Ornithological Monographs 15

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

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OrnithologicalMonographs,No. 15, x + 173 pp.
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Issued November 1, 1973

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TABLE

PREFACE

CONTENTS

.............................................................................................

INTRODUCTION

...............................................................................

ACKNOWLEDGMENTS
METHODS

OF

AND

...........................................................................

MATERIALS

.............................................................

FIELD STUDIES ..................................................................

DISSECTION AND DRAWING ...............................................

ix
1
7
9
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

1. Lateral view of the bill of Loxops .......................................... 139
2. Dorsal and ventral view of the bill of Loxops ..........................

141

3. Skull of Loxops v. virens........................................................ 143
4. Skull of Loxops m. mana ........................................................

145

5. Skull of Loxopsm. newtoni.................................................... 147
6. Skull of Loxops c. coccinea.................................................... 149
7.

Details of the skull of L. v. virens ............................................

151

8. Detailsof the quadrateandmandibleof Loxops.................... 153
9. 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 1. Distributionof the speciesand subspecies
of Loxops
in the Hawaiian
2.

Islands ..........................................................

Device used for measurement

of skull kinesis ....................

3. Food sourcesof Loxopsand other drepanidids......................

4
13

16

4. Skullof L. v. virensin obliqueview ........................................ 36
5.

Skull of L. v. virens in lateral view ........................................

37

6.

Skull of L. v. virens in ventral view ...............................

38

7.

Schematic model of L. v. virens to show movements .........

46

8. Schematicdrawingsshowingleaf-budopeningby L. c.
coccinea

..................................................................................

85

9. 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


is quite differentand becauseit becamea joint venturelate in its development, a few additionalcommentson responsibilities
must be given.
The responsibilityand all credit for field observations,obtaining of
specimens,dissectionsof the jaw and the tongue musclesand original
descriptions
and interpretations

belongto Richards. The systemsof identificationand terminologyfor the musclesare basedupon studiesby Bock,
but it shouldbe noted that few discrepancies
existedbetweenthe muscle
identifications
and terminologies
used by Richardsin his thesisand those
advocatedby Bock. Responsibilityfor the entire paper, functionalinterpretationsand conclusionson the adaptive significancesof these cranial
featuresand on the evolutionof the groupis sharedequallyas we reviewed,
discussedand rewrote the entire manuscript for publication. Hence we
look upon this paper as a truly cooperativeundertakingin spite of the
separateoriginsof the informationand ideas used in reachingthe interpretationsand conclusions
presentedherein.
Submitted for publication, April 1970
Final Revision, December 1972


INTRODUCTION

The family of oscinebirdsendemicto the HawaiianIslands,the Hawaiian
Honeycreepersor Drepanididae,is one of the most spectacularand geographicallycompactexamplesof adaptive radiation. Almost the entire
range of feedingmethodsand bill structureknown in passerinebirds is
found within the Drepanididae. This radiation is especiallyinteresting
becauseit has occurredat the low taxonomiclevel of the family and presumablywithin a short span of geologicaltime. Although details still
remain to be clarified, many evolutionaryphenomenaare well illustrated
by this groupof birds--alas,that of extinctionis all too well demonstrated
by lost membersof the Drepanididae(see Greenway,1967). Consequently,
the Hawaiian Honeycreepershave long held the interest of ornithologists
and evolutionists,and have been the subjectof severalmonographs(Wilson
and Evans, 1890-1899; Rothschild, 1893-1900; Wallace, 1880, 1902;
Perkins, 1901, 1903; Henshaw, 1902; Munro, 1944; Amadon, 1950;

Baldwin, 1953). Apparently,this family was too poorly known in the
middle of the last century to have any role in the initial developmentof
evolutionaryideas; Darwin seemsnot to have mentionedthem at all and
Wallace treats them very briefly in the early editionsof his "IslandsLife."
Amadon's (1950) study is of specialimportance,not only becauseit is
the most recent monograph of the family, but mainly because it is the
first (and to date, the only) review of the evolutionaryhistoryand classification of the Drepanididae using the ideas generatedby recent advances
in the New Systematicsand the SyntheticTheory of Evolution. He draws
together all of the available information on these birds as the foundation
for his conclusionson their phylogeny,patternsof speciation,nature and
sourcesof selectionforces,and systematics.His monographis, and quite
rightly so, the most authoritativetreatment of the Drepanididae and is the
source for most discussionsof this family in general evolutionarytexts.
In similar fashion,Baldwin'sstudy is the only analysisof the ecologyof
these birds using modern approachesto organism-environment
interactions.
The role of introduced diseasesin the widespread and rapid extinction of
the HawaiianHoneycreepers
hasbeendiscussed
elegantlyby Warner (1968);
his ideas are essentialto our conclusionson the adaptivenessof the several
speciesof Loxops.
Since fossils of these birds have not yet been discovered, and are
not likely ever to be found, the time of originalcolonizationof the Hawaiian
archipelagoby the form, or forms, ancestralto the present-daydrepanidids
is not known. Nor can the likely ancestralform be ascertainedexcept by
comparativeanalysisand inferencefrom living birds. Stearns (1946: 2,
85) indicatesthat the larger Hawaiian Islands were above sea level in

2

ORNITHOLOGICAL

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15

Tertiary times, perhaps as late as the end of the Pliocene epoch of that
period. The time of colonizationof the Hawaiian Islandsby the ancestral
stock cannot be dated more exactly than in the Tertiary, but it seems
doubtful that colonizationtook place near either extreme possibilityof as
early as seventy-fivemillionsof years ago (in the PaleoceneEpoch) or as
late as the Pleistocene,one million years ago (Knopf, 1949: 8). Zimmerman (1948: 44) considersthat land areascapableof supportingforests
have been in existencein these islandssince late Pliocene times, some five
millionsof yearsago. Carson,Hardy, Spiethand Stone (1970) presentan
excellentsummaryof the geologicalhistory of the Hawaiian Islands based
upon recentfindingsof global plate tectonics.
Whatever the actual time of colonization,a number of potential empty
ecologicalhabitatsfor passerinebirds were presentin the Hawaiian Islands.
The original habitatsmay have been the same as those found today or
they may have differed somewhat.In any event, some of these habitats
were filled by the ancestraldrepanidids(along with the few endemic,
probablylater arriving meliphagids,turdids and muscicapids)to the partial
or completelimits of the adaptationsand preadaptationsof these birds.
Subsequent
speciationand phyletic evolutioninto generaand subfamilies
(assumingthat the Drepanididaeare monophyletic)took place with repeatedreinvasionof the variousislandsand with competitionfor food as a

main selection force (Amadon, 1950:

235, 246; 1947:

63, 66).

The combined actions of adaptive radiation and extinction have presumablyobliteratedtraces of the ancestralstock of the Drepanididaeand
of its early radiation. One cannot simply assumewith any justification
that any of the extant forms are close representatives
of the ancestral
stock. No real argumentexiststoday that the Drepanididaearosefrom the
New World nine-primariedcomplex of oscine birds. Beyond that, most
ideas on the possibleancestorsof this family may be grouped into two
main theories. The earlier one, basedlargely on the structureand distribution of the tubular tongue, is that the Drepanididaearose from Neotropical Coerebidaeor Thraupidae. Becauseof the vaguenessof the
Coerebidaeand becauseof the close similarity of at least some of these
birds and the Thraupidae,we make no distinctionbetweenchoiceof either
of thesefamiliesas possibledrepanididancestorsin our discussion.Gadow
(1891, 1899) was the first worker to advocate this relationshipstrongly
with supportinganatomicaldata. Amadon (1950: 231-233), Beecher
(1951b: 283, 285; 1953: 312-313) and Baldwin (1953: 386-388)
acceptedGadow'sconclusionand suppliedadditionalsupportfor it, much
of it being evidencefrom jaw musclepatternsprovidedby Beecher'scomparativeanatomicalstudiesof the oscinebirds. The secondand later notion,
originallyadvocatedby Sushkin(1929) on the basisof skull and horny


1973

RICHARDS

AND

BOCK:

FEEDING

APPARATUS

IN

LOXOPS

3

palate morphology,is that the Drepanididaeevolvedfrom the cardueline
finchesof the Fringillidae,or from a group directly ancestralto the
carduelines
(includingthe genusFringilla). Carduelinerelationships
of the
HawaiianHoneycreepers
has beensupported
by Bock (1960b: 477-478)
on the basisof jaw muscles(in disagreement
with Beecher'sconclusion),
Tordoff (personalcommunication)
on the basisof generalnestinghabits,
and Sibley 1970: 104--105on the basisof comparative
studyof several
protein systems.For the purposesof this paper, we accepttentatively
the carduelinetheory for the ancestorsof the Drepanididae.The jaw
musclesof Loxopssupportthis theorybetter than the thraupidtheory,

but a soundcomparativestudy must be undertakenbefore more definite
conclusionscan be offered. Moreover, we emphasizethat the major
conclusions
of the presentstudydependto a veryminordegreeon accepting
the carduelinetheory of drepanididancestry.
Amadon(1950), whoseclassification
we follow,dividesthe Drepanididae
into two subfamilies,the Drepanidinaeand the Psittirostrinae.The correct
name for this family is the Drepanididae,not the Drepaniidae,following
thefavorabledecision
by theInternational
Commission
on Zoological
Nomenclature (Anon., 1961) on the proposalby Amadon (1960) to place the
name DrepanididaeGadow, 1891 on the Official List of Family-Group
Names. The Drep.anidinaeconsistsof five genera (Himatione, Palmeria,
Ciridops,Vestiaria,and Drepanis) and the Psittirostrinae
of four (Loxops,
Hemignathus,Pseudonestor,and Psittirostra).

Amadon (1950: 164-168) mergedfour genera of earlier workers
(Viridonia,Chlorodrepanis,
Paroreomyza,
and Loxops) into a singlegenus
Loxops, recognizingthree subgenera,Viridonia, Paroreomyzaand Loxops.
Each of thesesubgeneraare widely distributedthroughoutthe main islands

of the Hawaiianarchipelago(Fig. 1). While the final draft of this manuscriptwasbeingprepared,
volume14 of "Peters'Check-list,"
containing

the
Drepanididaewas published.Greenway(1968), in treatingthis family,
dividedAmadon'sLoxopsinto threegeneracorresponding
to the subgenera
recognizedby Amadon; unfortunately,no reasonswere given for this
change.Becauseour studyexcludedfeaturesof the externalmorphology
and many aspectsof their behaviorand life-history,and becausewe did
not includeall membersof the family, we are unableto evaluatethe merits
of Amadon'ssystemversusthat of Greenway. Discussions
betweenBock
and Greenwayof the reasonsunderlyingGreenway'streatmentof the Loxops
group as opposedto Amadon's could be summarizedas differencesin
opinionon the width of genericlimits in the Drepanododae.Our preference
is for broadergenericlimits, but even so, we lack comparativeevidence
on which to base any argumentincludingthe difficult questionon the
relationship
betweenthe membersof Loxopsand the membersof Hemig-


4

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1973

RICHARDS

AND

BOCK:

FEEDING

APPARATUS

IN LOXOPS

5

nathus. However,becausewe prefer broader genericlimits, and more
importantly
because
of the practicalreasons
of the easeof stylein dealing
with one, not three genera,we continueto follow (without prejudice)
Amadon'sgenerictreatmentof the genusLoxops.

The subgenus
Viridonia containsthree species,the Amakihis,Loxops
virens; the Anianiau,Loxopsparva (Kauai); and the GreaterAmakahi,
Loxopssagittirostris
(Hawaii, extinct). The last two are monotypicspecies.
L. virens, however, containsfour races which inhabit six islands: L. v.

virens(Hawaii), L. v. wilsoni(Maui, Molokai,Lanai), L. v. chIoris(Oahu)
and L. v. stejnegeri(Kauai); stejnegeriis quite different in bill structure
from other membersof L. virens. The subgenusParoreomyzacontains

onespecies,
Loxopsmaculata,
the Creepers,
whichis composed
of six subspeciesinhabitingsix islands: L. m. mana (Hawaii), L. m. newtoni
(Maui), L. m. /lammea (Molokai, extinct), L. m. montana (Lanai), L. m.
maculata (Oahu), and L. m. bairdi (Kauai). The subgenusLoxops con-

tainsone species,the Akepas,Loxopscoccinea,whichhas four raceson
four islands: L. c. coccinea(Hawaii), L. c. ochracea(Maui), L. c. ru/a
(Oahu, extinct) and L. c. caeruleirostris(Kauai).
The generaof Hawaiian Honeycreepers
differ widely with respectto

shape
andsizeof thebill andtongue,
andpresumably
in associated
anatomical
features.In manycases,as mightbe expected,directcorrelations
can be
made betweenjaw and tonguemorphologyin the severalgeneraand the
uses(biologicalroles) to which thesestructuresare put by the birds in
obtaining food. However, the details of these correlationsand similar
intragenericcorrelationshave not yet been described; such conclusions
dependupona combination

of precisefield observations,
morphological
dissectionsand, if possible,experimentalstudies.
Considerablefield observationson the habitats,food and feedingmethods
of Hawaiian Honeycreepers
are available,most of them done by a few
workerswho had the opportunityto reside on the Hawaiian Islandsfor
severalyears. Many of theseobservations
cannotbe repeatedtoday becauseseveralspecies
of drepanidids
are extinctor existin smallerpopulations
than they did at the time these earlier workerswere active. The more
importantwritingson the natural historyof the Hawaiian Honeycreepers
include Perkins (1893, 1895, 1901, 1903), Munro (1944), Henshaw
(1902), Bryan (1908) and Baldwin (1953).
Anatomical investigationsof the drepanididshave been scanty,far fewer
than the availablefield observations
and far fewer than permittedby longavailable materials.

In truth most of these anatomical studies should be

classedas descriptiveexternal morphology. The earliest and still most
extensivework is that of Hans Gadow whose results were publishedas

supplements
to Wilsonand Evans' great monograph(1891 and 1899:


6

ORNITHOLOGICAL

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15

219-249). Most of the remainingwork (Rothschild, 1893-1900: pls.
82 and 83; Hartert, 1893: xx; Lucas, 1897: fig. 3b; Gardner, 1925:
27-28, and pl. 3, fig. 19, pl. 13, fig. 140; Sushkin,1929: 379-381; and
Munro, 1944: 100, 119) dealswith the structureof the tongue,rhamphotheca (includingthe horny palate) and skull structure. Amadon (1950:
213-229) has a sectionon comparativeanatomyin whichhe discusses
and
figuresthoseaspects
of drepanididmorphology
described
by earlierworkers
and commentsupon the systematicrelevanceof these features. Finally,
Beecher(1951b: 283, 285, fig. 5; 1953: 310, 312-313, fig. 15) hypothesizeson the relationships
of the Drepanididaeto the Thraupidaevia the
medium of jaw musculaturepattern, horny palate, tongue architectureand
other features.

A detailedinvestigation
of the structuraland behavioraladaptations
for
feedingin this highly interestingexampleof adaptiveradiation has been
long overdue.Not only is the amountof publishedwork sadlyinsufficient
for any theorizingon the possiblerelationships

and evolutionof this family,
but much of it was done many years ago when our understandingof
functionalmorphology,in general, and of the avian jaw and tongue apparatus,in particular,was inadequatelyknown. Moreover, recent developments in many fundamental conceptsof comparative morphologyhave
revitalizedthe entire field and have provideda far sounderbasisfor comparative anatomical-evolutionary
studies. We proposeto undertakean extensiveinvestigationof the adaptiveradiation of the feeding apparatusin
the Drepanididaebaseduponthe recentlydevelopedconceptsof evolutionary
morphology.
As a start into this project,we choseto studythe functionalmorphology
and evolutionof the feedingapparatusin the genusLoxops, concentrating
upon the following taxa: L. sagittirostris(in part only), L. virens virens,
L. maculatamana, newtoni,and L. coccineacoccinea. The rhamphothecal,
skeletal and muscularfeaturesof the jaws and tongue apparatuswill be
describedand comparedin detail. Types of food taken and methodsof
feedingwill be correlatedas far as possiblewith the morphological
features
of the jaws and tongueand with their functionalinterpretations.Finally, we
hopeto speculate
on the evolutionof thesefeedingadaptationsand of the
taxa within Loxops.

The genusLoxops is particularlyadvantageous
for this initial study. It
has been long consideredas the mostprimitivegroupin the Psittirostrinae
and dose to, if not, the mostprimitivestockin the whole family. Moreover,membersof thisgenusshowconsiderable
variationin their morphology
and feeding methodswhich include: (a) nectarivorous-insectivorous
leaf
gleaners; (b) insectivorousleaf and bark gleaners; (c) bark and other

1973

RICHARDS

AND

BOCK:

FEEDING

APPARATUS

IN

LOXOPS

7

creviceprobers;and (d) cross-billed
insectivorous
leaf-budand bean-pod
openers.The speciesof Loxops have widespreadsympatrywith almost
every major island possessing
races of the three commonspecies(virens,
maculata and coccinea). These speciesare still sufficientlycommon to
permit field observationson their feeding methods. Moreover, several
practicalreasonsdeterminedthe choiceof this genusand of the particular
speciesstudied. Some specimensof L. virens and maculatawere already
availableto Richardsat the outsetof the study, and the other forms were

sufficientlycommonto permit taking of additionalspecimens.Members
of L. virens, maculata and coccineacould be observedon Maui and Hawaii,

islandson which living accomodations
were readily availableto Richards
as well as possessing
sufficientroads allowing travel to the interior of the
islandswhere the birds are found. Moreover, a searchfor L. sagittirostris
could be undertakenon Hawaii. Sufficientfunds and living accomodations
on Kauai were not availableto Richardsto permit inclusionof L. parva
in this study.
ACKNOWLEDGMENTS

The unusualdevelopmentof this study with one author (Bock) joining
the projectlong after completionof the originalresearchand writing of the
thesis,necessitates
separationof the acknowledgements.
Each part of these
acknowledgements
will be signedand referenceof the first personpronouns,
be they singularor plural, shouldbe readily apparent.
So many people have aided me in my field work and researchin so
many ways that it will be difficult to acknowledgeall of them for the
thanks they are due. I am indebtedto many friends and relativesin the
Hawaiian Islandswho so generouslyaided and showedme hospitalityand
gave me accessto their homes, mountain cabins, ranch lands and roads,
vehiclesand saddlehorses. Included amongthese people are my grandmother,IsabelleJones,my parents,Robert and CatherineThompson,my
uncle and aunt, Howard and Helen Farrar, my friend William Harkins of
Maul and a number of the cattlemen of the Kona coast and Mauna Kea,
Hawaii: R. L. Hind, Sr. and Jr:, Norman Greenwell, SherwoodGreenwell,

William Thompson,Herbert Shipman,Hartwell Carter, and RogerWilliams.
I wish to thank Colfin Lennox, Donald Smith and the other members of
the Board of Commissioners
of Agricultureand Forestryof the Territoryof
Hawaii for appointingme honorarybiologistand issuingpermits for the
collectionof drepanidids
in the forestreserves;RobertHiatt of the University
of Hawaii, for giving me equipment and suppliesfor the preservationof
specimens;membersof the staff of the Hawaii National Park Servicefor
giving me accessto cabinsand other facilities at Kilauea and Haleakala;


8

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EdwinH. Bryan,Jr., Curatorof Collections
at the BishopMuseumHonolulu,
for loan of specimens,
Alden H. Miller, directorof the Museumof Vertebrate
Zoologyat Berkeley,California,for accessto drepanididskeletalspecimens
and for generouslyputting at my disposalphotographicequipmentand
supplies.To my wife, ChristinaM. Richards,and my goodfriend, Robert
H. S. Glaserof Sacramento

JuniorCollege,California,I am gratefulfor
aid in the translationof parts of Germanpublications
on avian anatomy.
PaulH. Baldwinof ColoradoAgriculturaland MechanicalCollege,gaveme
much valuableadvice,informationand encouragement
before and during
the conducting
of my field work; furthermore,he put at my disposalsixteen
alcoholicspecimens
of Drepanididae,four of whichwere usedin this study.
William Beecherof the ChicagoNatural History Museumalso passedon
to me useful advice and information and answeredfor me many questions
put to him in correspondence.
I wish to thank my advisor,Dr. Hobart M.
Smith, and former advisors,Drs. Alden H. Miller and Harvey I. Fisher, for
their patience,encouragement
and helpful advice. This dissertation(Richards, 1957) was written in partial fulfillment of the requirementsfor the
doctor of philosophydegreeat the University of Illinois, Urbana.-•L. P.
Richards.

We wish to thank Mrs. Frances Jewel who devoted much skill and care

in assembling,
correcting
andlabelingthe originalfiguresdrawnby Richards
andusedin histhesisintothe final platesusedin thisstudy,and in drawing
a numberof new platesand text figuresthat becamenecessary
duringthe
final phasesof this study. We would alsolike to thank Miss SuzanneBudd
who completedmuch of the labelingand undertookthe long and arduous

task of final correctionsand additionsto the figures. We would like to
thank Drs. H. Morioka, R. S. Hikida, J. L. Cracraft and C. R. Shear for

their many helpful commentsand suggestions
given in the courseof many
discussions
duringthe summerof 1968 and thereafter.The final manuscript
was typed by Mrs. Julia Cracraft who transformedour handwrittenscrawl
into a clean typescriptwonderfully free of mistakes. Dr. Dean Amadon
made the facilitiesof the Departmentof Ornithology,American Museum
of Natural History available to us and provided us with much valuable
adviceand suggestions
from his extensiveknowledgeof the Drepanididae
for whichwe are mostgrateful. Supportfor the completionof this project
and for readyingthe manuscriptand figuresfor publicationcame from a
grant to W. J. Bock from the National ScienceFoundation (N.S.F.-G.B.
6909X) for studieson the feeding apparatusof the New World nineprimariedoscines.We wish to thank the National ScienceFoundationfor
agreeingto changesin the use of thesegrant funds which was the critical
factor permittingthe completionand publicationof this study.-•L. P.
Richards

and W. J. Bock.


1973

RICHARDS

AND

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METHODS

FEEDING

AND

APPARATUS

IN

LOXOPS

9

MATERIALS

Field Studies: Becausethe goal of this study was to correlatesomeof
the anatomicalstructures
of the headregionwith useof the bill and tongue
in feeding,not onlywerespecimens
of the Drepanididaeneededbut alsoas
many recordedobservations
as possibleon the methodsof feeding. Even
thoughsuchmen as Perkins,Munro, Henshawand Bryan recordedmuch
valuableinformationon feedingbehavior,they undoubtedlydid not write
with the thoughtin mindthat their observations
wouldbe usedsubsequently
in studiesof functionalanatomy.Therefore,it was importantthat the

feedingof thesebirdsbe observed
personally
undernaturalconditions
and
the minutiaeof useof the bill and tonguerecordedas fully as possiblefrom
the standpointof one interestedin the muscularand skeletalapparatuses
involved.

BetweenAugust11, 1950, and January17, 1951, a total of 59 days
were spentby LawrenceRichardsin the forestsof Hawaii, Maul and Oahu,

collecting
and observing
drepanidids.
Prior and subsequent
to this period,
five otherdayswere spentfor the samepurposes.Duringtheseperiods,
94 pagesof speciesaccountson drepanididswere written, of which 35
were on Loxops, and 48 drepanididswere collected,of which 23 were

Loxops.PaulH. BaldwingaveRichards
sevenadditional
alcoholic
specimens
of this genus,and the BishopMuseum loanedtwo incompletealcoholic
specimens
of sagittirostris,
on whichonly the occipitalregionsof the crania
remained. Of these32 specimensof Loxops, 25 were studied: L. sagittirostris(2 alcoholics),L. v. virens(8 alcoholics),L. m. mana (3 alcoholics,
1 skeleton),L. m. newtoni (5 alcoholics,2 skeletons),L. c. coccinea(3

alcoholics,1 skeleton). In additionto thesespecimens,
27 skeletonsof
L. v. virens and one of L. m. mana were available from the Museum of

VertebrateZoology. Admittedly,the numberof specimens
of each form
availablefor dissection
and studyis pitifully small,and thesesmallnumbers
of specimens
had to be usedas the basisfor statements,
suppositions,
and
conclusions
concerning
the wholelivingpopulationof eachspeciesor race
studied. We realize that this is not necessarilyscientificallysoundbut feel
thatthisstudyandits conclusions
arejustifiedin spiteof thesesmallsamples
becausethe Board of Commissioners
of the Departmentof Forestryand
Agriculturefor the Territory of Hawaii allowedunder specialpermit only
three spedmensof only certainspeciesor subspecies
of drepanididsto be
collected;because
someof the formsof drepanidids
collectedare practically
extinct;because
it sometimes
wasexceedingly
difficultto locatethe highly

localizedand sometimesseasonallyvarying rangesof some of the forms;
and becauseno onehad ever attemptedsucha functionalanatomicalstudy
on thisfamilynor had (and may neverhaveagainin futureyears) as highly


10

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a representative
collectionof specimens
of forms in this genus. All conclusionsmadeconcerning
any particularrace or speciesstudiedhave been
madeguardedlyandwith the reservation
duethembecauseof the smallsizeof
the sampleof availablespecimens.This fact waskept in mind at all times.
It can be surmisedthat, for a particularsubspecies,
sexualdimorphism,
age, and individualvariationwould not play importantroles in the morphologyof thoseparts of the skeletonand the importantdivisionsof the
jaw and tongue musculaturestudied, with one exception. This one exceptionis the rare Hawaii Akepa, Loxopsc. coccinea,in whichage and
individualfeedingbehavioraldifferencesmight, and probablydo, make
qutea bit of differencein the ontogenetic
development
of its asymmetrical

rhamphothecae,
jaw skeletonand jaw musculature.The study of this form
was basedmainly on adult males.
The specimens
werepreservedin the field in one of two ways. They were
eitherskinned,eviscerated
anddriedto be cleanedsubsequently
by dermestid
larvae as skeletalspecimens,
or they were preservedas "alcoholics."The
latter methodinvolvedinjectionof the abdominalcavity,usuallywithin a
few minutesafter deathwith 10 per cent formalin,and later wettingthe
feathersand skin with soap and water. The specimens
were then placed
in a fixing and preservedsolutioncomposedof 90 parts by volume of 70
per cent ethyl alcohol, five parts full strengthformalin and five parts
glycerin; the solutionwas changedonce. The specimens
were kept in the
preservingsolutionuntil the end of the field trip and were transferredto
70 per cent ethyl alcoholin the laboratory.
Dissectionand Drawing: In the laboratorythe heads of the alcoholic
specimens
wereskinnedpartiallyand the attachments
of the extrinsictongue
musculatureseparatedfrom the mandibleand skull, the floor of the buccal
cavityseveredfrom its lateralwallsand from the esophagus,
and the glossal
and laryngealapparatuses
removed. The glossaland attachedlaryngeal
apparatusand headwerepinnedto the wax bottomof a smallplasticdissectingpan, partiallyfilled with 70 per cent ethyl alcohol,and the tongue

and jaw musculatures
were then dissected
under a 20 power binoculardissecting microscope.

Drawingsof the tonguesweremadeto scalefrom the specimens.Drawings
of the tonguemusculature
weremadeon penciltracingsof ink drawingsof
glossal
skeletons.Drawingsof thejaw muscles
weremadeon penciltracings
of ink drawingsof the skulls.
The ink drawingsof the skulls were made in the following manner:
Photographs
weremadeof the bestpreserved
specimenof a skull for every
form studiedexceptsagittirostris,
for whichno skullwasavailable.For these
photographs
the mandibleswere gluedto the skullsin the closedposition.
Every skull was photographed
in three views-•lateral,left front oblique


1973

RICHARDS

AND

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FEEDING

APPARATUS

IN

LOXOPS

II

(i.e., looking posteriorlyand ventrallyinto the left orbit from the left
front), and ventral. Enlargedprints were made from these negativesso
that cranialheightin the lateral and obliqueviewsalwayswas kept constant
for all species.Cranialwidth, on the otherhand,in the ventralviewsvaried
proportionately
with the constantcranial heightin the four forms studied.
(It was assumedthat, in a singlegenusor family of birds of narrowlylimited
range in body size of the speciescomprisingthe group, the cranial height
would be proportional,or isometric,to the body size. This assumption
appearsto be reasonablefor the genusLoxopswhosememberspeciesare
uniform in height of the brain case; however,it remainsto be verified
for the whole family.) Thus photographsof the skullsof all speciesin the
genuswere then of differing magnifications,allowing differencesin shapes
and relative sizesof the bills and other, possiblyallometric,structureson
the skulls to become more evident.

From thesephotographsink tracingswere made of the three views of
the skull, upon which the jaw muscleswere drawn.
In the drawingsof the glossalskeletonsthe length of the fusedbasihyale

plus urohyale was kept constantin all species; therefore, magnifications
of the drawings of the glossal skeletonsof the four forms are not the
same. It was reasonedthat this length would probablyremain most stable
in evolutionarylengtheningor shorteningof the tongue and that it would
be isometricallyproportionalto body size throughoutthe family. The tongue
muscleswere drawn on these tracingsof the tongue skeleton.
The drawings of the tongues are at different magnificationsbut are
related to the constantlength of basihyaleplus urohyalein that they were
drawn at a magnificationtwice that of the corresponding
drawingsof the
glossalapparatus,except for the tongue of L. m. newtoni which is three
timesthe magnificationof the drawingof the glossalapparatusof that form.
All dissections,
descriptions
and preparations
of the figuresof the rhamphothecae,jaw skeletonand muscles,and glossalskeletonand musculaturewere
done, with the following exceptions,by Lawrence P. Richards between
1951 and 1956. The sknllsof the severaltaxa studiedwere jointly described
from specimens
by Walter J. Bock and LawrenceP. Richardsin light of
new knowledgeof avian cranial kinesispublishedsince 1957. Severaladditional drawingsof the rhamphothecae
and of the skull were preparedby
Mrs.

Frances

Jewel.

Plates: To preserveclarity in the figures of the skeletalelements,the
pertinentstructures

were labeledon a separatetext figure (Figs. 4, 5, 6
and 12); comparisonof this figure with thosein the platesshouldposeno
problems. Both the jaw and the tongue musculatureare sufficientlycomplex that the plates of each specieshad to be labeled fully; however,
obviousmuscles,such as the m. depressormandibulae,were not indicated


12

ORNITHOLOGICAL

MONOGRAPHS

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15

in all plates. The abbreviations
usedin the text figuresand platesand those
usedin the text are summarizedin the glossary.
Unlessotherwisespecified,the specimens
usedfor illustratingthe skull
and the glossalmechanismand the outlinesof theseskeletalelementswhen
drawing the musculatureare as follows: L. v. virens, juv. 9, no. MVZ
118, 763; L. m. mana, ad. •, no. MVZ 118, 823; L. m. newtoni, juv.(?)
•, no. MVZ 122, 615; L. c. coccinea,right-billed,ad. •, no. MVZ 122,
613; and L. sagittirostris,only occipitalregion of skull, age and sex unknown, no number,BPBM. In the descriptionsof the plates of the jaw or
the tonguemusculature,the museumcatalognumbersor the field catalog
numbers (of Paul H. Baldwin or Lawrence P. Richards) refer to the
specimens
usedfor the dissectionand drawingsof the soft parts; the age

and/or sex of the specimens
are statedwhen known. The magnifications
are indicatedby an "x" followedby a numbergivingthe degreeof magnification. Abbreviations used are MVZ, Museum of Vertebrate Zoology,
University of California, Berkeley; BPBM, B.P. Bishop Museum, Honolulu, Hawaii (these specimensdo not have catalognumbers); LPR, collected by Lawrence P. Richards and not as yet repositedin a museum;
PHB, collectedby Paul H. Baldwin, ColoradoState University,Ft. Collins,
and not as yet repositedin a museum.
Kinetics: In order to measurethe kinetics of the skulls (see section under

anatomyon osteologyof jaws and skull), a machinewas designedand built
(Fig. 2); detailson the construction
and operationof this measuringdevice
may be obtainedfrom Richards (1957).
Relative size differencesof the jaw muscles: An initial working hypothesis was made that muscle size is, in general, a rough index of muscle
strengthamong homologousmuscles. On the basis of this assumption,
Richardsjudgedthe relative size differencesof the jaw musclesin the four
taxa of Loxops studied; these are summarizedin Table 3. The two sides
of coccineawere consideredseparately,giving a total of five classesin this
comparison.L. sagittirostris
was excludedfrom this comparisonbecause
only its m. depressormandibulaewas available. This judgementwas done
by assigning
ratingnumbers,designating
relativesize,to almosteverymuscle
part for all taxa. The number"1" wasgivento the speciesor race (or side
of coccinea)havingthe largestmuscleor part of a muscleamongthe series
of homologous
musclesin the severaltaxa under study; number "2" was
aSSigned
to the taxon with the secondlargestmuscleand so on. If two or
more forms has a musclepart of approximatelythe samesize, these two

or more were given the same rating.
In this systemof rating the relative sizes of homologousmuscles,no
attemptwas madeto distinguish
quantitativedifferencesamongthe forms.
Furthermore,judgementof the sizeswas done visuallyand not by means


1973

RICHARDS

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13


14

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of measuringlinear dimensions,
volumeor mass. The necessary
large sample
of specimens
for determination
of size by methodsof significantaccuracy
were not available. Moreover,the attachmentsof the musclesand the lengths
of their momentarmswere not considered
so that the torquesproducedby
thesemuscles(Bock, 1968) were not compared;thesetorques,rather than
the forces,producedby the musclesare the more importantmeasurements
in comparingthe contributionof each muscleto the action of the skeletal
system.

The initial assumptionused in this comparisonis not valid for all comparisonsof skeletalmusclesas pointed out by Gans and Bock (1965).
Rather

one should

measure

the total

cross-sectional

area

of the muscle

fibers as an index to force production,the length of the fibers as an index
to displacementabilities,and the angle of pinnatenessas an index to the
force and displacement
componentalong the vector directionof the muscle
pull. Unfortunately,thesefactorsare more easilydiscussed
than measured,
and we realize fully the shortcomingsof our comparisonsin not undertaking thesemeasurements.Size as used in thesecomparsionsis a relatively
valid measurementof the severalfunctionalpropertiesin a seriesof homologous muscles not too dissimilar in size and fiber arrangement such as
those under considerationin this study. And the conclusionsreached on
the basisof these comparisons
are relativelyrough ones that do not go
beyondthe assumptions
employed.
TYPES

OF FOOD

AND

FEEDING

METHODS

In this sectionwe have not only consultedRichards'field notes but
have drawn heavily upon the publishedobservationsof ornithologistssuch

as Robert C. L. Perkins, George C. Munro, Henry W. Henshaw,William
A. Bryan and Paul H. Baldwin who have studied drepanididsover long
periods and at first hand in the field. This information is somewhat
scatteredin the literature, and we believe a useful purposeis served by
summarizingit, in that the ideasof severalnaturalistsbasedupon extensive
observationare brought to bear on the intricaciesof feeding behavior in
this genus. The original observationsreported in this chapter are those
of LawrenceP. Richardswho assumes
primaryresponsibility
for the material
presentedherein; the pronoun 'T' refers to him.
HAWAII AMAKIHI, Loxops virens virens

Types of Food Taken: Accordingto Baldwin (1953: 287) this species
feeds on insectsand other arthropods,nectar, and juices of fruits in this
order of importance.By and large this statementis substantiated
by the
observationsof Perkins (1893, 1903), Henshaw (1902), Munro (1944)
and myself.