FUNCTIONAL ANATOMY EVOLUTION ADAPTIVE APPARATUS FEEDING HAWAIIAN AND OF IN THE THE HONEYCREEPER GENUS LOXOPS (DREPANIDIDAE) BY LAWRENCE P RICHARDS AND WALTER ORNITHOLOGICAL J BOCK MONOGRAPHS PUBLISHED THE AMERICAN BY ORNITHOLOGISTS' 1973 NO UNION 15 FUNCTIONAL ANATOMY ADAPTIVE EVOLUTION FEEDING APPARATUS HAWAIIAN AND OF IN THE THE HONEYCREEPER GENUS LOXOPS (DREPANIDIDAE) BY LAWRENCE P RICHARDS AND WALTER ORNITHOLOGICAL J BOCK MONOGRAPHS PUBLISHED THE AMERICAN BY ORNITHOLOGISTS' 1973 NO UNION 15 ORNITHOLOGICAL MONOGRAPHS This series,publishedby the American Ornithologists'Union, has been established for major paperstoo long for inclusionin the Union's journal, The Auk Publicationhas been made possiblethroughthe generosityof Mrs Carll Tucker and the Marcia Brady Tucker Foundation,Inc Correspondence concerningmanuscriptsfor publicationin the series should be addressedto the Editor, Dr John William Hardy, Department of Natural Science, The Florida State Museum, University of Florida, Gainesville, Florida 32611 Copiesof OrnithologicalMonographsmay be orderedfrom the Treasurer of the AOU, Burt L Monroe, Jr., Box 23447, Anchorage,Kentucky 40223 (See price list on inside back cover.) OrnithologicalMonographs,No 15, x + 173 pp Editor-in-chief, John William Hardy SpecialAssociateEditor for this issue,Richard L Zusi, U.S National Museum, Washington,D.C Issued November 1, 1973 Price $6.00 prepaid ($4.75 to AOU Members) Library of CongressCatalogueCard Number 73-88386 Printed by the Allen Press,Inc., Lawrence,Kansas66044 TABLE PREFACE CONTENTS INTRODUCTION ACKNOWLEDGMENTS METHODS OF AND MATERIALS FIELD STUDIES DISSECTION AND DRAWING ix 9 10 PLATES 11 KINETICS 12 RELATIVE SIZE DIFFERENCES OF THE JAW MUSCLES 12 TYPES OF FOOD AND FEEDING METHODS 14 HAWAIIAMAKIHI,Loxoes tIRE,rstIRE,rs 14 Typesof foodtaken 14 Methodsof feeding 18 GREATER AMAKIHI,LoxoPsSAGITTIROSTRIS 20 HAWAIICREEPER, LoxoPsMACULATA MANA 20 Typesof foodtaken 20 Methodsof feeding 21 MAUI CREEPER,Loxoes M,•CVL.•t.••V•WtO•Vl 22 Typesof foodtaken 22 Methodsof feeding 22 HAWAIIAKEPA,Loxoes coccI•v•.• coccI•v•.• 23 Typesof foodtaken 23 Methodsof feeding 23 SUMMARY OF FOODS AND METHODS OF FEEDING L v vtn•vs L $AGITTIROSTRIS 26 26 26 L M M.•N.• 26 L M NEWTONI 26 L C COCCINE.• 27 iii RHAMPHOTHECAE OF THE DESCRIPTION BEAK FUNCTIONAL INTERPRETATION CRANIAL OSTEOLOGY 27 27 30 35 INTRODUCTION 35 SKULL OF n •' VIRE:VS 35 CRANIAL KINESIS 44 GAPINC ADAPTATIONS 48 COMPARISON OF THE SKULL IN LOXOPS 48 CRANIAL ASYMMETRIES IN L ½ ½O½½INEA 52 JAW MUSCULATURE INTRODUCTION DESCRIPTION OF INDIVIDUAL MUSCLES 53 53 54 A) M protractorpterygoideiet quadrati 54 M protractorpterygoideisensustricto 54 2) M protractorquadraft 55 56 B) M adductor mandibulae extemus M adductor mandibulae externus rostralis 56 a) M adductor mandibulae extemus rostralis temporalis 56 b) M adductormandibulaeextemusrostralis lateralis 57 c) M adductor mandibulae extemus rostralis medialis M adductor mandibulae externus ventralis 2) M adductor mandibulae externus caudalis 3) 58 58 59 a) M adductormandibulaeextemuscaudalis"a" _ 59 b) M adductormandibulaeextemuscaudalis"b" _ 60 C) M adductormandibulaeposterior 61 M adductor mandibulae intemus 62 D) M pseudotemporalis superficialis 62 E) M pseudotemporalis profundus 63 F) M pterygoideus 63 l) M pterygoideus ventralislateralis 64 2) M pterygoideus ventralismedialis 66 3) M pterygoideus dorsalislateralis 67 4) M pterygoideus dorsalismedialis 69 5) M pterygoideus retractor 71 G) M depressormandibulae 73 SUMMARY OF COMPARISON OF JAW MUSCLES 74 FUNCTIONAL 78 ANALYSIS OF JAW MECHANISMS THE ASYMMETRICAL THE TONGUE JAW APPARATUS OF L COCCINEA APPARATUS INTRODUCTION 81 94 94 THE CORNEOUS TONGUE 94 OSTEOLOGY OF THE TONGUE 96 MUSCULATURE OF THE TONGUE 98 A) B) C) D) E) F) G) H) M M M M M M M M mylohyoideus 99 ceratohyoideus 99 stylohyoideus 100 serpihyoideus 100 branchiomandibularis 101 genioglossus 101 ceratoglossus 102 hypoglossus anterior 102 I) M hypoglossus obliquus 103 J) M tracheohyoideus 103 K) M thyreohyoideus 104 FUNCTIONAL INTERACTIONS OF THE TONGUE MUSCULATURE 104 FUNCTIONAL AND ADAPTIVE SIGNIFICANCES OF THE TONGUE 108 DISCUSSION FEEDING ADAPTATIONS 111 111 A) Loxops virens virens 113 B) Loxops sagittirostris 114 C) Loxops maculata maria 115 D) Loxops maculata newtoni 117 E) Loxops coccinea coccinea 118 ADAPTATION AND EXTINCTION 121 EVOLUTIONARY I-HSTORY OF THE GENUS LOXOPS 122 SUMMARY LITERATURE APPENDIX CITED I-•GLOSSARY OF ABBREVIATIONS 128 129 134 ILLUSTRATIONS Plate Lateral view of the bill of Loxops 139 Dorsal and ventral view of the bill of Loxops 141 Skull of Loxops v virens 143 Skull of Loxops m mana 145 Skull of Loxopsm newtoni 147 Skull of Loxops c coccinea 149 Details of the skull of L v virens 151 Detailsof the quadrateandmandibleof Loxops 153 Detailsof the quadrateandmandibleof L c coccinea (right-billedindividual) 155 10 Jaw muscles of L v virens 157 11 Jaw muscles ofL v virens 158 12 Jaw muscles of L m mana 159 13 Jaw muscles of L m mana 160 14 Jaw muscles of L m newtoni 161 15 Jaw muscles of L m newtoni 162 16 Jaw musclesof L c coccinea(right-billedindividual) 163 17 Jaw muscles of L c coccinea(right-billedindividual) 164 18 Jaw musclesof L c coccineaand L sagittirostris 165 19 Corneoustongueof Loxopsin dorsaland lateralviews (L v virens,L m manaand L n newtoni) 166 20 Corneoustongueof Loxopsin dorsalandlateralviews (L c coccineaandL sagittirostris) 167 21 Tongueskeleton of Loxopsin ventralview 168 22 Tongueskeletonandmuscles of L sagittirostris 169 23 Tonguemuscles ofL v virens 170 24 Tonguemuscles of L m mana 171 25 Tonguemuscles of L m newtoni 172 26 Tonguemusclesof L c coccinea 173 vi Figure Distributionof the speciesand subspecies of Loxops in the Hawaiian Islands Device used for measurement of skull kinesis Food sourcesof Loxopsand other drepanidids 13 16 Skullof L v virensin obliqueview 36 Skull of L v virens in lateral view 37 Skull of L v virens in ventral view 38 Schematic model of L v virens to show movements 46 Schematicdrawingsshowingleaf-budopeningby L c coccinea 85 Schematicdrawingsshowingmovementof bill tips of L c coccinea in closed-bill method 87 10 Schematicdrawingsshowingmovementof bill tips of L c coccineain opened-billmethod 90 11 Schematicdrawingsshowingopeningof koa seed-pods by L c coccinea 91 12 Tongueskeletonof L v virens 97 13 Functionsof tonguemusclesof L v virens 105 14 Dendrogram of Loxops 123 vii PREFACE This studywas originallyconceivedand plannedby LawrenceP Richards as an inquiry into the functionalmorphologyand evolutionof the cranial morphologyof the Hawaiian Honeycreepers,an aspect of the adaptive radiation of these birds that is still largely unknown The field studies were conducted in 1951-52, and the initial dissectionsstarted in 1952 Soon afterwards,it was apparentthat the original plan to cover the entire Drepanididaewas not feasible at that time so that the study was restricted to the genus Loxops The resulting thesis "Functional anatomy of the head region of the Hawaiian HoneycreepergenusLoxops (Aves, Drepaniidae)" was presentedin partial fulfillmentfor the Ph.D degree,University of Illinois in June 1957 Lack of support and encouragementand, more importantly, lack of suitable publicationpossibilitiesprecludedits publication at that time Moreover, the generaldeclineof interestin studieson passerinejaw and tongue musculaturein the second half of the 1950's made this period not propitiousfor such a study These factors and subsequentdevelopmentof interest by Richards in other areas of vertebrate biology causedabandonmentof the project for several years In the fall of 1961, Professor Hobart M Smith showed Richard's thesis to Walter J Bock, who had just joined the staff of the Department of Zoology, University of Illinois, expressinghis hope that it could be published without further delay After initial contacts were made, Bock urged Richards to ready his thesis for publication Further discussions and some work in the summer of 1963 followed, but a series of field trips and changesin positionby both Richardsand Bock delayedany significantwork Moreover, a number of papers on passerinejaw and tongue musclesand on functional analysesof cranial features necessitated a rathercompletereviewof the thesisand a reworkingof severalsections The task of reviewingthe pertinentstudiesthat appearedin the decade since1957 was formidablein itself,but was renderedimpossible by the constantdevelopmentof new ideas and the modification(some still unpublished)of earlierstatements, and by the fact that someof the essential studies(on the redescript-ion of the jaw and tonguemuscles)by Bock and his studentswere still unpublished.Largely becauseof the latter fact, we decidedearlyin 1968 to work togetheron the final preparation of this study for publication,so as to bring togetherthe specialknowledgeof Richardson the naturalhistoryand morphology of the HawaiianHoneycreepers and the specialknowledge of Bock on the functionalmorphology of the passerine jaw and tongueapparatuses.This projectoccupiedmost of the summerof 1968 Becausethe historyof eachauthorin this project 160 ORNITHOLOGICAL MONOGRAPHS m ptd mptd NO m 15 m ptr mptd ma/ m pt d m m ptvm m pt v I mptvm fan Plate 13 Jaw musclesof L m mana A) Ventral view of m pterygoideus;ventral layer removed on left side of head B) Ventral view of some tongue muscles and more dorsal jaw muscles Plate 14 Jaw musclesof L m newtoni A) Oblique view B) Lateral view of superficial muscles C) Lateral view of deeper muscles 1973 RICHARDS AND BOCK: FEEDING APPARATUS IN LOXOPS A mptdm mptdma m ptd rn ps amert mamec •amerl mamer B mame namp mptdm mptdma mptdl• C mpspmpss mamp ameca 161 162 ORNITHOLOGICAL MONOGRAPHS NO 15 mptdmp mpt dma,• m ptvm ,,mpp B q mp$ $••• Plate 15 Jaw muscles of L m newtoni A) Ventral view of m pterygoideus; ventrallayer removedon left sideof head B) Ventralview of sometonguemuscles and more dorsal jaw muscles Plate 16 Jaw musclesof L c coccinea(right-billed individual) A) Lateral view of superficial muscles of the right side B) Lateralview of superficialmuscles of the left side C) Lateral view of deeper musclesof the left side 1973 RICHARDS AND BOCK: FEEDING APPARATUS IN LOXOPS A •Ila meca m pt m ptdm m ptdm mptdl B mpsp mdm amev mameca ptvl c /mpsp mdm 163 ORNITHOLOGICAL 164 MONOGRAPHS NO m pt d rn p• ,m a m e mptvl• mptd ma• • ti' • '•'/•• m p•vm mdm • m ptr mptdI' mptvI/ '•• mptvm/ '••a me-mdm d m mptd m pt r B mptdl m ptdml• mdm rn pss d 113 C Ppq mpsp mdm 15 1973 RICHARDS AND BOCK: FEEDING APPARATUS IN LOXOPS 165 A mptr• amert m ptd mdm mamecb amerl mamev npsp •ptdma ptdm p •/,/• m d!•:• Plate 18 Jaw muscles of L c coccinea and L sagittirostris A) Oblique view of the left-side of L c coccinea (right-billed individual) B) Lateral view of the hind end of the head of L sagittirostris showing the m depressor mandibulae Plate 17 Jaw muscles of L c coccinea (right-billed individual) A) Ventral view of the M pterygoideus and some surrounding muscles (left-side of head uppermost) B) Ventral view of dorsal layer of M pterygoideus (ventral layer removed on both sides) C) Ventral view of some tongue musclesand more dorsal jaw muscles, 166 ORNITHOLOGICAL MONOGRAPHS NO 15 B Plate 19 Corneoustongue of Loxops in dorsal and lateral views A) L v virens B) L m mana C) L m newtoni 1973 RICHARDS AND BOCK: FEEDING APPARATUS IN LOXOPS 167 Plate 20 Corneoustongue of Loxops in dorsal and lateral views A) L c coccinea B) L sagittirostris 168 ORNITHOLOGICAL MONOGRAPHS Plate 21 Tongue skeleton of Loxops in ventral view mana C) L m newtoni D) L c coccinea NO 15 A) L v virens B) L m 1973 RICHARDS AND BOCK: FEEDING APPARATUS IN LOXOPS 169 m hgo gg mthh ,m trh st h ,mbrn rncg o mbmp mtrl brn sh Plate 22 Tongue skeleton and musclesof L sagittirostris A) Tongue skeleton in ventral view B) Tongue musclesin ventral view; superficialmuscleson right side, deeper muscles on left side 170 ORNITHOLOGICAL MONOGRAPHS NO 15 msh• Ill Ill mcg m ch m tr m trh I / m gg rn • mbm ch m hgo cg •mtrl mtrh mth Plate 23 h Tongue musclesof L v virens in ventral view A) Superficial muscles B) Deeper muscles 1973 RICHARDS AND BOCK: FEEDING APPARATUS IN LOXOPS 171 msh mm h• m cg m ch A m trl m trh mgg mbm mhgo• ch B tr tr I h mcg Plate24 Tonguemuscles of L m manain ventralview A) Superficial muscles B) Deeper muscles 172 ORNITHOLOGICAL MONOGRAPHS NO 15 st h mch tr h m trl m s h mbmp m gg mbm mch B mtrh mtr! m hg o th h Plate 25 Tonguemusclesof L m newtoniin ventralview A) Superficial muscles B) Deeper muscles 1973 RICHARDS AND BOCK: FEEDING APPARATUS IN LOXOPS A 173 ch sh mbma mcg mbmp mgg m sfh mbm rn fh ch B mtrl mhgo Plate 26 mtrh Tongue musclesof L c coccineain ventral view A) Superficial muscles B) Deeper muscles ORNITHOLOGICAL MONOGRAPHS No A DistributionalStudyof the Birdsof British llonduras, by StephenM Russell 195 pp., color plates 1964 Price $4.50 ($3.60 to AOU members) No A ComparativeStudyof SomeSocialCommunicationPatternsin the Pelecaniformes, by Gerard Frederick van Tets 88 pp., text figures 1965 Price $2.00 ($1.60 to AOU members) No The Birds of Kentucky, by RobertM Mengel Cloth bound,xiv q- 581 pp., color platesplus text 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and Adaptive Evolution of the FeedingApparatus in the Hawaiian HoneycreeperGenusœoxops(Drepanididae),by LawrenceP Richards and Walter J Bock vii + 173 pp., 14 text figures + 26 plates 1973 Price $6.00 ($4.75 to AOU members) Like all other AOU publications,OrnithologicalMonographsare shippedprepaid Make checkspayable to "The American Ornithologists'Union." For the convenienceof thosewho wish to maintain completesetsof OrnithologicalMonograpsand to receivenew numbersimmediatelyupon issue,standingorderswill be accepted Order from: Butt L Monroe, Jr., Treasurer, American Ornithologists' Union, Box 2a447,Anchorage,Kentucky 402•a ... (DREPANIDIDAE) BY LAWRENCE P RICHARDS AND WALTER ORNITHOLOGICAL J BOCK MONOGRAPHS PUBLISHED THE AMERICAN BY ORNITHOLOGISTS' 1973 NO UNION 15 ORNITHOLOGICAL MONOGRAPHS This series,publishedby the American... Copiesof OrnithologicalMonographsmay be orderedfrom the Treasurer of the AOU, Burt L Monroe, Jr., Box 23447, Anchorage,Kentucky 40223 (See price list on inside back cover.) OrnithologicalMonographs,No... virens 151 Detailsof the quadrateandmandibleof Loxops 153 Detailsof the quadrateandmandibleof L c coccinea (right-billedindividual) 155 10 Jaw muscles of L v virens 157 11 Jaw