Evolutionary Trends and Woodhewers

Home , Anabacerthia, Anabazenops, Aphrastura, Automolus, Campylorhamphus, Certhiaxis

EVOLUTIONARY TRENDS IN THE NEOTROPICAL OVENBIRDS AND WOODHEWERS

ALAN FEDUCCIA

ORNITHOLOGICAL MONOGRAPHS NO. 13

PUBLISHED BY

THE AMERICAN ORNITHOLOGISTS' UNION

1973 EVOLUTIONARY TRENDS IN THE NEOTROPICAL OVENBIRDS AND WOODHEWERS

ALAN FEDUCCIA

ORNITHOLOGICAL MONOGRAPHS NO. 13

PUBLISHED BY

THE AMERICAN ORNITHOLOGISTS' UNION

1973 ORNITHOLOGICAL MONOGRAPHS

This series,published by the American Ornithologists'Union, has been establishedfor major paperstoo long for inclusionin the Union's journal, The Auk. Publicationhas been made possiblethrough the generosityof Mrs. Carll Tucker and the Marcia Brady Tucker Foundation,Inc.

Correspondenceconcerning manuscripts for publication in the series shouldbe addressedto the Editor, Dr. JohnWilliam Hardy, Florida State Museum, Universityof Florida, Gainesville,Florida 32601.

Copiesof OrnithologicalMonographs may be orderedfrom the Treasurer of the AOU, Burt L. Monroe, Jr., Box 23477, Anchorage,Kentucky 40223. (See price list on insideback cover.)

OrnithologicalMonographs, No. 13, iv q- 69 pp. Editor-in-chief,John William Hardy SpecialAssociate Editors for this Issue, Stuart L. Warter and Peter L. Ames

Issued July 10, 1973 Price $2.00 prepaid ($1.60 to AOU Members) Library of CongressCatalogue Card Number73-81856 Printed by the Allen PressInc., Lawrence,Kansas 66044 TABLE OF CONTENTS

INTRODUCTION ......

COMPARATIVE ANATOMY OF THE SKULL ...... 9 Anatomical material ...... 11 Woodhewer skulls ...... 12 Ovenbird skulls ...... 14 Philydorine skulls ...... 17 Skulls of the "intermediates" _...... 22 Jaw muscles ...... 24 Functionalaspects of the skull types...... 25 STERNUM ...... 34

EVOLUTION OF THE SCANSORIAL FOOT ...... 36 Limb proportions...... ß..... 36 Distal end of the tarsometatarsus ...... 41 Femur and tibiotarsus ...... 42 The digits ...... 43 TAIL ...... 45

SYRINGEAL ANATOMY ...... 45 ELECTROPHORESISOF HEMOGLOBIN ...... 48 Methods and materials ...... 48 Results and discussion ...... 49 CLUSTER ANALYSIS ...... 51 A PHYLOGENY ...... 59 A BEHAVXORIAL MODEL ...... 61

CLASSIFICATION ...... 64

SUMMARY ...... 65

LITERATURE CITED ...... 68 INTRODUCTION

The Neotropical ovenbirds (Furnariidae) and woodhewers (Dendro- colaptidae) have long been consideredto be closelyrelated on the basisof derivedcharacters which are sharedby the two groupsbut not foundin other suboscinebirds. Generalplumage patterns in the two groupsare amongthe significantlystriking similarities, as almostall specieshave light brownto red- dish-brownbody plumage with variousdegrees of spottingon the breastand back,often with light throat patches. A spinytail, usuallyof chestnutor ferrugi- nouscolor, which is usedin the woodhewersas a brace in climbing,is found in variousdegrees of developmentin many membersof the Furnariidaeand is well developedin certain ovenbirdswhich foragelike the woodhewers,by climbingup tree trunks. These scansoffalfurnariids, including Pseudo- colaptes,Xenops, Pygarrhichas, the Margarorniscomplex, and somespecies of Cranioleuca,are of interestin that, althoughthey are behaviorallysimilar to the woodhewers,being tree-trunk foragers and possessingstiff, spinytails, they are clearlymembers of the Furnariidaeon the basisof suchcharacters asthe syrinx,cranial morphology, and feet. Commonwing patterns are found in the Furnariidaeand Dendrocolaptidae.In addition,syringeal and osteo- logicalcharacters ally the two groups.It is onlywithin the Dendrocolaptidae and Furnariidaethat two pairs of intrinsicsyringeal (tracheo-bronchial) musclesare found (Ames, 1971). This sharingof charactershas led manyornithologists to questionthe dis- tinctness of the two families. Thus the familial classification of the furnariids and dendrocolaptidshas long beenin a stateof uncertainty,and at present thereis little agreementamong ornithologists concerning the recognitionof familiesin the group. Recentclassifiers have generally followed either von Ihering (1915), who presentedevidence which he consideredfavored merg- ingthe two families, or Ridgway(1911 ), whorecognized two families. Strese- mann (1934) unitedthe ovenbirdsand woodhewersinto one family. In 1951 threeclassifications were proposed. Wetmore (1951) retainedtwo families becausehe consideredvon Ihering'sevidence inconclusive; Peters (1951) also recognizedtwo families. However,Mayr and Amadon (1951) treated the entiregroup as a singlefamily, as did Storer (1960). Early classifiers(see Garrod, 1873; and Beddard, 1898) placedconsider- able importanceon the condition of the nasal bones in the classificationof the higher categoriesof birds. Two basic arrangementsof the nasal open- ingswere distinguished,schizorhinal and holorhinal. In the former, the nasal openingextends posterior to the nasal-frontalhinge; in the latter, the posterior extent of the openingis anteriorto the hinge. The conditionin Furnar- ius and other ovenbirds,which was originallytermed schizorhinal(see Gar- rod, 1877), was later recognizedas not homologousto the conditionin other

1 2 ORNITHOLOGICAL MONOGRAPHS NO. 13 schizorhinalbirds (charadriiform birds, etc.), and F'tirbringer(1888) pro- posedthat the term pseudo-schizorhinalbe appliedto the conditionin those ovenbirdsin which the posteriorextent of the nasal openingis rounded,insteadof endingin a slit asin "true" schizorhiny. Garrod (1877) emphasizedthat the conditionof schizorhiny(= pseudo- schizorhiny)in the ovenbirdswas of sufficienttaxonomic importance to separate the groupfrom the holorhinalwoodhewers. However, Garrod had ex- aminedonly a small numberof species.Von Ihering (1.915) examineda muchlarger series of speciesand concludedthat therewas actuallyno clear- cut divisionbetween the pseudo-schizorhinalovenbirds and the woodhewers, and that the differencesbetween pseudo-schizorhiny and holorhiny repre- sentedslight modifications from a basicpattern and were thereforeof little taxonomicimportance, except perhapsin characterizinggenera. Ridgway (1911), however,had maintainedthat the differencein the arrangementof the nasal openingplus the differencesin the feet were of sufficientimpor- tance to separatethe Dendrocolaptidaefrom the Furnariidae. In the Furna- riidae(sensu Ridgway) the outertoe is shorterthan the middletoe and the hallux without the claw is not shorter than the inner toe (no. II) without the claw. The middletoe is unitedto the outertoe by lessthan the wholeof the secondphalanx. In the Dendrocolaptidae(sensu Ridgway) the outer toe is aboutas long as the middletoe and muchlonger than the inner toe, and the hallux without the claw is shorter than the inner toe. The three anterior toesare unitedfor the entirelength of the basalphalanx, and the middletoe is fusedto the outerby almostthe full extentof the secondphalanx. Ames(1971) in his systematicconclusions of the Furnariiemphasized that the syringealmusculature of the ovenbirdsand woodhewerswas an indication of closeaffinity of the two groups.Both groupspossess two pairsof intrinsic syringealmuscles, a characterwhich separatesthe two families from the antbirds (Formicariidae) and tapaculos(Rhinocryptidae). However, the ovenbirdsare apparentlyseparable from the woodhewerson the basisof the absencein the ovenbirds of horns on the Processi vocales (except in the genusGeositta). It is alsoof interestto note that thereis far more syringeal variation within the Formicariidae than within the woodhewer-ovenbird assemblage. Attemptsby many classifiersto place animalsinto distinguishablegroups without examiningin detail the charactersinvolved has led in many cases to classificationsbased on the most adaptivefeatures of the birds, namely the bill and feet (the classicalexample being hawks and owls which were at one time classifiedtogether on the basisof havingsimilar feet and bills) with little emphasison decipheringthe evolutionarypathways involved. The problem in the woodhewer-ovenbirdgroups has been the same as that for other 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 3

Figure 1. Two "strong-billed"woodhewers, an "intermediate,"and two philydorine furnariids.From top to bottom: Xiphorhynchu.•lachrymos'us' (actual length, 229 ram), Xiphorhynchusguttatus', Dendrocincla anabatina, Syndactyla subalaris, Automolus ochrolaemus. 4 ORNITHOLOGICAL MONOGRAPHS NO. 13 groupsof passerinebirds where there is a largeamount of adaptiveradiation for particularmodes of life. The woodhewer-ovenbirdproblem is of interestfor severalreasons. First, the two groupsare very closelyallied, yet exhibitperhaps the greatestadap- tire radiationin any group of New World passefinebirds, with climbing formsapparently having evolved independently in manysituations. Second, cranialmorphology in the two groupsdiffers; therefore, the possibilityof resolvingthe polarity of this evolutionexists. Most important,however, are four genera,Dendrocincla, Sittasomus, Deconychura, and Glyphorhynchus, whichare normallyplaced in the Dendrocolaptidaebecause they possessmost of the charactersof that family, but which showother charactersthat ally them with the Furnariidae. These forms, which I shall term the "intermediates,"form the startingpoint of this study (see Fig. 1). Initially, my main interestwas in the evolutionof the differenttypes of cranialmorphology in the ovenbirdsand woodhewers.An examinationof the skulls of woodhewersshowed that most forms of the Dendrocolaptidae conformedto a basicpattern. These genera, which include all of the wood- hewersexcept the four intermediates,are the formsthat I shall term the "strong-billed"dendrocolaptids; they appear to representa monophyletic groupon the basisof the skull and other characters.The "intermediates," Dendrocincla,Sittasomus, Deconychura, and Glyphorhynchus,are of particularinterest. Except for Dendrocincla(which forages in a varietyof pos- tures) the "intermediates"are behaviorallylike the woodhewersin that they forageby hitchingup tree trunks. They alsopossess the woodhewertype of syrinxand foot arrangement.However, they are clearlyintermediate betweenthe holorhinaland pseudo-schizorhinaltypes of nasal bone arrange- ments. Further, it was of interestto find that, of the four subfamiliesof the Furnariidae(which appearto be fairly well defined),the membersof the subfamilyPhilydorinae, the forest-dwellingfurnariids, are the formsthat pos- sessan intermediatearrangement in the conditionof the nasalbones, and some,such as Hyloctistesand Automolus,are similar to the "intermediate" woodhewersmentioned above. The other subfamiliesof the Furnariidae, the Synallaxinae,Furnariinae, and Sclerurinae,are composedalmost entirely of memberswhich are pseudo-schizorhinal,although in somespecies the nasal foramen is somewhat shortened. This interestingsituation led me to a literaturesurvey in whichI foundthe one importantpaper on the relationshipsof the woodhewersand ovenbirds, that of yon Ihering (1915). In it he discussesthe findingsof his investiga- tions of the cranial morphologyof the two groupsand recordsmuch the same observationsthat I have discussedabove. He stated (1915: 147) that, "Pronouncedholorhiny is foundonly amongthe Dendrocolaptinaeof which, 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 5 6 ORNITHOLOGICAL MONOGRAPHS NO. 13 however,some genera... Sittasomus,Dendrocincla and probablyothers... are typically schizorhinal."At that time he had not examinedthe genera Glyphorhynchusand Deconychura. He furtherstated that, "The Philydorinae (Philydor,Xenicopsis, Xenops, etc.) form a transitiongroup leading up to the Dendrocolaptinaeand the speciesare schizorhinalwith the exceptionof Automolus and Anabazenopswhich have the nasal foramen shortened." Although yon Ihering's divisionsare not easy to discernit is clear that an intermediatecondition of the nasalopenings exists in membersof the Dendro- colaptidaeand the subfamilyPhilydorinae of the Furnariidae. An examina- tion of the skinsof theseintermediate species of dendrocolaptidsproved even moreinteresting, for in theseforms the plumagepatterns are in someaspects alsointermediate. One strikingplumage character that seemedparticularly significantwas a rufouswing stripe(see Figs. 2 and 3) whichoccurs in various membersof the Furnariidae,but within the Dendrocolaptidaeis found only in Glyphorhynchusand Sittasomus. In Dendrocincla anabatina there is a similarbut more diffusewing stripe. However,Dendrocincla is intermediatein othercharacters. The tail doesnot possessthe striking,stiff, spine- like rectricescharacteristic of all othermembers of the Dendrocolaptidaeand is, in fact, morelike the typepossessed by membersof the Philydorinae.Also the bill and generalbody shapeof Dendrocinclaappear to be more philydorine-likethan dendrocolaptine.My own field observations,as well as those of other authors, show Dendrocincla to be intermediate in behavior (see Feduccia,1970). The speciesof Dendrocinclahitch up tree trunkslike the otherwoodhewers, but alsoforage in a varietyof otherways. Thus,the four genera, Dendrocincla, Sittasomus, Deconychura, and Glyphorhynchus, although not sharing identical characters,all possesssome features that are intermediatebetween the Dendrocolaptidaeand Philydorinae. These"intermediates" may representsimply "old" formsthat have retained many primitive characters.However, becausethe advanced(derived) character stateswithin the "strong-billed"dendrocolaptids are indeed those that are concernedwith tree-trunk foraging, and the "intermediates"(with the exceptionof Dendrocincla) are virtually identical to the "strong-billed" woo.dhewersin their climbingbehavior, the situationis indeed curious. It would seemreasonable to expectthe evolutiono.f thosecharacters that in- crease efficiency in climbing and tree-trunk foraging to occur, as has oc- curred in other unrelatedtree-trunk foraginggroups. One can test whether or not a given characterstate representsan actual climbing adaptationby looking at the samecharacter state in unrelatedgroups of birds (see Richard- son, 1942). The possessionby the "intermediates"of charactersintermediate between perchingand scansorialadaptations, plus the possessionof plumageand 1973 EVOLUTION IN OVENBIRDS AND WOODHEWFRS 7

Figure 3. The x•ingsof ^!ar,.,arornisrubiginosus (upper left). X{nops mimttns (upper right). Dendrocittcla attttbtttit•tt(center). Glyphorhynclnt$ .•pirttrtts (1ouer left), and Sittasomus griseicapillus (1ox•er right). 8 ORNITHOLOGICAL MONOGRAPHS NO. 13 other characterstypical of the ovenbirds,makes the "intermediates"suspect of being separateevolutionary lines of woodhewerscoming from ancestors that resembledthe present-dayphilydorine furnariids. Theseforms may have reacheddendrocolaptid grade with respectto the charactersused to classify the family Dendrocolaptidae(= scansorialadaptations), but still possess many featureswhich reveal a more recent ancestryfrom philydorinestock. In other words, the possibilityof a di- or polyphyleticDendrocolaptidae cannot be obviated. The alternativeis that the "intermediates"are simply part of an original mo.nophyleticradiation of woodhewerswhich have retainedmany "primitive" characters,and are forms occupying"intermediate" niches. It wasnot surprisingto find a statementby von Ihering (1915: 149) that "... we can presumethat the Dendrocolaptinaesprang from two different groupsof the Philydorinae." I thereforecontinued my investigationsof this groupin order to obtainevidence concerning the evolutionarylines involved in the ovenbird-woodhewerradiation, while emphasizingmainly the origin of the woodhewers.The main focusof this studyhas therefore been the dendrocolaptid-philydorineboundary, but data from the othergroups of the Furnari- idae are used where necessary.I have made the generalassumption th'at tree-trunkforagers represent the more derived condition. The assumption may be logicallyextended to includea philydorine-likeancestor as a logical choicefor a pre-dendrocolaptid.This assumptionis not only logical from anatomicalstudies, but alsofrom zoogeography,as philydorinesand dendro- colaptidsshare a near-commonzoogeographical range, both reachingtheir highestdensity in Amazonia. Anatomicalstudies often have failed to solvethis type of problembecause convergentadaptations may mask the actualphylogenies. It seemedto me that usefulcharacters might be found in a comparisonof proteinsof the vari- ousgroups. The useof electrophoreticpatterns of proteinsin systematicshas beendiscussed by variousauthors and will not be reviewedhere. The reader is referredto Kitto and Wilson (1966), and Sibley (1970) for examplesof studiesutilizing electrophoresis of proteinsin birds. AlthoughI examined variousblood, muscle,and eye lens proteins,only with hemoglobinswas I able to separatethe two families. The remainderof this paper is a presentationof variouscharacters of the ovenbirdsand woodhewersand an evaluationof the positionof the "intermediates"with respectto thesecharacters. After the anatomicalevolutionary trends are discussed,the hemoglobindata are presented,and phylogenetic considerations are made on the basis of all of the characters. In the various sectionsof this paperI have attemptedto answerseveral primary questions. First, what are the major featuresof the anatomicalevolutionary trends in- 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 9 volvedin the evolutionof the tree-trunkforaging (derived) woodhewers,and second,what anatomicaland historical position do the "intermediates"oc- cupy? ACKNOWLEDGMENTS I am indebted to the following personsand institutionsfor assistance throughoutthis investigation.The membersof my doctoralcommittee, Rob- ert W. Storer, Claude W. Hibbard, Robert R. Miller, and Harrison B. Tordoff, providedcriticism and encouragementduring the entirestudy. JohnB. Burch of the Mollusk Divisionof The Universityof MichiganMuseum of Zoology made his laboratoryavailable to me for biochemicalstudies, and Gene K. Lindsayinstructed me in variouslaboratory techniques. The Departmentof Zoologyof The Universityof Michiganand John M. Allen providedvarious piecesof laboratoryequipment. Members of the Departmentof Biology of the Universityof Costa Rica and particularlyDouglass Robinson provided laboratoryspace and other facilities. CharlesF. Walker of The University of MichiganMuseum of Zoology,Joseph A. Tosi, Jr. of the Tropical Science Center, and JorgeR. Campabadalof the Organizationfor Tropical Studies were of greathelp duringthe CentralAmerican phase of the study. Maxwell Cone kindly permittedme to use his finca for studieswhile I was in Costa Rica. Richard L. Zusi of the U.S. National Museum and James H. Hunt of the LouisianaState University Museum of Zoologyprovided measurements of certainbones. PeterL. Ames and Mary HeimerdingerClench provided useful informationabout their doctoral dissertations.Martha B. Lackey skillfully renderedall of the anatomicalillustrations except Figure 16, and Louis Martonyi took all of the photographs.Frank B. Gill offeredmany usefulsug- gestionsthroughout this study. Arnold G. Klugeand JohnLundberg offered much assistanceand advice with the numerical taxonomy section of this paper. Financialsupport was providedby a grant from the Frank M. Chap- man MemorialFund of the AmericanMuseum of Natural History and by a grant from the National ScienceFoundation, GB-6230, to N. G. Hairston, The University of Michigan, for researchin Systematicand Evolutionary Biology. This paper is a modificationof a doctoral dissertationsubmitted to the Facultyof The Universityof Michiganin partial fulfillmentof the require- mentsfor the Ph.D. degree,1969.

COMPARATIVE OSTEOLOGY OF THE SKULL Althoughthis section covers most of the skulltypes found in the Furnariidae and Dendrocolaptidae,it is not intendedas an extensivetreatise on the skulls with inclusionof all the minute variations. Instead, I have attemptedto con- densethe variationsinto meaningfulcharacter states in each groupso as to 10 ORNITHOLOGICAL MONOGRAPHS NO. 13

np pmx

ß-,?:;:;i';i?i!i! ;!?!;!!!??';'"...... B

.p nf

c \m-p

ib I cm bt pr Figure 4. Dorsal (A), lateral (B), and ventral (C) aspectsof the skull of the woodhewer, Xiphorhynchusguttatus. Abbreviationsare as follows: bt p, basitemporal plate;bt pr, basipterygoidprocess; e p, ectethmoidplate; e n, externalnaris; f, frontal; 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 11 attemptto uncoverthe generalevolutionary trends, but not all of the intra- groupvariation. There is still controversyconcerning osteological nomencla- ture; however,in this paper the terminologyfor skull charactersgenerally followsthat of Bock( 1963).

ANATOMICAL MATERIAL The followingis a list of the skeletalmaterial examined during the course of thisstudy: The speciesDendrocincla fuliginosa, 2 specimens;D. anabatina, 2; Deconychuralongicauda, 2; Sittasomusgriseicapillus, 11; Glyphorhynchus spirurus, 10; Dendrexetastesrufigula, 1; Xiphocolaptespromeropirhynchus, 1; Dendrocolaptescerthia, 2; D. picumnus,2; D. platyrostris,3; Xiphorhyn- chuspicus, 3; X. obsoletus,2; X. pardalotus,2; X. guttatus,7; X. flavigaster, 4; X. lachrymosus,1; X. triangularis,7; Lepidocolaptesleucogaster, 4; L. angustirostris,4; L. affinis, 3; L. albolineatus,3; Campylorhamphuspusillus, 1; Geositta paytensis, 1; G. cunicularia, 4; Upucerthia dumetaria, 3; U. validirostris,1; Ochetorhynchusruficaudus, 2; O. certhioides,2; Cinclodes antarcticus,2; C. fuscus,5; C. atacamensis,2; C. taczanowskii,1; Furnarius rufus, 8; Sylviorthorhynchusdesmursi, 1; `4phrastura spinicauda, 4; Phleo- cryptesmelanops, 5; Leptasthenuraandicola, 1; L. aegithaloides,1; L. platensis, 3; Spartanoica maluroides, 4; Schoeniophylax phryganophila, 11; Sy- nailaxis ruficapilla, 1; S. frontalis, 6; S. albescens,4; S. brachyura, 6; S. gujanensis,2; S. rutilans, 2; Certhiaxis cinnamomea,6; Cranioleucasulphu- rifera, 2; C. obsoleta,2; C. pyrrhophia,1; C. erythrops,1; `4sthenesdorbignyi, 1; ,4. baeri, 2; ,4. humicola, 1; ,4. modesta,2; ,4. humilis, 1; ,4. hudsoni,2; Phacellodomusrufifrons, 1; P. striaticollis,8; Coryphisteraalaudina, 5; ,4num- bius annumbi, 4; Margarornis rubiginosus,4; Premnoplex brunnescens,3; Pseudocolapteslawrencii, 2; Pseudoseisuralophotes, 3; Hyloctistessubulatus, 2; Syndactylarufosuperciliata, 16; ,4nabacerthiastriaticollis, 3; Philydor lichtensteini,6; P. rufus, 1; ,4utomolusochrolaemus, 6; Heliobletus contaminatus, 1; Thripadectesrufobrunneus, 1; Xenopsminutus, 3; Pygarrhichasalbogularis, 1; Sclerurusguatemalensis, 1. Alcoholicspecimens of the followingspecies were examined: Dendrocinclaanabatina, Deconychuralongicauda, Glypho- rhynchusspirurus, Dendrocolaptes certhia, Xiphorhynchus guttatus, X. lachrymosus,X. triangularis,Lepidocolaptes souleyetii, Campylorhamphus pusillus, Synallaxisalbescens, Margarorrds rubiginosus, Pseudocolaptes lawrencii,

i p, interpalatine process;i s, interorbital septurn;j b, jugal bar; m f, mandibular foramen (not presentin Xiphorhynchus); m p, mediopalatineprocess; m-p, maxillo-palatine; m s p, median shelf of the palatine; n, nasal; n f, nasal floor; n-f h, nasal-frontal hinge; n p pmx, nasal process of the premaxilla; o p q, orbital process of the quadrate; p, palatine; p p, postorbital process;pt, pterygoid; q, quadrate; t f, temporal fossa; t p, transpalatine process;v, vomer; z p, zygomatic process. 12 ORNITHOLOGICAL MONOGRAPHS NO. 13

Hyloctistessubulatus, Automolus ochrolaemus and nestling,Thripadectes rufobrunneus,and Xenopsminutus and nestling.

WOODHEWER SKULLS The skullof Xiphorhynchus(Fig. 4) is typicalof thewoodhewers and will be usedas the basisof the descriptionof the skullsof the group. Theupper jaw differslittle in basicstructure from that of otherpasserMe birds,except for therather long, slightly decurved, heavily ossified bill. The bill accountsfor approximatelythree-fifths of the lengthof the entireskull, butits characteristicsare typicallypasserine, there being a long,oval external naris,and an unossifiednasal septurn (perforate naris). The posteriorextent of thenasal opening ends well anterior to thenasal-frontal hinge; it is therefore holorhinal. The nasal-frontalhinge is well developedas in most pas- serinesas an areaof thinningof the nasalbones posteriorly; the suturesof the nasalbones are visible. There is a slightdepression of the frontalbones at the junctionof the nasalbones, but theydo not curveanteriorly over the nasals,as in manywoodpeckers. The actualnasal-frontM hinge area appears verybroad in relationto the restof the skull. Thisis owingnot onlyto the broadhinge, but alsoto the dorsalarticulations of the lateralbars of the nasalbones, which are thick andmeet the frontalbones at an areaof broad- ening,and are at approximatelythe samelevel as the nasal-frontalhinge. The lachrymalis apparentlyabsent. The ectethmoidis a fairly thickbone, whichis constrictedmesially and sendslaterally a bar whichapproaches the jugalbar. Thereis a singleforamen where the ectethmoidbone fuses im- perceptiblywith the nasaland frontal bones and the orbitalseptum dorsally andmesially. The orbitalseptum is verywell ossified,but thereare two major openingsposteriorly, a fontanellepostero-dorsally and a largeforamen for thepassage of theoptic nerve. There are several small foramina for thepas- sageof othernerves and vessels. The orbital septum ends at the areawhere the ectethmoidplates meet mesially, just below the nasal-frontalhinge; there is no extensionof the septuminto the nasalcavity. The postorbitaland zygomaticprocesses are present; both are strongly built, but of mediumlength for passerines.The two processes are well separa ted from each other by the largetemporal fossa. The remainderof thebraii t caseis typicallypasserine withseveral exceptions. The supraorbitalarea of ' he frontal bones is extraor- dinarilybroad, the temporalfossa is extremelylarge, and the two fossae almostmeet each other posteriorly at the supraoctipital region. The quadrate is a strong,well-developed bone. There are threearticular condyles, but the lateralcondyle merges smoothly into the posteriocondyle. There is a large sesamoidbone present at the posteriorcondyle in some specimens.The quadratesends out a massiveorbital process that is expandedat its tip. 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 13

The ventral aspectof the skull is characterizedby being heavily ossified anteriorlyexcept for the internasalsepturn, which is essentiallyabsent, and the floor of the nasal cavity. The maxillo-palatinesare medium-sized,but the distalends are not exceptionallybroadened, as in many passetines,and only come into slight contactwith the vomer mesially. The palatinesare situatedfar apart anteriorlyat their fusion with the premaxillae. The trans- palatineprocess is fairly broad at its base,but tapersrapidly makingan ex- tremelylong, thin structurepointed at its tip. The interpalatineprocess is present,but short. The mediopalatineplate is constrictedand ends quickly to give rise to the large mediopalatineprocesses, which are somewhatfolded and fuseposteriorly with the pterygoids.The pterygoidsare heavy and have prominentdorso-medial processes near the quadrate articulations,which are the orbital processesof the pterygoids.The vomer is a short,broad plate of bone that is dividedanteriorly in typicalpasserinc fashion, but the posterior diastemacharacteristic of passetinesis obscuredby ossification.The jugal bars are thin, but strong,and convergeslightly anteriorly as they fuse im- perceptiblywith the maxillaein a broad area of fusion. The palatineprocess of the premaxillais not visibleand is probablyfused. Bock (1960: 436) reportedthe palatineprocess of the premaxillato be presentin all generaof woodhewers,but the relative degreeof fusion betweenthe processand the palatinevaries in the differentgenera. He generalizedthat the processis only slightlyfused in specieswith a long curvedbill, and heavilyfused in species havinga short,straighter and heavierbill. In Xiphorhynchusthe processis slightlyfused. The remainingcharacters of the baseof the skull appearto be, in general,typically passefine. Anteriorly,the stronglower jaw is fusedtogether for approximatelytwo- fifths of its entire length. There are no outstandingfeatures of the woodhewer lower jaw exceptfor its sturdystructure and the near absenceof a mandibular foramen typical of passetines.The foramen is reduced to an almost in- visiblevestige of pinholesize, or is completelyabsent. The forms that I shall term the "strong-billed"woodhewers, Dendro- colapres, Xiphorhynchus, Xiphocolaptes, Dendrexetastes,Lepidocolaptes, and Campylorhamphus,generally conform in skullcharacters to the foregoing description.Although I have not examinedthe skullsof the generaHyle- xetastes,Nasica, and Drymornis,they appearto be typicalof the groupfrom externalmorphology and skull X-rays of study skins. The variation in the skullsof the "strong-billed"woodhewers involves such charactersas length and shapeof the bill, whichvaries somewhat going from the Xiphorhynchus- Lepidocolaptestype of moderatelength, somewhatcurved at the tip, to the broad-basedtype found in Dendrocolaptes,to the very long, curvedbill of Campylorhamphus.However, it is of interestthat the basictype of bill strut- 14 ORNITHOLOGICAL MONOGRAPHS NO. 13 ture doesnot seemto alter greatlythe other skull characters.There are minor differenceswhich will be treatedin a genericreview of the groupwhich I am presentlypreparing but none that leave any doubt as to a givenbird being withinthis group. In the wide-billedDendrocolaptes, and in Dendrexetastesand Xiphocolaptes, the medialpalatine plate is somewhatmore expanded than in Xiphorhynchus. There is also other palate variationthat seemsto be correlatedwith the type of bill, but the basic structure is the same. There is some variation in the amountof ossificationof the nasalregion. This anatomicalseries begins with less ossifiednasal regions in Lepidocolaptes,Xiphorhynchus, and Dendro- colaptesand proceedsto the greatly increasedossification in Xiphocolaptes (with the anterior part of the nasal region being imperforate) culminatingin Campylorhamphuswhere ossificationhas occurredto the degree that the nasal opening is a small oval hole. The situation is somewhatdifferent in Dendrexetastes(one of the very strong-skulleddendrocolaptids) where the actualnasal openingends dose to the nasal-frontalhinge, but the skull is amphirhinal(see Feduccia,1967). It would appear in this case that the amphirhinalcondition may be compensationfor the lack of ossificationin the nasalregion.

OVENBIRD SKULLS The descriptionof typical ovenbirdskulls is difficult. While the woodhewersare very uniformwith respectto skull structure,the ovenbirdassem- blageshows great diversity. However,for the purposesof this studyonly two typesneed be distinguished,those that are typicallypseudo-schizorhinal, which are found in the subfamilies Synallaxinae, Furnariinae, and Sclerurinae (Pygarrhichas is also pseudo-schizorhinal),and those that tend towards holorhiny,such as thoseof certain membersof the Philydorinae. Although one can otherwisegenerally characterize the varioussubfamilies of the Furna- riidae,they are only partiallyseparable by the structureof the skull, sofor this studyonly the typicalpseudo-schizorhinal skull and the intermediatephily- dorinecondition will be described.The skull of Asthenes(Fig. 5) is clearly pseudo-schizorhinaland formsthe basisfor the descriptionof that skull type. In generalform the skull appearsfragile comparedto the more massive bonesthat composethe woodhewerskull. The slightlydecurved bill is small and thin and constitutesless than half the lengthof the entire skull. The nasal septurnis very long and is perforate. There is no ossificationwithin the sep-

Figure 5. Dorsal (A), lateral (B), and ventral (C) aspectsof the skull of the ovenbird, Asthenes modesta. See Fig. 4 for abbreviations. New terms are: n s, nasal septurn; o p pt, orbital processof pterygoid;and p pm, palatine processof premaxilla. 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 15

,np pmx

n-f h

p p and z p,fuse

,nf

c sp p pm P

Icm 16 ORNITHOLOGICAL MONOGRAPHS NO. 13 tum. The long nasalopening extends posterior to the nasal-frontalhinge (in- operativein this case), but is rounded,unlike the "true" schizorhinalcon- ditionof the Charadriiformes,where the nasalopening ends posteriorly in a slit. The nasal-frontalhinge is visibleas an area of thinningof the nasalbones posteriorly.The dorsalbar of the uppermandible is very thin as are the ventral bars. The frontal bonesmeet the nasalssmoothly, there being no anterior curving of the former. The nasal struts, unlike those of the woodhewers,are very thin. The dorsal hingesof the nasal struts are displaced dorso-caudally,unlike the condition in Xiphorhynchus,where the dorsal hingesform the lateral areasof the nasal-frontalhinge. Therefore,the actual area of the nasal-frontalhinge is very constrictedcompared to that of the woodhewers.There is very little ossificationof the orbital septum,but there is a small,thin plate of bone anteriorin the septurn,which meets the mesial extentof the ectethmoidplates. Unlike the conditionin the woodhewers,a bony septurnextends anteriorly just beneath the dorsal bar of the upper mandible,slightly anterior to the nasal-frontalhinge area. No lachrymalis present,as is alsotrue of the woodhewers,but the ectethmoidplate is unlike the woodhewercondition. This broadplate has very little mesialconstriction, and sendsoff a very slightlateral strut that doesnot reach the jugal bar. The dorsalforamen of the ectethmoidplate is relativelymuch smaller than that of the woodhewers,but is single. The lateral bordersof the entire ectethmoid plate are tilted anteriorly, unlike the woodhewercondition in which the platesare almostat right anglesto the orbitalseptum. The postorbitaland zygomaticprocesses are fusedto form a foramenfor the passageof the adduc- tor muscle. The temporalfossa is small and much more poorly developed than that of the woodhewers.The supraorbitalarea of the frontal bones is constricted, unlike the woodhewer condition and more like the condition found in most other passerines,but the remainderof the brain case shows no exceptionalfeatures. The quadrateis very weak comparedto that of the woodhewers.The quadratehas three articularprocesses and, as in the woodhewers,the lateralcondyle merges smoothly with the posteriorcondyle. How- ever, the lateral condyleconstitutes a broader area than in the woodhewers. A sesamoid,which is retainedin some preparations,is presentat the posterior condyle. The orbital processof the quadrateis thin and the tip is not expanded. In ventral view, the skull is generallyless heavily built and showsless os- sificationthan in Xiphorhynchus. The maxillo-palatinesare very thin, small, andform a longposteriorly projecting plate as in mostpasserines, but fail to fusewith the vomer. The vomeris a bonyplate, which like that of mostpasserines,has a median diastema that extends anterior to the level of the maxillo-palatines.Anteriorly, the vomer appearsmuch like that of Xipho- 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 17 rhynchus,is bifurcat½,but continuesrelatively farther anteriorlythan in wood- hewcrs. The medianshelf of the palatineis relativelybroader in Asthenes than in Xiphorhynchusand other woodhcwcrs.Bock (1960:436-438), re- ported on the palatineprocess of the prcmaxillain furnariidsas follows: "In mostgenera, the processis present,lying alongthe palatineand not fused with that bone. In Furnarius. . . the processlies free in the spacebetween the palateand the dcntaryprocess of the prcmaxillaand in someways re- semblesan ossifiedtendon. Rarely is the processfused or absentas in the caseof Leptasthenuraor Synallaxis.The lengthof the processvaries some- whatbetween the genera."The processis unfusedin Asthenes.As theycon- tinue posteriorly,the palatinesdiverge laterally but do not becomewider until they mergewith the main bony plate of the palatineposteriorly. The interpalatineprocess is present,but does not extend far anteriorly. The mediopalatineprocess is small and extendsslightly posterior. The palatines are fused to the pterygoidsposteriorly. The pterygoidsshow no special featuresexcept for their orbital processeswhich are relativelymuch smaller than in the woodhewers.The jugalsare thin and their anteriorfusion with the maxillaeis markedwith a slightchange in anglewith the ventralbar of the upperjaw. Thereis no contactof the lateralwing of the ectethmoidwith the jugalbar. The lowerjaw is relativelymuch weaker than that of the woodhewersand has a largemandibular foramen. Althoughthere is muchvariation in the skullsof ovenbirds,the basicpattern seemsto remain fairly constantuntil the philydorinesare included(see next section). The main variation is seenin the amount of ossificationof the interorbitalsepturn, the positionof the posteriorextent of the nasal opening, and sizeof nasalopening, the shapeof the bill, and the generalstrength of the entire skull. There is also variation in the postorbitaland zygomatic processes.In somespecies the two processesare fused,forming a canal for the passageof the adductormuscle; in other speciesthey are separateand the temporalfossa is larger in thesecases. Also, the ectethmoidplate varies somewhat,with somespecies approaching the woodhewercondition of the character. Aside from these points, there is uniformity in ovenbird skull anatomy.

PHILYDORINE SKULLS The genusAutomolus will be describedhere as an exampleof the holorhinal ovenbird skull, intermediate in structurebetween the woodhewer and other pseudo-schizorhinalovenbird skulls. The bill in Automolus(Fig. 6), like that in most of the ovenbirds,accounts for about half the length of the entire skull, but in this genusthe bill is much more heavily built than in Asthenesand the synallaxinesin general. There is a fairly long, oval-shaped externalnaris, comparativelyless extensivethan in Asthenes,but more so 18 ORNITHOLOGICAL MONOGRAPHS NO. 13

n nppmx

is f •p

,n-f h

,t p

mp J btp • I cm • Figure6. Dorsal(A), lateral(B), andventral (C) aspectsof theskull of Automolus ochrolaemus.See Fig. 4 for abbreviations. 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 19 than in Xiphorhynchus.The dorsaland ventral bars of the upper mandible are strongerthan in Asthenesbut weakerthan in Xiphorhynchus.As in other ovenbirdsthe naris is perforate. The nasal-frontalhinge is visible as an area of thinningof the nasal bones. The frontal bones meet the nasals smoothly. The dorsal hingesof the nasal struts are somewhatdisplaced dorsocaudally,though less so than in Asthenes,and in generalthey appear more like thoseof the woodhewers,where they form the lateral bordersof the nasal-frontalhinge. The skull of Automolusis typicallyholorhinal, and the externalnaris endsanterior to the nasal-frontalhinge. The nasal struts are thicker than thoseof Asthenesbut thinner than thoseof Xiphorhynchus. The orbitalseptum is like that of Asthenes,there being a largepostero-dorsal fontanelleand an anteriorperforation of the septum,but the bony part of the septumis of muchstronger material than that of Asthenes.The anterior part of the orbital septummeets the mesial extent of the ectethmoidplates. The bony interorbitalseptum extends only slightlyanterior into the nasal cavity. The actualectethmoid plates are more like thoseof the woodhewers; they are composedof strongmaterial and are greatlyconstricted mesially. They sendout laterallya long thin bar whichmeets the jugal bar. The lateral extensionof the ectethmoidsis tilted slightlyanteriorly, but less so than in Asthenes;more so than in the woodhewers.There is a singledorsal foramen as in the otherovenbirds and in the woodhewers,but it is relativelylarger than in Xiphorhynchus. The postorbital and zygomatic processesare well- developed(but lessso than in Xiphorhynchus)and are separatedby a broad and deeptemporal fossa, similar to that of Xiphorhynchusbut relativelyless extensive. The supraorbital area of the frontal bones is broader than in Asthenesbut more constrictedthan in Xiphorhynchus. The supraoccipital regionis somewhatbulged but lessso than in Xiphorhynchus.The quadrate is a strongbone with three articularcondyles, and like thoseof Asthenesand Xiphorhynchus,the lateral articular condylesmerge smoothlyinto the posterior condyle,but the jugal articulationis broadenedlaterally, as in Asthenes. The quadratesends off a strongorbital processwith an expandedtip as in Xiphorhynchus.The vomer of A utomolusis somewhatlike that of Asthenes, beingbifurcate anteriorly with a largemedian diastema that extendsto the level of the maxillo-palatinesanteriorly. The maxillo-palatinesare thin as in other ovenbirdsand form a plate that extendsposteriorly, and they almost meet the anterior extent of the interpalatineprocesses. The median shelf of the palatinesis broad as in Asthenesand other ovenbirds.The interpalatine processesaxe small and extendslightly forward, and the mediopalatinepro- cessesaxe relatively larger than in Asthenesand are slightlyflared laterallyat their posteriorextent. The palatinesare fusedto the pterygoidsposteriorly. The pterygoidsare relativelystronger than in Asthenesand each sendsoff 20 ORNITHOLOGICAL MONOGRAPHS NO. 13 an orbital processof relativelygreater size. The jugal bars are relatively thicker than those of Asthenes. The skull of Automolus,which is fairly representativeof the philydorine furnariids,is somewhatintermediate between that of the majority of the ovenbirds,which have a weaklybuilt pseudo-schizorhinalskull, and that of the woodhewers,typified by the strong,holorhinal skull of Xiphorhynchus. The upper jaw of Automolusis strongerthan that of the typicalovenbirds, the externalnaris is of intermediateexpansion, and the nostrilis holorhinal, but the dorsal articulationsof the nasal struts are somewhatdorso-caudally displacedas in the ovenbirds.The ectethmoidplate is more like that of the woodhewers,but in some respectsis intermediate. The orbital septum is strongerthan that found in most ovenbirds,but is typicalof the furnariids, havinglarge fontanelles.The supraorbitalregion is constrictedlike that of other ovenbirds,but less so than that of the typicallypseudo-schizorhinal types. The postorbitaland zygomaticprocesses and the temporalfossae are morelike the conditionof Xiphorhynchusthan that of Asthenes.These char- actersindicate a strongadductor muscle. In generalthe palate is more like that of most ovenbirds.The vomer is clearlybifurcated anteriorly, and there is a largemedian diastema in the vomer. The medialpalatine plate is broadlike that of mostovenbirds, and the trans- palatineprocesses are ovenbird-like.The maxillo-palatinesare thin and have a posteriorlyextending plate like that of most ovenbirds.The quadratehas the lateral bulgeof the jugal articulationas in the other ovenbirds,but has a strongorbital processwith an expandedtip as is typicallyfound in the woodhewers. There is a mandibular foramen in the lower jaw as in the other ovenbirds. Most of the philydorinefurnariids are not quite so intermediatein skull charactersas is Automolus, and there is a completeanatomical series going from the fragile ovenbirdpseudo-schizorhinal skull type to the strongholo- rhinal type found in A utomolus.Most of the philydorinestend to be less holorhinal than Automolus, with the dorsal articulations of the nasal struts being more dorso-caudallydisplaced. Also, in most speciesthe bill and the skulls, in general, are of weaker construction.The orbital processof the quadrateis not expandedat its tip in mostspecies, and thereis an anatomical seriesgoing from Philydor and Anabacerthiawith no expansionof the tip, throughHyloctistes and Thripadecteswith slight expansion,to Automolus whichhas the tip expandedto the extentfound in the woodhewers.In mostof the philydorinesthe ectethmoidplate tendsto be more like that found in the

Figure 7. Dorsal (A), lateral (B), and ventral (C) aspectsof the skull of Sit- tasomusgriseicapillus. See Fig. 4 for abbreviations. 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 21

n np pmx

c msp mp

bt p Icm 22 ORNITHOLOGICAL MONOGRAPHS NO. 13

Dendrocolaptidae.The formswhich most closely approach this condition are Hyloctistes,Pseudocolaptes, Philydor, Automolus, and Anabacerthia. Of the non-philydorines,Sclerurus, Pygarrhichas, Margarornis, and Premnoplex have somewhatdendrocolaptid-like ectethmoid complexes. Most of the palatalcharacters of the philydorinesare clearlyovenbird-like, and even the strong-billedforms such as Automolusshow much the samepalatal structure. Thereis a completeseries in the relativeextent of the supraorbitalarea of thefrontal bones, from the veryconstricted condition in the synallaxinefurna- riidssuch as Asthenesto the philydorines,where such forms as Xenopsare more like the woodhewers in this character.

SKULLS OF THE "INTERMEDIATES" The skullsof the genera$ittasomus (Fig. 7), Deconychura,Dendrocincla (Fig. 8), and Glyphorhynchusdeserve special attention. The skullsof Sit- tasomusand Deconychura are very similar in structureand are described to- gether. Both Sittasomusand Deconychuraare weak-billedwoodhewers that share charactersof the skullwith both the ovenbirdsand the "strong-billed"woodhewers.The billsof bothgenera are weakly constructed, and the nasalopening is verylong, the posteriorextent ending at the levelof, or slightlypos- terior to, the nasal-frontalhinge. The dorsalarticulations of the nasalstruts are somewhatdorso-caudally displaced. The supraorbitalregion of the fron- tals is somewhatbroader than that of most of the ovenbirds,but lessso than the "strong-billed"dendrocolaptids. The remainderof the braincase shows no exceptionalfeatures. There is a supraoccipitalbulge, the postorbitaland zygomaticprocesses are fairly well developed, and the temporal fossa is well developedas in the philydorinesand woodhewers.The articularsurface of the quadrateis like thatof the woodhewers,but the orbitalprocess of the quadrateis likethat of theovenbirds, being slender with a non-expandedtip. The orbitalseptum is lessossified than that typicalof the woodhewers,and thereis a largepostero-dorsal fontanelle. Also, as in the ovenbirds,an an- terioropening through the septumis present.The ectethmoidplate is the philydorine-dendrocolaptinetype,but its lateralborder is tiltedanteriorly as in the ovenbirds,although less so than in most. The palatinesand pterygoids showno outstandingfeatures that would be of any helpin thisanalysis. The medialpalatine plate is smallin Sittasomus,but largerin Deconychura.The vomeris bifurcatedanteriorly, and in Deconychurathere is no mediandiastema. However,in Sittasomusthere is a slightdiastema in the most pos-

Figure 8. Dorsal (A), lateral (B), andventral (C) aspectsof the skullof Dendro- cincla anabatina. See Fig. 4 for abbreviations. 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 23

r•-f h

,•rl

I cm I • 24 ORNITHOLOGICAL MONOGRAPHS NO. 13 terior part of the vomer. Thus, the generaSittasomus and Deconychurapre- sent a mosaicof dendrocolaptidand furnariid charactersin their skulls. The short-billedGlyphorhynchus, the wedgebill,is differentfrom all other generaof woodhewers.Because this woodhewer,unlike the others,pecks tree trunksand brancheslike a small woodpeckeror piculet,its cranial features are differentand shallbe coveredin detailin a separatepaper. For the purposesof this paper it is sufficientto note that Glyphorhynchusis intermediate between the ovenbirds and woodhewers in some cranial characters. The posteriorextent of the nasalopening is almostto the nasal-frontalhinge, and the nasalstruts are very thin. The ectethmoidhas a slightanterior tilt. The orbital processof the quadrateis thin and doesnot have an expanded tip, and the jugal articulationof the quadrateis pronouncedlaterally. The foregoingare ovenbirdskull characters.An obviouspecking adaptationis found in the frontal bonesbeing curved anteriorly over the nasalsas in some woodpeckers.Otherwise, Glyphorhynchus is like the woodhewersin having a largetemporal fossa with well-developedpostorbital and zygomaticprocesses, dendrocolaptine-philydorinetype of ectethmoidcomplex, ossified interorbital septum, and an expandedsupraorbital area of the frontal bones. In general appearanceit is a stronglyconstructed skull. The skull that is most like that of the ovenbirdsis that of Dendrocincla, which resemblesmany of the philydorinefurnariids. Its basic skull characters are like those of Sittasomusand Deconychura,but the skull is more heavily built, and in generalform very closelyresembles the philydorine generaHyloctistes and Thripadectes.The posteriorextent of the long nasal openingends slightly anterior to, or at the level of, the nasal-frontalhinge, but the nasal struts are sturdier than in Sittasomusand Deconychuraand are less displaceddorso-caudally at their dorsal articulations.The ectethmoid platesare morebulbous than in the otherforms but are displacedvery slightly anteriorly. The supraorbitalarea of the frontalsis expandedrelatively more than in the philydorinesbut lessso than in the "strong-billed"woodhewers. This charactervaries somewhatin the three speciesof Dendrocinclathat I examined. The orbital septurnis more ossifiedthan in Sittasomusor De- conychurabut still has an openingthrough the septum. The postorbitaland zygomaticprocesses are well developed,and there is a well-developedtem- poral fossa. The quadrate,like that of Sittasomusand Deconychura,sends out an orbital processwith a non-expandedtip. The palate showsno diag- nosticfeatures. The maxillo-palatinesare unusuallybroad, and the vomer hasa slightdiastema posteriorly.

J^w MUSCLES Alcoholicspecimens of ovenbirdsand woodhewerswere examinedto de- termineif there were any significantdifferences in jaw musculaturebetween 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 25 the two groupsthat were not decipheredfrom the skull anatomy. As mostof the observed variation was confined to such variable areas of the skull as the palateand its associatedparts, muscles will not be coveredin this paper. However, there are severaljaw musclesthat deservespecial attention at this point. The tremendousdevelopment of M. adductormandibulae is one of the moststriking features of the exposedwoodhewer head. Especiallynote- worthyare the externusrostralis portions of this muscle,the posteriorextents of which nearly meet at the posteriormedian plane of the skull abovethe occipitalcondyle. This stronglybipennate muscle has fibersconverging on a centralaponeurosis which is ossifiedin the "strong-billed"woodhewers and is oftenpreserved in the dried skeletons.The muscleis muchless developed in the ovenbirds. Of great interesthere are the "intermediates,"all of which appearto be morelike the woodhewers.In Dendrocincla,however, M. adductormandibulae is more poorlydeveloped and is more like that of ovenbirds. Sinceno alcoholicspecimen of $ittasomuswas available,the outline of the origin of this muscleon the skull forms the basisof my observation. The areasof origin of both M. adductormandibulae and M. depressorman- dibulaeare clearly visiblein the dried skull, and the extent of theseorigins is easilyascertainable. In $ittasomusM. adductormandibulae is more like that of the woodhewers,but is apparentlyless developed than in the "strong- billed" forms. M. depressormandibulae is anothermuscle which is much more stronglydeveloped in the woodhewers.Dendrocincla is again intermediatein this character. The only other jaw muscleof great interestfor the purposesof this paper is M. pseudotemporalisprofundus, which is, again, very stronglydeveloped in the woodhewers.This muscle,which originates on the orbital processof the quadrate,is clearlycorrelated in its size with the relativedegree of expansionof the tip of this process.Since none of the intermediatesexhibits an expandedtip of the orbital processof the quadrate, M. pseudotemporalisprofundus is likewisenot enlarged.In the philydorineswhich have an expandedtip of the orbital processof the quadrate, for example,Automolus, M. pseudotemporalisprofundus is correspondingly large and resemblesthat of the woodhewers.Major jaw ligamentsare well developedin both the ovenbirdsand woodhewersbut, as expectedfrom other characters,are heavier in the woodhewersthan in the ovenbirds.

FUNCTIONAL ASPECTS OF THE SKULL TYPES Severalrecent papers deal with the functionof the avian skull; the reader is referred to the works of Bock (1964) and Zusi (1962, 1967) for the cleareststatements and summariesof the subject. The functionof some of the charactercomplexes is muchthe samein mostbirds. In this paper I am consideringonly thoseaspects of skullfunction that seemto bear directlyon 26 ORNITHOLOGICAL MONOGRAPHS NO. 13

TABLE 1 SUMMARY OF EXTREMES IN SKULL CHARACTERS

Character Dendrocolapfidae Furnariidae bill stronglybuilt, approx. % weakly built, approx.% skull length skull length nasal condition holorhinal pseudo-schizorhinal external naris short, oval long, oval nasal septum periorate periorate orbital septum ossified, does not extend largely periorate, and ex- anterior to nasal-frontal tends slightly anterior to hinge nasal-frontalhinge ectethmoid greatlyconstricted expanded,lateral process mesially, lateral process doesnot meetjugal bar abutsagainst jugal bar supraorbitalarea of broad narrow frontal bones maxillo-palatines short, slightly expanded long, expanded vomer median diastema absent mediandiastema present median shelf of somewhat constricted broad palatine orbital process tip expanded tip not expanded of quadrate postorbital and large, well-developed medium development, zygomatic processes sometimes fused temporal fossa greatly expanded medium development mandibular absent present foramen ovenbirdand woodhewerskulls. Therefore,only those points of the jaw muscleanatomy that seempertinent to the functionalanalysis will be discussed,and no detailedjaw muscledescriptions will be given, as I feel that theywould add little to the over-allstudy. In beginningthis sectionit seemsadvisable to statethe differencesbetween the pseudo-schizorhinaltype of skull describedearlier for Asthenesand the holorhinal skull found in the "strong-billed"dendrocolaptids, typified by Xiphorhynchus (see Table 1 ). If we assumethat the holorhinal skull is a derivativeof the ovenbirdpseudo-schizorhinal skull type, as seemslogical from previousarguments, then it wouldfollow that the characterstates leading to the woodhewerholorhinal condition have been molded by selectionforces operatingon dendrocolaptidevolution. Thesecharacter states should be correlated with the behavioralinformation for the group. This type of correla- tion shall thereforebe attempted,after a summarydescription. As has been statedpreviously, there appearsto be a generaltrend in the 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 27 dendrocolaptidstowards increased ossification in severalcharacter complexes. The anatomicalseries goes from the philydorinesthat showtendencies in this directiontoward the "strong-billed"woodhewers in which it culminates.This increasein ossificationappears to be the first step in the transition from pseudo-schizorhinyto holorhiny in these birds. Those trends which have taken place in the evolutionof the woodhewerskull includeossification of the nasalregion to the point that the dorsalarticulations of the nasal struts form the lateral bordersof the nasal-frontalhinge. Concomitantwith these changesin the ventral displacementof the dorsal articulationsof the nasal struts are a parallel movementof the ectethmoidplate and retractionof the anteriorpart of the nasal septumto a point posteriorto the nasal-frontal hinge. Other changesinclude a generalthickening of the nasalstruts, along with a strengtheningof the bill. In the brain casethere is a broadeningof the supraorbitalarea of the frontal bones,a deepeningof the temporalfossa, and a strengtheningof the postorbitaland zygomaticprocesses. There is also a great increasein the ossificationof the orbital septum, enlargementof the orbitalprocess of the quadrate,expansion of the tip of the orbitalprocess, a general increasein the strengthof the bones that comprisethe palate, and obliterationof the mediandiastema of the vomer. The type of variationsthat exist in the charactersof the palate and in the ectethmoidcomplexes makes difficult decipheringthe trends in these systems. In the lower jaw the mandibularforamen is obliteratedby ossification.Let ns now considerthe functionalconsequences of thesechanges, and their behavioralcorrelations. In order to understandbetter the evolutionof the skull types, one must first considerthe functioningskull. Birdspossess a kineticskull, that is, there is movementwithin the skull and the upper jaw movesrelative to the brain case. As it is beyondthe purposesof thispaper to discussin detail the kinetics of the avian skull, the reader is referred to Bock (1964) for a detailed dis- cussionof the topic. Here I shall only be concernedwith the differencesin function between the woodhewer and ovenbird skulls. Bock (1964) distinguishestwo types of skulls, prokinetic and rhynchokinetic. Bock (1964:4 and 14) stated that, "The prokinetic skull is characterizedby a hinge or region of bendingat the junction of the nasal and frontal bones;hence the upper jaw movesas a unit.... The rhynchokinetic skull is characterizedby a region of bendinglocated somewherealong the dorsalbar of the upperjaw." The prokineticskull is the commonavian skull, and is the characteristicpasserine skull; rhynchokineticskulls are commonly found in the Charadriiformesand in someother groups. One strikingfeature of theseskull typesis that prokineticskulls are generallyassociated with the holorhinal nasal condition, and rhynchokineticskulls with a schizorhinal nasalcondition. In the rhynchokineticskull the orbitalseptum is presentan- terior to the base of the upper jaw, thus making any bending at the area of 28 ORNITHOLOGICAL MONOGRAPHS NO. 13 •______••/dorsal hingeofnasal strut ___•..•'x•/ /region ofbending I • d/ /dorsalbar •• •ventralbar • / qateralbar schizorhinal nostril A

/ regionof--dorsalbending bar

• I 'holorhinal•ventral nostrilbar ' ' ' "• latera I bar

Figure 9. The skulls of A, an ovenbird, and B, a woodhewer, to show the regions of bendingin the skulls (diagrammatic). the old nasal-frontalhinge impossible.Therefore, the area of bendingin the rhynchokineticskull is somewherealong the dorsalbar of the upperjaw between the anterior extent of the orbital septum and the posterior extent of the nasalseptum. As Bock (1964: 14) pointedout, "Rotationof the upper jaw in rhynchokineticskulls occurs when the ventralbars are pushedforward exactlyas in the prokineticskull. But onlythe anteriorsection of the upper jaw movesupward while the base of the dorsalbar remainsstationary." He further statedthat "... the ventral bar, which movesforwards and backwards, mustbe isolatedfrom the stationarybase of the dorsalbar, a problemunique 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 29 to the rhynchokineticskull .... "This separationof the dorsal and ventral barsis accomplishedby the schizorhinalnostril in the Charadriiformes."The lateral bar is thus free to move with the ventral bar, bendingat its junction with the brain case,i.e., at the regionof the old nasal-frontalhinge." (Bock, op. cit.). Zusi (1962: 37) pointedout that in the schizorhinalskull "... the dorsalhinges of the nasal struts,which in holorhinalbirds form the lateral extremesof the fronto-nasalhinge, are displaceddorsocaudally. This means that the nasal strutsare no longer integral parts of the upper jaw, but that they swingabout their own pivots,and tend to changethe shapeof the upper jaw during protraction or retraction." Since the nasal struts are no longer associatedwith the upper jaw proper, they form a new set of hinges,thus making a doubleset of hingesfor the schizorhinaljaw. So, the functional consequencesof this systemare that the upper jaw, insteadof movingabout one hinge and as a singleunit as in the prokineticbirds (woodhewers),has a long area of bendingalong the dorsalbar which effectsbill shapechange during protractionand retractionand bill tip movement.The only anatomical differencesappear to be in the bony hinge system,and as Bock (1964: 15) pointedout, "All other parts of the skull, ligamentsand jaw musclesof the rhynchokineticskull are similar to those in the prokinetic skull. Thus it is reasonableto assumethat the operatingmechanism is the same in the two typesof kinesis." In the case of the typical ovenbirds,the nostril is schizorhinal,but the orbital septumextends only a very short distancebeyond the old nasal-frontal hinge (Fig. 9). The result is that althoughthe type of kinesisfalls within the rhynchokineticrange, since the area of bendingis alongthe dorsalbar of the upper jaw insteadof at an easily definablenasal-frontal hinge, the area of bendingis generallyvery closeto the base of the upper jaw so that for the most part the upper jaw moves as a unit. The main differenceseems to be that somebending does occur, and as a consequencethe tip of the bill does move to somedegree independently of the movementof the entire upper jaw. As Bock (loc. cit.) pointed out, "Some birds have a form of kinesis that cannotbe easilyassigned to either prokinesisor rhynchokinesis.In the gull (Larus), for example,the regionof bendingis of the rhynchokinetictype, but it is soclose to the baseof the skullthat the entireupper jaw movesas a unit." Within the ovenbirdsthere is sucha continuousseries, going from the typical schizorhinaltypes through the philydorinesto the holorhinaltypes, that many cannotbe assignedto a specifictype of kinesis. One can only say that at one extremethere appear to be typical rhynchokineticskulls and at the other ex- treme,prokinetic skulls. To summarizethe foraging behavior of each group one might say that the woodhewersforage by usingthe bill in probing,prying, and somepecking. 30 ORNITHOLOGICAL MONOGRAPHS NO. 13

r•

o 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 31 32 ORNITHOLOGICAL MONOGRAPHS NO. 13

The bill is alsoused in theseforms in graspingrather large or strong-bodied prey. Though the woodhewernatural history literature typically contains accountsof thesebirds hitchingup tree trunks and feedingmost commonly by peeringinto bark crevicesafter insectsand smallvertebrates, woodhewers do probeand pry into bark, flake bark, and evenpound on trunksupon oc- casionsin typicalwoodpecker fashion (see Feduccia,1970). Althoughthere is great diversityamong the ovenbirds,they may be characterizedgenerally as insect-eaters,and most of the food taken is small insects.Among the philydorines,which show a general strengtheningof the skull and a reduction of schizorhiny,the food taken is often heavierand harder-bodiedinsects than in the synallaxinesand furnariines. Small cold-bloodedvertebrates are also taken, and many speciespeck, pry, and probe in their foraging behavior (Table 2). Althoughthe precisefunctions of manyparts of the skullsare still unknown, the charactersin woodhewersseem to conformto functionalanatomical pre- dictions.In the woodhewersit resultsin a generallystronger, more completely ossifiedskull, and in the ovenbirds,a weak, less ossifiedskull. In the woodhewersthe bill is generallystrong, and the dorsalarticulations of the nasalstruts form the lateralborders of the nasal-frontalhinge, thereby strengtheningthe bill and forming a broad hinge. This hinge functionsto protectthe bill from the stronglateral forcesto which it is subjectedin prying, probing,and other suchactivities. In addition,woodhewers are powerful graspers.These functions require a generalstrengthening of the skull, which is shownin the bill, the ossificationof the orbital septurn,the strengthening of the nasal struts,enlargement of the postorbitaland zygomaticprocesses, deepeningof the temporalfossa (hence enlargement of the adductormuscle), generalstrengthening and broadeningof the palatal bones,strengthening of the orbitalprocess of the quadrateand expansionof its tip, strengtheningof the jugalbar, strengtheningof the ectethmoidplate, and its extensionphalange to contact the jugal bar. In general, the woodhewerskull shows great strength. As Bock (1963: 112) has pointed out in Loria (Paradisaeidae) concerningthe expandedtip of the orbital processof the quadrateand the large M. pseudotemporalisprofundus muscle, two charactersthat the woodhewerspossess, "These features are clearlycorrelated with one anotherfunc- tionally;they act to closethe mouthmore forcibly either by depressingthe upperjaw or raisingthe mandible."One functionalaspect of the strongforce for adductionwould be holdingand crushingstrong-bodied insects and small cold-bloodedvertebrates, food commonlytaken by woodhewers.Thus, the strongskulls and powerfuljaw musclesof the woodhewerscleafly seemto be correlatedwith the foragingbehavior and type of food taken. In the ovenbirds the situation is somewhat more difficult because there is 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 33 suchdiversity in skullstructure. In the synallaxinesand mostof the furnariines,the skullsare generallyweaker than woodhewerskulls. The naresare pseudo-schizorhinal,the orbital septurn is unossified,the post-orbitaland zygomaticprocesses are small,and comparedto woodhewersthe temporal fossaeare relatively smaller, the palateis weaker,and the jaw musclesare not somassive and powerful. These skull characters of synallaxinesand most fur- nariinesseem to correlatewith the feedinghabits of theseforms as they are generallysmall-insect eaters. But perhapsthe main questionthat has not beenanswered and the onethat will probablynot receivea completelysatis- factoryanswer at thisstage is why the nasalcondition is pseudo-schizorhinal in the ovenbirds,and not holorhinalas in, for example,the wood warblers and mostpassetines, which feed on muchthe sametype of food and in much the samemanner. True schizorhinyin shorebirdsappears to be correlated with probingrelated to bill tip movement.It is of interesthere that Sclerurus, whichhas well-developedpseudo-schizorhiny, does probe into soft mud on the forestfloor. It mightalso be of interestto note that mostovenbirds lack a hookedbill tip, as is foundin manypasserines. Perhaps this is in someway associatedwith probingmovements. One mightthink that the woodhewers needslow, powerful jaw actionfor the large,hard-bodied prey that theytake, andthis is certainlyachieved by the woodhewerskull. Perhapsfor the ovenbirds,a quickeraction of the tip of the bill is advantageousfor insecteating. This quickertip actionis achievedby pseudo-schizorhinyin which the tip may movesomewhat independently of the movementof the entire upperjaw. Whatever were the exact selectionforces for the evolutionof the pseudo- schizorhinalskull in the ovenbirds,now it is certainlya functionallydiverse skulland is usedin manyways, including the buildingof largestick nests and hole excavation.But, in general,the skull type seemsto be adaptedfor a generalizedinsect-eating mode of life. As hasbeen pointed out previously,the strengtheningof the skull in the philydorinesseems to be correlatedwith the type of foragingbehavior and the food takenby theseforms, as they approachthe woodhewersin these characteristics. We maynow ask the questionwhy doesthe pseudo-schizorhinalskull type occur in the furnariids and not in other generalizedinsect-eating passefine birdswhich appearto have similarfeeding habits? Hofer (1954) presentsa gooddiscussion of the holorhinalskulls as comparedto schizorhinal,and furtherasks the questionas to whichis the more primitive;Jollie (1958) followswith this generaltheme. The holorhinalnostril is consideredthe typicaland primitivecondition in the Passeriformesowing to its widespread occurrence,and as Jollie (op. cit.) pointsout, the schizorhinaland super- holorhinal (with a more roundednasal margin as in many passerineswith 34 ORNITHOLOGICAL MONOGRAPHS NO. 13 short,thick bills) skull types are probablythe most specialized.However, how many differenttypes of holorhinyoccur in passerinesis a questionthat remainsuninvestigated, and one would have to look at the entire jaw ap- paratusto discoverthis. The point is that the type of holorhinyin one group of passerinesmay be moreprimitive than anothertype of holorhinyin another group. The termsholorhinal and schizorhinalare generalterms that refer to a largespectrum of possiblenasal conditions. It is of interesthere that certain birds undergoontogenetic changes in the conditionof the nostril and con- sequentlyin the type of cranial kinesis. Bock (1964: 15) points out that in Rynchops,Balaeniceps, and Rhinoplax, the kinetic hinge shifts from rhynchokineticin the young to prokineticin the adult. This changein the positionof the kinetic hinge correspondsto changesin the nasal condition from schizorhinyin the youngto holorhinyin the adults. It shouldbe ap- parentby now that the holorhinalskull type in the woodhewersrepresents the specialized,derived type in the furnariid-dendrocolaptidassemblage, and has possibly(I think very likely) evolvedunder selectionpressures for stronger bite, grasp,and probingabilities that causeexceptional forces to be exerted on the woodhewerbill. But, a weak holorhinalskull is the type found in most other passerinebirds. Such a skull has similar kinetic abilities to those of woodhewersbut lacksossification of the orbital septumand generalstrength- eningof the woodhewerskull. The pseudo-schizorhinalskull of furnariids, like the holorhinal skull of otherpasserines, is now not confinedonly to generalizedinsect eating, for it servesin its sameanatomical form as a skull capableof buildingthe largestick nestsfound in the ovenbirdsand the earth excavationsthat somespecies make. It evenserves for excavatingnesting holes in treesin Pygarrhichas.This same functionaldiversity is alsofound, but perhapsto a lesserdegree, in the "true" schizorhinalbirds such as the shorebirds,etc., where the same general ana- tomicalskull type is certainlynot confinedto one functionalend.

THE STERNUM The variation in the notchesof the posteriorborder of the sternum is coveredelsewhere (Feduccia, 1972) and will only be summarizedhere. The majorityof both ovenbirdsand woodhewerspossess sterna with two posterior notches.These may show a tendencyto open (more than two notches), or to close (less than two notches). Throughoutthe ovenbirdsthere is a two- notchedsternum, but with a tendencyto open. There is no ovenbirdknown whichshows a tendencytoward closure of the posteriorborder of the sternum. However, in the "strong-billed"woodhewers, although there is a tendency to open the posteriorborder in some,in many there is a strongtendency toward closure. I concluded(op. cit.) that this increasein ossificationof 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 35

Figure 10. The sterna of Cinclodes ]uscus (upper), and Xiphorhynchus guttatus (lower), left lateral aspect. the posteriorborder of the sternum,which also occursin the woodhoopoes, and by a different meansin the woodpeckers,is probably associatedwith increasingthe strengthof the sternum for tree-trunk foraging. It is of great interestat this point to considerthe "intermediates,"for all the generaare totally ovenbird-likewith respectto the posteriorborder of the sternum. In all of the "intermediates"there is a typical two-notched sternum, a tendency to open the posterior border in two, Sittasomusand Dendrocincla,and no tendencytoward closurein any species. Another sternal character that differs between the ovenbirds and woodhewersis the size and shapeof the sternalkeel (Fig. 10). In the ovenbirds the keel is generallylarge, and in profile hasa somewhatrounded appearance in many species.In the woodbowersthe keel is relatively smaller, and does not appearrounded in profile, but tapersin a straightline posteriorly.This charactermight be correlatedwith the positionof woodhewerson tree trunks, but is probablyalso associatedwith the amountand type of flight performed by the woodbowers. There is much variation within the ovenbirds in the size and shapeof the keel. As one might expect,the sternalkeel in the woodhewersis relativelymore constant. The "intermediates"conform to the wood- hewerpattern of sternalkeel. 36 ORNITHOLOGICAL MONOGRAPHS NO. 13

EVOLUTION OF THE SCANSORIAL FOOT The type of foot found within the furnariidsand dendrocolaptidsis the typical anisodactylfoot found in all other passerinebirds. This type of foot structureis characterizedby having the hallux (generally long) posteriorto the tarsometatarsus,and the second,third, and fourth toes pointing anteriorly. Within the Passeriformesthe anisodactylfoot, with minor modifications, seemsto be well suitedto perching,climbing or walking. For present purposes,I shallbe concernedonly with modificationsthat have occurredin the transitionto the creepingor scansorialtype of foot foundin the Dendro- colaptidae.The foot type within the ovenbirdsis, with a small amountof variation,the same. As many of theseobservations have alreadybeen covered by Richardson(1942) and Bock and Miller (1959), only the main points will be treated in this section. If we assumethat the dendrocolaptidsarose from the philydorinefurnariids,then at least some differencesbetween the two groupsshould in- dicatethe climbingadaptations of the anisodactyltype of foot and the selection forcesoperative in this case. Richardson(! 942), in his paperon tree-trunkforaging in birds,compared Certhia, $itta, Thryomanes,Dryobates, and Dendrocolaptes.He felt that featuresin commonbetween the differenttree-trunk foragers would be hints to the actual adaptationsfor tree-trunk foraging. In regard to many characters,the comparisonof Thryomaneswith Dendrocolaptesis much like a comparisonof ovenbirdswith woodhewerssince in Thryomanesfewer actual climbingadaptations are found than in the other creepingforms. In general, charactersof the pelvic region in most ovenbirdsare closerto Thryomanes than to the dendrocolaptids,owing to the perchingtypes of feet foundin both. It wouldbe redundantto coverall the pointsmade by Richardson(1942), so I havechosen the pointsthat I considerto be of greaterimportance here, and alsopoints that were not coveredby Richardson.For the generalmyological features,the reader is referredto Richardson(1942), as most of the gross comparisonsare covered. Here I stressthe osteologicaldifferences between the ovenbirdsand the woodhewers,with specialreference to the climbing adaptationsin the woodhewers,and the positionof the "intermediates"with respectto thesecharacters. Many of the pointscovered by Bock and Miller (1959) are only briefly treatedhere. The readeris referredto their excellentpaper on the evolution of perchingand climbing feet in birds.

LIMB PROPORTIONS One of the most significantchanges in the evolutionof climbingbirds occursin the proportionsof the pelviclimb elements.Here I have considered 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 37 the relativelengths (in millimeters)of the femur, tibiotarsus,tarsometatarsus, and the total leg, and have comparedthe ovenbirdsto the woodhewersby usingratios of thesebone lengths to the lengthof the sternum(greatest length from the metasternumto the posteriorborder of the sternum). The ratio of each limb element to the sternum was calculated,and the mean of the ratios from eachspecies was usedas part of the samplefrom eachfamily. The sternumwas the only bodymeasurement that waspossible for mostskeletons, as many specimenswere disarticulated.Engels (1940') has discussedthe use of suchratios. First, only elementswhich presumablyvary somewhatin- dependentlyof eachother should be usedfor the ratios. Second,measure- mentsthat do not tend to vary adaptivelyfrom one speciesto anothershould be usedrather than ones that vary,for example,according to the sizeof the organism.Although I cannot"prove" all of thesequalifications in the useof sternallength, the obviouspredictions emerge using ratios of the variouslimb elementsto sternallength. Measurementswere taken from the following speciesof woodhewers and ovenbirds: Dendrocinclaanabatina (3), D. fuliginosa(3), Decony- chura longicauda(3), $ittasomusgriseicapillus (9), Glyphorhynchusspir- urus (7), Dendrexetastesrufigula (1), Dendrocolaptescerthia (1), D. picumnus( 1), Xiphorhynchuspicus (3), X. obsoletus(2), X. pardalotus(2), X. guttatus(6), X. flavigaster(4), X. lachrymosus(1), X. triangularis(7), Lepidocolaptesleucogaster (4), L. souleyetii(4), L. angustirostris(4), L. affinis (3), L. albolineatus(3), Campyloramphuspusillus (1), Geosittapay- tensis(1), G. cunicularia(2), Upucerthiadumetaria (3), U. validirostris(1), Ochetorhynchuscerthioides (2), Cinclodesantarcticus (2), C. fuscus(4), C. atacamensis(1), C. taczanowskii(1), Furnariusrufus (8), Aphrastura spinicauda(2), Phleocryptesmelanops (5), Leptasthenuraandicola (1), L. aegithaloides(1), L. platensis(1), Spartanoicamaluroides (2), $choeni- phylax phryganophila(10), Synallaxisfrontalis (6), S. albescens(4), S. brachyura(5), Cranioleucasulphurilera (1), C. erythrops(1), Asthenes modesta(2), A. baeri (2), A. hudsoni(2), Phacellodomusstriaticollis (4), Coryphasteraalaudina (5), Anumbius annumbi (3), Premnoplexbrun- nescens(3), Hyloctistessubulatus (2), A nabacerthiastriaticollis (3), Phily- dor lichtensteini(6), Automolusochrolaemus (4), Heliobletuscontaminatus (1), Thripadectesrufubrunneus (1), Xenopsminutus (3), Pygarrhichasal- bogularis(1). In Figure11 the ratiosof the limb elementsto the sternallength are given. It seemsapparent from the figuresthat the main modificationsin the evolution of the dendrocolaptidpelvic limb elementsare the reductionin the length of the tibiotarsusand the tarsometatarsus.The femur data are less obvious.Total leg length seems to be clearlyreduced in the dendrocolaptids. 38 ORNITHOLOGICAL MONOGRAPHS NO. 13

2.00'

1.80'

1.10' 1.60'

.90' 1.40- 0

x• .70' 1.20' 8

ex D .5O 1.00 FEMUR TIBIOTARSUS

4.00-

1.50- 3.50-

1.25- 3.00,

1.00' 2.50.

.75 2.00 TARSOMETATARSUS TOTAL LEG LENGTH 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 39

2.00.

1.50-

1.00-

.50- i A B C I Figure 12. Ratios of the different leg elements to sternal length in the dendrocolaptids (left), and in the furnariids (right). The elements are A, femur; B, tibiotarsus; and C, tarsometatarsus.

Bar graphsof the meansof the ratios of the limb elementsfor both families are givenin Figure 12. The intermediatesare not includedin thesedata. Richardson(1942) found much the samething from his comparisonsthat I have presentedhere. His data indicated that, "Dryobates and Dendro- colapteshave relativelyvery shortlegs when comparedto either Thryomanes or Corvus." Richardson'sstatement that probablythe most significantfactor in the shorteningof the leg in trunk-foragingis the shorteningof the tibiotarsus seemsto holdtrue from my data(Fig. 12). He pointedout, also referring to thework of Stolpe(1932), that, "The weightof the bodyof the climbingbird continuallyacts through the leg to pull the bird outwardand downward,and to extendthe jointsof the leg.... The leverageof thisforce of gravityacting

Figure 11. Comparison between ratios of lengths of femur, tibiotarsus, tarsometatarsus,and total leg to sternal length in the dendrocolaptids(D), and the furnariids (F). The "intermediates"are designatedas follows: Glyphorhynchusspirurus, an X; Sittasornusgriseicapillus, open diamond; Deconychura longicauda, closed diamond; Dendrocincla anabatina, open circle; and Dendrocincla fuliginosa, closed circle. The observedrange and mean ___1 standarddeviation (enclosedarea) and + 2 standard errors of the mean (black area) are shown for each group. 40 ORNITHOLOGICAL MONOGRAPHS NO. 13

TROCH. DIG. MET.

Figure 13. Camera lucida drawingsof the posteriorsurface of the distal ends of tarsometatarsi of A, PhaceIIodomus striaticolIis; B, SyndactyIa rufosuperciliata; C, PhiIydor lichtensteini;D, Synallaxis aIbescens;E, Dendrexetastesru[igula; F, Dendro- colaptes certhia; G, Xiphorhynchus guttatus; H, LepidocoIaptessouIeyetii; I, Pseudo- colaptes lawrencii; J, Margarornis rubiginosus;K, Pygarrhichas aIboguIaris; L, Xenops 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 41 to extendthe intertarsaljoint is decreasedwith the shorteningof the tibiotarsus." This does seem to be one factor involved in the shorteningof the legs,but, as Richardsonalso pointed out, this shorteningalso brings the feet anteriorlyto a betterposition for climbing. For each limb elementthe positionof the "intermediates"with respectto the rangeof the two familiesis shownbetween the two family rangediagrams. Althoughthese forms generallyconform to the dendrocolaptidrange as one might expectfrom climbinghabits, they are often at the end of the range of the dendrocolaptids,nearing the furnariidrange, and in only a few casesex- tend towardsthe extremerange of the dendrocolaptids.However, the "intermediates"clearly possess woodhewer "climbing" adaptations with respectto the relativelength of the leg elements.Sittasomus, however, is closerto the ovenbirds in a number of these limb characters.

DISTAL END OF THE TARSOMETATARSUS The distal end of the tarsometatarsusshows striking differencesbetween the woodhewersand ovenbirdsand thereforedeserves special attention. Fig- ure 13 showsthe distalends of the tarsometatarsiin a variety of ovenbirds and woodhewers.Several main pointsare immediatelyapparent. First, the size of the metatarsalI variesgreatly between the two groups. This metatarsal, the only one to remain unfusedin passerinebirds, functionsas an articularsurface for the baseof the halluxand alsoas a pulleyfor the tendon of M. flexor hallucislongus (see Richardson,1942, for a more completedis- cussionof this character). The sizeof metatarsalI is directlycorrelated with the lengthof the hallux. In the woodhewers,metatarsal I is short,correspond- ing to a shorthallux, a characterthat is associatedwith climbing.In the ovenbirds the metatarsalis long, indicatinga long hallux, a commonfeature of perchingbirds. Of specialinterest here are the "intermediates,"which are in the woodhewerrange with respectto this characterbut are somewhatintermediate,especially Dendrocincla and Sittasomus.Of the climbingtypes of furnariids,Pygarrhichas and Xenops showsome reduction of metatarsalI, and the conditionin Margarornisapproaches that of the woodhewers. The degreeof separationof the articularcondyles is an expressionof the amountof basalspread of the toes. In climbingbirds, where selectionforces are operativefor a strongset of opposabletoes, spread of the condylescould help facilitatethis end. In the woodhewersthis is the case,and thereis relatively greaterseparation of the trochleafor the digitsthan in the ovenbirds.

rninutus; M, Dendrocincla anabatina; N, Glyphorhynchus spirurus; O, Deconychura longicauda;and P, Sittasornusgriseicapillus. A through D are typical ovenbirds,E-H, "strong-billed" woodhewers, I-L, aberrant ovenbirds, and M-P, the "intermediates." 42 ORNITHOLOGICAL MONOGRAPHS NO. 13

^ B Figure 14. Posteriorsurface aspects of the proximal ends of the left femora of A, Furnarius rufus, and B, Xiphorhynchusguttatus.

The "intermediates"are somewhatintermediate in thischaracter, although I foundno quantitativemeans of showingthe difference. The third character of the distal end of the tarsometatarsus that is of interestis thetrochlea for digitIII. In thewoodhewers this trochlea is deeply excavated;in the ovenbirds,much less so. Althoughthis characterstate is not clearlyunderstood, it wouldseem to serveto help hold the third toe in firm position,even when the toes are fully extended.Whatever the exact functionof thischaracter, it seemsan obviousclimbing adaptation since the same type of excavationof the trochleafor digit III is also found well developedin Certhiaand Sitta (see Richardson, 1942: 339), andas Figure 13 shows,Pseudocolaptes, Margarornis, Pygarrhichas, and Xenops, all climbing typesamong the ovenbirds,show varying degrees of excavationof the trochlea. Excavationis greatestin Pygarrhichas.The "intermediates"are of greatinterest with respectto this characteras Dendrocinclaand Glypho- rhynchusare particularlyintermediate between the woodhewersand typical ovenbirds.

FEMUR AND TIBIOTARSUS Althoughthere are very few charactersthat differ qualitativelybetween thewoodhewers and ovenbirds in the pelvicregion and the limb elementsin- 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 43 volvedin that system,there are a few noteworthyexceptions. One is the presenceof a foramen or severalforamina in the proximal end of the femur (Fig. 14), presentand well defined in all of the woodhewersand in the "intermediates"except in Glyphorhynchus(nearly absent in Dendrocincla). A foramenis absentin most of the ovenbirds,except in the philydofineswhere it is presentin about half of the forms examined. However, in the phily- dorinesit is reducedwhere present and is usuallyrepresented by severalsmall foramina. It is alsopresent in a few other speciesof ovenbirds.Whether or not this representsa trend towardsincreased pneumatization and hence reductionof weightin the pelvicregion is unknown. The most strikingqualitative difference in the limbs lies in the characters of the tibiotarsus. Whereas the proximal end of the ovenbird tibiotarsusis typicalof passerinebirds in general,the proximalend of the woodhewertibio- tarsusdiffers greatly from the passefinepattern and is almost identical to that of the woodpeckers.This remarkableexample of convergencelies mainly in the expansionof the anteriorregion of the proximalend of the tibiotarsus to increasethe areasof origin of the flexor of the tarsometatarsus,M. tibialis anterior (see Richardson, 1942), and the extensorof the three anterior toes, M. extensordigitorum longus. Figure 15 showsthe great similarityof the tibiotarsusof woodpeckersand woodhewers,as compared to the different "passerine"and ovenbirdpattern. Some philydorinesappear to approach the woodhewercondition of the proximalend of the tibiotarsus,but only in Xenops is this clearly the case. The "intermediates"show the woodhewer conditionwith respectto this character,but Dendrocinclais somewhatintermediate.

THE DIGITS The next foot characterto deserveattention is the relative length of the variousdigits. This charactercomplex is of particularinterest since it was originallyone of the main charactersby whichthe familyDendrocolaptidae was separatedfrom the Furnariidae. The woodhewersare separablefrom the ovenbirdsby havingthe third and fourth toes approximatelyequal in length, and this length is greaterthan that of the digit II. The hallux is shorter than the inner toe, and the three anterior toes are united for the entire lengthof theirbasal phalanges. The middletoe is fusedto the outerby almost the full extentof the secondphalanx. In the ovenbirds,the toesare more like the typicalpasserine condition. Digits II and IV are aboutequal in length, and digit III is longer. The hallux without the claw is not shorter than the inner toe (No. II) without the claw. The basal phalangesof digits III and IV are fusedtogether for most of their length. Thesetwo basicpatterns are illustratedin Figure 16. 44 ORNITHOLOGICAL MONOGRAPHS NO. 13

A B C Figure 15. Anterior surface of proximal ends of tibiotarsi of A, a woodpecker. Dendrocopus villosus, B, Xiphorhynchus guttatus, and C, Furnarius ru/us.

Althoughthe two basicpatterns are generallyreliable to separatethe two groupsas presentlydefined, there is much variation,especially among the variousovenbirds which engage in sometypes of climbingbehavior. As Richardson(1942: 323) pointedout, the basalsegments of the digits of Certhia,Sitta, and Thryomanesare hardlyseparable from eachother, being fused. This is also true of some of the climbing and clingingforms within the ovenbird assemblage.In Margarornis, Premnornis,Premnoplex and in someof the speciesof Cranioleucathere is a tendencytoward this condition. The three basal phalangesare fused exteriorlyfor their entire length. In thesespecies there is a slightamount of fusionbetween the secondphalanges of digitsIII and IV. Many of the philydorinesshow the sametendency toward fusionof the basalphalanges, and Pygarrhichasand Xenopsshow essentially the woodhewercondition with respectto the fusion of the basal phalanges leadingfrom the typical ovenbirds(the typical passerinecondition) through the climbingovenbirds and the philydorinesand Pygarrhichasto the typical woodhewers.That this is a trend towardsan efficientclimbing type of foot seemsto gain credencefrom the occurrenceof the same conditionin other climbingpasserines such as Certhia and Sitta. 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 45

THE TAIL Sfiffeningof the tail feathersis a characteristicfeature of trunk-climbing birds,and the woodhewersshow a high degreeof modificationof the tail with respectto this character.Woodhewers generally have long, stiff tails, the distaltips of whichcome into contactwith the tree in climbingby the long, often bare, inward-curvingshafts. No attemptwas made here to correlatewith trunk-climbing the lengthof the tail andthe strengthof the shafts. The main point of interestfor the purposeof this paperis that mostof the trunk-climbingovenbirds show this tail adaptationand actuallypossess the stiff, woodhewer-likerectrices. The forms include Margarornis, Premnornis, Premnoplex,Pygarrhichas, some speciesof Cranioleuca,and others to a lesserdegree. It is of interesthere that manyof the non-climbingovenbirds possesssome degree of stiffeningof the tail feathersand may havethe barb- lessrami protrudingdistally. Even the long-tailed,titmouse-like species of the genusœeptasthenura apparently use their stiff rectricesfor supportand balancein their foragingbehavior. The possessionof thesetypes of tails, particularlyby the philydorines,would certainlybe a good preadaptation for tree-trunkforaging. The tail of Dendrocinclashows a lesseramount of stiffeningof the rectricesthan doesthat of the other woodhewers. As an indexof the degreeof generaltail-muscle development, the pygostyles of woodhewersand ovenbirds(same species as for the limb data) were compared. The measurementtaken was the height of the pygostylefrom the dorsalextreme of its crestto the ventral marginof the disc. These measure- mentsare expressedas ratios to the sternallength (Fig. 17). As expected, the woodhewersshow a much greaterdevelopment of the pygostylethan do the ovenbirds. The "intermediates"are plotted betweenthe range diagrams. Note the positionof Dendrocincla(closed circle). The pointsthat compose the upperpart of the furnariidrange are the tree-trunkforagers.

SYRINGEAL ANATOMY In hisexcellent study of the passeriformsyrinx, Ames (1971: 146) stated of the Furnarioideathat, "This superfamilyof the suborderhas the most clear-cutphylogeny, from the syringealpoint of view, of any passerincgroup, but their syrinx[sic] suggestsnothing about their relationto other groups. The Membranaetracheales were probably nearly or whollyevolved before the groupdiversified into the wide varietyof formspresent today. The Mem- branae are the mostuniform featureof the furnarioidsyrinx, exceptfor the absenceof the pessulus.Apparently the pessuluswas lost earlyin the evolution of thisgroup, for no traceof it hasbeen found in any modernfurnarioid. The diversificationof syringealtypes led to two major stocks.The ovenbird- woodhewerline (Furnariidaeand Dendrocolaptidae)evolved a dorsoventrally 46 ORNITHOLOGICAL MONOGRAPHS NO. 13 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 47 symmetricalsyrinx with two pairsof muscles.The woodhewersevolved more elaborateProcessi with projectinghorns for the attachmentof muscles.It is not dear whetherthe presenceof hornson the Processiin Geosittarepre- sentsan independentappearance from thosein the woodhewers." He furtherstates in his systematicconclusions (p. 146) that, "The syrinx of the woodhewersis distinguishedfrom thoseof othermembers of thissub- order in possessingprominent dorsal and ventral horns on the Processi vocales.Only thisfamily and the Furnariidaepossess two pairsof intrinsic syringealmuscles. The presenceof hornson the Processiof Geosittacould be taken to indicatethat Geosittais more dosely allied to the woodhewers than to the ovenbirds(Furnariidae) but it appearsto be a fairly typicaloven- bird in otherrespects. It is possiblethat the needfor greatermechanical ad- vantagefor the syringealmuscles has causedthe evolutionof hornsin the syrinxof Geositta,independently of the Dendrocolaptidae,but in this case one wouldexpect to find hornson the Processiof other ovenbirds,which musthave been subjected to similarselective pressures." Ames states of the Furnariidaethat, "The dose relationshipof this groupto the woodhewersis indicatedby the similarityof syringealmusculature, which setsthe two families apart from the antbirds (Formicariidae) and tapaculos (Rhinocryp- tidae) ." So, althoughthe differencesin syringealanatomy between the Furnariidae and Dendrocolaptidaeare not great,the two groupsare separable,and Geo- sitta possessesthe dendrocolaptidtype of syrinx. Why Geosittashould possessthe woodhewertype of syrinxis difficultto understand.It stronglysug- geststhat the syrinxmay, at times,be a homoplasticcharacter. Geosittais cl,early not a dose ally of the woodhewers,and on the basisof anatomyand plumagecharacters occupies an unequivocalposition in the subfamilyFur- nariinaeof the Furnariidae. The origin of the woodhewertype of syrinx is further difficult to understandfrom a functionalstandpoint. Although we know little of syringealfunction, it would seemreasonable to assumethat selectionwould operatein the samedirections for the samefunctional ends. In the case of Geositta, however, it is difficult to understandwhat similar functionwould be demandedof this lark-like opencountry bird, that would be similarto the deep-forestinhabiting woodhewers. The originof the woodhewer-likesyrinx in Geosittadoes suggest, however, that the originof that type of syrinxmay be a fairlysimple change. Whether the woodhewer-typesyrinx aroseseveral times in the evolutionof the dendrocolaptids,or if all of the dendrocolaptidsarose from the philydorineswith the woodhewer-typeof syrinxis impossibleto determine.One mightexpect that similarsel•tion forcesmight operate on the syringesof trunk-foragingbirds, but the problem must await further investigation. 48 ORNITHOLOGICAL MONOGRAPHS NO. 13

The woodhewertype of syrinx was discoveredby Ames in the following genera: Dendrocincla, Sittasomus, Glyphorhynchus,Drymornis, Xiphoco- laptes, Dendrocolaptes,Xiphorhynchus, Lepidocolaptes,Campylorhamphus, and Geositta,and the furnariidtype was found in Furnarius,Cinclodes, Upu- certhia,Limnornis, A phrastura,Phleocryptes, Synallaxis, Certhiaxis, Asthenes, Phacellodomus,Anumbius, Pseudocolaptes,Pseudoseisura, Anabazenops, Philydor, Automolus, Heliobletus, Xenops, Megazenops, Pygarrhichas,and Sclerurus.

ELECTROPHORESIS OF HEMOGLOBIN METHODS AND MATERIALS Becauseof the difficulty of obtaininglive material, the birds were shot, and blood was extractedimmediately either from the brachialregion or from a slit in the throat. Most of the birdswere still alive after beingshot, but when the specimensdied immediately,heart extractionwas often necessaryto ob- tain sufficientblood. The blood was extractedinto a culturetube containing a tablet of potassiumoxalate (Cambridge Chemical Products, Inc.) dis- solvedin 2.0 ml of physiologicalsaline solution. The solutionwas then placed immediatelyon ice. Red blood cellswere precipitatedby centrifugationand hemoglobinwas preparedby washingthe red cells three times with saline and lysingthe cellswith distilledwater. The final solutionwas approximately 5 percenthemoglobin. Disc electrophoresiswith acrylamidegel modifiedfrom the techniquede- scribedby Ornstein(1964) and Davis (1964) was employed. This tech- niquehas beenused previously for avian serumproteins by Desboroughand Irwin (1966). In this techniqueone utilizes a 2.5-inch glasstube that is layeredwith three acrylamidegels, each of which is polymerizedwithin the tube. The loweror "running"gel, which is a 7.5 percentacrylamide solution, is pouredto a heightof 2 inches.The next gel is a ¾4-inchlayer of a 3 per- cent acrylamidesolution known as the "spacer"gel. Having a larger pore sizethan the "running"gel, the "spacer"serves to stack the variousprotein componentsin decreasingorder of mobility before reachingthe "running" gel. The upper gel, which has the same gel compositionas the "spacer"but is 50 percentmore concentrated,is mixed with the sample. The tubescon- tainingthe gelsare placedin the electrophoresisapparatus so as to bridge the gap betweentwo buffer solutionsof the same composition.The buffer usedhere was a Tris-glycinesolution at pH 8.5. Brom-phenolblue was added to the buffer as a standardmarker. Ten gel tubeswere electrophoresedsimul- taneously,with eachtube conducting5 ma. The apparatuswas kept in a coldroom at a constant50 ø F duringthe run time, whichwas approximately 30 minutes. The currentwas terminatedwhen the Brom-phenolblue front 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 49 had migrated32 mm. Then the gel columnswere removedfrom the glass tubesand stainedfor proteinby 0.2% Amido Black in a 5:5:1 solutionof water,methanol, and aceticacid. The gelswere destained in 8% aceticacid and storedin a solutionof the samecomposition. To assurethat the result- ing electrophoreticbands representedonly hemoglobin,a dianisidinestain specificfor hemoglobinwas used occasionallyas a check. As a control for gel consistency,human serum was electrophoresed with eachrun. When the humanserum runs were not consistentwith previoussamples, additional runs weremade until consistencywas achieved. Becauseprecise quantification of the hemoglobinsamples that were elec- trophoresedwas extremelydifficult, severalruns of different concentrations were made for each sampleto insurethat concentrationdid not affect the qualitativenature of the bands. The concentrationin no way affectedthe nature of the bands,except their widths.

RESULTS AND DISCUSSION In the systemutilized here two anodallymigrating hemoglobin bands were resolved. To check for cathodal bands, the tubes were reversed; no bands were noted. The hemoglobinpattern (Fig. 18) from the following species of woodhewerswere nearly identical: Xiphorhynchus triangularis, X. lachrymosus, X. guttatus, Campylorhamphus pusillus, Lepidocolaptes souleyetii,and Dendrocolaptescerthia. The "dendrocolaptid"pattern is characterizedby one very stronglystaining band that migratesapproximately 4-5 mm from the origin, and a very lightly staining,faster migratingband that migrates approximately12-13 mm from the origin. The hemoglobinpatterns from the following speciesof ovenbirdswere nearly identical: Synal- laxis albescens, Margarornis rubiginosus, Cranioleuca erythrops, Auto- molusochrolaemus, Thripadectes ruIobrunneus, Hyloctistes subulatus, Xenops minutus,and Pseudocolapteslawrencii. The "furnariid" pattern is charac- terized by two anodallymigrating bands of more equal quantity than those of the dendrocolaptids.There is a strongerstaining band that remainsat the origin and a lighter stainingband that migratesapproximately 10-11 mm from the origin. The patternswere so easilyseparable that I coulddistinguish within 15 minutesafter the beginningof the run whether or not the tube in questioncontained furnariid or dendrocolaptidhemoglobin by observingthe conspicuousred bands migrating within the gels. I am therefore confident, althoughin mostcases the samplesize is small,that the differencespresented here are real, and are not due to any error in techniqueor procedure. With patternsestablished for each group, it was of great interest to in- vestigatethe hemoglobinpatterns from the "intermediate"genera of dendrocolaptids,Dendrocincla, Sittasomus, Deconychura, and Glyphorhynchus.Two 50 ORNITHOLOGICAL MONOGRAPHS NO. 13

.5 x

D .4

PYGOSTYLE Figure 17. Comparison between ratios of height of pygostyle to stemal length in dendrocolaptids (D), and furnariids (F). The "intermediates" are designated as in Fig. 14, and the statisticsare of the same type. 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 51 sampleswere obtainedfrom Glyphorhynchusspirurus; the hemoglobinpattern is indistinguishablefrom that of the other dendrocolaptids.One sample from each of Sittasomusand Deconychura was obtained. These two forms have hemoglobinpatterns very much similarto each other and more like the dendrocolaptidthan the furnariid pattern, but slightly different from the former. These two generashow one very stronglystaining band approximately in the same positionas the equivalentdendrocolaptid band, but the fastermigrating band is strongerthan its dendrocolaptidequivalent, and mi- grates15 mm in both Sittasomusand Deconychura. Blood sampleswere obtained from three specimensof Dendrocinclaanabatina, but unfortunately from no other speciesof the genusDendrocincla. The hemoglobinelectro- phoreticpattern is indistinguishablefrom that of the furnariids.Owing to the consistencyof the hemoglobinelectrophoretic patterns within other genera of birdsI shalltentatively assume that D. anabatinais typical of the genus. Hemoglobinfrom four specimensrepresenting four generaof Tyrannidae and two of Cotingidaewas examined;both groupswere characterizedby two strongbands each migratingfrom the origin. In addition, three genera of Formicariidaeproved different also, being characterizedby only one band. Thus, althoughthese comparisons are meager,they do illustratethe difference of the woodhewerand ovenbird electrophoreticprofiles from those of other closely allied suboscines;however, these data should serve only to promptfurther study.

CLUSTER ANALYSIS The purposeof this exerciseis to attemptto categorizethe charactersthat I have discussedthroughout this paper in somemore orderlyfashion, and to clusterthe ovenbirdand woodhewer groups in a more objectivefashion, without overemphasizingcertain charactersto which I am biased. Since the publicationof "Principlesof numericaltaxonomy" (Sokal and Sneath, 1963), much progresshas been made in methodologyand very re- fined computerclustering programs now exist. The gleaningof evolutionary informationfrom suchclusters is anothermore complexproblem. I have utilized a clusteringprogram now known as the "Prim Network" (see Prim, 1957; Edwards and Cavalli-Sforza,1964; Kluge, 1969; and Zug, 1971, for more detailedinformation) which expressesphenetic difference (which is, "... linear sumof unit characterdifferences." Farris, 1967) betweenany two species(OTUs: Operational Taxonomic Units) as a numerical value from which one may constructthe type of diagrampresented in Figure 19. The lines betweenOTUs in Figure 19 are the linear sumsof characterdifferences between the two OTUs. 52 ORNITHOLOGICAL MONOGRAPHS NO. 13 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 53

CHARACTER CODING The processof codingcharacters presents many problems,especially in dealingwith the transitionof qualitative,non-morphometric data to a coded dataset. An evengreater problem in passerinebirds is thelimitation presented by thelack of charactersfrom thebirds themselves. In the dataset (Table 3) I find that I haveweighted certain features by the mere numberof coded charactersused from given complexes,but I have attemptedto choosea "reasonable"number of charactersfrom each complex. There are seven charactersassociated with the hind limb (nos. 1-7), six with hemoglobin (nos. 10-15), six with cranialmorphology (nos. 20-25), two with tail structure (nos.8 and 18), twowith wingpattern (nos. 17 and 18), onewith syrinx (no. 9), onewith sternum(no. 19), onewith nest (no. 26), and one with the habitat (no. 27). Therefore, the characterswith the most weight in the analysisare the hindlimb, cranialmorphology, and hemoglobin,with the tail, wingpattern, syrinx, sternum, nest, and habitatplaying a significantalthough minor role. One mightcriticize the use of hemoglobinas six separatecharacters. However, the only effect of deemphasizinghemoglobin is to reduce the distancebetween OTUs at pointswhere hemoglobin differs; that is, there is no changein the diagramfrom Dendrocincla to the far left or from Xipho- rhynchustriangularis to the far fight (see resnitssection). The types of charactersthat I have coded are not the types that vary greatlybetween dosely related genera. The purposeof this analysisis to dus- ter the major naturalgroups within the ovenbirdsand woodhewers,and for this purposethe codingof minor derivedcharacter states that characterize some generabut pfimarily speciesseems superfluous. One should immediately note from the data set that the only charactersthat separatea number of dosely related forms are thoseinvolving morphometric data.

CHARACTERCODING (TABLE 4) 1-4. Ratios of limb elementsand pygostyle(Figs. 11 and 17). The mean lengthsof the tarsometatarsus(character no. 1), tibiotarsus(no. 2), femur (no. 3), and pygostyle(no. 4), are expressedas ratios to sternallength. These are the only morphometriccharacters used. 5. Fossain proximal end of femur (Fig. 14). The fossais generallyabsent (0) in the ovenbirdsand present(2) in the woodhewers.The intermediate condition (1) is the state of having a medium-sizedfossa, or a number of very smallforamina. 6. Proximalend of tibiotarsus(Fig. 15). The typical passefineconformation for the proximal end of the tibiotarsus(0) is presentin most of the ovenbirds. Great expansionof the proximal end of the tibiotarsusfor the origin 54 ORNITHOLOGICAL MONOGRAPHS NO. 13

o o

[.i.1

o 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 55 56 ORNITHOLOGICAL MONOGRAPHS NO. 13 of the extensormuscle of the toes (2) is found in most woodhewers. A number of intermediates( 1 ) are present. 7. Distal end of tarsometatarsus(Fig. 13). The typical passerinecondition (0) with a large metatarsalI, only slightexcavation of the trochleafor digit III, and a not greatlyexpanded base of the distalend is foundin mostof the ovenbirds. The woodhewer tarsometatarsus(2) exhibits a small metatarsal I (an indicationof a small hallux), great excavationof the trochleafor digit III, and expansionof the base of the distal end. A number of intermediate characterstates are known (1). 8. General foot structure (Fig. 16). The typical anisodactylfoot (0) is found in most ovenbirds. There are intermediates (1) which lead to the woodhewercondition (2) in which the third and fourth toes are of equal length, a reducedhallux is present,and there is externalfusion of the basal phalanges,and strongly curved anterior claws. 9. Syrinx. There are two characterstates of the syringesof ovenbirdsand woodhewers.The woodhewercondition (1) with elaborateProcessi having projectinghorns for the attachmentof musclesis derivedfrom the ovenbird condition (0) in which horns are lacking on the Processi. Although Ames (1971) did not examinecertain genera included here, I am assuming tentatively that Coryphistera,Cranioleuca, Margarornis, Hyloctistes,Syn- dactyla, Anabacerthia,and Thripadectesamong the furnariids possessthe syrinx without horns on the Processi,and that Deconychuraand Dendre- xetastesamong the unexamineddendrocolaptids possess the syrinxwith horns on the Processi. 10-15. Hemoglobinelectrophoretic pattern (Fig. 18). Each OTU is coded for the absence(0) or presence(1) of each of the six differenthemoglobin bands that occur in the ovenbirds and woodhewers. Those ovenbirds and woodhewersfor which no hemoglobindata are availableare assumedto pos- sessthat of their respectivegroup. 16. Wing stripe (Fig. 3). A rufouswing stripe (1) is presentin many furnariids and in the "intermediates,"but absent (0) in the "strong-billed" dendrocolaptids.The diffusewing stripein Dendrocinclaanabatina is coded as 1. 17. Solid reddishwing (Fig. 2). The "strong-billed"woodhewers possess a solidreddish wing (1). All otherforms are coded0. 18. Tail (see skin photographs,Fig. 1). The degreeof stiffeningof the tail is coded from the lack of stiffness (0) to the most advancedcondition of stiffeningfound in the woodhewers(3). 19. Sternalnotches (see Feduccia, 1972). The posteriorborder of the sternum 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 57

TABLE 4 COMPARISONOF THE CLASSIFICATIONSOF SCLATER(1890), AND HELLMAYR (1925)

SCLATER HELLMAYR

Family Dendrocolaptidae Family Furnariidae SubfamilyFurnariinae SubfamilyFurnariinae Subfamily Synallaxinae SubfamilySynallaxinae SubfamilyPhilydorinae SubfamilyMargarornithinae SubfamilySclerurinae SubfamilyPhilydorinae SubfamilyDendrocolaptinae x Subfamily Sclerurinae Family Dendrocolaptidae2 Sclater included Margarornis, Premnornis,Premnoplex, and Pygarrhichaswithin the Dendrocolaptinae. Excluding those genera, Sclater's order for the subfamily was: Sit- tasomus,Glyphorhynchus, "strong-billed" woodhewers, Dendrocincla (which included Deconychura), and the "strong-billed"dendrocolaptids. The order in Hellmayr's Dendrocolaptidaeis: "strong-billed"woodhewers, Glypho- rhynchus,$ittasomus, Deconychura, and Dendrocincla. of mostovenbirds is generallytype 3. Many speciespossess type 3 sternabut showa tendencyto openfurther (0), somepossess only type 3 sterna(1), and somepossess type 3 sternabut with sometendency to closefurther (2). 20. Nasal condition(Figs. 4-8). The pseudo-schizorhinalcondition is found in a largenumber of ovenbirds(0). An intermediatecondition (1) leadsto the solidholorhinal skull (2) found in most of the woodhewers. 21. Orbital processof the quadrate(Figs. 4-8). The tip of the orbital process of the quadrategoes from the conditionin the ovenbirdswith no expansion (0) through intermediatestages of expansion(1) to the great expansion foundin the "strong-billed"woodhewers (2). 22. Ectethmoidcomplex (Figs. 4-8). The ovenbirdcondition (0) of having a broadplate tilted anteriorly,with a slightwing that doesnot meet the jugal bar, goesthrough intermediatestages (1) to the woodhewercondition (2) of havinga relativelysmaller but strongerplate which is not tilted anteriorly, but which is constrictedmesially and sendsout a large wing that meets and abutsagainst the jugalbar. 23. Supraorbitalarea of frontal bones(Figs. 4-8). The narrow conditionof the supraorbitalarea of the frontal bones(0) in the ovenbirdsgoes through intermediatestages (1) to the broadcondition (2) foundin the woodhewers. 24. Interorbital septum(Figs. 4-8). An unossifiedinterorbital septum (0) in the ovenbirdsgoes through intermediatestages of ossificationin the 58 ORNITHOLOGICAL MONOGRAPHS NO. 13 philydorines(1) to the extremelyossified condition (2) found in the woodhewers. 25. Zygomatic and postorbitalprocesses and temporal fossa (Figs. 4-8). Small processesand a small fossa (0) are presentin most of the ovenbirds. Intermediatesin the philydorines(1) lead to the strongprocesses and deep fossa(2) that characterizethe "strong-billed"woodhewers. 26. Nest. Most of the ovenbirdsbuild large stick structures(0). The mud structure of Furnarius is arbitrarily coded (0). Some ovenbirds excavate tunnels(1) or nestin holesor cavitiesin treesor stumps(2) as do the woodhewers. 27. Habitat. The habitat is codedas non-forest(0), or forest (1).

RESULTS AND CONCLUSIONS The resultsof the Prim Network are shownin Figure 19. The Prim Net- work supportsthe following. The "strong-billed"woodhewers represent a cohesivetaxonomic unit, fairly well separatedfrom the furnariids,but bridged by four intermediategenera. There is no attempthere to decipherany cladisticinformation from the Prim Network. However, I should point out that the Network in no way con- tradictseither a monophyleticor multiple origin hypothesisfor the Dendro- colaptidae(sensu Ridgway), but in fact, the Prim Network doesshow Den- drocinclacloser to the philydorinefurnariids than to the "strong-billed" dendrocolaptids.Additionally, it showsSittasomus and Deconychuraas being very closelyallied, and Glyphorhynchusapproximately halfway between the philydorinesand the "strong-billed"dendrocolaptids. As suspectedthe philydorinesas a group are closerto the woodhewersthan are any of the other ovenbirds.Also, the philydorinesseem to form a cohesivetaxonomic unit, thus lending support to their subfamilial status. The placement of Xenopsclosest to the "intermediates"and other woodhewersis not surprising, and has been suggestedat differentplaces throughout this paper on the basis of singlecharacters. The areaof the synallaxinesand furnariines on the Prim Network is more confused,for thesetwo groupsare probablymore closely allied to each other than is either to any other group within the ovenbird- woodhewerassemblage. The lack of a largenumber of derivedspecific charactersin this analysisprohibits drawing any major conclusionsfrom the far left-hand side of the Prim Network, except that the synallaxinesand fur- nariinesare very closelyrelated. The only point of interestis that mostof the presentlyclassified synallaxines cluster with each other, as do the furnariines. Again, one might questionthe use of hemoglobinas six separatecharacters insteadof one. I must emphasizethat it has little effect on the major con- 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 59 clusionsof the Prim Network, for when the samecomputer program is run withoutusing any hemoglobincharacters the only effectsare as follows: 1) the pheneticdifferences between Dendrocincla and Sittasomus,and between Dendrocinclaand Glyphorhynchusare reducedby a linear distanceof ap- proximatelyone-half the lengthshown in Figure 19; and 2) Xiphorhynchus triangulariscomes off from Deconychura rather than from Glyphorhynchus. In other words, Glyphorhynchusis less woodhewer-likeif hemoglobinis ex- cluded from consideration.

A PHYLOGENY A hypotheticalphylogeny of the furnariidsand dendrocolaptidsis shown in Figure20. The evolutionof trunk-foragingtypes in the groupsunder consideration has involvedtwo major ancestraltypes. On the one hand the philydorines haveapparently given rise to the woodhewergroups from possiblyone or several different lines, and on the other hand the synallaxineshave probably given rise to a number of creepingtypes, includingthe Margarornis-Premn- ornis-Premnoplexcomplex, and Cranioleuca,some species of which hitch up tree trunks in their foragingbehavior. There is alsoPygarrhichas, which, although closestto the members of the Furnariinae and Sclerurinaein cranial morphology,must remain in the category"incertae sedis." The zoogeographic data are perfectlycompatible with the abovestatements. The Philydorinae and the woodhewersare both primarily Amazon Basin forest groupsand occur in almostequal numbersin every countryin which they are found, whereasthe synallaxinesoccur primarily outside of the Amazon Basin for- estedregions, as do alsothe trunk-foragingforms, Margarornis,Premnornis, Premnoplex,and Cranioleuca. Most of theseforms occur in highland situations where the numbersof woodhewerspecies are greatly reduced. Pygar- rhichasoccurs in a regionwhich has no woodhewers. The anatomical evidence advocates a derivation of the woodhewers from philydorine-likeancestors. There appearsto have been one great radiation of woodhewersthat resultedin what I term the "strong-billed"woodhewers, which includesthe generaDrymornis, Nasica, Dendrexetastes,Hylexetastes, Xiphocolaptes, Dendrocolaptes,Xiphorhynchus, Lepidocolaptes, and Cam- pylorhamphus.Other generamay be later derivativesfrom philydorine-like ancestors.Some possess a furnariidwing pattern and many anatomicalfea- turesthat ally themwith the ovenbirds,although in creepingbehavior they are identicalto other woodhewers.These generainclude Glyphorhynchus, which possessessome cranial characters and other anatomicalfeatures which ally it with the philydorines,and the wing stripe commonlyfound in ovenbirds, but has the electrophoretichemoglobin pattern of the woodhewergroup. 60 ORNITHOLOGICAL MONOGRAPHS NO. 13

DECONYCHURA

SITTASOMUS

Figure 19. The Prim Network. The length of the lines between the various OTUs is a direct indication of the phenetic distanceas decipheredby the computer. The actual names of the OTUs are as follows: Furnarius ru/us, Certhiaxis cinnamomea, Synallaxis brachyura, Margarornis rubiginosus,Anumbius annumbi, Coryphistera alaudina, Upu- certhia dumetaria, Cinclodes ]uscus, Geositta cunicularia, Phacellodomus striaticollis, Cranioleuca erythrops, Phleocryptes melanops, Syndactyla ru]osuperciliata, Pseudo- colapreslawrencii, Thripadectesrufobrunneus, Hyloctistes subulatus,Automolus ochrolaemus, Philydor lichtensteini,Anabacerthia striaticollis, Xenops minutus, Dendrocincla anabatina, Sittasomusgriseicapillus, Deconychura longicauda, Glyphorhynchus spirurus, Xiphorhynchus triangularis, Xiphorhynchus guttatus, Lepidocolaptes souleyetii, Den- drocolaptes certhia, Dendrexetastesru]igula, and Campylorhamphus pusillus.

Deconychuraand Sittasomusalso appear to be closer to philydorine-like ovenbirds.These forms possess some cranial and other anatomicalcharacters that ally them with the philydorines,but in skull structureare very similarto each other. Although Deconychurapossesses the dendrocolaptidwing pattern, Sittasomushas the samewing stripe that is found in Glyphorhynchus and commonlyin ovenbirds. The hemoglobinpatterns in both Sittaso- mus and Deconychura are different from either the woodhewer or the furnariidpatterns, but are like eachother. The last "intermediate,"Dendro- cincla,also appearsvery philydorine-likein its characters.Of the "intermediates" Dendrocinclais closestto the philydorinesin skull structure and in other anatomicalcharacters, and in behavioris a perfectintermediate between the philydorinesand the woodhewers.The wingpattern of mostof the species of Dendrocinclais like that of the woodhewers;D. anabatinapossesses a wing stripe similar to that of many furnariids,but somewhatmore diffuse. The hemoglobinof Dendrocinclais identical to that of ovenbirdsin its elec- trophoreticpattern. Of all the charactersanalyzed in this paper, the "intermediates"appear 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 61 furnariid-likein someand dendrocolaptid-likein others. One seeminglyim- portantwoodhewer character which all of the "intermediates"possess is the woodhewertype of syrinx;Geositta, however, a typical furnariid in most othercharacters, also has a dendrocolaptid-likesyrinx. Heimerdinger(pers. comm.) hasfound that Dendrocincla,Sittasomus, and Glyphorhynchusconform to the woodhewerpterylographic pattern. The total analysisseems to indicatethat therewas onelarge radiation of woodhewersfrom philydorine-likeancestors that resultedin the evolutionof the "strong-billed"woodhewers. Whether or not subsequentoffshoots from the philydorine-likeancestors resulted in the "intermediate"genera (see Fig. 20) is difficultto determine.The alternativeto a more recentorigin of the "intermediates"from philydorinestock is that they simplyrepresent wood- hewersof an initial monophyleticradiation that haveretained many primitive characters,but aswe are dealingwith tree-trunkforagers one wonders why a woodhewerwould retain primitive (=less efficient) tree-trunkforaging adaptationsthrough time. The total pheneticdistance within the ovenbirds and woodhewersis expressedby a computerclustering program (Fig. 19). Thesedata are compatiblewith eithera mono-or polyphyleticorigin of the woodhewers. The relationshipswithin the ovenbirdsare evenless clear. The exactposi- tion of the synallaxines,furnariines, and sclerurineswould be very difficult to ascertain. It seemsreasonable, however, that some "holorhinal"pre- passerineor passefineprobably gave rise to a "schizorhinal"group which re- sultedon the onehand in the evolutionof the philydorines,the forestoven- birds, and on the other hand, the synallaxine-furnariinegroups. Later, generalossification of the skullincreased in the philydorinesdue to selection forcesfor strongerskulls associated with foraginghabits. This led to a seriesof holorhinalphilydorines, which, concomitantwith scansorialten- dencies,gave rise to woodhewer-likeforms, and eventuallyto a radiationof woodhewersinto their new adaptive zone.

A BEHAVIORAL MODEL If we assumethat the woodhewersare derivedfrom ancestorsresembling the livingphilydorine ovenbirds, and this seemsto be a safeassumption on the basisof anatomy,behavior, and zoogeography, then we shouldbe ableto summarizemore properly the types of evolutionarytrends involved in a transitionto the woodhewergrade by looking at anatomicaland behavioral seriesin the Recentforms. One thingthat seemsto be fairly well established is that all that is really neededto producea climbingbird from any group of the Passeriformesis the necessarybehavioral adaptations. The passerine bodyform, although typically for a perchingbird, is suitedfor trunkclimbing 62 ORNITHOLOGICAL MONOGRAPHS NO. 13

DENDROCOLAPTIDAE

,....I ,,....i Z Z •':> •"O

m. ..., "•ZO""

HOLORHINY % '•HEMOGLOBIN CHANGE

_OTHER SCHIZORHINY •' SUBOSCINES HOLORHINY

*HORNS IN SYRINX Figure 20. Hypotheticalphylogeny of furnariidsand dendrocolaptids.Bracketed groupsshown to the rightabove were included in the Dendrocolaptidaesensu Ridgway. also,and there are climbingforms in manyof the passerinefamilies. In the furnariids,the preadaptationsfor trunkclimbing seem very apparent.One of themore obvious of theseis the stiff, spiny tail found in manynon-climbing forms.Also, many of thephilydorines that cling and forage in a varietyof wayspossess various degrees of developmentof curvedclaws, and other foot charactersassociated with climbing. 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 63

Of great interestis the genusDendrocincla, members of which foragewith diversity,both from a typicalperching bird stance,and from the trunk climbing stance. As Willis (1966: 667) has summarized,"This woodcreeper... ordinarilyclings to the trunksof treesand saplingsin or near tropicallow- land forestsand salliesout like a flycatcherto snapprey off the groundor vegetation.It occasionallypecks prey off the surfacevegetation, but it rarely movesabout peeringand probinginto the bark or tangledvegetation in the fashionof many speciesin the family Dendrocolaptidae."Willis (op. cit.) studiedthese birds in tropicalforest situations where Dendrocincla is a nor- mal constituentof mixed flocksthat follow army ant swarms,where the arthropodsand small vertebratesthat flee the advanceof the ant swarm are easy prey for the ant-followingbirds. In these situationsWillis recorded the changesin the foragingbehavior of Dendrocincla[uliginosa by record- ing "... changesof heightof waitingbirds or changesin heightsat which prey items are taken." He (1oc. cit.) found that, "When Plain-brown Wood- creepers(Dendrocincla fuliginosa) follow swarmsof army ants on Barro ColoradoIsland, Panama Canal Zone, they forage in the zonenear the ground more frequentlywhen OcellatedAntthrushes (Phaenosticus mcleannani) are absent.The ground-foragingantthrushes regularly supplant the smallerwood- creepers,which then moveto higheror to peripheraland lessproductive zones. This seemsa clearexample of competitiveexclusion by dominance.On Trini- dad, wherecompeting low-foraging antbirds are nearly alwaysabsent, fuliginosa foragesnear the ground at swarms. In British Guiana, where several smallantbirds saturate the lower levelsover the ants,[uliginosa again forages high in the undergrowth."Thus, Dendrocincla[uliginosa appears to forage morediversely when competitors are present,and as Willis (op. cit., p. 670) says,"By wideningits foragingzone in the presenceof competitors,[uliginosa probablyobtains more food than it would if it continuedto forage in the narrow zone near the ground." In other words, in this case it may be that competitionin thesemixed speciesforaging flocks causes some species, like Dendrocincla[uliginosa, which are capableof diverseforaging behavior, to includenew strategiesin foragingbehavior and therebyincrease their food intakewith a minimumof aggressivedistractions. Let us now examinewhat might be involved in the evolution of a woodhewertype from a philydorinefurnariid. Both woodhewersand philydorines are frequent army ant followers, althoughforms of Dendrocinclaare more nearly obligate followersthan other woodhewers.In these situationswhere frequentaggressive encounters occur, it may be of greatselective advantage to be very flexible in foragingbehavior, and one can imaginehow a scansorial foragingstrategy might be advantageous.The majorityof philydorinesforage in a greatvariety of waysand manyspecies hitch up tree trunksat times. In 64 ORNITHOLOGICAL MONOGRAPHS NO. 13 somehighland situations where woodhewers are absentexcept for one or at most two species,the margarornithinefurnariids (Margarornisand related genera),and Pseudocolaptes frequently forage like woodhewers,hitching up tree trunks. In the high Andes,Cranioleuca antisiensis forages by hitching up tree trunks;it existsin areaswhere no woodhewersare present,as does Pygarrhichasof southernSouth America. Sincethe necessarypreadaptations are presentin the furnariidsfor tree- trunkforaging, all that is reallynecessary is selectionfor behavioralflexibility that will allow tree-trunkforaging to begin,whether because of the lack of woodhewers,or becauseof advantagesgained where competitionis great, as in lowland rain forest situations.In these cases,the first step may have beentaken in becominga woodhewer.Selection forces can then operateon perfectionof theseadaptations for tree-mink foraging,and oncethis transition zonebetween creeping and perchingis abandoned,selection for adaptationsfor moreeffective trunk foragingmay occur. Theseselection forces may thenbe operatingon the perfectionof climbingadaptations, including changes in cranial morphology,limb proportions,and other morphologicalfeatures that leadto the woodhewerlevel of organization.

CLASSIFICATION One of the practicalproblems that arisesfrom this studyis that of the classificationof the group. In traditionallinear classificationsit has been customaryto place thoseforms showingthe greatestnumber of primitive charactersfirst in the linearsequence. For mostof the ClassAves this has beenimpossible, owing to the fact that we simplydo not know which forms are the more primitive. For example,looking at the classas a whole, there is no compellingreason why suchbirds as the ratites,or loons and grebes shouldbe placednear the beginning of the linearsequence, thus implying that they are amongthe most primitiveof birds. Both loons and grebesare very specialized.So, in most avian classificationsthe linear sequencerepresents a convenientclassification that has no basisin termsof placementof primitive and advancedforms, but which is, in itself, useful. In the case of the furnariidsand dendrocolaptidsI would proposethat we now have sufficient information at least to place those forms with the greatestnumber of ad- vancedcharacters last and the less specializedforms first in the sequence. The evidencenow seemscompelling that the furnariidsand dendrocolaptids are a monophyleticgroup within themselvesand different from other suboscinebirds. It also seemsreasonable to follow the evidence indicating a closeaffinity of woodhewersto philydorinefurnariids. These lines of evidence do not seemincompatible with the classificationused by Sclater (see Table 4), with a few changes.I would recommendthat the more generalizedSynal- laxinae precedethe more specializedFurnariinae. The terrestrial or semi- 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 65 terrestrialFurnariinae are perhapslikely derivativesof the more "general- ized" synallaxines.Sclater had includedMargarornis, Prernnornis, and Premnoplex(the margarornithines)within the Dendrocolaptinaeprobably owingto theirscansorial habits, and general resemblance to the woodhewers. Theseforms, however, are clearly "ovenbirds" and are probably closely allied to the synallaxines,at leastin cranialosteology. I wouldrecommend their placementat the end of the Synallaxinae.Sclater had also includedthe enigmaticgenus Pygarrhichas within the Dendrocolaptinae.Because its systematicposition remains elusive it shouldbe placedin or near the Sclerurinae and Philydorinae,perhaps as "incertaesedis." The placementof the "intermediates"within the Dendrocolaptinaeshould be as follows: Dendrocincla (mostovenbird-like), followed by Sittasomus,Deconychura, Glyphorhynchus, and the "strong-billed"woodhewers. It is my opinion that the foregoing classificationwould best reflect any of the alternatephylogenies of the group. In addition,I wouldpropose that the familyname Furnariidae be usedbe- causethe preponderanceof speciesare foundwithin the Furnariinae.

SUMMARY 1. The furnariids (ovenbirds) and dendrocolaptids(woodhewers) are two very closelyrelated groups of suboscinebirds. The groupof ovenbirdsmost closelyrelated to the woodhewersis the subfamilyPhilydorinae, which shares an almostidentical range with the dendrocolaptids.The philydorinesare the heavy-bodiedforest furnariids, and they form the link in an almostperfect anatomicalseries going from the synallaxinesand furnariinesto the woodhewers. There are four generaof woodhewers,Dendrocincla, Sittasornus, Deconychura,and Glyphorhynchus,which appearto be the most primitive of the woodhewers(less divergedfrom the ovenbirdpattern), and in fact, sharemany characterswith the ovenbirdsincluding a wing stripepeculiar to the furnariids. These four genera are termed the "intermediates."The re- mainder of the woodhewers,which are called the "strong-billed"woodhewers are very homogeneous.The problemof paramountinterest involves decipher- ing the evolutionaryrelationships. Are the "intermediates"separate off- shootsfrom philydorineancestral stock, or are they simply woodhewers which have retainedmany primitivecharacter states? The great chancefor convergencein tree-trunkforaging birds makesdeciphering the phylogenies very difficult. Anatomicaland other charactersare evaluatedby establish- ing anatomicalseries from non-creepingto creepingforms, and then the character states of the "intermediates"are examined. The primary assumption is that the woodhewersrepresent an advancedstate of derived characters and that the ovenbirds'suite of charactersmore closely resemblesthe primitivestate. 66 ORNITHOLOGICAL MONOGRAPHS NO. 13

2. The skulls of furnariids differ from those of the "strong-billed" dendro- colaptidsin manycharacters. Most of the furnariidsare pseudo-schizorhinal; all of the "strong-billed"dendrocolaptids are holorhinal.A summaryof the character differencesis available in Table 2. The ovenbird skull is, in general, a muchweaker and flexibleskull, compared to the heavilyossified woodhewerskull. Most of the skull characterscorrelate with the foragingbehavior and type of food taken. Most of the furnariidsfeed on small insects. Most of the "strong-billed"dendrocolaptids feed on medium-to-largesized hard- backedbeetles, and on smallvertebrates such as frogsor lizards,which occur on tree trunks. These birds may frequentlyforage by probingand prying into bark and leaf and vine clusters,etc., and somemay occasionallypeck like a woodpecker.Some of the philydorinefurnariids and all of the "intermediate"woodhewer genera possess a mosaicof woodhewer-ovenbirdchar- acters. Those philydorineswhich approachthe woodhewerskull condition are thoseheavy-bodied forest forms which (for thosewhere informationis available) feed more in a woodhewermanner and on large prey, and may peck, pry, and probe in their feedingbehavior. There is an anatomicalse- quencefrom a weak, pseudo-schizorhinalskull through the philydorinesand "intermediates"to the strongwoodhewer skulls. 3. Both the furnariids and dendrocolaptidshave basically a two-notched sternum,but with greatvariation. Someforms show a tendencytoward opening of the posteriorborder of the sternum, while others show a tendency toward the closingof it. The furnariids show a tendencytoward an open posteriorborder of the sternum;none showsa tendencytoward its closure. The "strong-billed"dendrocolaptids show a tendencytoward closure. The "intermediates"are clearly furnariid-likein this character. All possesstwo- notchedsterna, but nonewith a tendencytoward closure, and two formswith a slighttendency toward opening. 4. The hind limb bones (as expectedfrom other creepingforms) are shorter in the woodhewers than in the ovenbirds. The "intermediates" are somewhat intermediate between the ovenbirds and woodhewers in these characters. The distal end of the tarsometatarsus in ovenbirds differs from that in woodhewers. In the woodhewers,metatarsal I is short, correspondingto a short hallux;the amountof separationbetween the condylesis great; and the trochlea for digit III is deeply excavated. The "intermediates"are betweenthe ovenbirds and woodhewers in all of these characters. It is of interest here that some of the tree-trunk foraging furnariids are close to the woodhewer condition,indicating convergence. The femur of woodhewershas a foramen or many small foraminain the proximal end; ovenbirdsgenerally lack the foramen. It is presentin Glyphorhynchus(nearly absentin Dendrocincla), but absentin the other "intermediates."The proximal end of the tibiotarsus 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 67 in the woodhewersshows expansion of the area for the origin of the main extensor muscle of the toes. Most of the "intermediates" are woodhewer-like in thesecharacters, but Dendrocinclais somewhatintermediate, and Xenops, a philydorinefumariid, is very woodhewer-likein its tibiotarsus.The feet (digits) of woodhewersdiffer from thoseof ovenbirdsin havingdigits III and IV nearly equal in length,and this lengthis greaterthan that of digit II. Also, the three anteriortoes are fusedexteriorly for the entirelength of their basalphalanges. The woodhewerhallux is short. The ovenbirdfoot is, for the mostpart, the typicalpassefine anisodactyl foot. Althoughwoodhewers and ovenbirdsare generallyseparable by the charactersof the feet, there are someintermediates, and manytree-trunk foraging birds (includingovenbirds) approachthe woodhewercondition. 5. Ames (1971) reportedthat the syringesof the ovenbirdsand woodhewers are very similar, but differ betweenthe two groups. The "intermediates" (Deconychurawas not examined) possessthe woodhewertype of syrinx, but Geositta(a typicalfurnariid in other characters)possesses the woodhewertype of syrinx. 6. The disc (acrylamide) electrophoreticpatterns of hemoglobinin ovenbirds are differentfrom thosein woodhewers.Of the "intermediates,"Glypho- rhynchusshows a hemoglobinpattern identicalto that of the woodhewers; Sittasomusand Deconychurashow patterns like eachother, but differentfrom both the woodhewerand ovenbirdpatterns; and Dendrocincla(anabatina) showsa patternidentical to that of the ovenbirds. 7. A computercluster analysis was performedto determinequantitatively the overallsimilarity of selectedOTUs. The Prim Network (Fig. 19) confirms the positionof the "intermediates." 8. There are two possiblephylogenies for the woodhewers.The woodhewers may be of multiple origin from philydorine-likeancestors, or monophyletic,if the "intermediates"are simplyforms which have retainedmany primitivecharacters. 9. A behavioralmodel involvingcompetition for feeding space in mixed speciesforaging flocks may be a possibleexplanation for the origin of tree- trunk foragingbehavior. 10. Classificationsshould best reflect phylogenies, and in linear shouldprefer- ably beginwith the more primitive forms (where known) and end with the more specialized.None of the existingclassifications accomplishes this end, thoughSclater's classification certainly approximates a primitiveto specialized scheme(see Table 4). I would recommendfollowing the classificationof Sclaterat the familial and subfamiliallevels. However, I would stronglyrec- 68 ORNITHOLOGICAL MONOGRAPHS NO. 13

ommendthat the more generalizedSynallaxinae precede the more specialized (primarilyterrestrial or semi-terrestrial)Furnariinae, and I wouldadditionally recommendgeneric transfers (now commonlydone) as follows. Margarornis, Premnornis,and Premnoplexare ovenbirdsand shouldbe transferredprobably to the Synallaxinae.Sclater had includedthe margarornithineswithin the Dendrocolaptinae.Pygarrhichas (which Sclaterhad alsoincluded within the Dendrocolaptinae)should be placedin or near the Sclerurinaeand Philyd- orinae as "incertaesedis"; its systematicposition remains elusive. And finally, the sequencewithin the Dendrocolaptinaeshould be: Dendrocincla, Sittasomus,Deconychura, and Glyphorhynchus,followed by the "strong- billed"woodhewers. Finally, the familyname Furnariidae is mostappropriate for theovenbird-woodhewer assemblage.

LITERATURE CITED AMES, P.L. 1971. The morphology of the syrinx in passerinebirds. Bull. Peabody Mus. Nat. Hist., Yale Univ., No. 37: 1-194, 21 pls. BEI•I•A•a•,F. E. 1898. The structure and classification of birds. Longmans, Green and Co., London. BOCK,W.J. 1960. The palatine processof the premaxilIa in the Passeres. Bull. Mus. Comp. Zool., 122: 361-488. BOCK,W. J. 1963. Relationshipsbetween the birds of paradise and the bowerbirds. Condor, 65: 91-125. Boca:, W.J. 1964. Kinetics of the avian skull. Jour. Morph., 114: 1-41. BoCK,W. J., ANI• W. D. M•LLER. 1959. The scansorialfoot of the woodpeckers,with comments on the evolution of perching and climbing feet in birds. Amer. Mus. Novit., No. 1931: 1-45. Dnws, B.J. 1964. Disc electrophoresisII--method and application to human serum proteins. Ann. New York Acad. Sci., 121: 404-427. DESBOROUGH,S., AND M. R. IRWIN. 1966. Additional variation in serum proteins in Columbidae. Physiol. Zool., 34(1): 66-69. E•wnm•s, A. W. F., nNI• L. L. CnWL•-SFogzA. 1964. Reconstruction of evolutionary trees. Syst.Assoc. PubI., 6: 67-76. ENOg•S,W.L. 1940. Structural adaptationsin thrashers (Mimidae: genus Toxostoma) with comments on interspecificrelationships. Univ. California Publ. Zool., 42: 341-400. FARRIS,J.S. 1967. The meaning of relationship and taxonomic procedure. System- aticZool., 16: 44-51. FEDUCCIA,J.A. 1967. The amphirhinal condition in the Passeriformes. Wilson Bull., 79: 453-455. Fgl•t•cc•n, J.A. 1970. Natural history of the avian families Furnariidae and Dendro- colaptidae. J. Grad. Res. Center, Southern Methodist Univ., 38: 1-26. Fgl•t•cc•n, A. 1972. Variation in the posterior border of the sternum in some tree- trunk foraging birds. Wilson Bull., 84: 315-328. F'I.•BRINGER,M. 1888. Untersuchungenzur Morphologie und Systematik der Vogel. Vol. I, T. J. Holkema, Amsterdam. GARROD,A.H. 1873. On the value in classification of a peculiarity in the anterior margin of the nasal bones in certain birds. Zool. Soc. London, Proc. 1873: 33- 38. 1973 EVOLUTION IN OVENBIRDS AND WOODHEWERS 69

GAllROD,A.H. 1877. Notes on the anatomy of passerinebirds. Part II. Zool. Soc. London, Proc. 1877: 447-453. HELLMAYR,C.E. 1925. Catalogue of birds of the Americas and adjacent islands . . . Part 4. Field Mus. Nat. Hist., publ. 234, Zool. Ser., No. 13, 390 pp. HOFER, H. 1954. Neuere Untersuchungenzur Kipfmorphologie der Vi3gel. Acta XI Congr. Internat., Ornith., pp. 104-137. JoLLIE,g. 1958. Commentson the phylogenyand skull of the Passeriformes.Auk, 75: 26-35. KrrTo, G. B., ANDA. C. WILSON. 1966. Evolution of malate dehydrogenasein birds. Science, 153: 1408-1410. KLIJGE, A. G. 1969. The evolution and geographical origin of the New World Hemidactylus mabouia-brookii complex (Gekkonidae, Sauria). Misc. Publ. Mus. Zool., Univ. Michigan, No. 138:78 pp. MAYR, E., AND D. AM•ON. 1951. A classification of Recent birds. Amer. Mus. Novit.,No. 1496: 1-42. ORNSTEIN,L. 1964. Disc electrophoresisI--background and theory. Ann. New York Acad. Sci., 121: 321-349. PETERS,J.L. 1951. Check-list of birds of the World. Vol. 7. Harvard Univ. Press, Cambridge, Massachusetts. Pp. i-x, 1-318. RICHARDSON,F. 1942. Adaptive modifications for tree-trunk foraging in birds. Univ. California Publ. Zool., 46: 317-368. PRIM, R. C. 1957. Shortest connecting networks and some generalizations. Bell Syst. Tech. Jour., 36: 1389-1401. RIDGWA¾,R. 1911. The birds of North and Middle America .... Part 5. U.S. Natl. Mus. Bull., No. 50, pp. i-xxiii, 1-859. SCLATER,P.L. 1890. "Catalogue of birds in the British Museum." Vol. XV, London. SIBLEY,C.G. 1970. A comparativestudy of the egg-whiteproteins of passerinebirds. Bull. Peabody Mus. Nat. Hist., Yale Univ., No. 32: 1-131. SoK•L, R. R., ANDP. H. A. SNEATH. 1963. Principles of numerical taxonomy. W. H. Freeman and Co., San Francisco and London. STORER,R.W. 1960. The classification of birds. Pp. 57-91 in Biology and comparative physiologyof birds, I (A. J. Marshall, ed.). AcademicPress, New York. STOLPE,M. 1932. Physiologisch-anatomischeUntersuchungen uber die hintere Ex- tremitat der Vogel. Journ. fi•r Ornith., 80: 161-247. STRESEMANN,E. 1927-1934. Aves. in Handbuch de Zoologie, Vol. 7 (Part 2). (W. Kukenthal und T. Krumbach, eds.). Walter de Gruyter, Berlin. VON IHER•N•, H. 1915. The classificationof the family Dendrocolapidae.Auk, 32: 145-153. WETMORE,A. 1951. A revisedclassification for the birds of the world. Smithsonian Misc. Coil., 117, No. 4, 22 p. WILLIS, E. O. 1966. Interspecificcompetition and the foraging behavior of Plain- brown Woodcreepers.Ecology, 47: 667-672. Z•Jo,G.R. 1971. Buoyancy,locomotion, morphology of the pelvic girdle and hindlimb, and systematicsof cryptodiranturtles. Misc. Publ. Mus. Zool., Univ. Mich- igan, No. 142: 1-98. Z•JsI,R.L. 1962. Structuraladaptations of the head and neck in the Black Skimmer. Publ. Nuttall Ornith. Club, No. 3, viii q- 101 pp. Z•JsI,R.L. 1967. The role of the depressormandibulae muscle in kinesisof the avian skull. Proc. U.S. Natl. Mus., 123: 1-28. ORNITHOLOGICAL MONOGRAPHS

No. 1. A Distributional Study of the Birds of British Honduras, by Stephen M. Russell. 195 pp., 2 color plates. 1964. Price $4.50 ($3.60 to AOU members). No. 2. A ComparativeStudy of SomeSocial Communication Patterns in • the Pelecaniformes, by Gerard Frederick van Tets. 88 pp., 4 text figures. 1965. Price $2.00 ($1.60 to AOU members). No. 3. The Birds of Kentucky, by Robert M. Mengel. Cloth bound, xiv + 581 pp., 4 color plates plus text figures and vignettes. 1965. Price $10.00 ($8.00 to AOU members). No. 4. Evolution of SomeArctic Gulls (Larus): an Experimental Study of Isolating Mechanisms, by Neal Griffith Smith. 99 pp., 62 text figures. 1966. Price $2.50 ($2.00 to AOU members). No. 5. A ComparativeLife-history Study of Four Speciesof Woodpeckers, by Louise de Kiriline Lawrence. 156 pp., 33 text figures. 1967. Price $3.75 ($3.00 to AOU members). No. 6. Adaptationsfor Locomotionand Feeding in the Anhinga and the Double-crested Cormorant, by OscarT. Owre. 138 pp., 56 text figures. 1967. Price $3.50 ($2.80 to AOU members). No. 7. A DistributionalSurvey of the Birdsof Honduras,by BurrL. Monroe, Jr. 458 pp., 28 text figures, 2 color plates. 1968. Price $9.00 ($7.20 to AOU members). No. 8. An Approachto the Studyof EcologicalRelationships among Grass- land Birds, by John A. Wiens. 93 pp., 30 text figures. 1969. Price $2.50 ($2.00 to AOU members). No. 9. Mating Systems,Sexual Dimorphism, and the Role of Male North American PassefineBirds in the Nesting Cycle, by JaredVerner and Mary F. Willson. 76 pp. 1969. Price $2.50 ($2.00 to AOU members). No. 10.The Behaviorof SpottedAntbirds, by EdwinO. Willis,vi + 162 pp., 3 color plates,27 text figures. 1972. Price $6.00 ($4.75 to AOU members). No. 11.Behavior, Mimetic Songsand SongDialects, and Relationshipsof the Parasitic Indigobirds (Vidua) of Africa, by Robert B. Payne, vi + 333 pp., 2 colorplates, 50 text figures,40 audiospectrographs.1973. Price $8.00 ($6.40 to AOU members). No. 12. Intra-island Variation in the Mascarene White-eye Zosterops borbonica, by Frank B. Gill, vi + 66 pp., 1 color plate, 31 text figures. 1973. Price $2.00 ($1.60 to AOU members). No. 13.Evolutionary Trends in the Neotropical Ovenbirds and Wood- hewers, by Alan Feduccia,iv + 69 pp., 20 text figures. 1973. Price $2.00 ($1.60 to AOU members). Like all other AOU publications,Ornithological Monographs are shipped prepaid. Make checkspayable to "The American Ornithologists'Union." For the convenienceof those who wish to maintain complete sets of Ornithological Monographsand to receive new numbersimmediately upon issue,standing orders will be accepted. Order from: Butt L. Monroe, Jr., Treasurer, American Ornithologists' Union, Box 23447, Anchorage,Kentucky 40223