a functional and evolutionary analysis of rhynchokinesis

A Functional and EvolutionaryAnalysis of Rhynchokinesis

in Birds

RICHARD L. ZUSI

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY • NUMBER 395

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in Birds

Richard L. Zusi

SMITHSONIAN INSTITUTION PRESS

City of Washington

1984

ABSTRACT

Zusi, Richard L. A Functional and Evolutionary Analysis of Rhynchokinesis inBirds. Smithsonian Contributions to Zoology, number 395, 40 pages, 20 figures, 2 tables1984.—In this paper avian cranial kinesis is analysed in terms of the configuration ofbony hinges found in the upper jaw. Three basic forms of kinesis are recognized:prokinesis, amphikinesis, and rhynchokinesis; rhynchokinesis is subdivided into double,distal, proximal, central, and extensive rhynchokinesis. Schizorhiny is discussed and isregarded as a partial synonym of rhynchokinesis. In distally rhynchokinetic birds, neitherthe term "holorhinal" nor schizorhinaP is applicable.

In schizorhinal birds and most rhynchokinetic birds the presence of two hinge axes atthe base of the upper jaw imposes a requirement of bending within the jaw during kinesis.Bending takes different forms according to the number of hinges and their geometricconfiguration within the upper jaw. Proximal rhynchokinesis and distal rhynchokinesisapparently evolved from double rhynchokinesis by loss of different hinges. Extensiverhynchokinesis is an unusual and probably specialized variant. Kinesis in hummingbirds isstill little understood.

Downbending of the symphysis of the upper jaw during retraction is a property ofamphikinesis and of double ana distal rhyncnokinesis, and is judged to play an importantrole in grasping prey, particularly in slender-billed birds that probe. The adaptivesignificance of rhynchokinesis in certain non-probing birds is not yet known. It is hypoth-esized that the schizorhinal skull in proximally rhynchokinetic birds reflects ancestry, buthas no adaptive explanation, in many living species.

Either prokinesis or some form of rhynchokinesis could be primitive for birds. Rhyn-chokinesis is not compatible with the presence of teeth in the bending zone of the ventralbar of the upper Jaw, and it probably evolved after their loss. Neognatnous rhynchokinesis,however, probably evolved from prokinesis. The evolutionary origin of rhynchokinesisfrom prokinesis required selection for morphological changes that produced two hingeaxes at the base of the upper jaw. Once evolved, the properties of these axes were subjectto selection in relation to their effects on kinesis. The various forms of kinesis arehypothesized to have evolved by simple steps, and pathways to each kind of kinesis aresuggested. In neognathous birds, prokinesis was probably ancestral to amphikinesis, andamphikinesis to rhynchokinesis in most cases, but prokinesis has also evolved secondarily

of simple models is valuable in formulating hypotheses about the functionalproperties and evolutionary history of different forms of kinesis. The functional analysisof kinesis provides a rationale for adaptive radiation and convergence in avian orders thatinclude rhynchokinetic members, ana suggests polarities and evolutionary directions thatmay be useful in phylogenetic analysis.

OFFICIAL PUBLICATION DATE is handstamped in a limited number of initial copies and isrecorded in the Institution's annual report, Smithsonian Year. SERIES COVER DESIGN: The coralMontastrea cavernosa (Linnaeus).

Library of Congress Cataloging in Publication DataZusi, Richard L. (Richard Lawrence), 1930-A functional and evolutionary analysis of rhynchokinesis in birds.(Smithsonian contributions to zoology ; no. 395)Bibliography: p.Includes index.1. Birds—Physiology. 2. Birds—Evolution. 3. Rhynchokinesis. I. Title. II. Series.QL1.S54 no. 395 591s 83-20230 [QL698] [598.2' 1852]

Contents

Page

Introduction 1Methods and Materials 1Acknowledgments 2

Terminology 2Avian Cranial Kinesis 2

Prokinesis 4Amphikinesis 4Rhynchokinesis 4

Double Rhynchokinesis 5Distal Rhynchokinesis 5Proximal Rhynchokinesis 5Central or Paleognathous Rhynchokinesis 5Extensive Rhynchokinesis 5

Holorhiny and Schizorhiny 7Functional Analysis of Cranial Kinesis 12

Prokinesis, Amphikinesis, and Double Rhynchokinesis 16Proximal Rhynchokinesis 17Distal Rhynchokinesis 20Extensive Rhynchokinesis 20Central Rhynchokinesis 21Hummingbirds 23

Evolution of Rhynchokinesis 23Adaptive Aspects of Rhynchokinesis 23Origin of Rhynchokinesis 24Pathways of Evolution 26

Distal Rhynchokinesis 28Proximal Rhynchokinesis 28Prokinesis 30

Directions of Evolution 30Discussion 31Appendix 33Literature Cited 36Index to English and Scientific Names (excluding Appendix) 38


in Birds

Richard L. Zusi

Introduction

All modern birds have the capacity to movethe upper jaw, or some portion of the upper jaw,with respect to the brain case. This functionalproperty is known as cranial kinesis (kinetics, orkinematics), and its mechanism includes, in ad-dition to the upper jaw, various portions of thecranium, the lower jaw, the quadrate and bonypalate, the jugal bars, certain jaw muscles, liga-ments, and various articulations and bony hinges.Thus, much of the morphology of the avian headrelates to cranial kinesis. This paper is concernedmainly with the upper jaw and the effects offorces acting on it through the kinetic mecha-nism. Emphasis is placed on rhynchokinesis, inwhich bending within the upper jaw accompanieskinetic motion of the jaw as a whole.

The literature on avian cranial kinesis is exten-sive, beginning, perhaps, with Herissant (1752)and continuing to the present. Many of the mor-phological and functional properties of kinesisare understood, but others, even some of thebasic ones common to many birds, are not. Inaddition, certain aspects of the diversity of jawstructure in birds are unexplained. For example,

Richard L. Zusi, Department of Vertebrate Zoology, NationalMuseum of Natural History, Smithsonian Institution, Washington,DC. 20560.

a variety of forms of kinesis that fall under thecurrent term "rhynchokinesis" has been knownfor many years (Nitzsch, 1816, 1817), but de-tailed functional analysis has been largely re-stricted to the particular form of rhynchokinesisfound in woodcock and snipe (Marinelli, 1928;Schumacher, 1929). Only recently has a set ofterms for the variants of rhynchokinesis beenproposed (Biihler, 1981). Another source of con-fusion has been the extent and nature of theinteraction between schizorhiny and holorhinyon the one hand, and cranial kinesis on the other.The present paper seeks to clarify the terminol-ogy and interrelationships of cranial kinesis andschizorhiny, to analyse functional properties ofthe various forms of kinesis, and to offer clues tothe origin and evolution of rhynchokinesis.

METHODS AND MATERIALS.—The data for thispaper pertain primarily to variations in the pat-tern of bending zones or hinges in the upper jawof birds. I determined the presence and locationof bending zones by direct examination ofcleaned skulls in the collection of the Smithson-ian Institution and from radiographs of the skullsof selected species. The presence of a hinge wasusually manifested by flattening of bone thatproduced a more or less restricted bending axis.A hypothesis of flexibility was tested by manipu-lation of water-soaked skulls whenever skull

1

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

structure did not permit a clear interpretation.In a few cases, noted in the text, manipulation offresh birds provided evidence of hinges. Spatialrelationships of the bony hinges in skulls of 26species were plotted on paper by means of acamera lucida. I determined patterns of bendingin a hypothetical upper jaw with different config-urations of hinges by assuming a jaw structure oftwo-dimensional, inflexible bars connected bypin hinges, and by laying out the required shapesof the jaw under different degrees of protractionor retraction with a ruler, protractor, and com-pass. These patterns were confirmed by manip-ulation of a simple, two-dimensional cardboardmodel of the upper jaw. The chief sources ofpossible error in my methods were in distinguish-ing among several forms of kinesis in borderlinecases, and in characterizing flexibility of the ven-tral hinge of the lateral nasal bar of the upperjaw in a few species. The hypotheses concerningkinetic configurations presented in this papershould be tested against accurate description ofbill movement in living birds.

I made the original drawings of skulls with theaid of a microscope and camera lucida, or bytracing projected photographic transparencies.Relative sizes of illustrations were adjusted insome instances to make all skulls more readilycomparable.

Anatomical terminology generally follows thatof Baumel et al. (1979). I followed the nomencla-ture of Morony et al. (1975) for scientific namesof birds. The Index identifies to family orsubfamily all English and generic names used inthis paper. The species and number of specimensof the skeletons examined for this study areshown in the Appendix.

ACKNOWLEDGMENTS.—This paper developedfrom an earlier and still unfinished study of cra-nial kinesis in the Charadrii begun by me at theUniversity of Michigan Museum of Zoology. Per-mission to use the collections and radiographicfacilities at UMMZ is gratefully acknowledged. Ialso thank the curators of the British Museum(Natural History) for making their collectionsavailable and for the loan of specimens. The late

Leon Kelso generously undertook a major trans-lation from Russian for minimal compensation.Carolyn Cox Lyons rendered the skull drawingsin ink and Ellen Paige drew the diagrams andlabelled the figures, except for figures 7 and 17,which were done by the author. I benefited froman early discussion of terminology with WalterBock, and, more recently, from his criticisms andthose of Storrs Olson on one or more drafts ofthe manuscript. Their suggestions were generallyfollowed, but those that were not neverthelessstimulated further study that greatly improvedthe paper. This research was partially supportedby Smithsonian Research Awards Sg 0663049and Sg 3374156. Finally I thank my wife, Luvia,for typing parts of the manuscript, and for herpatience and understanding during its prepara-tion.

Terminology

AVIAN CRANIAL KINESIS

Cranial kinesis in various groups of vertebrateshas been described by Frazzetta (1962), Bock(1964), Buhler (1977), and others. Here I rec-ognize prokinesis, rhynchokinesis, and amphiki-nesis as basic forms of avian kinesis (Figure 1).Although the term "amphikinesis" has been ap-plied within other vertebrate classes in otherways, confusion may be avoided by adding theadjective "avian" as proposed by Bock (1964:3).I follow Buhler (1981) in subdividing rhyncho-kinesis into five categories that are here called"proximal," "central," "distal," "double," and "ex-tensive" rhynchokinesis (Figure 1) according tothe position or extent of bending zones in thedorsal bar of the upper jaw. I have substitutedthe term "central" for Biihler's "intermediate,"and "extensive" for "extended," only becausethese adjectives form more familiar adverbswhen modifying "rhynchokinetic."

Throughout this paper I refer to flexible orinflexible bones. While recognizing that all bonesare somewhat flexible, I use inflexible to meanthat bending is not readily noticeable under nor-

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PROKINESIS

SYMPHYSIS EXTERNAL DORSAL ^CR ANIOFACIAL HINGENARIS BAR /

MESETHMOID

LATERAL BAR

VENTRAL BAR

AMPHIKINESISv

DOUBLE

DISTALPROXIMAL

CENTRAL EXTENSIVEFIGURE 1.—The forms of avian kinesis (stippled figures show upper jaw in closed position; P= protraction, R = retraction; solid pointer indicates craniofacial hinge; open pointers indicateadditional bending axes on dorsal bar).


mal stresses. Bones that bend are usually notablyflattened, and I use the term "hinge" to mean alocalized region of flexibility—not an articula-tion.

The upper jaw of birds is not easily defined. Itcould be stated to consist of the nasal, premaxil-lary, and maxillary bones as defined by mostauthors, but the homologies of some of thesebones have been questioned (McDowell, 1978),and the limits of the bones are lost by fusion inadult birds. A functional definition is more prac-tical. In this paper I draw the caudal limits of theupper jaw dorsally at the craniofacial hinge andventrally at the hinges of the jugal bars andpalatines. Thus, the upper jaw consists of a dorsalbar, two lateral bars, two ventral bars (sometimesfused into one), and a symphysis (Figure 1). Insome birds the medial portion of the craniofacialhinge has shifted forward, and in them I regardthe caudal limit of the upper jaw to lie at thelevel of the cranial attachments of the lateralbars. The lateral bar maintains a roughly con-stant relationship with the ectethmoid, prefron-tal, frontal, and orbit in related birds, whereasthe mesethmoid and overlying medial portion ofthe craniofacial hinge may vary considerably intheir position relative to the above features, evenin closely related birds.

Cranial kinesis includes upward and downwardrotation of the upper jaw relative to the braincase. These motions are usually referred to asprotraction and retraction of the upper jaw, al-though the terms apply better to associated mo-tions of the palate with respect to the sphenoidalrostrum. Both protraction and retraction canoccur either above or below the closed positionof the upper jaw (Figure 1). The ability to pro-tract the upper jaw is related to a variety of avianadaptations (Beecher, 1962; Bock, 1964; Yudin,1965; Zusi, 1967), but the increase in manipula-tive versatility of the avian jaw that is affordedby retraction of the upper jaw beyond its closedposition is probably most important for an un-derstanding of rhynchokinesis and amphikinesis(see also Zusi, 1967). The phenomenon of cou-pled kinesis (Bock, 1964) is not directly pertinent

to this paper except for one point. Bock statedthat "in a majority of birds, those having a cou-pled kinetic skull, depression of the upper jawbeyond the normal closed position does not seempossible" (Bock, 1964:24), but he acknowledgedthat mechanisms to effect depression beyond theclosed position might exist. Zusi (1967) proposedtwo such mechanisms and cited evidence thatretraction beyond the closed position occurs inliving birds with coupled kinesis. This fact isimportant for an understanding of the signifi-cance of rhynchokinesis.

PROKINESIS (Figure 1).—In a prokinetic skullthe upper jaw itself is inflexible and it pivots upand down around the craniofacial hinge. Bend-ing occurs in a flattened region of the nasalprocesses of the premaxillary bones and in theadjacent premaxillary processes of the nasalbones just rostral to, or dorsal to, the meseth-moid bone (Figure 2). The premaxillary andnasal bones continue backward from the bendingaxis to fuse with the frontal and mesethmoidbones in adult birds. In rare cases the craniofacial"hinge" is a true articulation. Typically the bonynarial openings end rostral to the craniofacialhinge and the nasal bones provide a firm basefor the distribution of protraction and retractionforces to the entire upper jaw.

AMPHIKINESIS (Figure 1).—This form of ki-nesis differs from prokinesis in that the narialopenings extend back almost to the level of thecraniofacial hinge, and the dorsal and ventralbars are flexible near the symphysis. In addition,the lateral bar is flexible near its junction withthe dorsal bar. As a result, protraction and re-traction forces are transmitted primarily to thesymphysis via the lateral and ventral bars. Be-tween the craniofacial and rostral hinges thedorsal bar may be thickened and inflexible, oronly slightly flexible. During protraction the en-tire upper jaw is raised and the tip of the jaw isbent up in addition; in retraction the tip bendsdown with respect to the rest of the upper jaw.

RHYNCHOKINESIS (Figure 1).—In all forms ofrhynchokinesis, bending of the dorsal bar occursrostral to the base of the upper jaw as delimited

NUMBER 395

by the cranial attachments of the lateral bars.Different forms of rhynchokinesis are character-ized by the location, number, and extent of thehinges on the dorsal bar. Unlike prokinetic birds,rhynchokinetic birds never have a single cranio-facial bending zone that includes the nasal bonesand the nasal processes of the premaxillae. In-stead they have one bending axis passing throughthe dorsal ends of the lateral bars, and one ormore others farther rostral on the dorsal bar.The nasal openings either terminate at the levelof, or rarely caudal to, the cranial attachmentsof the lateral bars, and thus they extend caudallybeyond the bending zone(s) of the dorsal bar.

The description of five kinds of rhynchokinesisis somewhat arbitrary because hinges may shiftposition in the course of evolution, as well asappearing de novo. However, I shall argue laterthat hinges generally have not made extensiveevolutionary "migrations" along the bill, and Ifind that most rhynchokinetic birds can be clas-sified as one of the five kinds.

Double Rhynchokinesis (Figure 1): In this formof rhynchokinesis there are two hinges on thedorsal bar—one near its base and one near thesymphysis. Double rhynchokinesis differs fromamphikinesis in having two bending axes ratherthan one at the base of the upper jaw—the basalhinge of the dorsal bar, and the dorsal hinges ofthe lateral bars. Other workers have describedthis form of kinesis without naming it (Nitzsch,1816; Kripp, 1935; Hofer, 1955; Beecher, 1962;Yudin, 1965). Most workers have regarded dou-ble rhynchokinesis as an unusual form of aviankinesis and have not dealt with it in their func-tional analyses. Yudin (1965:69-70) thought thatit represented a transitional phylogenetic stagebetween "little-differentiated rhynchokinesis"and "secondary prokinesis." My examination ofskulls, radiographs of skulls, and manipulation ofsoaked skulls from all schizorhinal groups ofbirds strongly suggests that double rhynchoki-nesis is much more common than previouslysupposed (Table 1). A brief discussion of themechanics of double rhynchokinesis is given byZusi (1962:36-38).

Distal Rhynchokinesis (Figure 1): Distal rhyn-chokinesis differs from double rhynchokinesis inthat flexibility of the basal hinge of the dorsalbar is absent. Bending occurs on the dorsal baronly behind the symphysis in a restricted or ex-tended portion of flattened bone. Only the sym-physis of the upper jaw is raised or lowered.Characteristically the mesethmoid is expandedforward and fused with the base of the dorsalbar, and the entire dorsal bar is stiffened caudalto its hinge. The lateral bar has a well-definedhinge near its attachment on the cranium, exceptin kiwis (Apteryx).

Proximal Rhynchokinesis (Figure 1): This formof kinesis differs from double rhynchokinesis inthat flexibility of the dorsal bar near the sym-physis is absent and flexibility of the dorsal baris limited to its basal portion. There are two axesof bending at the base of the upper jaw as indouble rhynchokinesis, one on the dorsal bar andone on the lateral bars. The dorsal bar may bestrongly constructed but the ventral bar is alwaysflexible at some point.

Central or Paleognathous Rhynchokinesis (Figure1): This is the "intermediate rhynchokinesis" ofBiihler (1981). The single bending zone of thedorsal bar is located approximately midway be-tween the symphysis and the lateral bars and thenares extend back to the cranial attachments ofthe lateral bars. Central rhynchokinesis is char-acteristic of most ratites and most tinamous, andit includes a variety of distinctive characteristicsother than the central location of the bendingzone.

Extensive Rhynchokinesis (Figure 1): A fewbirds have an extended zone of bending alongthe dorsal bar between its cranial attachment andthe symphysis. The bar is generally flattenedthroughout with no evidence of localized hinges.The term "bone spring kinetics" was used byBeecher (1962:28-29) in describing this form ofthe upper jaw in a tinamou {Tinamus major). Hestated that some plovers and sandpipers (Char-adrii) display a combination of a basal hinge andbone spring kinesis, whereas I regard most plov-ers as doubly rhynchokinetic. Yudin (1958,


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NUMBER 395

1965), Marinelli (1928), Moller (1970), and oth-ers refer to extended flexibility of the dorsal barbetween the symphysis and its base as an unspe-cialized or little-differentiated form of rhyncho-kinesis. In almost every case I regard the exam-ples they cite as proximally, doubly, or distallyrhynchokinetic. It is not always easy to knowwhether a skull is extensively kinetic, but I haveclassified as doubly rhynchokinetic any skull witha dorsal bar that, no matter how slender, showsgreater flexibility near its base and near thesymphysis than between those points. Similarly,proximal and distal rhynchokinesis are recog-nized in slender-billed birds by the differentia-tion of a hinge only near the base of the dorsalbar, or only behind the symphysis.

HOLORHINY AND SCHIZORHINY

Many years ago, Garrod (1873) described twokinds of avian skulls, which he termed "schizo-rhinaP and "holorhinal." By his definition, theholorhinal skull is characterized by bony externalnares whose concave caudal borders lie rostral tothe caudal ends of the nasal processes of thepremaxillae (Figure 2a). Referring to the pre-maxillary and maxillary processes of the nasalbone, he stated, "These two processes becomecontinuous behind with the body of the bone,and with one another, there being no interrup-tion of any kind between them" (Garrod,1873:33). In the schizorhinal skull, the caudalborders of the external nares form an angularspace or slit that usually terminates behind theends of the nasal processes of the premaxillae(Figure 2b). As a result, the maxillary process ofthe nasal bone is "free" and "almost detached"from the premaxillary process (Garrod,1873:36). Garrod (1873, 1877) used holorhinyand schizorhiny as a taxonomic character, withlimited success.

Because the shape of the caudal border of thenares does not necessarily correlate with its po-sition relative to the nasal processes of the pre-maxillae, both Hofer (1955) and Yudin (1965)used the terms "atypical" and "typical" to modify

"schizorhinal" and "holorhinal." For example,Hofer described Cursorius (Glareolidae) as atypi-cally holorhinal, by which he meant that it washolorhinal in the shape of its nares but function-ally schizorhinal in having the lateral bars of thebill independent of the dorsal bar (Figure 2c).Yudin also used "secondary" to indicate ontoge-netic change in these features and, by implica-tion, phylogenetic change, whereas by "primary"he meant no such change. In addition, he used"secondary" to indicate a phylogenetic trend in-ferred from comparison of a series of living spe-cies. Thus in describing Fratercula as a bird with"secondary atypical schizorhinal" nasal openings,he meant that the caudal borders of the nareswere slit-like (schizorhinal), that the borders didnot extend caudally as far as the border of thenasal processes of the premaxillaries (atypical),and that the atypical features represented anevolutionary trend away from typical schizorhiny(secondary) as seen in a graded series of theAlcidae from Cepphus, Uria, and Alca throughCerorhinca and Lunda to Fratercula.

The shape of the caudal border of the naresin birds varies from truncate to rounded to slit-like, reflecting the relative width of the bill orthe intrusion of bony elements into the narialopening, and probably other variables (Figure 3).Anatomical relationships such as the position ofthe nares relative to the caudal end of the nasalprocess of the premaxillary differ within ordersor families, or from young to adult stages. How-ever, most birds that are schizorhinal by theoriginal anatomical definition share certain func-tional properties that differentiate them frommost holorhinal birds. These properties are di-rectly related neither to the shape of the poste-rior borders of the nares, nor to their positionrelative to the nasal processes of the premaxillae.Bock and McEvey (1969) therefore recom-mended that "the distinction between the holor-hinal and the schizorhinal nostril be based uponwhether the posterior end of the nostril stopsanterior to, or projects behind, the nasal-frontalhinge (i.e., separates the hinge of the medialdorsal bar from the hinge of the lateral nasal


NASAL PROCESS OF PRE MAXILLARY

a

LATERAL BAR

DORSAL BAR

SYMPHYSIS

NASAL PROCESSOF PREMAXILLARY

NASALPREMAXILLARY PROCESS

NASAL

EXTERNAL NARIS,

V

MESETHMOID

NASAL fPREMAXILLARY PROCESSMAXILLARY PROCESS

FIGURE 2.—Features of holorhinal and schizorhinal skulls: a, holorhinal skull (Cyanocitta stelleri);b, schizorhinal skull (Pluvialis squatarola); c, "atypical holorhinal" (=schizorhinal) skull (Cursoriuscoromandelicus). (Left, lateral view; right, dorsal view; solid pointer indicates craniofacial hinge;open pointer indicates additional hinge axis on dorsal bar.)

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FIGURE 3.—Configurations of external narial openings in holorhinal and schizorhinal birds: a,Sittasomus griseicapillus; b, Philydor guttulatus; c, Upupa epops; d, Phoeniculus purpureus; e, Cheli-doptera tenebrosa;/, Rallus aquations; g, Eurypyga helias; h, Glareola nordmanni; i, Pterocles orientalis.(Solid pointer indicates craniofacial hinge; open pointer indicates additional bending axis ondorsal bar; arrow shows additional hinge on lateral bar; a-f, holorhinal; g-i, schizorhinal.)

10 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

bars)." By "nasal-frontal hinge" they meant thebasal hinge of the dorsal bar. Their definitionemphasizes the functional differences betweenthe two skull types, but it fails to cover thosespecies in which the nostril terminates near orprecisely at the level of the craniofacial hinge, asin some woodcreepers (Dendrocolaptidae), oven-birds (Furnariidae), Hoopoes (Upupidae), andrails (Rallidae) (Figure 5a-c,f). The omission isnot trivial because one must deal with skulls ofthis type to explain the origin of schizorhiny orrhynchokinesis. More importantly, their defini-tion does not indicate the relative positions ofthe basal hinge of the dorsal bar and the dorsalhinge of the lateral bars (original craniofacialhinge), i.e., whether they lie along a single trans-verse axis or on different, axes.

For reasons already presented (page 4), I re-gard the schizorhinal skull as one in which themedial portion of the craniofacial hinge hasshifted forward. If this condition evolved from aholorhinal bird in which the nasal openingsreached back to, or nearly to, the craniofacialhinge, the medial hinge of the dorsal bar in theschizorhinal bird would always lie rostral to thecranial attachment and hinge of the lateral bar,and be separated from it by the nares. Thelocation of the original craniofacial hinge, or baseof the upper jaw, would be represented by theattachments of the lateral bars, as already ex-plained. Regardless of the precise evolutionarypathways to schizorhiny, the result is that allschizorhinal birds have two hinge axes at thebase of the upper jaw. Examples of their diver-sified form, and of holorhinal birds, are shownin Figure 3.

All schizorhinal birds are rhynchokinetic butsome rhynchokinetic birds are not schizorhinal.By my definitions "schizorhiny" is a partial syn-onym of "rhynchokinesis." As a result, the terms"schizorhinal" and "rhynchokinetic" can be usedseparately, but they may be redundant when usedtogether, and no bird is both rhynchokinetic andholorhinal.

Paleognathous birds (the ratites and tinamousamong living birds) are rhynchokinetic (Figure4), but Bock (1963) considered them to be ho-

lorhinal. However, they meet my criteria forschizorhiny in that the hinge of the dorsal barlies rostral to the lateral bar and is thereforefunctionally separated from the lateral and ven-tral bars. The ratites are unusual in having aninterrupted lateral bar, the parts of which areconnected by a ligament. Bending occurs mainlyat the ligament, which may be in the position ofthe dorsal hinge (rheas) or farther ventrally(other ratites). In tinamous the lateral bar iscomplete and it has a dorsal hinge; it may rep-resent the ancestral condition for the ratites. Inany case, the hinge of the dorsal bar lies rostralto the base of the upper jaw, and it probablyrepresents the displaced medial portion of anancestral craniofacial hinge. Paleognathous birdsdiffer from other schizorhinal birds in that thehinge of the dorsal bar appears to have migratedfarther forward from the base of the upper jaw,perhaps even to the extreme level found in kiwis.

A few rhynchokinetic birds have evolved spe-cializations such that the term "schizorhiny" doesnot apply. In most distally rhynchokinetic birdsthe medial part of the craniofacial hinge hasdisappeared (not shifted far forward as oftenstated). These birds are therefore no longerstrictly schizorhinal although their schizorhinalancestry is clear. They have only a single hingeaxis at the base of the upper jaw, but that hingeis interrupted and restricted to the upper endsof the lateral bars. By my definitions neither"holorhinal" nor "schizorhinal" can be appliedusefully to these birds.

Bock (1964) stressed the isolation of the lateraland ventral bars from the dorsal bar as the mostimportant functional attribute of the schizorhinalskull and he regarded that isolation as essentialfor rhynchokinesis. He distinguished "paleog-nathous rhynchokinesis," in which the ventral baris isolated from the dorsal bar by an interruptedlateral bar, from "charadriiform rhynchokinesis,"in which the ventral bar is isolated by the externalnares. I distinguish "paleognathous rhynchoki-nesis'' from all other forms of rhynchokinesis,which I lump under "neognathous rhynchokine-sis."

Functional independence of the lateral bars of

NUMBER 395 11

FIGURE 4.—Upper jaws of some paleognathous birds: a, Rhea americana, immature, lateral view(dashed line = unossified nasal septum); b, Casuarius casuarius, lateral view; c, Struthio camelus:lateral view (left), dorsal view (right); d, Eudromia elegans: lateral view (left), dorsal view (right).(Solid pointer indicates craniofacial hinge or break in lateral bar; open pointer shows rhyn-chokinetic hinge.)


the jaw from the dorsal bar in some birds wasknown to Nitzsch (1816) and has been muchdiscussed in relation to rhynchokinesis since thattime. I agree that isolation of the lateral andventral bars is essential for rhynchokinesis (andit is a corollary of my definition of rhynchokine-sis), but it is not limited to schizorhinal or rhyn-chokinetic forms and is thus not diagnostic ofthem. In amphikinetic birds and some prokineticones, the lateral and ventral bars are isolatedfrom the dorsal bar without a forward shift ofthe medial portion of the craniofacial hinge. Thecraniofacial hinge is essentially complete and lim-ited to a single hinge axis at the base of the upperjaw, whereas that of a schizorhinal bird and mostrhynchokinetic birds is separated into two hingeaxes. The importance of the double hinge willbe evident in the analysis of kinesis that follows.

Functional Analysis of Cranial Kinesis

In prokinetic birds, bones that form the cra-niofacial hinge are relatively thin and flattenedin the frontal plane. The craniofacial hinge in adried skull may or may not be clearly differen-tiated anatomically in dorsal view (Figure Se,d,respectively). When the upper jaw rotates, anygiven point on the jaw travels an arc whose radiuscenters at the bending axis; as the arcs of allpoints in the jaw are concentric, the points canmaintain constant spacial relationships with eachother during kinesis (Figure 5). As a result, con-struction of the bill may be rigid and bulkywithout restricting kinesis.

In rhynchokinetic and amphikinetic birds thelateral and ventral bars of the upper jaw arefunctionally independent of the dorsal bar at itsbase. Because the conjoined lateral and ventralbars of the bill are connected to the cranium andsymphysis respectively, none of the force appliedto these bars by the palate and jugal bars istransmitted directly to the base of the dorsal baras it is in a typical holorhinal bill.

Assuming for the moment that the lateral bars,the ventral bar, the dorsal bar, and the symphysisform an inflexible unit hinged to the cranium,

FIGURE 5.—Effects of basal hinge axes on kinetic upper jaw:upper, single axis, all points (P) on jaw follow concentric arcswith no constraint; lower, two axes, constrained because pointP must follow two arcs (1 and 2), preventing kinesis inhypothetical jaw illustrated. (Arrows indicate direction offorces from palate.)

kinesis of a schizorhinal upper jaw would not bepossible because each point on the jaw would berequired to follow two diverging paths simulta-neously. As shown in Figure 5, point P wouldhave to follow arc 1, whose radius centers at thecranial hinge of the lateral bar, and at the sametime arc 2, centering on the cranial hinge of thedorsal bar. All other points on the jaw would alsohave to follow two arcs, and the jaw would breakif moved. Whereas flexibility within the upperjaw of the amphikinetic skull is not controlled inany way by its single basal hinge, the presence oftwo basal hinge axes in the rhynchokinetic skullrequires flexibility within the upper jaw if kinesisis to occur at all. Flexibility within the upper jawsof schizorhinal birds almost always occurs at com-parable locations in the upper jaw and palate,which is to say that certain hinge locations canbe identified and predicted. These hinges are inpart the basis for the five kinds of rhynchokinesis,and the letters that I will use to designate them

NUMBER 395 13

are as follows (see Figure 6a): A, lateral bar nearjunction with cranium; B, dorsal bar near junc-tion with cranium or mesethmoid extension; C,dorsal bar near junction with symphysis; D, ven-tral bar near junction with symphysis; E, lateralbar near junction with ventral bar. (Flexible por-tions of the jugal bars and palatine bones are notpertinent to this paper.) All five hinges (A-E) arepresent in only a few species of rhynchokineticbirds. In most species, flexibility is lacking at oneor more of the designated hinge locations.

FIGURE 6.—Kinetic hinges and kinesis: a, full complementof hinges (A-E); b, two of many possible bill shapes afterprotraction from E to £'; c, loss of E stabilizes bill duringprotraction and retraction.

Most authors assume that many rhynchoki-netic birds have an extensively flexible dorsalbar. Such birds are said to represent the gener-alized state of "rhynchokinesis," an intermediatestage in the shift of a hinge from the base of thebill toward the tip (Hofer, 1945), or a shift fromthe tip toward the base (Moller, 1970). As ex-plained below, hinge B is probably limited in theextent to which it has shifted forward from theancestral condition in most schizorhinal birds,and with few exceptions, the various forms ofrhynchokinesis have been derived through lossof either hinge B or C, or both, from a doublyrhynchokinetic ancestor. The taxonomic distri-butions of amphikinesis and the five forms ofrhynchokinesis are summarized in Table 1.

An inflexible and complete lateral bar immov-ably attached to the cranium would block kinesis,and hinge A is therefore present in all rhyncho-kinetic birds except those with an incompletelateral bar. Assuming that each of the hinges (Bthrough E) may be either present or absent, thereare 16 possible combinations of their presenceor absence with hinge A. Of these, 11 combina-tions would theoretically block kinesis (e.g., ABshown in Figure 5b). All of the remaining fivecombinations would permit kinesis, and four ofthem are found in living birds (ABCE is notfound). Each of these four combinations corre-sponds to a named form of rhynchokinesis, asfollows:

ABCDE double rhynchokinesisABCD double rhynchokinesisACDE distal rhynchokinesisABDE proximal rhynchokinesis

If the central hinge of tinamous correspondsto hinge B, then ABDE would also describe cen-tral rhynchokinesis. One of the combinations(ABD) that would theoretically block kinesis isfound in the Tooth-billed Pigeon (Didunculusstrigirostris), but in fact it does not prevent kinesisin that species for reasons given on pages 18, 19.

When all hinges are present (e.g., Actitis: Scol-opacidae) the bill is weak and easily bent byexternal forces applied to it, whether or not the


palate is stabilized (Figure 6b). In many doublyrhynchokinetic species the bill is strengthened bythe absence of hinge E; in this prevalent form ofrhynchokinesis (Table 1) the lateral and ventralbars act as a rigid unit connecting hinges A andD, and the dorsal bar connects hinges B and C.The following discussion applies to this form ofrhynchokinesis (i.e., ABCD), in which bendingof the upper jaw during protraction and retrac-tion is determined by the arcs of radii AD andBC, centering on axes A and B respectively (Fig-ure 6c). The configuration of the arcs of AD andBC prescribes the degree and direction of rota-tion of the symphysis with respect to the dorsaland ventral bars during motions of the upperjaw. The paths of the two arcs depend upon thepositions of hinges A, B, C, and D relative toeach other. When referring to horizontal or ver-tical distances between hinges A and B, horizon-tal distance is measured along the long axis ofthe base of the dorsal bar and vertical distance ismeasured on a line 90° to the horizontal axis.

The effects on kinesis of a change in positionof hinges A, B, C, or D are demonstrated inTable 2, in which degrees of rotation of thesymphysis at hinge C are indicated for specifieddegrees of protraction and retraction of the up-per jaw around hinge B. The data were deter-mined graphically, using compass, protractor,and ruler, from a basic hinge configuration andfrom variations on that pattern (Figure 7). Datafrom each pattern are shown in the rows of Table2, and the pattern of hinges (from Figure 7) thatcorresponds to each row is listed in the table.Effects of change can be appreciated by compar-ing various rows with the pattern in row 1 andby comparing other rows that show sequentialchange of hinge position.

In these hypothetical examples, when otherrelations are constant, the degree of protractionand retraction of the symphysis during protrac-tion and retraction of the upper jaw is increasedby: (1) increased vertical distance of hinge Aabove hinge B (compare rows 2 and 1 of Table2); (2) caudal shift of hinge B toward a positiondirectly ventral to hinge axis A (compare rows 6,

1, and 5); (3) a more dorsoventrally depressed orslender bill (i.e., dorsal and ventral bars, andtherefore hinges C and D, closer together, com-pare rows 1 and 15); (4) a rostral shift of hingeD relative to hinge C (compare rows 9, 1, and10); (5) rostral shift of both hinges C and D(compare rows 11, 12, 1, and 12).

For an understanding of kinesis in some speciesit will be important to note that rotation of thesymphysis during kinetic motions of the upperjaw is minimal or absent when hinge B lies di-rectly between hinges A and D, that is, on a linejoining A and D in lateral view (Figure 7). Thisconfiguration applies to row 7 of Table 2, and itis approximated in row 13. In these examples itis clear that there is little or no bending at hingeC, and that that hinge could be lost, producingproximal rhynchokinesis, without detriment tokinesis.

Certain configurations of A, B, C, and D wouldcause antagonistic motion of the bill tip—down-ward rotation during protraction of the upperjaw, upward rotation during retraction, or both.These detrimental motions would occur duringkinesis if hinge B lay dorsal to a line passingthrough hinge axes A and D during kinesis. Thisconfiguration applies to row 8 of Table 2. Ref-erence to Figure 7 will show that such a dorsalposition of B would result from rostral migrationof hinge B along the dorsal bar until B passedline AD. Hinge A lies dorsal to the level of hingeB in doubly rhynchokinetic birds, and theamount of hypothetical forward shifting of hingeB that is possible before the hinge crosses lineAD is proportional to the vertical distance be-tween hinges A and B. The position of line ADrelative to hinge B changes during kinetic mo-tions of the upper jaw in a given species, but lineAD probably does not normally cross hinge B inthe hinge configurations of living birds, as it doesat maximum retraction in the example in row 7of Table 2. It is clear that any location of hingeB rostral to A but ventral to line AD produces acomplementary effect on bill tip bending duringkinesis (Figure 8a; Table 2, rows 1, 5, 6) but thata more rostral location of hinge B produces the

NUMBER 395 15

TABLE 2.—Hypothetical effects of different configurations of hinges A, B, C, and D on bendingat the symphysis during protraction and retraction of upper jaw. Rows show degrees ofprotraction or retraction around hinge C at given degrees of kinetic rotation around hinge B(hinge configurations correspond to Figure 7; italicized numbers = degrees of reversed rotationaround hinge C)

* Hinge configuration:1 A B C D 5 A B'C D2 A'BCD 6 AB2CD3 A2B C D 7 AB'CD4 A'BCD 8 A B4C D

Hingeconfiguration*

123456789

10111213141516

Protraction

8°

6.54.00.52.59.04.01.01.55.0

10.53.57.02,04.0

17.09.0

4°

3.01.00

2.04.52.00

1.02.55.01.03.01.02.07.53.5

2°

1.00.50.50.52.00.50

1.01.01.51.02.00

0.53.01.5

Retraction

4°

2.51.50.51.54.01.00

1.52.02.52.03.50.51.07.03.0

6°

3.52.01.02.56.01.50

2.52.54.02.55.01.02.09.04.0

8°

4.52.01.54.07.02.00.54.03.05.03.06.51.02.5

11.05.0

9 ABC D1

10 A BC D2

11 A BCD5

12 ABC2D4

13 A4BCD14 A'BCD15 A BCD5

16 A'BCD5

rw ..*:

FIGURE 7.—Hinge positions in hypothetical, doubly rhynchokinetic upper jaw lacking hinge E(alternate positions of hinges A, B, C, and D are numbered; solid lines show jaw in closedposition; dotted line connects hinges A and D; dashed lines show other bill shapes; see Table 2for kinetic effects).

opposite effect (Table 2, row 8). In addition, ashinge B approaches hinge C, an increasinglysharp kink in the dorsal bar between the twohinges would appear during retraction of the

upper jaw (Figure 8b). I think it is for thesereasons that hinge B typically lies only a shortdistance rostral to hinge A in doubly rhynchoki-netic birds.


FIGURE 8.—Kinetic effects of rostral shift of hinge B: a, innormal position of B, retraction of symphysis complementsretraction of jaw; b, with hypothetical rostral shift of B,symphysis protracts during retraction of jaw. (Dashed lineshows long axis of dorsal bar in closed position; dotted linesshow long axis of retracted ventral bar.)

Complementary bending of the symphysis alsodecreases and eventually gives way to reversebending as the vertical distance between hingesA and B is reduced and hinge B lies dorsal ratherthan ventral to line AD (see Table 2, rows 3 and4). In rhynchokinetic birds, differences in therelative positions of hinges A and B are typicallyas shown at A, A1, A4, or A5 rather than at A2

or A3 in Figure 7, and the likelihood of reversedbending of the symphysis as a result of line ADfalling below hinge B is therefore slight.

The preceding discussion of particular hingeconfigurations is based on hypothetical patterns,but the patterns were chosen to approximateconfigurations found in a variety of species ofrhynchokinetic birds. For example, in 12 doublyrhynchokinetic species of nine families for whichI plotted the pattern of hinges on paper, all hadconfigurations in which complementary motionof the symphysis would be comparable to thoseshown in Table 2 (rows 1, 2, 6, 9, 10, 12, 14-16). The species included were Eudocimus albus,Grus canadensis, Eurypyga helias, Pluvialis squatar-ola, Vanellus indicus, Himantopus mexicanus,Jacanaspinosa, Nycticryphes semicollaris, Tringa Jlavipes,

Ducula bicolor, Columba speciosa, and Goura scheep-makeri.

PROKINESIS, AMPHIKINESIS, AND DOUBLERHYNCHOKINESIS.—During retraction of the up-per jaw the backward pull of jaw muscles on thepalate applies tension forces to the ventral bar,and during protraction of the jaw, compressionforces are applied. The upper jaw resists defor-mation under these forces on the ventral bar invarying degree depending upon the flexibility ofthe bars and the amount of ossification aroundthe nares. Birds with relatively small nasal open-ings have correspondingly rigid bills, and areprokinetic. The prokinetic upper jaw is com-monly constructed to withstand bending underthe forces of grasping or biting along the tom-ium, or breakage under compression forces (asin woodpeckers). This type of bill is also easilymodified for ornamental purposes without im-pairing its other functions (Hofer, 1955).

In some prokinetic birds the nasal openingsreach back to the level of the craniofacial hinge(see Figure 3). This feature appears to haveevolved under different circumstances. It isfound in certain philydorine ovenbirds (Furna-riidae, e.g., Philydor guttulatus) and woodcreepers(Dendrocolaptidae, e.g., Sittasomus griseicapil-lus)—groups that have apparently evolved fromproximally rhynchokinetic furnariids (Feduccia,1973). These prokinetic birds exhibit a flattenedventral bar and caudally extended nares thatprobably reflect their rhynchokinetic ancestry.By contrast, in Hoopoes (Upupidae) the naresreach the craniofacial hinge, but the upper jawis extensively ossified and the ventral bar stronglyconstructed; their nearest relatives, the woodhoopoes (Phoeniculidae) and other Coraci-iformes are prokinetic, with nares that do notreach the craniofacial hinge. The backward ex-tension of the nares in the Upupidae is thusderived from prokinetic ancestors and probablyhas nothing to do with kinesis.

Some rails (Rallidae) are amphikinetic, withjaws constructed of slender bars and with largenasal openings. In them the dorsal and ventralbars are flexible caudal to the symphysis and the

NUMBER 395 17

nasal openings extend caudally almost to thecraniofacial hinge. I found the amphikinetic up-per jaw only in the genus Rallus and in the lateQuaternary rail, Capellirallus, of New Zealandshown in Figure 9 (also see Olson, 1975; 1977).In these genera, the lateral and ventral bars arerelatively independent of the dorsal bar, eventhough the nasal opening does not reach caudallyas far as the craniofacial hinge. The lateral bar isflexible at its juncture with the dorsal bar justrostroventral to the craniofacial hinge (Figure3/). As a result, forces applied to the ventral barduring protraction or retraction of the palateproduce rotation of the symphysis relative to thedorsal and ventral bars, and in addition, rotationof the upper jaw around the craniofacial hinge(demonstrated in soaked skulls). During protrac-tion and retraction the angle between the lateraland dorsal bars (from lateral view) decreases orincreases, respectively, reflecting independentmotion of the ventral and lateral bars and motionof the bill tip. Rotation of the bill tip reduces theeffect of forces from the palate on rotation ofthe dorsal bar around the craniofacial hinge. Thepresence of a dorsal hinge on the lateral barwithin the upper jaw, separate from the completecraniofacial hinge, suggests that amphikinesis inrails was derived from prokinesis.

Amphikinesis may be more widespread amongbirds with large nasal openings and slender dorsaland ventral bars, but it would be difficult toidentify unless hinges C and D were morpholog-ically distinct. Hofer (1955:114) stated that thedorsal bar was flexible in Gavia (loon) and Podi-ceps (grebe), but I could not verify that in water-soaked skulls.

As a consequence of the flexibility of the upperjaw in amphikinetic and doubly rhynchokineticbirds with hinge E, their jaws are less suited forstrong biting along the tomium than those ofmost prokinetic birds. However, as I demon-strated with a simple model of the upper jaw,they are capable of several different forms ofgrasping with the bill tip that make even slenderbills unusually versatile. In the model, the sym-physis can bend down around a simulated preyitem to meet the partially depressed lower jaw,with or without depression of the dorsal bar. Thesymphysis can also bend down to meet the closedlower jaw even when the dorsal bar is raised.When prey is grasped, the response of these weakupper jaws is apparently to "wrap around" theprey (Figure 10). It is of interest to compare thehypothetical consequence of the loss of hinge Ein an amphikinetic jaw with that in a doublyrhynchokinetic one (see Figure 11). If the upperjaw were strengthened by loss of E, an amphiki-netic jaw would then become prokinetic. By con-trast, loss of hinge E in a doubly rhynchokineticjaw would strengthen the jaw without removingmobility of the symphysis; however, the "wraparound" action would no longer be possible be-cause it would require shortening of radius AD.

PROXIMAL RHYNCHOKINESIS.—Many proxi-mally rhynchokinetic birds probably evolvedfrom doubly rhynchokinetic ancestors, that is,from birds with at least hinges A, B, C, and D,by loss of hinge C (Figure 12, compare d and e).The ventral bar in most rhynchokinetic forms,unlike that of most prokinetic birds, is flattenedand flexible, either as a localized hinge at D oras a more extensive zone of flexibility (Figure 12,

FIGURE 9.—Amphikinetic upper jaw of Capellirallus (solid pointer indicates craniofacial hinge;open pointer indicates hinge near bill tip; arrow shows bending point on lateral bar).


FIGURE 10.—Versatility of kinesis in amphikinetic jaw withhinge E; bill tip can "wrap around" prey with lower jaw open(above) or closed (below) (dashed line shows long axis ofclosed jaws).

FIGURE 11.—Effect of loss of hinge E on retraction ofamphikinetic and rhynchokinetic jaws: a, amphikinetic jawwith E; b, amphikinetic jaw lacking E; c, doubly rhynchoki-netic jaw lacking E. (Dashed line shows position of closedupper jaw; dotted line shows long axis of retracted ventralbar; arrow shows retraction force.)

compare b and/with a and e). Loss of hinges Cand E would cause akinesis if hinge D wererepresented by a narrowly restricted bendingzone because of divergence between arcs AD andBD. Instead, the flexibility of the ventral bar isusually more extensive and it probably bends as

if there were multiple hinges along its length.Stresses that would arise within the upper jawduring kinesis from the double hinges A and Bin the absence of hinge E would be partiallyalleviated by the presence of extensive flexibilityin the ventral bar. An example of this configu-ration is the Limpkin (Aramus: Figure 12?).

The effect of extensive flexibility of the ventralbar can be simulated most simply by a modelwith two hinges along the bar as shown in Figure13. Protraction is probably weakened by thepotential for buckling of the ventral bar undercompression (Figure 13b), but retraction is notnecessarily weakened because a flexible bar maybe capable of transmitting strong tension forces(Figure 13c). During retraction, however, theventral bar could bend in a complicated waydepending upon the configuration of the hingesand the amount of retraction. Such bending isapparently negligible in proximally rhynchoki-netic birds for a variety of reasons: hinges A andB are often in close apposition, hinge B may lieclose to a line joining hinges A and D' (Figure13a), or the flexible portion of the ventral barmay extend caudally such that hinge D' becomesa functional analog of hinge E. Furthermore, theextent of retraction in living birds is probablynot great. In a hypothetical model, an awkwardbowing of the ventral bar becomes more pro-nounced as the vertical distance of hinge A aboveB is reduced, or as hinge B shifts rostrally awayfrom hinge A. In paleognathous birds, hinge Alies on or below the long axis of the dorsal bar,and B lies farther rostral along the dorsal barthan in other birds. Downward bowing of theventral bar during retraction (as shown in Figure13d) and separation of the palate from the sphen-oidal rostrum would therefore occur in paleog-nathous birds during retraction of the upper jawwere it not for the presence of an interruptedlateral bar or hinge E. (Figure 13 shows a hypo-thetical situation in which hinge E is absent.)

The Tooth-billed Pigeon (Figure 12b) is prox-imally rhynchokinetic, lacks hinge E, and has anarrowly restricted hinge at D. It is thus theoret-ically akinetic, as mentioned on page 13. How-

NUMBER 395 19

FIGURE 12.—Jaws of some rhynchokinetic and prokinetic birds: a, Ducula bicolor; b, Didunculusstrigirostris; c, Raphus cucullatus; d, Grus leucogeranus; e, Aratnus guarauna;/, Furnarius leucopus;g, Xiphorhynchus guttatus. (Solid pointer indicates craniofacial hinge; open pointers indicateother bending points or zones.)

ever, in this species hinges A and B are not widelyseparated, and hinge B lies on a line connectinghinges A and D when the bill is closed; diver-gence of arcs AD and BD during protraction orretraction is therefore minimal (Table 2, row 7).Thus, the theoretical restrictions on kinesis areessentially removed within the normal range ofkinetic rotation of the dorsal bar by the specialconfiguration of hinges A, B, and D.

In the proximally rhynchokinetic Black Skim-mer (Rynchops niger), hinges A and B are widelyseparated, but the ventral bar is extensively flex-

ible, hinge E is well developed, and line ADpasses through hinge B. These combined fea-tures maximize kinetic mobility in skimmers (seeZusi, 1962) by removing the opposition to pro-traction inherent in the proximally rhynchoki-netic upper jaw.

Proximally rhynchokinetic species commonlyexhibit a configuration in which line AD passesthrough, or nearly through, hinge B, minimizingthe tendency for internal bending of the upperjaw during kinesis. Such was the case in eightspecies of seven families for which I plotted the

20

D D1

FIGURE 13.—Kinetic properties of proximal and centralrhynchokinesis (hinge E lacking; extensive flexibility of ven-tral bar (D-D'); a-c, proximal rhynchokinesis): a, upper jawm closed position; b, upper jaw protracted; c, upper jawretracted; d, hypothetical centrally rhynchokinetic jaw re-tracted; rostral position of B and ventral position of Aproduce kink in ventral bar. (Dashed line shows closedposition.)

hinge positions on paper (Turnix sylvatica, Dromasardeola, Attagis malouinus, Rynchops niger, Pteroclesbianctus, Didunculus strigirostris, Furnarius leuco-pus, Margarornis rubiginosw). Six species (Chionusalba, Cursorius coromandelicus, Alle alle, Aramusguarauna, Sterna hirundo, Larus Philadelphia)from five additional families more closely ap-proached the configurations typical of doublyrhynchokinetic species.

DISTAL RHYNCHOKINESIS.—This form of ki-


nesis occurs only in certain charadriiform birds,in kiwis (Apteryx), and possibly in some humming-birds. The dorsal bar bends just caudal to thesymphysis rather than at or near its juncture withthe cranium. The distally rhynchokinetic upperjaw of charadriiform birds and kiwis is usuallyrigid because the dorsal bar is strengthened andhinge B is lost. At the same time the jaw remainscapable of powerful gaping or grasping at thetip.

Loss of hinge B imposes certain requirementson a kinetic jaw: the ventral bar must be flexiblecaudal to the symphysis and the base of the lateralbar (hinge E) must be flexible, or the bar incom-plete. Should hinge E be lacking, then point Dwould have to follow an arc of radius AD, movingessentially perpendicular to the long axis of therigid dorsal bar (Figure 14). However, point Dwould also have to follow an arc of short radius,CD, and move in a direction that is initiallyalmost parallel to the long axis of the dorsal barOnly through the flexibility of hinge E can thisconflict be resolved such that the ventral bar(and point D) follows the arc of radius CD.

EXTENSIVE RHYNCHOKINESIS.—This form ofkinesis is characterized by a lack of hinges B andC m the dorsal bar. Instead the bar is dorsoven-trally flattened throughout its length and bendsevenly between the symphysis and mesethmoid.This is an uncommon form of kinesis; I found itonly in some tinamous, some specimens of oys-tercatchers (Haematopus), some specimens ofturnstones (Arenaria), and in the Banded Stilt(Cladorhynchus) and avocets {Recurvirostra). Otherspecies with gracile construction of the dorsal bar

FIGURE 14.—Diagram of distally rhynchokinetic jaw (hingeE allows D to move along arc of radius CD rather than AD;arrows show motions of ventral bar).

NUMBER 395 21

closely approach extensive rhynchokinesis andthey may show slight bending along that bar, butI include them with other kinetic types accordingto the pattern of their localized hinges. Examplesof species that approach extensive rhynchokinesismay be found among the following kinetic types:central or proximal rhynchokinesis (some tina-mous, the White-breasted Mesite (Mesitornis var-iegata), the Lesser Painted Snipe (Nycticryphes sem-icollaris), some Furnariidae); double rhynchoki-nesis (some tringine sandpipers (e.g., SpottedSandpiper, Actitis macularia), some plovers (Char-adriidae), some pigeons (Columbidae)); and dis-tal rhynchokinesis (some specimens of oyster-catchers and turnstones, and the Buff-breastedSandpiper, Tryngites subruficollis).

Extensively rhynchokinetic species differ fromeach other in their patterns of jaw structure. Intinamous the ventral bar is extremely flattenedin the frontal plane throughout its length, andthe lateral bars are flexible at both ends andweakly connected to the cranium and ventralbars. In oystercatchers and turnstones some spec-imens are extensively rhynchokinetic but othersshow a hinge near the symphysis and are distallyrhynchokinetic. Hinge E is present and the ven-tral bar is flexible within its rostral half. In theBanded Stilt (Cladorhynchus) and avocets (Recur-virostra), E is absent and the ventral bar is flexiblein its rostral half (Cladorhynchus) or only near thesymphysis (Recurvirostra). Thus we see that exten-sive rhynchokinesis occurs in association withfour different hinge patterns and is present inonly four families. I anticipate that extensiverhynchokinesis will be shown to have differentadaptive explanations among the four families,and will prove to represent a specialized, ratherthan an unspecialized, form of rhynchokinesis.

CENTRAL RHYNCHOKINESIS.—This form of ki-nesis is characteristic of the paleognathous birds,including at least the Struthionidae, Rheidae,Casuariidae, some Tinamidae, and probably themoas (Dinornithiformes) and elephantbirds (Ae-pyornithiformes) (see illustrations in Archey,1941; Parker, 1895; Lamberton, 1930). Someauthors have regarded the ratites as akinetic and

others have postulated limited or passive kinesis.By manipulating the jaws of fresh specimens ofStruthio camelus, Rhea americana, and Casuariuscasuarius, I found that the upper jaw can bendupward and slightly downward at the axes shownin Figure 4. Whether or not ratites actively pro-tract the upper jaw above the closed position, theflexibility of their upper jaws indicates kinesis. Afully developed kinetic mechanism is necessaryto counteract upward forces on the flexible up-per jaw, to effect a strong grasp, and to achievesome downbending of the upper jaw duringgrasping.

Most tinamous possess hinges A and B; thecomplete lateral bar meets the ventral bar by aweak syndesmosis and bending occurs near thejunction of the two bars (hinge E). In ratites, thelateral bar is incomplete and partially ligamen-tous. The ligament of the Ostrich (Struthio) liesat the base of the lateral bar; in rheas (Rhea,Pterocnemia) the ligament is near the cranial at-

Q

FIGURE 15.—Retraction of jaw in prokinetic and centrallyrhynchokinetic birds: a, prokinetic; b, centrally rhynchoki-netic. (Note difference in angle of upper to lower jaw.)


tachment of the lateral bar; in cassowaries (Cas-uarius) it is near the middle of the bar; in Emus(Dromaius) the bar is largely ligamentous; and inkiwis (Apteryx) the lateral bar may closely ap-proach the ventral bar, but there is no ligamen-tous connection. Thus, as explained by Bock(1963), all ratites have flexibility in the inter-rupted lateral bar that permits craniocaudal mo-tion of the ventral bar, independent of the dorsalbar. The long, straight, rostral extension of thesphenoidal rostrum characteristic of paleognathsforms a gliding plane for the vomers, which inturn are attached to the maxillary bones; thebasal portion of the ventral bar of the lower jawis therefore restricted to rostrocaudal motion. Ifa complete lateral bar lacking hinge E were pres-ent in ratites, the basal portion of the ventral barwould be forced to rotate upward or downward

around hinge A, compressing the vomers againstthe rostrum during protraction and separatingthe palate from the rostrum during retraction.Such inefficient motions do not occur becausethe lateral bars of ratites are incomplete. Thelateral bar in tinamous is complete but it meetsthe ventral bar almost vertically and the directionof motion of its distal end is thus primarily ros-trocaudal.

In paleognathous birds, the rostral location ofhinge B, accompanied by extension of the mes-ethmoid or partial ossification of the nasal sep-tum, provides a greater angle between upper andlower jaws during a given retraction of the upperjaw than would obtain in a comparable prokineticbird (Figure 15). This configuration may in-crease the efficiency of grasping by the flexibleupper jaw.

FIGURE 16.—Upper jaw of schizorhinal hummingbird (Campylopterus largipennis): above, lateralview; below, dorsal view. (Solid pointer indicates craniofacial hinge; open pointer shows rhyn-chokinetic hinge; arrow indicates equivocal bending.)

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HUMMINGBIRDS.—Hummingbirds of a fewgenera are apparently prokinetic (e.g., Phaethor-nithinae: Glaucis, Threnetes, Ramphodon, Phaethor-nis, Eutoxeres), but most are proximally rhynchok-inetic. Hinge axes A and B, however, are notwidely separated relative to the length of the bill,and hinge A is not elevated markedly above B(Figure 16). It is thus doubtful that, during ki-nesis, the double hinges of most hummingbirdsproduce enough stress within the upper jaw torequire distal bending. Immediately rostral tothe craniofacial hinge, the dorsal bar is thickenedand it supports bony flanges on either side thatare associated with the nasal passages. Fartherrostrad the dorsal bar becomes dorsoventrallyflattened, and, with the two laterally compressedventral bars, forms an inverted trough that con-tains the tongue and most of the closed lowerjaw. Extensive flattening of the rostral portionof the dorsal bar suggests flexibility in the distalportion of the jaw in all hummingbirds. A fewgenera (e.g., Coeligena, Ensifera) have lost hingeB and thus resemble the configuration of distalrhynchokinesis, with an extended anterior hinge(C). However, hummingbirds differ from all dou-bly or distally rhynchokinetic birds in having theflattened surface of the ventral bars orientedvertically in opposition to the direction of bend-ing, rather than horizontally. Thus the osteolog-ical evidence does not point clearly to a particularkind of kinesis. I noted no bending within theupper jaw while manipulating fresh specimens ofCalypte and Mellisuga, and in hummingbirds thereis no line of softer rhamphotheca between thedorsal and ventral bars comparable to that foundin all other rhynchokinetic birds in relation tothe independent motion of the ventral bar. Itentatively conclude that most hummingbirds areproximally rhynchokinetic.

In living hummingbirds an illusion of bill-tipmotion in the upper jaw occurs during a slightdepression of the largely ensheathed lower jawbecause only the tips of the mandibles separate.The problem of hummingbird kinesis might bestbe solved from photographs of opened andclosed bills of live birds taken in lateral view.

Evolution of Rhynchokinesis

ADAPTIVE ASPECTS OF RHYNCHOKINESIS

Up to now I have dealt mainly with anatomicaland functional properties of kinesis in the upperjaw. The functional property common to rhyn-chokinetic skulls is obligatory bending within thejaw during kinesis. How this relates to the diversefeeding adaptations found among rhynchoki-netic birds is largely unknown and can only betouched on here. Many rhynchokinetic and am-phikinetic birds probably have a special need fordownbending of the distal part of the upper jawas a consequence of the shape and use of theirbills. Many of them employ probing in soft sub-strates as part of their feeding patterns. Theirbills are consequently slender, without a hook orabrupt curvature at the tip, and are capable ofstrong grasping only through retraction of thesymphysis of the upper jaw. Bending at the tippermits withdrawal of animals or plants frommud or sand. In addition, the flexible tip may beused to push food into the mouth as describedby Burton (1974) for snipe.

The importance of probing as a feedingmethod in many distally rhynchokinetic birds iswell known (e.g., woodcock, snipe, godwits, dow-itcher, calidridines, oystercatchers, kiwi). Prob-ing is also an important element in the feedingpatterns of the amphikinetic rails (Rallus:Meanly, 1969; Bent, 1926), and in the doublyrhynchokinetic ibises (Threskiornithidae: Kush-lan, 1977; Raseroka, 1975), cranes (Gruidae:Walkinshaw, 1949; Allen, 1952; Walkinshaw,1973), kagus (Rhynochetidae: Steinbacher,1962), plovers (Charadriidae: Burton, 1974), andtringine sandpipers (Scolopacidae: Burton,1974).

Although I have emphasized downbending ofthe bill tip, the possible importance of upbendingof the symphysis during protraction of the upperjaw in all forms of rhynchokinesis, except proxi-mal rhynchokinesis, should not be overlooked.Bending of the upper jaw allows a bird to graspa larger food item with the tip of the bill than it


could without such bending—a feature of possi-ble importance to fruit-eating pigeons.

Proximally rhynchokinetic birds generallyhave feeding patterns that include little, if any,probing, but that require a stronger bill orsharper tomia for biting or grasping. Limpkins(Aramidae) deliver blows to mussel shells andlarge snail opercula (Snyder and Snyder, 1969);coursers and pratincoles (Glareolidae) take manylarge, hard-bodied insects (Maclean, 1976); CrabPlovers (Dromadidae) grasp crabs in the bill andbatter them to death or insensibility before swal-lowing (Gilliard, 1958); Sheathbills (Chionididae)rip open the skin from carcasses of penguinchicks and adults (Burger, 1981); seedsnipe(Thinocorus) bite pieces off succulent leaves andgraze other forms of vegetation (Maclean, 1969);gulls, skuas, jaegers, terns, skimmers, and alcidsoften take large prey that require a strong grasp,and terns, skimmers, and alcids carry slipperyprey in the bill from feeding sites to the nestingcolony. In all of these birds rhynchokinesis mayhave more phylogenetic than adaptive signifi-cance.

The adaptive significance of rhynchokineticjaw structure is essentially unknown for the mes-ites (Mesitornithidae), button quails and hemi-podes (Turnicidae), sunbitterns (Eurypygidae),ibisbills (Ibiborhynchidae), jacanas (Jacanidae),painted snipe (Rostratulidae), plains wanderer(Pedionomidae), sandgrouse (Pteroclididae), pi-geons and doves (Columbidae), ovenbirds (Fur-nariidae), New Zealand wrens (Xenicidae), andthe paleognathous birds.

ORIGIN OF RHYNCHOKINESIS

The origin of birds and the evolution of aviancranial kinesis are still matters of controversy andspeculation. Walker (1972) presented evidencefor the common origin of birds and crocodiliansfrom a thecodont ancestor, and he argued thatthe structure of the skull in modern and fossilcrocodiles suggested a former prokinesis, similarto that of birds, that was subsequently lost incrocodiles. By contrast, Ostrom (1973, 1976)

regarded Archaeopteryx as a derivative of a coe-lurosaurian dinosaur, and Colbert and Russell(1969) thought that Dromaeosaurus albertensis, acoelurosaurian, was mesokinetic. Versluys(1910), Bock (1964), and Wellnhofer (1974)thought it most likely that Archaeopteryx was me-sokinetic, but Whetstone (1983) studied a newpreparation of Archaeopteryx and concluded thatit was not metakinetic, mesokinetic, prokinetic,or rhynchokinetic, without precluding the pres-ence of some form of kinesis. Disagreementsamong these authors regarding kinesis stem fromthe equivocal interpretation of the presence ofarticulations or flexibility at several critical pointsin the somewhat crushed or incomplete fossils.

Unlike Archaeopteryx, coelurosaurs, or theco-donts, all modern birds and the Cretaceoustoothed birds lack bony connections of the preor-bital and postorbital bars with the jugal bar, andthe external naris has enlarged or shifted cau-dally at the expense of the antorbital fenestra.Freedom of motion of the jugal bars is essentialfor all of the known forms of avian kinesis andfor the peculiar maxillary kinesis hypothesizedfor Hesperornis by Gingerich (1976). Bending ofthe dorsal and ventral bars in the region of theexternal nares of both reptiles and birds wouldconstitute rhynchokinesis; bending in the regionof the antorbital fenestrae would constitute pro-kinesis. There is nothing to prevent the devel-opment of prokinesis when teeth are extensivelydistributed along the ventral bar. However, thenecessity for a thin and flexible ventral bar in theupper jaw of rhynchokinetic and amphikineticbirds implies that these forms of kinesis evolvedafter the loss of teeth from the flexible portionof the premaxillary and maxillary bones of theventral bar, at least in the region of the externalnares. Various dinosaurs (e.g., Ornithomimus; seeRomer, 1956:153) and Hesperornis lacked teethin the rostral portion of the upper jaw. In Hes-perornis the only changes necessary to producerhynchokinesis would be interruption of the lat-eral bar and flexibility in the dorsal and ventralbars. Thus, both prokinesis and some form ofrhynchokinesis could have been among the firstforms of avian kinesis.

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The schizorhinal skull of neognathous birdsexhibits a complicated configuration of bendingzones near the base of the upper jaw in whichtwo hinge axes are separated from each other inthree dimensions—rostrocaudally, dorsoven-trally, and mesiolaterally. Neognathous rhyn-chokinesis is absent from most living birds, fromall fossil birds, and Archaeopteryx, and from cro-codilians and coelurosaurian dinosaurs, and it isthus probably a derived state within birds. In thediscussion that follows I shall assume that neog-nathous rhynchokinesis evolved from holorhinalancestors. To understand the evolutionary originof schizorhiny and rhynchokinesis we must there-fore explain the rostral shift of the medial por-tion of the craniofacial hinge. In a hypotheticalmodel, a rostral shift is incompatible with kinesisunless the nasal opening extends back to, ornearly to, the original craniofacial hinge. For thisreason the ancestor from which neognathousrhynchokinesis evolved was most likely proki-netic with large nasal openings, or amphikinetic.

Two anatomical changes would serve to sepa-rate the craniofacial hinge into two hinge axes.One is a forward extension of the mesethmoidunder the dorsal bar. The flexible zone of thedorsal bar would also shift rostrally from theoriginal craniofacial hinge with extension of themesethmoid; otherwise retraction of the upperjaw would be blocked. The other change is ashift of the dorsal bar ventrally toward the ven-tral bars. The first change would separate thecraniofacial hinge horizontally and the secondwould separate it vertically. In many neognath-ous, schizorhinal birds both changes have appar-ently occurred, with the result that the hinge ofthe dorsal bar lies rostroventrad from the origi-nal craniofacial hinge axis.

Several possible explanations for extension ofthe mesethmoid come to mind: (1) to increasethe bony support for the olfactory membranesand conchae; (2) to act as a retractor stop bylimiting downward rotation of the dorsal barrostral to the hinge; (3) to increase the effect ofretraction of the palate on downbending of thesymphysis in flexible-billed birds by limitingdownbending at the craniofacial hinge; (4) to

increase the angle of the retracted upper jaw byshifting the dorsal bending zone toward the sym-physis, as in central rhynchokinesis (see Figure15).

The prokinetic bustards (Otididae) may serveas a model for an early stage of evolution ofschizorhiny or rhynchokinesis by rostral exten-sion of the mesethmoid. (Bustards do not neces-sarily represent such a stage; they may, in fact,be secondarily prokinetic.) In them the meseth-moid protrudes rostrally beyond the cranial at-tachment and bending axis of the lateral portionof the nasal bone. The external naris is large,but it does not reach the craniofacial hinge (Fig-ure 17). To judge from manipulation of water-soaked skulls of Neotis cafra and Choriotis kori, thecraniofacial hinge does not form a single trans-verse axis; rather, the medial portion lies some-what rostral to the lateral portion. The thin sheetof bone constituting the caudal border of thenaris bends during protraction or retraction,contrary to a hypothetical model in which bend-ing is not possible and kinesis is blocked. Thisbending and some flexibility of the flattenedventral bar allows a change in shape of the exter-nal nares during kinetic rotation of the upperjaw; the change is caused by motion of the lateraland ventral bars relative to the dorsal bar. Suchbending at the narial border might lead to phys-iological adaptation, and eventually evolutionaryadaptation, that would block the development ofossification in the region of bending and therebyextend the external naris caudally to produceschizorhiny. These changes might occur rapidlyin an evolutionary sense, leaving few, if any,examples of the intermediate stage among livingbirds. I hypothesize that the development ofschizorhiny in the manner just described mostlikely would occur in birds preadapted for rhyn-chokinesis by flexibility of the distal portion ofthe dorsal and ventral bars (hinges C and D),such that independent motion of the lateral anddorsal bars and bending at the narial borderwould be increased. In this way prokinesis couldlead to double rhynchokinesis through an am-phikinetic stage. The amphikinetic skull as itoccurs in Rallus is less likely to lead to schizorhiny


FIGURE 17.—Skull of Choriotis kori, left lateral view (arrows L and M indicate regions of bendingof lateral and medial portions of craniofacial hinge; curved arrow shows bending region ofnarial border; dotted outline represents mesethmoid).

because independent motion of the lateral barcan be fully developed within that configurationwithout modifying the caudal narial border.

The second change leading to schizorhiny andrhynchokinesis—an evolutionary ventrad shift ofthe dorsal bar—would produce a more slenderbill that might be advantageous for penetratingcrevices or flowers, or probing vegetation ormud. Comparison of the two ibises in Figure 18shows how shifts of the dorsal bar and changesin the mesethmoid relate to increased separationof the basal hinge axes. These shifts undoubtedlycan be reversed under selection for a stouter bill.For example, in adult spoonbills (Figure 18a) thesolid, paddle-like construction of the prokineticupper jaw is adapted for side-to-side sweepingthrough the water (Allen, 1942; Vestjens, 1975).The skeleton of a 54-day chick of the RoseateSpoonbill (Ajaia ajaja; USNM 554780) has ex-ternal nares that extend caudally beyond thecraniofacial hinge; its dorsal and ventral bars areunfused almost to the paddle-like symphysis, andthe dorsal bar is flattened and flexible caudal tothe symphysis (see also Hofer, 1955, fig. 14).The young spoonbill has a single craniofacialhinge axis, but the structure of the juvenile jawsuggests that spoonbills evolved from an ibis-likeform by fusion of the dorsal and ventral bars and

melding of hinges A and B into a single bendingaxis.

Once the rhynchokinetic jaw had evolved, itsfurther development would probably be guidedby selection for more efficient bending of the billtip, although such bending is not unique to rhyn-chokinetic birds. Bill tip motion in a bird lackinghinge E requires the presence of a second hingeaxis at the base of the bill (Figure 11). A fewdoubly rhynchokinetic birds have flexibility at E,but most apparently need the added strengthand stability afforded by thickening of the lateralbar at its junction with the ventral bar. Thepresence of a second basal hinge axis thus appearsto be a necessity for any bird that needs thetemporary grasping capacity afforded by bill-tipmotion as well as the stability afforded by theloss of hinge E. Natural selection would maintainor modify the double hinge, once evolved, be-cause of its functional relation to rhynchokinesis.

PATHWAYS OF EVOLUTION

In the absence of a fossil record of skull struc-ture in most rhynchokinetic orders we must relyon inferences about the evolution of morpholog-ical features from living species. Such inferencesrequire a knowledge of the mechanics of kinesis.

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FIGURE 18.—Bending zones at base of upper jaw in spoonbill (a) and ibises (b,c): a, Ajaia ajaja;b, Hagedashia hagedash; c, Eudocimus albus. (Solid pointer indicates craniofacial hinge; openpointer indicates rhynchokinetic hinge; see text for explanation.)


Before presenting a hypothetical scheme for theevolution of different jaw morphologies I willdiscuss the key questions: how did distal rhyn-chokinesis evolve?; how did proximal rhyncho-kinesis evolve?; how often did prokinesis re-evolve from rhynchokinesis?

DISTAL RHYNCHOKINESIS.—There is no me-chanical reason why distal rhynchokinesis couldnot evolve by forward migration of the medialpart of the craniofacial hinge (B) from a proki-netic ancestor with large external nares, if certaincombinations and configurations of hinges werealready present in the upper jaw. As noted ear-lier, kinesis would be blocked by the presence oftwo hinge axes at the base of the upper jaw unlessone of the following hinge combinations werepresent: hinge D in the form of extended flexi-bility of the ventral bar; hinges D and E (or aninterrupted lateral bar); hinges C, D, and E; orhinges C and D. I have already discussed theeffects on kinesis of a forward shift of hinge B ina jaw with hinges C and D (see Table 2); thehypothesized reversal of bill tip motion afterhinge B passed dorsal to line AD makes thispathway to distal rhynchokinesis extremely un-likely. We can also discard the first alternative,because kinesis would become increasingly awk-ward and inefficient as hinge B moved forward(Figure 13d).

I know of no way to choose between the othertwo possibilities by examination of any singledistally rhynchokinetic species, because the spe-cialized end-products of each alternative pathwaycould be the same. Comparison of related spe-cies, however, suggests that both pathways areunlikely. Assuming forward migration of hingeB from an ancestor with hinges D and E, onewould expect to find relatives of the distallyrhynchokinetic forms in different stages of mi-gration of hinge B. As a corollary, one would notexpect to find double rhynchokinesis to be theprevalent form of kinesis in relatives of distallyrhynchokinetic forms. By these criteria this path-way is virtually eliminated as a possibility for theScolopacidae and Haematopodidae, but it re-mains a viable explanation for the Apterygidae.

If the ancestor had hinges C, D, and E, we wouldexpect to find birds in which hinge B approachedhinge C to varying degrees, with the dorsal barstiffened caudal to hinge B. There is no supportamong the relatives of Scolopacidae, Haemato-podidae, or Apterygidae for this explanation.

Another route to distal rhynchokinesis wouldbe limited forward migration of hinge B (produc-ing schizorhiny) from an ancestor with hinges Cand D, followed by loss of hinge B. In this case,we would expect to find gradations of flexibilityat hinge B in different species, and many doublyrhynchokinetic relatives of the distally rhyncho-kinetic forms, with E present or absent. This iswhat we find for the Scolopacidae and Haema-topodidae, but not for the Apterygidae. Theprobable evolutionary route to distal rhynchoki-nesis in the Charadrii can be simulated by ar-ranging various species of the Scolopacidae in amorphocline from double rhynchokinesis tostrongly developed distal rhynchokinesis (Figure19a-d). An extensive forward migration of hingeB is not indicated; instead, the dorsal bar be-comes progressively thickened and distal rhyn-chokinesis arises by obliteration of hinge B. ThusI conclude that there is strong evidence for theevolution of distal rhynchokinesis from doublerhynchokinesis in the Charadrii, and weaker ev-idence, for lack of close relatives, of the evolutionof distal rhynchokinesis in the Apterygidae by asimple forward migration of hinge B.

It is worth noting that only one change wouldbe necessary to produce distal rhynchokinesisfrom an amphikinetic bird—loss of flexibility ofthe medial portion of the craniofacial hinge. Theresult would be a transfer of all protraction andretraction forces from the palate to the tip of thejaw via the lateral and ventral bars. However, Ihave found no amphikinetic birds among theclose relatives of distally rhynchokinetic ones.

PROXIMAL RHYNCHOKINESIS.—Evolution ofproximal rhynchokinesis by a limited forwardshift of the medial portion of the craniofacialhinge from an ancestor with no other hinges orwith only hinge D is unlikely because these com-binations would block kinesis (see page 12). Only

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FIGURE 19.—Morphocline from double to distal rhynchokinesis: a, Actitis macularia; b, Philo-machus pugnax; c, Calidris alpina; d, Limnodromus griseus. (Solid pointer indicates craniofacialhinge; open pointers show additional hinges; arrow shows reduced hinge.)

in the event that hinge B shifted forward alongthe path of a line joining hinges A and D wouldkinesis remain effective. However, kinesis wouldnot be blocked if hinge D were extensively flex-ible or if hinges D and E were present. Similarly,a doubly rhynchokinetic bird could becomeproximally rhynchokinetic through loss of hingeC, without blocking kinesis, if hinge D wereextensively flexible or if hinges D and E wereboth present. A flattened and extensively flexibleventral bar is a feature commonly found in rhyn-chokinetic birds, but in prokinetic birds, otherthan certain Passeriformes, it is found mainly ingroups that may be secondarily evolved fromrhynchokinetic ancestors. Hinge E is also rare inprokinetic forms. Thus the evolution of proximalrhynchokinesis directly from a prokinetic formis unlikely because of mechanical restrictions,and there is no clear example of it among birds.Derivation of proximal rhynchokinesis from adoubly rhynchokinetic ancestor by a subsequent

loss of hinge C is therefore the most likely path-way because these birds already have a flexibleventral bar, and sometimes hinge E as well.

Proximal rhynchokinesis occurs in three fam-ilies of Gruiformes, many Charadrii, the Lari andAlcae, the Columbiformes, the Trochilidae, andthe Furnariidae (Table 1, page 6). The preva-lence of doubly rhynchokinetic forms in theGruiformes, Charadriiformes, and Columbi-formes further supports a hypothesis of the de-rivation of proximal rhynchokinesis from doublerhynchokinesis in those orders. The Furnariidaeremain equivocal because, to judge from osteol-ogy alone, they appear to lack doubly rhyncho-kinetic species. However, some have slender billsthat may in fact be doubly rhynchokinetic.Though many have hinge E, in some it is poorlydefined and some lack it.

A return to prokinesis does not necessarilyfollow the secondary evolution of proximal rhyn-chokinesis. As long as there is no need for strong


biting along the ventral bar, the bar can remainflexible. There is also no need to reduce hingesA and B to a single axis if their effects on kinesisare essentially neutralized by appropriate config-urations of hinges A, B, and D. On the otherhand, if the bill were regularly stressed by pound-ing, prying, strong maxillary biting, or someother use, the ventral bar would probably beheavily ossified and the upper jaw would be aninflexible unit. A return to a single craniofacialhinge axis would then be the most efficient meansof maintaining kinesis (see Figure 12c,g).

PROKINESIS.—Prokinetic birds have appar-ently evolved from rhynchokinetic ancestors insome instances. The following taxa are especiallypertinent to this problem because of their asso-ciation with rhynchokinetic forms in current clas-sification: Plataleinae (spoonbills), Heliornithidae(sun grebes and finfoots), Otididae (bustards),Cariamidae (seriamas), Psophiidae (trumpeters),Rallidae (rails and allies), Burhinidae (thick-knees), Pluvianus (Egyptian Plover), Phoenicop-teridae (flamingos—if included in Charadri-iformes), Raphus (Dodo), Phaethornithinae (her-mits), Dendrocolaptidae (woodcreepers), andXenicus (Bush Wren, Rock Wren). An evolution-ary return to prokinesis could be virtually unre-cognizable, as pointed out by Bock (1964), butone or more of the following features might beretained in a prokinetic bird of rhynchokineticancestry: (1) a flattened, flexible ventral bar; (2)an osteological gap or any other suggestion offormer separation of the lateral bar from thebase of the dorsal bar; (3) a rostral extension ofthe mesethmoid beyond the cranial attachmentof the lateral portion of the craniofacial hinge.

The first feature is developed to varying de-grees in the Otididae, Psophiidae, Rallidae, Bur-hinidae, Pluvianus, and Xenicus longipes, but it isnot necessarily evidence of former rhynchokine-sis because it also occurs in some prokinetic pas-seriform birds (e.g., some Troglodytidae (wrens),Mimidae (mockingbirds and allies), Turdinae(thrushes)) for which there is no other evidenceof rhynchokinetic ancestry. The second featureis seen only in the Plataleinae and in Raphus. Inthem the slit-like gap typically terminates at the

craniofacial hinge and it apparently indicates for-mer rhynchokinesis in Raphus because the cra-niofacial hinge is still slightly separated into twoaxes, and in Plataleinae for reasons given on page26. The third feature is pronounced only in theOtididae and Phaethornithinae. Prokinesis in theOtididae could be interpreted either as a prea-daptation for rhynchokinesis or as a modificationfrom rhynchokinetic ancestry. In hummingbirds,lack of dorsoventral flexibility in the ventral barsuggests that the protruding mesethmoid is nota sign of former rhynchokinesis. It may simplyserve as a support or retraction stop for the longbill in all hummingbirds.

DIRECTIONS OF EVOLUTION

The most probable sequence of evolutionarysteps to each form of kinesis is shown in Figure20, based on hypothetical mechanical conse-quences of a change from one form to the nextas presented in this paper. In general, I thinkthat evolutionary reversal, that is, direct returnto an immediately ancestral form of kinesis, oc-curred infrequently because a reversal of theinitial changes in morphology and function is notlikely to be advantageous. For example, if usedfor probing, a slender, prokinetic upper jaw withlarge nares might become amphikinetic and thenevolve toward double rhynchokinesis by forwardextension of the mesethmoid and hinge B, be-cause these changes would improve its functionas a probing and grasping instrument. A returnto amphikinesis or prokinesis would provide noadvantage in a probing bill. Proximal rhyncho-kinesis can evolve from double rhynchokinesisonly because of the presence of hinges associatedwith double rhynchokinesis. Specializations foruses other than probing reduce the chance of areturn to probing and double rhynchokinesis. Inthe evolution of distal rhynchokinesis, any lessen-ing of flexibility in hinge B and strengthening ofthe base of the dorsal bar of a doubly rhyncho-kinetic bird would increase its effectiveness inprobing, while reducing its efficiency in forcepsfeeding. Subsequent weakening of the dorsal barof a distally rhynchokinetic form, however,would not improve probing, and forceps feeding

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would not improve until hinge B were reconsti-tuted.

Paleognathous rhynchokinesis in birds couldhave evolved directly from some form of kinesisin reptilian ancestors, or it could have developedfrom avian prokinesis through a proximally rhyn-chokinetic stage. Hinge C is absent from adultpaleognathous birds and from juvenile skeletalspecimens of Rhynchotus, Struthio, Rhea, Dromaius,and Casuarius that I have examined; thus thehinge on the dorsal bar in paleognaths probablyrepresents part of an original craniofacial hingethat shifted forward through evolution, accom-panied by ossification of the underlying septum.There is no evidence that double rhynchokinesiswas involved in the evolution of paleognathousrhynchokinesis, as it was in many neognaths.Furthermore, the paleognathous birds differfrom rhynchokinetic neognaths in that the dorsalbar did not shift toward the ventral bar and awayfrom the level of the original craniofacial hingein the course of evolution. For these reasons andothers presented by Bock (1974), rhynchokinesisin paleognaths and neognaths probably evolvedby different pathways.

Discussion

This paper serves to introduce the complexi-ties of the rhynchokinetic, amphikinetic, and pro-kinetic skulls of birds without exploring theirmorphology in detail. It is intended to clarifyconcepts and terminology related to kinesis, tofocus attention on the unsolved problems in thisfield, and to stimulate new research.

I have shown that the double hinge axes of therhynchokinetic skull impose certain restrictionson kinesis of the upper jaw. The double hingeaxis is a significant feature in the analysis offunction of both schizorhiny and rhynchokinesis.By my definitions schizorhiny and holorhiny arereduced to partial synonyms of rhynchokinesisand prokinesis, respectively.

Much of the analysis of kinesis in this paper isbased on the mechanical properties of hypothet-ical models that assume inflexible bars connectedby pin hinges. The application of this method is

particularly successful within the Charadrii,many of which have well-defined and restrictedhinges and in which some of the functional prop-erties are easily understood and often clearlyrelated to specific feeding methods (Zusi, in prep-aration). In some other rhynchokinetic groupsthe theoretical conditions of the model are lessclosely approximated by the birds—hinges arenot well-defined, the inflexibility of "inflexible"bars is open to question, the adaptations involvedare not evident, and the configurations of hingesare theoretically detrimental to kinesis. I havenevertheless applied a consistent method of anal-ysis throughout the rhynchokinetic birds becausethe significance of morphological configurationsin difficult groups was clarified first by themodels. For example, the structure of the upperjaw in proximally rhynchokinetic birds was mostprobably derived from a doubly rhynchokineticancestor. This conclusion came from hypotheti-cal models that demonstrated the following: first,a simple step-wise derivation of double rhyn-chokinesis from prokinesis; second, a simple de-rivation of proximal rhynchokinesis from doublerhynchokinesis; third, the kinetic conflicts asso-ciated with proximal rhynchokinesis; and fourth,the different hinge configurations that wouldserve to overcome the conflicts. The presence ofsuch configurations in proximally rhynchokineticbirds was thus explained. It was not possible tounderstand the structure of the proximally rhyn-chokinetic skull, even with a full appreciation ofits functional properties and adaptive value, with-out reconstructing its probable morphologicalhistory. These conclusions could not have comeonly from manipulation of skulls or observationsof kinesis in living birds. The functional impli-cations of models have been essential for theirformulation.

Reference to Table 1 (page 6) reveals a highfrequency of probable evolutionary shifts fromdouble rhynchokinesis to proximal rhynchoki-nesis. This change is usually associated withstronger biting or pounding or with the takingof larger prey, and its prevalence is related to awide diversity of feeding habits among thesebirds. By contrast, the evolution of distal rhyn-


chokinesis from double rhynchokinesis is a rareevent outside the Charadrii and appears to bealmost exclusively associated with deep probingand the support of a long, slender bill. Foodresources that are obtainable by deep probingand that are also sufficiently concentrated andconstant to support the specialization of distalrhynchokinesis may be restricted to invertebratesin moist or wet soil, and nectar in long tubularflowers. The Charadrii have largely monopolizedthe former food source except in New Zealand,where the kiwi replaces the woodcock. Feedingon nectar in tubular flowers requires neither astiffened upper jaw nor bill-tip grasping. Thusdistal rhynchokinesis is not found in passerinenectar feeders and is poorly developed, if presentat all, in hummingbirds.

The analysis of kinesis has taxonomic applica-tions of several kinds. Through functional-mor-phological analysis this paper demonstrates theprobable directions of evolution in a complexmorphocline (Figure 20) and suggests polaritiesamong morphological states that could serve forphylogenetic analysis. Interpretation of polarityis somewhat clouded by the circular configura-tion of part of the morphocline, which makes thedetermination of the most primitive state diffi-cult and implies that convergence to that statehas occurred. Nevertheless, I have presented ev-idence that, within neognathous birds, amphiki-nesis is an evolutionary derivative of prokinesis,that double rhynchokinesis is derived relative toprokinesis, and that distal rhynchokinesis andmost or all cases of proximal rhynchokinesis arederived relative to double rhynchokinesis. Pa-leognathous rhynchokinesis may be derived rel-ative to avian prokinesis, or it may represent aprimitive state from an early radiation of paleog-nathous birds.

I have found that the origin and subsequentmodification of each of the forms of neognathousrhynchokinesis can be traced and explained bysimple steps. The probable evolutionary trans-formations of even the most specialized mor-phologies, such as those of the skimmers (Ryn-chops) and woodcock (Scolopax), can be readily

HOLORHINAL

PROKINESIS —

AMPHIKINESIS

SCHIZORHINAL

. CENTRAL" > RHYNCHOKINESIS —

PROXIMALRHYNCHOKINESIS

A

DOUBLERHYNCHOKINESIS

VDISTAL

RHYNCHOKINESIS

FIGURE 20.—Hypothetical evolutionary routes to differentkinds of cranial kinesis (dashed arrows refer to paleognath-ous birds; solid arrows refer to neognathous birds).

visualized. In this way, functional analysis is be-ginning to provide a rationale for the remarkablediversity in bill structure found in such orders asthe Gruiformes, Charadriiformes, and Columbi-formes. Still unexplained is the evolutionaryprocess by which the morphological diversity ofthese and other orders arose. This problem willrequire different approaches and methods. Butmany questions concerning the pattern of struc-ture and function of the upper jaw in birds alsoremain to be answered. These problems couldbest be solved in the immediate future by studyof the nasal region and its relation to bill struc-ture and function, by detailed comparative stud-ies of jaw structure within and among manyorders of birds, by accurate mapping of kineticmotions in a wide variety of species, by obtainingnew information on developmental anatomy ofthe jaws, by studies of kinesis in live birds, bycomparing detailed accounts of foraging behav-ior of rhynchokinetic birds and their prokineticand amphikinetic relatives, and by the discoveryof enlightening fossils.

Appendix

Species and Numbers of Skeletons of Rhynchokinetic Birds Examined

In addition to studies on the rhynchokinetic species listed below, compar-isons were made with a variety of prokinetic and amphikinetic birds, withemphasis on the following: Plataleinae, Psophiidae, Rallidae, Heliornithi-dae, Cariamidae, Otididae, Burhinidae, Glareolidae (Pluvianus), Raphi-dae, Trochilidae (Phaethornithinae), Dendrocolaptidae, Xenicidae (Xeni-cus).

TINAMIDAE: Tinamus too 2, 7. solitarius 1, T. major 3;Crypturellus dnereus 1, C. soui 4, C. undulatus 1, C.idoneus 1, C. cinnamomeus 2, C. boucardi 1, C. parvi-rostris 1, C. tataupa 3; Rhynchotus rufescens 4, Notho-procta perdicaria 1, Nothura maculosa 11, Eudromiaelegans 13.

STRUTHIONIDAE: Struthio camelus 3.RHEIDAE: Rhea americana 2, Pterocnemia pennata 2.CASUARIIDAE: Casuarius casuarius 2, C. unappendiculatus

2.DROMAIIDAE: Dromaius novaehollandiae 4.APTERYGIDAE: Apteryx australis 5.THRESKIORNITHIDAE: Threskiornis aethiopicus 8, T. melan-

ocephalus 1; Carphibis spinicollis 2, Nipponia nippon 1,Hagedashia hagedash 1, Harpiprion caerulescens 2,Theristicus caudatus 2, 7. branickii 1, 7. melanopis 1;Mesembrinibis cayennensis 2, Eudocimus albus 7, E. ruber3; Plegadis falcinellus 6, P. chihi 6, P. ridgwayi 1.

MESITORNITHIDAE: Mesitornis variegata 1, Monias benschi1.

TURNICIDAE: Turnix tanki 3, 7. suscitator 1, 7. varia 2.

EURYPYGIDAE: Eurypyga helias 5.GRUIDAE: Grusgrus 5, G. monacha 1, G. canadensis 10, G.

japonensis 2, G. americana 4, G. w/wo 1, G. antigone 4,G. rubicunda 1, G. leucogeranus 4; Bugeranus caruncu-latus 1, Anthropoides virgo 5, A. paradisea 4; Balearicapavonina 5, J5. rugulorum 1.

ARAMIDAE: Aramus guarauna 6.CHARADRIIDAE: Vanellus vanellus 6, V. armatus 4, V. j/>i-

noms 2, V. duvaucelii 1, V. tecftw 3, V. albiceps 2, V.coronatus 1, V. senegallus 3, V. cayanus 2, V. chilensis5, V. indicus 2, V. tricolor 1, V. OTJ/« 1; Pluvialisdominica 7, P. squatarola 5; Charadrius hiaticula 2, C.semipalmatus 7, C. placidus 5, C. dubius 2, C. wilsonia5, C. vociferus 5, C melodus 2, C. pecuarius 2, C.sanctaehelenae 4, C. tricollaris 1, C. alexandrinus 5, C.

collaris 2, C. falklandicns 3, C. mongolus 5, C. asiaticus2, C. modestus 4, C montanus 4; Anarhynchus frontalis2, Eudromias ruficollis 1.

GLAREOLIDAE: Rhinoptilus cinctus 1, /?. chalcopterus 1, Cur-sorius coromandelicus 1, G. temminckii 1; Glareola pra-tincola 1, G. maldivarus 2, G. nordmanni 1, G. nuchalis4, G. /actea 3.

DROMADIDAE: Dromas ardeola 3.CHIONIDIDAE: Chionis alba 5, C. minor 3.HAEMATOPODIDAE: Haematopus ostralegus 10, / / . bachmani

3, / / . leucopodus 5, / / . ater 7.RECURVIROSTRIDAE: Himantopus himantopus 5, H. mexi-

canus 5; Cladorhynchus leucocephalus 1, Recurvirostraavosetta 4, /?. americana 4.

IBIDORHYNCHIDAE: Ibidorhyncha struthersii 3.JACANIDAE: Actophilornis africana 5, Hydrophasianus chirur-

gus 5, Metopidius indicus 2,Jacana spinosa 1 1 , / jacana5.

ROSTRATULIDAE: Rostra tula benghalensis 5, Nycticryphessemicollaris 1.

PEDIONOMIDAE: Pedionomus torquatus 1.THINOCORIDAE: Attagis malouinus 1, Thinocorus orbignyi-

anus 2, 7". rumkivorus 5.SCOLOPACIDAE

TKINGINAE: Limosa limosa 2, L. haemastica 5, L. lappon-ica l,L.fedoa 5; Numenius minutus 1, iV. borealis 5, JV.phaeopus 5, iV. tahitiensis 5, AT. arquata 2, AT. madascar-iensis 2, iV. americanus 5; Bartramia longicauda 7,Tringa totanus 1, 7". nebularia 1, 7. melanoleuca 8, 7".

Jlavipes 8, 7". ochropus 2, 7. solitaria 4, 7. glareola 3;Catoptrophorus semipalmatus 8, X?nus dnereus 1, Acfifishypoleucos 3, A. macularia 7; Heteroscelus brevipes 2, //.incanus 3, Prosobonia cancellata 1.

ARENARIINAE: Arenana interpres 5, A. melanocfphala 1.PHALAROPODINAE: Phalaropus tricolor 2, P. lobatus 1, P.

fulicarius 1.SCOLOPAQNAE: Scolopax rusticola 5, S. minor 5.

33


GALLINAGONINAE: Gallinago stenura 3, G. megala 1, G.gallinago 5, G. paraguaiae 3, G. nobilis 4, G. jamesoni1; Lymnocryptes minimus 1, Limnodromus griseus 5, L.scolopaceus 5.

CALIDRIDINAE: Aphriza virgata 1, Calidris canutus 5, C.alba 5, C. pusilla 5, C wiawn 5, C ruficollis 4, C.minuta 1, C. temminckn 1, C. subminuta 1, C. minutilla5, C. fusckollis 5, C. 6ainftt 5, C. melanotos 5, C.acuminata 1, C maritima 3, C ptilocnemis 5, C. alpina5, C. ferruginea 4; Eurynorhynchus pygmeus 1, Limicolafalcinellus 1, Micropalama himantopus 5, Tryngites sub-ruficollis 2, Philomachus pugnax 9.

STERCORARIIDAE: Catharacta skua 3, C maccormicki 3;Stercorariuspomarinus 3 ,5. parasiticus 5,5. longicaudus5.

LARIDAE

LARINAE: Gabianus scoresbii 4, Pagophila alba 4, Lan«fuliginosus 3, L. crassirostris 2, L. audouinii 1, L. canus9, L. argentatus 4, L. californicus 4, L. occidentalis 4, L.dominicanus 3 , L. schistisagus 3, L. marintw 3, L. g/au-cescens 3, L. hyperboreus 5, L. ichthyaetus 1, L. atricilla5, L. cirrocephalus 3 , L. pipixcan 2, L. novaehollandiae3, L. bulleri 1, L. maculipennis 1, L. ridibundus 3, L.g*n« 1, L. Philadelphia 5, L. sounder si 1; Rhodostethiarosea 3 , fltwa tridactyla 5, /?. brevirostris 3; Creagrus

furcatus 2, X«na 5afc'nt 4.STERNINAE: Chlidonias hybrida 1, C. leucoptera 2, C. nigra

4; Phaetusa simplex 2, Gelochelidon nilotica 2, Hydro-progne caspia 4, Sterna hirundinacea 4 ,5 . hirundo 5 ,5.paradisaea 7, 5. vittata 5, S.forsteri 4 , 5 . dougallii 4 ,5 .striata 2, S. sutnatrana 2, S. aleutica 2, S. lunata 3, 5.anaethetus 2, S.fuscata 5 ,5 . superdliaris 2 , 5 . albifrons6; Thalasseus bergii 3, 7". maximus 5, 7. sandvicensis 4;Larosterna inca 4, Procelsterna cerulea 5, Anous stolidus5, A minutus 5; G^i5 a/6a 5.

RYNCHOPIDAE: Rynchops niger 5, fl. flavirostris 2.ALCIDAE: A/fe a//* 3, Pinguinus impennis 2, A/ca tonfa 5,

f/na lomvia 5, £/. aa/ge 5; Cepphus grylle 6, C. columba5, C. car/»o 3; Brachyramphus marmoratus 1, A ir«w-roj/ris 1, A hypoleucus 1; Synthliboramphus antiquus 5,Ptychoramphus aleuticus 3, Cyclorrhynchus psittacula 5,Aethia cristatella 4, A. pusilla 4, A. pygmaea 1; Oro-rhinca monocerata 4, Fratercula arctica 4, F. corniculata4; Lunda cirrhata 4.

PTEROCLIDIDAE: Syrrhaptes paradoxus 2, Pterocles alchataI, P. orientalis 1, P. gutturalis 2, P. burchelli 3, P.bicinctus 4.

COLUMBIDAE: Columba livia 4, C. rupestris 1, C. guinea 4,C. palumbus 4, C. hodgsonii 2, C. leucocephala 3, C.squamosa 2, C. speciosa 4, C. fasciata 3, C. araucana 1,C. cayennensis 2, C. inornata 3, C. plumbea 2, C.subvinacea 1; Streptopelia orientalis 1, 5. decaocto 2, S.semitorquata 3, S. capicola 3 , 5. vinacea 1, S. tranque-barica 2, S. chinensis 3 , 5. senegalensis 3; Macropygiaunchall 3, Turacoena manadensis 1, Turtur chalcospilos

3, r . a/^r 3, T. brehmeri 2; O n a capensis 2, Chalcophapsindica 2, Phaps chalcoptera 1, Ocyphaps lophotes 2,Petrophassa plumifera 2, P. ferruginea 1, P. smithii 2;Geopelia cuneata 1, G. tfria/a 3, G. humeralis 2; L^uco-sarcia melanoleuca 3, Ectopistes migratorius 3, Zenaidamacroura 5, Z. auriculata 3, Z. aurita 4, Z. asiatica 3;Columbina passerina 5, C. buckleyi 2, C. talpacoti 3, C.picui 3; Claravis pretiosa 2, Scardafella inca 3, Leptotilaverreauxi 4, L. rufaxilla 2, L. plumbeiceps 3, L. jamai-censis 3, L. cassini 1; Geotrygon chrysia 3, G. montana3; Starnoenas cyanocephala 2, Caloenas nicobarica 3,Gallicolumba tristigmata 1, Goura cristata 4, G. scheep-makeri 1, G. victoria 2; Didunculus strigirostris 1, PAa-pitreron leucotis 1, P. amethystina 1; Treron vernans 5,T. pompadora 2, T. curvirostra 1, 7. phoenicoptera 1, 7.ca/t/a 2; Ptilinopus occipitalis 1, P. leclancheri 1, P.roseicapilla 1, P. purpuratus I, P. dupetithouarsii 2, P.iozonus 1, P. melanospila 1; Ducula radiata 1, D. a*na<?5, £>. pacifica 1, D. ocrantca 1, £>. aurorae 1, Z). fcia'ta2, D. bicolor 1, D. luctuosa 1, Z). spilorrhoa 1; Hemi-phaga novaeseelandiae 1.

TROCHILIDAE

TROCHUJNAE: Dorifera ludovicae 1, Androdon aequatori-alis 1, Phaeochroa cuvierii 1, Campylopterus curvipennis1, C. largipennis 1, C. ensipennis 1, C. villaviscensio 1;Eupetomena macroura 1, Florisuga mellivora 1, Colibridelphinae 1, C coruscans 1; Anthracothorax viridigula1, A. dominicus 1; Eulampis jugularis 2, Sericotes holos-ericeus 2, Chrysolampis mosquitus 1, Orthorhyncus cris-tatus 1, X/au guimeti 1, Abeillia abeillei 1, Stephanoxislalandi 1, Popelairia conversii 1, Chlorestes notatus 1,ChlorostUbon maugaeus 1, C. gibsoni 1; Cynanthus lati-rostris 1, Cyanophaia bicolor I, Thalurania furcata 2,T. glaucopis 1; Panterpe insignis 1, Damophila julie 1,Lepidopyga coeruleogularis 1, Hylocharis leucotis 1, / / .cyanus 1; Chrysuronia oenone 1, Trochilus polytmus 1,Polytmus guainumbi 1, Leucippus taczanoswskii 1, Ama-zi/ta chionogaster 1, A. Candida 1, A. amabilis 1, A.beryllina 1, A. saucerrottei 1, A. fcaca*/ 1, A. violiceps 1;Eupherusa eximia 1, Chalybura urochrysia 1, Lampornisclemenciae 1, Adelomyia melanogenys 1, Phlogophilushemileucurus 1, Polyplancta aurescens 1, Heliodoxa gu-laris 1, Eugenes fulgens 1, Sternoclyta cyanopectus 1,Topaza pella 1, Oreotrochilus estella 1, Urochroa bougueri1, Patagona gigas 1, Aglaeactis cupripennis 1, Lafresnayalafresnayi 1, Pterophanes cyanopterus 1, Coeligena coeli-gena 1, C. wilsoni 1, C. torquata 2, C. lutetiae 1, C. iris1; Ensifera ensifera 2, Sephanoides sephanoides 1, /tou-sonneaua matthewsii 1, Heliangelus amethysticollis 1, / / .«cortt5 1; Eriocnetnis luciani 1, Haplophaedia aureliae 1,Ocreatus underwoodii 1, Lesbia victoriae 1, Sappho spar-ganura 1, Polyonymus caroli 1, Ramphomicron micror-hynchum 1. Metallura theresiae 1, Af. williani 1; C/w/-costigma rufkeps 1, C. stanleyi 1, Oxypogon guerinii 1,Aglaiocercus hngi I, Oreonympha nobilis 1, Augastes

NUMBER 395 35

lumachellus 1, Schistes geoffroyi 1, Heliothryx aurita 1,Heliomaster constantii 1, Rhodopis vesper 1, Philodiceevelynae 1, Archilochus colubris 2, A. alexandri 1; Calypteanna 2, Myrtisfanny 1, Chaetocercus jourdanii I.

FURNARIIDAE: Geositta cunicularia 6, Upucerthia certhioides1, U. dumeteria 2; Cindodes patagonicus 3, Chilia me-lanura 1, Furnarius leucopus 5, i \ n*/ks 3; Aphrasturaspinicauda 5, Leptasthenura platensis 1, L. aegithaloides3; Schizoeaca fuliginosa 1, Synallaxis phryganophila 1,S. azarae 1, S. albescens 3, S. 5/wct 1, S. brachyura 4, S.gujanensis 2, S. rutilans 1,5. castanea 1, S. erythrothorax1, S. cinnamomea 4; Certhiaxis erythrops 1, C. obsoleta1, C. subcristata 2, C. pyrrhophia 1, C. sulphurifera 1,

C cinnamomea 3; Thripophaga pyrrholeuca 1, 7. Ziumi-co/a 1, T. patagonica 1; Spartonoica maluroides 1, Phleo-cryptes melanops 1, Anumbius annumbi 1, Coryphisteraalaudina 1, Margarornis brunnescens 1, Af. rubiginosus2, M. squamiger 2; Lochmias nematura 1, Pseudoseisuralophotes 2, Pseudocolaptes boissonneautii 6, PhUydor gut-tulatus 3 , P. rufosuperciliatus 1, P. striaticollis 4, P.lichtensteini 1, P. ru/ks 4, P. dimidiaius 1; Thripadectesvirgaticeps 2, Automolus rectirostris 3 , Sclerurus albigu-laris 5,5. guatemalensis 1; Xenops minutus 5, X. rutilans2; Pygarrhichas albogularis I.

XENICIDAE: Acanthisitta Moris 1.

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the Black Skimmer Rynchops nigra Linnaeus. Pub-lications of the Nuttall Ornithological Club, 3: 101pages, 44 figures, 5 tables.

1967. The Role of the Depressor Mandibulae Muscle inKinesis of the Avian Skull. Proceedings of the UnitedStates National Museum, 123(3607): 1-28, 13 fig-ures.

In prep. Patterns of Adaptation in the Skull of Shorebirds(Aves: Charadriiformes, Charadrii).

Index to English and Scientific Names(excluding Appendix)

Actitis (Scolopacidae: Tringinae), 13macula ria, 21, 29

Aepyornithiformes, 21Aja'm ajaja (Threskiornithidae: Plataleinae), 26, 27Alca (Alcidae), 7Alcae, 6. 29alcid (Alcidae), 24Alcidae, 6, 7Alle alle (Alcidae), 20Apodiformes, 6Apterygidae, 6, 28Apteryx (Apterygidae), 5, 20, 22Aramidae, 6, 24Aramus (Aramidae), 18

guarauna, 19, 20Archaoepteryx (Archaeopterygidae), 24, 25Arenaria (Scolopacidae: Arenariinae), 20Attagis malouinus (Thinocoridae), 20avocet (Recurvirostridae), 20, 21

Banded Stilt (Recurvirostridae), 20, 21Black Skimmer (Rynchopidae), 19Buff-breasted Sandpiper (Scolopacidae: Calidridinae), 21Burhinidae, 30Bush Wren (Xenicidae), 30bustard (Otididae), 25, 30buttonquail (Tumicidae), 24

calidridine (Scolopacidae: Calidridinae), 23Calidris alpimi (Scolopacidae: Calidridinae), 29Calypte (Trochilidae: Trochilinae), 23Campyloplerus largipennis (Trochilidae: Trochilinae), 22Capellirallus (Rallidae), 17Cariamidae, 30cassowary (Casuariidae), 22Casuariidae, 6,21Casuarius (Casuariidae), 22, 31

casuarius, 1 1 , 2 1Cepphus (Alcidae), 7Cerorhinca (Alcidae), 7Charadrii, 2, 5, 6, 28, 29, 31, 32Charadriidae, 6, 21 ,23charadriiform, 20Charadriiformes, 6, 29, 30, 32Chelitloptera lenebrosa (Bucconidae), 9Chionididae, 6, 24Chionis alba (Chionididae), 20Choriotis kori (Otididae), 25, 26

Ciconiiformes, 6Cladorhymhus (Recurvirostridae), 20, 21

' €oeligena (Trochilidae: Trochilinae), 23coelurosaurian dinosaur, 24, 25Columba speriosa (Columbidae), 16Columbidae, 6, 21,24Columbiformes, 6, 29, 32Coraciiformes, 16courser (Glareolidae: Cursoriinae), 24Crab Plover (Dromadidae), 24crane (Gruidae), 23Cretaceous toothed bird, 24crocodile, 24crocodilian, 24, 25Cursorius (Glareolidae: Cursoriinae), 7

coromandelicus, 8, 20Cyanocitta stelleri (Corvidae), 8

Dendrocolaptidae, 10, 16, 30Didumulus strigirostris (Columbidae), 13, 19, 20Dinomithiformes, 21dinosaur, 24Dodo (Raphidae), 30dove (Columbidae), 24dowitcher (Scolopacidae: Gallinagoninae), 23Dromadidae, 6, 24Dromaeosaurus albertensis (Coeluridae), 24Dromaiidae, 6Dromaius (Dromaiidae), 22, 31Dromas ardeola (Dromadidae), 20Ducula bicolor (Columbidae), 16, 19

Egyptian Plover (Glareolidae: Cursoriinae), 30elephantbird (Aepyomithidae), 21emu (Dromaiidae), 22Ensifera (Trochilidae: Trochilinae), 23Eudocimus albus (Threskiornithidae: Threskiornithinae), 16,

27Eudromia elegans (Tinamidae), 11Eurypyga helias (Eurypygidae), 9 ,16Eurypygidae, 6, 24Eutoxeres (Trochilidae: Phaethomithinae), 23

finfoot (Heliomithidae), 30flamingo (Phoenicopteridae), 30Fratercula (Alcidae), 7furnariid (Furnariidae), 16Furnariidae, 6, 10, 16, 21, 24, 29Furnarius leucopus (Furnariidae), 19, 20

38

NUMBER 395 39

Gavia (Gaviidae), 17Glareola nordmanni (Glareolidae: Glareolinae), 9Glareolidae, 6, 7, 24Glaucis (Trochilidae: Phaethornithinae), 23godwit (Scolopacidae: Tringinae), 23Goura scheepmakeri (Golumbidae), 16grebe (Podicipedidae), 17Gruiformes, 6, 29, 32Gruidae, 6, 23Grus canadensis (Gruidae), 16

leucogeranus, 19gull (Laridae: Larinae), 24

Haematopodidae, 6, 28Haematopus (Haematopodidae), 20Hagedashia hagedash (Threskiornithidae: Threskiornithinae),

27Heliornithidae, 30hemipode (Turnicidae), 24hermit (Trochilidae: Phaethornithinae), 30Hesperornis (Hesperornithidae), 24Himantopus mexicanus (Recurvirostridae), 16Hoopoe (Upupidae), 10, 16hummingbird (Trochilidae), 20, 22, 23, 30, 32

Ibidorhynchidae, 6, 24ibis (Threskiornithidae: Threskiornithinae), 23, 26, 27ibisbill (Ibidorhynchidae), 24

jacana (Jacanidae), 24Jacana spinosa (Jacanidae), 16Jacanidae, 6, 24jaeger (Stercorariidae), 24

kagu (Rhynochetidae), 23kiwi (Apterygidae), 5, 10, 20, 22, 23, 32

Lari, 6, 29Laridae, 6Larinae, 6Larus Philadelphia (Laridae: Larinae), 20Lesser Painted Snipe (Rostratulidae), 21Limnodromus griseus (Scolopacidae: Gallinagoninae), 29Limpkin (Aramidae), 18, 24loon (Gaviidae), 17Lunda (Alcidae), 7

Margarornis rubiginosus (Fumariidae), 20Mellisuga (Trochilidae: Trochilinae), 23mesite (Mesitornithidae), 24Mesitornis variegata (Mesitornithidae), 21Mesitornithidae, 6, 24Mimidae, 30moa (Dinornithidae), 21mockingbird (Mimidae), 30

Neotis cafra (Otididae), 25New Zealand wren (Xenicidae), 24Nycticryphfs semicollaris (Rostratulidae), 16, 21

Ornithomimus (Omithomimidae), 24Ostrich (Struthionidae), 21Otididae, 25, 30ovenbird (Fumariidae), 10, 24oystercatcher (Haematopodidae), 20, 21, 23

painted snipe (Rostratulidae), 24paleognathous bird, 6, 10, 11, 18, 21, 22, 24, 31, 32Passeriformes, 6, 29Pedionomidae, 6, 24penguin (Spheniscidae), 24Phaethornis (Trochilidae: Phaethornithinae), 23Phaethornithinae, 23, 30Philomachus pugnax (Scolopacidae: Calidridinae), 29Philydor guttulatus (Fumariidae), 9, 16philydorine ovenbird (Fumariidae), 16Phoenicopteridae, 30Phoeniculidae, 16Phoeniculus purpureus (Phoeniculidae), 9pigeon (Golumbidae), 21, 24plains wanderer (Pedionomidae), 24Plataleinae, 30plover (Charadriidae), 5, 21, 23Pluvialis squatarola (Charadriidae), 8, 16Pluvianus (Glareolidae: Cursoriinae), 30Podiceps (Podicipedidae), 17pratincole (Glareolidae: Glareolinae), 24Psophiidae, 30Pterocles orientalis (Pteroclididae), 9

bicinctus, 20Pteroclididae, 6, 24Pterocnemia (Rheidae), 21

rail (Rallidae), 10, 16, 23, 30Rallidae, 6, 10, 16,30Rallus (Rallidae), 6, 17, 23, 25

aquaticus, 9Ramphodon (Trochilidae: Phaethornithinae), 23Raphus (Raphidae), 30

cucullatus, 19ratite, 5, 10 ,21 ,22Recurvirostra (Recurvirostridae), 20, 21Recurvirostridae, 6rhea (Rheidae), 10,21Rhea (Rheidae), 21,31

americana, 11 , 21Rheidae, 6, 21Rhynchotus (Tinamidae), 31Rhynochetidae, 6, 23Rock Wren (Xenicidae), 30Roseate Spoonbill (Threskiornithidae: Plataleinae), 26Rostratulidae, 6, 24Rynchopidae, 6Rynchops (Rynchopidae), 32

niger, 19, 20

sandgrouse (Pteroclididae), 24


sandpiper (Scolopacidae), 5Scolopacidae, 6, 13, 23, 28Scolopax (Scolopacidae: Scolopacinae), 32seedsnipe (Thinocoridae), 24seriama (Cariamidae), 30sheathbill (Chionididae), 24Sittasomus griseicapillus ( D e n d r o c o l a p t i d a e ) , 9 , 1 6skimmer (Rynchopidae), 19, 24, 32skua (Stercorariidae), 24snipe (Scolopacidae: Gallinagoninae), 1, 23spoonbill (Threskiornithidae: Plataleinae), 26, 27, 30Spotted Sandpiper (Scolopacidae: Tringinae), 21Stercorariidae, 6Sterna hirundo (Laridae: Sterninae), 20Sterninae, 6Struthio (Struthionidae), 21,31

camelus, 11 , 21Struthionidae, 6, 21sunbittem (Eurypygidae), 24sun grebe (Heliornithidae), 30

tern (Laridae: Sterninae), 24thecodont, 24thickknee (Burhinidae), 30Thinocoridae, 6Thinocorus (Thinocoridae), 24Threnetes (Trochilidae: Phaethornithinae), 23Threskiornithidae, 6, 23thrush (Muscicapidae: Turdinae), 30Tinamidae, 6, 21

tinamou (Tinamidae), 5, 10, 13, 20, 21, 22Tinamus major (Tinamidae), 5Tooth-billed Pigeon (Columbidae), 13, 18Tringa jhtvipes (Scolopacidae: Tringinae), 16tringine sandpiper (Scolopacidae: Tringinae), 21, 23Trochilidae, 6, 29Troglodytidae, 30trumpeter (Psophiidae), 30Tryngites subruficollis (Scolopacidae: Calidridinae), 21Turdinae, 30Turnicidae, 6, 24Turnix sylvalica (Turnicidae), 20turnstone (Scolopacidae: Arenariinae), 20, 21

Upupa epops (Upupidae), 9Upupidae, 10, 16Uria (Alcidae), 7

Vanellus indicus (Charadriidae), 16

White-breasted Mesite (Mesitornithidae), 21woodcock (Scolopacidae: Scolopacinae), 1, 23, 32woodcreeper (Dendrocolaptidae), 10, 16, 30wood hoopoe (Phoeniculidae), 16woodpecker (Picidae), 16wren (Troglodytidae), 30

Xenicidae, 6, 24Xenicus (Xenicidae), 30

longipes, 30Xiphorhynchusguttalus (Dendrocolaptidae), 19

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a functional and evolutionary analysis of rhynchokinesis

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