Myrmo- Potential parental species. —Because the borus, Hypocnemis, Myrmochanes, Myr- hybrid strongly resembles species of Phle- meciza, Myrmornis, and Hylophylax). Most gopsis in plumage pattern and color (Fig. 1) elements of the hybrid's plumage pattern and because its collection locality is known, and color are easily identified as interme- determination of the potential parental spe- diate character states or mosaics of char- cies seems straightforward: species of Phle- acters of Phlegopsis nigromaculata and P. gopsis, and related genera, , erythroptera. However, the buff and rufous 836 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON

Fig. 1. Lateral views of adult males (from left to right): Phlegopsis nigromaculata, "P. barringeri" (ANSP 162,675; -P. nigromaculata x P. erythroptera), and P. etythroptera. Note ocelli on wing coverts and back of hybrid. ocelli encircled by drop-shaped black spots brown with a terminal black spot (rounded on the feather tips of the mantle and wing triangle). The color pattern in P. erythrop- coverts of the hybrid are not found in either tera is markedly different—back feathers are parental species. By comparison, back entirely black with a narrow white subter- feathers in P. nigromaculata are olivaceous- minal band (back feathers of juvenile males VOLUME 105, NUMBER 4 837

Table 1. —Ranges and means of measurements (mm) of adult male Phlegopsis nigromaculata, P. erythroptera, and their hybrid (="/>. barringeri"). Phlegopsis specimens are from Ecuador and north of the Rio Amazonas in Peru. Significant f-values indicate that means of Phlegopsis species are different (two-tailed /-test).

Phlegopsis Phlegopsis P. nigromaculata nigromaculata erythroptera x P. erythroptera /'-value («- 15) in = 8) (ANSP 162,675)

Wing NS 87.1-94.0 88.6-93.6 90.9 91.4 93.7 Tail <0.001 58.5-64.5 59.6-68.0 61.6 65.2 61.9 Tarsus <0.001 29.2-32.4 30.1-33.3 30.6 32.2 31.2 Hallux <0.01 18.5-20.9 19.7-21.3 19.8 20.6 20.4 Bill length <0.05 12.0-14.6 11.9-13.7 13.2 12.6 12.8 Bill width <0.01 4.6-5.7 4.5-5.0 5.2 4.8 5.2

have broad rufous edges, e.g., LSUMNS ence or absence of subterminal band or ocel- 110,210). Pattern elements in the hybrid lus (expressed in P. erythroptera and hy- may be interpreted by identifying probable brid); and (5) color of subterminal band or homologues in the parental species. For ex- ocellus (expressed in P. erythroptera and hy- ample, the black spots of the hybrid and P. brid). Serial patterns among feather tracts nigromaculata are probably homologous, suggest that some genes affect several plum- while the buffy ocelli of the hybrid are ho- age tracts, for example, the terminal (or sub- mologous with the subterminal white bands terminal) black spots on the back, wings, in P. erythroptera. This suggests that during and tail of Phlegopsis nigromaculata. feather development in the hybrid, the sub- External morphology. —Variation of terminal band inherited from P. erythrop- morphological characters of avian hybrids tera invaginated to form an ocellus within falls within the ranges exhibited by their the black spot. Less complete ocellations are parental species (Buckley 1982, Graves found on the tertials and secondaries of the 1990), reflecting a polygenic mode of in- hybrid, where the terminal black spot failed heritance. As expected, the size of the hy- to enclose the irregularly shaped ocellus. brid antbird conformed to this pattern (Ta- This example offers rare insight into the ble 1). Phlegopsis nigromaculata and P. complexity of genetic control of plumage erythroptera are morphologically similar and patterns in antbirds. Because different pig- the percent difference between their char- ments are believed to be encoded by differ- acter means is small: wing (0.6%); tail (5.8%); ent genes, even within the same feather tract tarsus (5.2%); hallux (4.0%); bill length (Buckley 1982), a minimum of five genes or (4.8%); and bill width (8.3%). Measure- gene complexes and their modifers appear ments of the hybrid fall at or between the to control the color pattern of back feathers means for five of the six characters mea- in Phlegopsis, including those for: (1) ground sured on parental species. Meyer de color (expressed in both parental species and Schauensee's (1951:3) observation that the hybrid); (2) presence or absence of terminal hybrid had larger feet than other Phlegopsis spot (expressed in P. nigromaculata and hy- is erroneous. brid); (3) color of terminal spot (expressed Most potential parental species are con- in P. nigromaculata and hybrid); (4) pres- siderably smaller in all morphological di- 838 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON

0.05 I

•• o • • • 0.00 - • 8

O o D. -0.05 #

-0.10 i -0,10 -0.05 0.00 0.05 0.10 PCA I Fig. 2. Bivariate plot of principal component factor scores of Phlegopsis nigromaculata (=filled circles), P. erythroptera (=hollow circles), and their hybrid (=0), "P- barringeri."

mensions than the hybrid, including all taxa particular hybrid hypothesis could have been of Myrmoborus, Hypocnemis, Myrmo- rejected. From a statistical standpoint, the chanes, Sclateria, Percnostola, Pithys, Gym- likelihood that a third valid species of Phle- nopithys, and Rhegmatorhina. Myrmeciza gopsis would be intermediate in size and fortis, M. melanoceps, M. hyperythra, and shape between two other remarkably simi- Myrmornis torquata approach the size of lar, sympatric species seems remote. Phlegopsis, but can be eliminated as parents In summary, both plumage and morpho- of the hybrid on the basis of plumage char- logical data are consistent with the hypoth- acters. Morphological relationships of Phle- esis that Phlegopsis barringeri Meyer de gopsis species and the hybrid are shown by Schauensee represents a hybrid between first two axes of a principal components Phlegopsis nigromaculata and P. erythrop- analysis (Fig. 2, Table 2). Factor scores for tera. The name Phlegopsis barringeri is thus the hybrid are nearly centered between the available only for the purpose of homony- clusters of scores for the parental species. my in taxonomy. Intermediacy in complex shape variables, controlled by a multitude of genetic loci, Discussion constitutes strong evidence for the hybrid- ization hypothesis. Had the factor scores of Rarity of hybridization among the subos- the hybrid fallen outside the envelope of cines appears to be a real phenomenon rath- scores of the proposed parental species, this er than an artifact of taxonomic practices. VOLUME 105, NUMBER 4 839

Table 2. —Factor loadings for the first two principal the hybrid an third. Museum work was sup- components from analysis of Phlegopsis nigromacu- ported by grants from the Frank M. Chap- laia, P. erythroptera, and their hybrid, "P. barringeri" (ANSP 162,675) (see Fig. 2). man Fund of the American Museum of Natural History, and the Research Oppor- Principal component axes tunities Fund and Neotropical Lowland Re- Variable I II search Program, Smithsonian Institution.

Wing 0.001 0.006 Tail 0.013 0.006 Literature Cited Tarsus 0.012 0.008 Hallux 0.011 0.001 Buckley, P. A. 1982. Avian genetics. Pp. 21-110 in Bill length -0.010 0.021 M. Petrak, ed., Diseases of cage and aviary birds. Bill width -0.024 -0.001 2nd ed. Lea and Febiger, Philadelphia, 680 pp. Graves, G.R. 1990. Systematics of the "green-throat- Variance explained ed sunangels" (Aves: Trochilidae): valid taxa or Percent 48.1 25.2 hybrids?—Proceedings of the Biological Society of Washington 103:6-25. Gray, A. P. 1958. hybrids. Commonwealth Ag- ricultural Bureaux, Bucks, England, 390 pp. This position is supported not only by the Hilty, S. L., & W. L. Brown. 1986. A guide to the cumulative record of avian hybridization birds of Colombia. Princeton University Press, Princeton, New Jersey, 836 pp. (Gray 1958), but by several monographic Kroodsma, D. E. 1988. Contrasting styles of song works where extensive museum series of su- development and their consequences among boscine specimens were carefully studied birds. Pp. 157-184 in R. C. Bolles & (e.g., Wetmore 1972). M. D. Beecher, eds., Evolution and learning. The causes of this phylogenetic correla- Lawrence Erlbaum, Hillsdale, New Jersey. Lanyon, W. E. 1978. Revision of the Myiarchus fly- tion are unknown. However, I speculate that catchers of South America.—Bulletin of the the absence of vocal learning among subos- American Museum of Natural History 161:429- cines (Nottebohm 1972, Kroodsma 1988) 627. may be a factor. These species develop basic Meyer de Schauensee, R. 1951. Colombian zoolog- patterns of vocalizations without auditory ical survey. Part IX. A new species of ant-bird (Phlegopsis) from Colombia.—Notulae Naturae feedback and do not imitate songs or phras- 241:1-3. es of other species. Furthermore, geographic Nottebohm, F. 1972. The origin of vocal learning.— variation in song is reduced or absent (e.g., American Naturalist 106:116-140. Lanyon 1978, Payne & Budde 1979), re- Parker, T. A., & J. V. Remsen, Jr. 1987. Fifty-two sulting in stereotypy of vocalizations within Amazonian bird species new to Bolivia.—Bul- letin of the British Ornithological Club 107:94- regional populations of a species. As a con- 107. sequence, females may be less likely to make Parkes, K. C. 1961. Intergeneric hybrids in the family species recognition errors during mate se- Pipridae.-Condor 63:345-350. lection. The prevalence of dull, weakly pat- Payne, R. B., & P. Budde. 1979. Song differences and terned, or sexually monomorphic plumages map distances in a population of Acadian fly- among the suboscines, especially the Tham- catchers.—Wilson Bulletin 91:29-41. Short, L. L., Jr., & T. D. Burleigh. 1965. An inter- nophilida and Furnariida, suggests that vo- generic hybrid flycatcher (Contopus x Empi- calizations are the primary isolating mech- donax) from Idaho. —Proceedings of the Bio- anism between species in this assemblage. logical Society of Washington 78:33-37. Sibley, C. G. 1957. The evolutionary and taxonomic significance of sexual dimorphism and hybrid- Acknowledgments ization in birds. —Condor 59:166-191. I thank R. C. Banks, M. Isler, K. C. Parkes, , & B. L. Monroe, Jr. 1990. Distribution and taxonomy of birds of the world. Yale University K. V. Rosenberg, and M. B. Robbins for Press, New Haven, Connecticut, 1111 pp. comments on the manuscript, and Robbins Tyler, J. D., & K. C. Parkes. 1992. A hybrid Scissor- and F. B. Gill for permission to examine tailed Flycatcher x Western Kingbird specimen 840 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON

from southwestern Oklahoma.—Wilson Bulle- (D'Orbigny & Lafresnaye) (Aves, Formicari- tin 104:178-181. idae). —Revista Brasilia Biologica 39:117-159. Wetmore, A. 1972. The birds of the republic of Pan- ama. Pt. 3. Smithsonian Miscellaneous Collec- Department of Vertebrate Zoology, Na- tions 150 (3). Wilkinson, L. 1989. SYSTAT: the system for statis- tional Museum of Natural History, Smith- tics. SYSTAT, Inc., Evanston, Illinios. sonian Institution, Washington, DC. 20560, Willis, E. O. 1979. Comportamento e ecologia da U.S.A. Mae-de-Taoca, Phlegopsis nigromaculata