On the Systematic Position of Rhodinocichla Rosea

ON THE SYSTEMATIC POSITION OF RtlODINOCICttLA ROSEA

EUGENE EISENMANN

THE precedingarticle (Skutch, 1962) calls attention to a speciesmerit- ing furtherbehavioral and anatomicstudy. Field experiencewith Rhodino- cichlain Panamaaroused interest in its taxonomicstatus, and, as I ex- pressedto Dr. Skutch an opinionvery different from his, he generously suggestedthat I publish my comments. The resemblancesto the Mimidae seem to me convergentadaptations to a similar habitat niche. On the availableevidence Rhodinocichla may properlybe kept in the Thraupidae, whereHellmayr (1936) and mostsubsequent writers placed it.

RELATIONSHIP WITH THE MIMIDAE

The taxonomicvalue of the nine-primariedcondition. Mimidae are characterized,inter alia, by a rather long, well-developedtenth (outer- most) primarywing quill. Rhodinocichla,like othernine-primaried birds, hasthe tenthprimary represented by a tiny vestige,completely concealed by theprimary coverts. The nine-primaried condition is certainlynot conclu- siveof relationships;but it servesas a convenient"key" characterbecause it is usuallyassociated with a complexof other charactersfound in allied groups. There is an evident evolutionarytrend toward reductionin the numberof flight feathers. Many more "primitive" bird ordershave 11 or moreprimaries; most non-passerines have 10 (Indicatoridaenine). In the orderPasseriformes non-oscines generally have 10 (in a few genera11 primaries); in the song-birdsuborder Passeres (Oscines), the primariesare 10 or nine. Most oscinefamilies have 10 primaries;some seem to be in a transitionalstage (e.g., Dicaeidae, Ploceidae, Vireonidae); only a few are definitelynine-primaried. This conditionprobably evolved independently severaltimes, for it prevailsin the Hirundinidae,Motacillidae, and Zostero- pidae,families which seem quite distinctfrom the structurallyintergrading groupof familiesoften called the "Americannine-primaried assemblage." Modernsystematists generally agree that this large,anatomically similar aggregation,comprising at leastthe tanagers,cardinal grosbeaks, American sparrows,buntings, wood warblers, honeycreepers, and icterids,is probably of commonancestry. There is, however,much dispute as to family divisionswithin the assemblage,and as to whetherthe carduelinefinches, thevireos, and a fewanatomically aberrant genera should be included(cf. Wetmore,1951, 1960; Mayr and Amadon,1951; Beecher,1953; Tordoff, 1954; Mayr and Greenway,1956; Amadon,1957; Delacourand Vaurie, 1957; Bock,1960; Storer,in Marshall,1960: 88-89; George,1962: 23). The Mimidae,all systematistsagree, belong in a differentaggregation, 640 The Auk, 79: 640-648. October, 1962 Vol.Auk79 ] EXS•N•rANN,Position o/ Rhodinocichla rosea 641 includingthe thrushes,wrens, Old World flycatchers,and similargroups, whichintergrade structurally. Some authors (Mayr and Amadon,1951) treat the mockingbird-thrashergroup as a subfamilyof the "primitivein- secteaters," Muscicapidae sensu latu (with the thrushes,wrens, Old World warblersas other subfamilies).Even the majority,who preservefamily rank for the Mimidae,classify them in a differentgroup of oscininesfrom the American nine-primaried assemblage.

CHARACTERS OF RHODINOCICHL,4 NOT FOUND IN MX3•rXDAIg BUT PRESENT IN MANY THRAUPmAE

1. Only nine visibleprimaries•the tenth vestigialand wholly concealedby primary coverts (cf. Ridgway, 1902: 769; 1907: 180). 2. Middle toe adherent to inner toe for about half of basal phalanx (cf. Ridgway, 1902: 769; 1907: 180). 3. Lateral toes of equal length (cf. Ridgway, 1902: 769; 1907: 180-181). (Among Mimidae only Donacobiusshows this, but it has otherwisea different toe ar- rangement; cf. Ridgway, 1907.) 4. Bill rather stout and moderatelycompressed; not terete (cf. Ridgway, 1902: 769; 1907: 180). 5. Rictal bristlesobsolete, though present (cf. Ridgway, 1902: 769; 1907: 180). 6. Feathersof loresand frontal antiaewith bristly points,erect and harsh (Rhodino- cichla personallyexamined; cf. Ridgway, 1907: 180). 7. Bony palate "typically tanagrine" (Clark, 1913). 8. Sternum "typically tanagrine" (Clark, 1913). 9. I-Iyoideanstructures unlike Mimidae and typical of tanagersand other members of American "nine-primaried assemblage"(George, 1962: 8, 17, 23). 10. Jaw musculatureunlike Mimidae, agreeingwith tanagers (]ide W. J. Beechef, orally). 11. Rose-red color (presumablycarotenoid pigment) in male plumage. 12. Sexesdistinctly different in color. 13. Mouth lining of nestling red (cf. Skutch, 1954: 260; 1962, supra). Morphologyand anatomy. As appearsfrom the attachedlist, Rhodino- cichla showsnone of the structural features by which the Mimidae are distinguished.In thesecharacters it agreeswith the Thraupidae,and also with someof the other membersof the nine-primariedassemblage that in- tergradestructurally with the tanagers(see below). Commenton someof these characters seems in order. Clark's(1913) anatomicalstudy (concludingthat Rhodinocichlawas a tanager),although supported by featuresof externalmorphology, ad- mittedlywas limited in scopeand in the amountof availablecomparative material. For example,he was unableto examinethe HispaniolanChat- Tanager(Calyptophilus ]rugivorus), which in bill shape,and apparently in feedinghabits, resembles Rhodinocichla more closely than doesany other tanager(see Bond, 1936: 375-376), and which Bond (1956: 168) con- siders related. 642 EISENI•ANN,Position o!Rhodinocichla rosea [ Vol.Auk 79

RecentlyDr. William Georgehas made an elaboratestudy of the hy- oideanstructures (bones and musclescontrolling the tongue) in oscinine birds. He found (1962: 7, 8, 23-24) that in the undoubted members of the American nine-primariedassemblage (tanagers, cardinals, Americansparrows, buntings, wood-warblers, and their allies) thesestruc- turesare visibly different from thosein the Mimidae and other membersof the "primitive insect-eater"aggregation. The hyoidean apparatus of Rhodinocichlais typical of the nine-primariedassemblage. Dr. William J. Beecher,who very recently dissectedthe jaw musculature of a specimenof Rhodinocichla,found that it agreedwith that noted in tanagers,was very distinctfrom that in Mimidae, and also differed from that in the many generaof Icteridae and Parulidaehe has dissected(oral comm.). Further, stronglynegating alliance with the Mimidae is the fact that Rhodinocichlais sexuallydimorphic and that the male is largely rose-red below. In the Mimidae (as in their alliesthe Troglodytidae)the sexesare invariably alike, and there is no red (nor even orangeor yellow) in the plumage.The absenceof carotenoidplumage pigment in Mimidae and its conspicuouspresence in Rhodinocichlaand in many tanagers(and other membersof the Americannine-primaried assemblage) seems particularly significant. Rhodinocichlais a skulking species,keeping to the dark undergrowthin shadywoodland, which, as Skutchobserves, uses loud and persistentvocalizations to maintain contactbetween the sexes.Yet it pre- servesthe sexual dimorphismand rich red color (modified to magenta- rose) to be expectedin a bird usingvisual signal characters.To me this suggeststhat Rhodinocichla,although it has evolveda slendershape and superficiallythrushlike bill, suitableto its denseundergrowth niche and insectivorousfeeding, still betrays in its color pattern the fact that its ancestorslived in trees or fairly open niches--as do most tanagersand their allies. Indications of a similar, less-advancedevolution are apparent in two undergrowthtanagers of the genusHabia, studiedin British Hondurasby Willis (1960a, 1960b). Both ant-tanagersare sexuallydimorphic and the malespreserve red plumage,although the color is noticeablydulled and darkened. Like Rhodinocichla,these ant-tanagerslive in the dark, low vegetation,are largelyinsectivorous, probably remain paired throughall or mostof the year, and haveloud, melodioussongs. Moreover the species that feedsnearer the groundkeeps concealedwhen singingand tends to sing for a longerperiod during the day (Willis, 1960a: 76-78, 80). Al- thoughless terrestrial than Rhodinocichla,both ant-tanagersoccasionally do leaf tossingto find a fallen arthropod(Willis, 1960b). The Chat-Tanager (Calyptophilus]rugivorus) of Hispaniolasuggests Vol.^uk 79 'I] E•SZ•A•r, Position of RhodinocJchlarosea 643 evolution in bill shape. Like Rhodinocichlait is chiefly terrestrial, lives in thickets,has a largely arthropod diet, and utters loud, musicalnotes, said to be reminiscentof the North American Cardinal (Richmondena cardinalis) (Bond, 1936; Wetmore,425-428). Its apparentallies, the HispaniolanPalm Tanagers (Phaenicophilus),are much more arboreal, much less vocal, and have heavier bills (presumablyreflecting a more frugivorousdiet).

Calyptophilus,originally describedas a tanager, was removed by Ridgway (1907: 180, 278) to the Mimidae (with a questionmark) in the erroneousbelief that it had a very long tenth primary. Actually, as pointed out by W. deW. Miller (1918), Calyptophilushas the usual invisible, vestigial tenth primary of a tanager; since then systematistshave placed it in the Thraupidae betweenRhodinocichla and Phaeni- cophilus (Hellmayr, 1936: 357-359).

Nestlings. The nestlingsof Rhodinocichlahave red mouth linings. This, so far as known,is true of all tanagers(Skutch, 1954), as well as someof their allies,but not of any Mimidae. Juvenalplumage. Althoughthis plumageis not mentionedby Skutch, I checkedspecimens in the American Museum of Natural History to see what clueto relationship,if any, they mightprovide. While I am unable to drawany positive conclusions, perhaps because the comparativematerial for othergenera was inadequate, it seemsworthwhile to describethe young Rhodinocichla,as I haveread no gooddescription; Ridgway (1902: 771) had not personallyseen a juvenal.

The youngestRhodinocichla available, a femalewith wingsand tail not full grown, was taken at Esquintla,Sinaloa, Mexico, 20 October 1904, and representsthe paler race, R. roseaschistacea. The generallybrownish slate color above and below is re- lievedby a white superciliarystripe (not extendingabove the lores), and by a light tawny throat; a tawny tinge appearson the malars (suggestingan indistinctstripe) and on the upper breast; the feathers of the lower breast and abdomen are more or lessbroadly marked, subterminallyor terminally,with pale gray or whitish, producing a rather mottled effect. Specimensfrom Costa Rica and Panama, R. rosea eximia, although older and well advanced into the postjuvenal (first basic) plumage, indicate that the juvenal, while darker, would have a pattern similar to schistacea. I was able to examine juvenals of most genera of Mimidae, but of only about one third of the genera of Thraupidae and their allies in tropical America. Juvenals of all Mimidae examined (except Melanotis and Dumetella) were streaked below (including Mimus with unstreakedadults). Juvenals of all tanagershaving unstreakedadults were unstreakedbelow (except Piranga and Spindalis,the latter with streakedfemale in one form). Among American Oscinesin which the juvenal is ventrally mainly slaty and somewhat mottled with paler slate, I noted Melanotis hypoleuca (Mimidae), Seto- phaga [Myioborus?]picta (Parulidae), Tangara]ohannae and T. inornata (Thraupi- dae). In all of these, as in Rhodinocichla,much of the ventral surface in adults is differently colored from that in the juvenal plumage. I have not seena juvenal of Calyptophilus or of Donacobius. 644 EISENlVrANN,Position oJ Rhodinocichlarosea [ Auk [ Vol, 79

Voice. As I haveheard it in Panama,the voiceof Rhodinocichlaseems to me to lack the elaboratephrasing of thrashers(Toxostoma), mocking- birds (Mimus), or catbirds(Dumetella). To my ear Rhodinocichlashouts a loud,clear, repeated phrase, wheeoo-chedo, chwee, varied to cho-ho, chowed,or cheda-wo,chow•h. The notes are highly musical,but rather monotonous,and in their ringingrepetitiveness somewhat suggest the calls of tropical wrensof the genusThryothorus. Rhodinocichlaalso gives a distinctivealarm call, which I can characterizeonly as a fluttering or whirringchatter, and whenforaging often uttersa low whistle,syllabized by Major Chapelleas /ueeooo(probably the sameas Skutch'schio). On 18 April 1961 I saw a captiveadult male singinga rather soft, squeaky, but somewhatmusical, tew-kaddw-ka, tew-kad&v-ka, tew-kad•w--totally differentin quality from the usualringing notes. Singingby femalesoccurs in speciesof many families,including the nine-primariedassemblage. Antiphonal singing by both membersof a pair is characteristicof certaintropical birds (notablythe wrens),which skulk in the undergrowthand remainpaired for all or mostof the year. Such duettingregularly occurs in the North AmericanCardinal, Richmondena cardinalis(Gould, 1961: 247), and in the tropicalBuff-throated Saltator, Saltator maximus(Skutch, 1954: 64), formerlyallocated to the tanagers but currently includedin the cardinal grosbeaksubfamily--which many ornithologistsregard as belongingin the same family as the tanagers (Mayr and Amadon, 1951; Beecher,1953; Tordoff, 1954; Delacour and Vaurie, 1957). Nesting. The nest of Rhodinocichlaillustrated in P. Schwartz's fine photograph(in Gilllard, 1958: pl. 174), with its coarsetwig foundation, certainly is very thrasherlike. But, discountingthe differencein habitat, it seemsto me similar structurally to the nest of the arboreal Western Tanager (Piranga ludoviciana) illustrated in the same work (Gilliard, 1958: pl. 200). Accordingto Schwartz(in Gilliard, 1958: 378), Rhodino- cichlaeggs usually closely resemble those of the GrayishSaltator (Saltator coerulescens)and sometimesthose of the Silver-beakedTanager (Rampho- celuscarbo). Incubation by the male, recordedfor Rhodinocichla,is rare in oscinine birds. Among the Mimidae it has been reported only for thrashers. In the nine-primariedassemblage it is regular in the Rose- breastedand Black-headedgrosbeaks (Pheucticus ludoviciana and P. me- lanocephalus)of the cardinalgrosbeak group, and has beenreported, although perhapsmistakenly (see Skutch, 1954: 120), in the Summer Tanager (Pirangarubra) and a few tropicalCalliste (= Tangara) species. It shouldbe notedthat we have detailedpublished incubation data only for about 20 speciesand some10 generaof tanagers,out of morethan 200 speciesof morethan 60 generaof the familylisted by Hellmayr(1936). Vol.Auk79 ] EIS•I,I•VlAI,1I%Positiono! Rhodinocichla rosea 645

Foraging behavior. While "leaf-tossing"occurs in someMimidae, it is by no meansrestricted to that family. It prevailsin a variety of unrelated ground-feedingbirds. Hallinan (1924: 325) reportsfinding "hard shrub seeds" in the stomachs of two RY•odinocicY•la taken in Panama. Doubtless arthropodsare also eaten. Major (now Colonel) F. O. Chapellewrote me from Panama that the leaf tossingof RY•odinocicY•lareminded him of the Rufous-sidedTowhee (Pipilo erytY•roptY•almus)--anothermember of the nine-primariedassemblage. The descriptionof foragingby Calyptophilus, althoughnot fully detailed,suggests similar behavior (Bond, 1936). Zoogeography. The Mimidae seemnot to be a truly neotropicalgroup; of the 13 genera usually recognized,none breedsin continentaltropical Americasouth of Honduras,except the widely distributedMimus and the aberrant South AmericanDonacobius, whose place in the Mimidae has beenquestioned. The distributionof RhodinocicY•la,although interrupted, is certainly neotropical. Conclusion. Inclusion in the Mimidae seemsto be negatedby the ana- tomical and morphologicalevidence, all of which points to the American nine-primariedassemblage. The availablebehavioral information is in no way inconsistentwith this conclusion.

INC•,US•ON •N T•E TI-IRAUP•DAE

Much less clear is the questionof family allocation within the nine- primariedassemblage. The family divisionsin this groupare to a consider- able extent matters of convenienceand tradition, rather than of clearly defined structural distinctions. When we examine the varied multitude of neotropicalgenera in this assemblagewe find intergradation in all char- actersthat havebeen proposed to separatethe tanagersfrom the grosbeaks, emberzinefinches, wood warblers, and honeycreepers.It is not surprising that almostall recentclassifiers differ on family lines in this assemblage (see p. 640 supra). On known structural characters Rhodinocichla seems to fit best with the tanagers,which in this assemblageis the most varied group in bill and bodyshape. As Clark ( 1913), Hellmayr (1936), and subsequentsystema- tistsplaced it in the Thraupidae,a justifiable conservatismsuggests that it be kept there until definite evidenceto the contrary is produced.

Behavioral similarities with Saltator, generally allocated to the cardinal grosbeak group, can hardly warrant a transfer, for that group is separated from the tanagers only by a heavy, conical bill, while Rhodinocichla is more slender billed than most tanagers. The Chat-Tanager, Calyptophilus,which showsresemblances in bill and body shape, ties in to the thicker-bill type through Phaenicophilus.Calyptophilus also showsresem- blancesof pattern, although the rose is replaced below by white and on the supra- loral and carpal regions by yellow. These similarities may be convergent. 646 E•s•A•, Position o! Rhodinocichlarosea [ ^uk [ Vol. 79

Resemblancesin red or rose-colorpattern are apparent in two other groups. R.W. Storer (1958. Unpublished paper before American Ornithologists'Union) called attention to similaritiesof both sexesto Granatellus,a neotropicalgenus of small, thick- billed, arboreal birds, with a remarkably interrupted range. Granatellus is customarily placedin the Parulidae; it would fit about as well in the Thraupidae. To my eye two South American Icteridae, Leistes militaris superciliarisand Pezites militaris, show, in males, an even closer resemblancein color pattern---even to the extent of having red on the lesser wing coverts. These open grassland birds show the character by whichIcteridae are separatedfrom Thraupidae (unnotched,acute bill). Were Rhodino- cichla transferred to Icteridae there would be no basis for distinguishingbetween the two families. The resemblancesof pattern cannot be the result of adaptive con- vergence. They indicate, I believe, common descentfrom the stock that produced the nine-primaried assemblageand suggestthat the ancestorsof Rhodinocichla lived in a more open habitat. Rhodinocichladoes exhibit behavioral features adapted to its habitat niche,not reportedof any of the relatively few tanagersthat have been carefully studied. But, it shouldbe noted, the Thraupidae are a very variedaggregation in habits,as well as in body form and bill shape. They representthe major radiation in the American tropics of the great nine- primaried assemblage.Some of the generaof the traditional Coerebidae, now often transferredto the Thraupidaeas nectar-adaptedtanagers, are certainly more unlike traditional tanagersin bill and body shapeand behavior than is Rhodinocichla. The euphoniagroup of tanagers (Tanagra, Chlorophonia,Pyrrhuphonia) is more aberrant in internal anatomy, feed- ing habits, and nesting. Unlesswe are preparedto cut up the traditional tanager family into a number of families, there seemsno over-all gain in erectinga separatemonotypic family for Rhodinocichla--at least without anatomicbasis. The hyphenatedEnglish group name "Thrush-Tanager," proposedby Clark (1913), adoptedby Hellmayr (1936), and used as Rose-breastedThrush-Tanager by most recent authors,seems adequately to suggestthe taxonomicuncertainty and the appearanceof the bird.

ACKNOWLED½MENTS

I am indebtedto Dr. William G. Georgefor discussionof this question and for permissionto useunpublished material based on his studiesof the hyoidealstructures, to Dr. William J. Beecherfor dissectingthe jaw musculature of Rhodinocichlaand permittingme to publishhis conclusions,to Mr. Paul Schwartzof Venezuelaand to Colonel F. O. Chapelle for information on the living birds, and to Dr. AlexanderF. Skutch for stimulatingthe writing of this paper. SUMMARY

Rhodinocichlarosea, on the basisof all knownstructural characters, ap- pearsto be a memberof the groupcalled "American nine-primaried assem- Vol.Auk79 ] EISENlVIANN•Positiono! Rhodinocichla rosea 647 blage,"which includes the tanagers,cardinal grosbeaks, American sparrows, buntings,wood warblers, icterids, and their allies. The resemblancesto Mimidae (negatedby externaland internal structural features)appear to be convergentadaptations to a similarhabitat niche. The aberrant behavioral features occur also in certain other members of the Americannine-primaried assemblage. Inclusionin the varied family Thraupidae, first suggestedby Clark's anatomicalstudy, and adopted by Hellmayr and by mostsubsequent taxon- omists,seems the most reasonabletreatment on the basis of our present knowledge.

LITERATURE CITED

A•rADO•, D. 1957. Remarks on the classificationof the perching birds, order Pas- sedformes. Calcutta, Zool. Soc. Proc., Mookerjee Memorial voL, pp. 259-268. B•ECHER,W.J. 1953. A phylogenyof the Oscines.Auk, 70'- 270-287. BOCK,W.J. 1960. The palatineprocess of the premaxillain the Passeres.Bull. Mus. Comp. Zool., 11•2(8): 361-488. Boxn, J. 1936. Birds of the West Indies. Acad. Sci. Philadelphia. xiv q-456 pp. Boxn, J. 1956. Check-list of birds of the West Indies. 4th ed. Acad. Nat. Sci. Philadelphia. ix -[- 214 pp. CLAret,H.L. 1913. Notes on the Panama Thrush-Warbler. Auk, 30: 11-15. DELACOUR,J., and C. VAUmE. 1957. A classificationof the Oscines(Aves). Los AngelesCty. Mus. Contrib. Sci., No. 16: 1-6. GEOROE,W. G. 1962. The classificationof the Olive Warbler, Peucedramus tae- hiatus. Amer. Mus. Novit., No. 2103: 1-41. G•i.a.m), E.T. 1958. Living birds of the world. Doubleday & Co., Garden City, N.Y. 400 pp. GOU•D, P. J. 1961. Territorial relationshipsbetween Cardinal and Pyrrhuloxia. Condor, 63: 246-256. HA•,•naAta,T. 1924. Notes on some Panama Canal Zone birds with special refer- ence to their food. Auk, 41: 304-326. HE•L•AYR, C.E. 1936. Catalogueof birds of the Americasand the adjacentislands. Field Mus. Nat. Hist. Zool. Set., 13, Pt. 9: 1-458. MARS•rAL•,A. J. ed. 1960. Biology and comparativephysiology of birds. Vol. 1. Academic Press, New York and London. 518 pp. MAYR,E., and D. A•ADOZV. 1951. A classificationof recent birds. Amer. Mus. Novit., No. 1496: 1-42. MAYR, E., and J. C. GREEtaWAY,JR. 1956. Sequenceof Passefinefamilies (Aves). Breviora, No. 58: 1-11. Mn;LER,W. DEW. 1918. The systematicposition of Calyptophilus.Auk, 35: 356- 357. RmOWAY,R. 1901. The birds of North and Middle America. U.S. Natl. Mus. Bull., 50, Pt. 1. xxx q- 715 pp. Rm•wAY, R. 1902. The birds of North and Middle America. U.S. Natl. Mus. Bull., 50, Pt. 2. xx q- 834 pp. RmawAY,R. 1907. The birds of North and Middle America. U.S. Natl. Mus. Bull., 50, Pt. 4. xxii-• 973 pp. 648 EISEIV/V•AIVlV,Position of Rhodinocichlarosea [ Vol.Auk 79

SxvTc•r, A.F. 1954. Life historiesof Central American birds. Pac. Coast Avif., 31: 1-448. S•cvTca, A.F. 1962. On the habits of the Queo, Rhodinocichla rosea. Auk, 79: 633- 639. WET,ORE, A. 1951. A revised classificationfor the birds cf the world. Smith. Misc. Coii., 117(4): 1-22. W•z•ORE, A. 1960. A classification for birds of the world. Smith. Misc. Coii., 139(11): 1-37. Win•.ts, E. 1960a. Voice, courtship, and territorial behavior of ant-tanagers in British Honduras. Condor, 62: 73-87. Wirris, E. 1960b. A study of the foraging behavicr of two speciesof ant-tanagers. Auk, 77: 150-177.

American Museum of Natural History, New York 24, New York.