The Functional Morphology,/Systematics and
Behavioural Ecology of Parrotfishes (Family scaridae).
Volume 1
Morphology and systematics
Thesis submitted by
David Roy BELLWOOD BSc (Hons.) (Bath, U.K.)
in December, 1985
for the degree of Doctor of Philosophy in
the Department of Zoology at
James Cook University of North Queensland,
Australia.
I, the undersigned, the author of this thesis, understand that the
following restriction placed by me on access to this thesis will not
extend beyond three years from the date on which the thesis is
submitted to the University..
I wish to place restriction on access to this thesis as follows:
Access not to be permitted for a period of 3 years.
After this period has elapsed I understand that James Cook
University of North Queensland will make it available for use within
the University Library and, by microfilm or other photographic
means, allow access to users in other approved libraries. All users
consulting this thesis will have to sign the following statement:
"In consultingparaphrase itof the author;any assistance
this thesis I agree not to copy or closelyin whole or in part without the written consent
and to make proper written acknowledgement forwhich I have obtained from it."
.~ ...~.....
iiiABSTRACT
The functional morphology and behavioural ecology of the
parrotfishes (family scaridae) were investigated to assess the
degree of correlation between them.
Twenty-two species of parrotfishes from the subfamily Scarinae
were examined mainly from reefs around Lizard Island, Great Barrier
Reef, Australia.
Morphological studies of the osteology and myology of the heads
of adult parrotfishes revealed two morphological groups within the
genus Scarus, vtz. the 'sordidus' and 'frenatus' groups. species
in the 'sordidus' group are characterized by: uneven cutting edges
on the jaws, an entopterygoid lateral process, a tightly bound
interdigitating maxilla and premaxilla, three rows of teeth on the
upper pharyngeal bones, well developed adductor mandibulae sections
~, A2 and A3 and an additional unique muscle, the Awy. Species in
the 'frenatus' group are characterized by: even cutting edges on
the jaws, a slightly protrusible premaxilla, two rows of teeth on
the upper pharyngeal bones, fusion of the abductor muscle section
~a and A2 in some species and a thin strap-like A3 section which
inserts only on the articular. The morphology of the heads of
species in other genera, namely, Cetoscarus btcoLor, BoLbometopon
murtcatum and Htpposcarus Longtceps was marked by their possession
of a quadrato mandibularis internus muscle and the non-articulatory
articular-dentary joint in C. btcoLor and B. murtcatum.
iv
Analyses of the two morphological groups indicated a marked
difference in the functional abilities of species in the two groups.
The morphological characteristics of 'sordidus' group species enable
them to bite the substratum with a large powerful cracking bite.
Species in this group are therefore described as 'biters', The
morphological characteristics of 'frenatus' group species are
consistent with the requirements necessary for scraping
substratum with small, weak bites.
therefore described as 'scrapers'.
Species in this group are
Of the species examined in this study, the following species
are functional 'biters'~ S. bteekert, S. gtbbUS and S. sordtdus,
whereas the folloWing are functional 'scrapers': S. brevtfttts,
s. dtmtdtatus, s. ftavtpeatoratts, S. jrenatus, S. ghobban,
S. gtobtceps, S. tongtptnnts, S. ntger, S. ovtaeps, S. pstttacus,
S. rtvutatus, S. rUbrovtotaaeus, S, sahtegett, S. sptnus,
S. trtaotor and Scarus sp. (af. tunuta). Because they lack some
specialized morphological features associated with the biting or
scraping strategies of species in the genus Scarus, Cetoscarus
btcotor and Botbometopon murtcatum are considered 'proto-biters',
whilst Htpposaarus tongtaeps is considered a 'proto-scraper'.
These differences are not apparent in juvenile specimens less
than 50 mm standard length. specimens of Saarus smaller than this
are extremely similar. Small specimens « 14 mm S.L.), in
particular, differ markedly from the adults in the possession of
caniform teeth and a simple, non-sacculated intestine.
v
Functional interpretations of the anatomy of the head and
intestine of juvenile scarids suggest that they progress from an
initial carnivorous phase to a selective grazing stage before
becoming functional 'scrapers' at about 50 rom S.L. 'Biting' species
only possess the full complement of biting characteristics above
90 mm S.L,
Field observations of adults revealed two feeding guilds within
the genus Scarus which correspond with the two functional groups.
(1) 'Biting' t,e. 'sordidus' group species are characterized by: i)
infrequent, large bites which scar the Substratum, ii) a propensity
to feed upon convex substrata, and iii) aggressive interspecific
interactions, when displayed, predominantly directed towards other
'sordidus' group species. (2) 'scraping' t.e. 'frenatus' group
species are characterized by: i) numerous small bites which rarely
scar the substratum, ii) a tendency to feed on a range of substrata,
and iii) aggressive interspecific interactions, when displayed,
predominantly directed towards other 'frenatus' group species,
These feeding strategies strongly influence the roles played by
parrotfishes as coral predators and bioeroding agents. The major
coral predator is Botbometopon muricatum. Bioerosion is primarily
the result of feeding by 'sordidus' group species, Cetoscarus
bicotor and B. murtcatum. It is therefore proposed that the
distribution of these species within and between reefs may influence
the extent and rates of bioerosion, the topography of the substratum
and the distribution of various coral morphs.
viField observations of juvenile scarids revealed a wide range of
behavioural traits, although these did not correspond with the
'sordidus' and 'frenatus' groupings. s. frena~us in particular,
differed from other juvenile 'frenatus' group species in its feeding
behaviour. An analysis of the gut contents of the juveniles of
several species showed marked changes in the diet, from being
initially predominantly carnivorous to herbivorous. These changes
were strongly correlated with changes in morphology and behaviour.
In addition to functional considerations, the morphological
analyses in this study were used to examine the systematic
relationships between genera in the subfamily Scarinae. The present
generic status of Ce~oscarus, Bo~bome~opon and Htpposcarus is
supported. The genus Scarus contains two distinct groups which may
be recognized at the generic level.
A descriptive account of the ontogeny of the colour patterns of
the juvenile phase of 22 species is presented to facilitate the
study of juvenile scarids in the field. The colour patterns of
juvenile scarids are interpreted in terms of concealment
colouration, including crypticism, camouflage and mimicry. In the
species examined, there is a strong correlation between schooling
behaviour, the range of patterns displayed, and the speed with which
the patterns may be changed.
TABLE OF CONTENTS
ABSTRACT
TABLE OF CONTENTS
LIST OF FIGURES
LIST OF TABLES
ACKNOWLEDGEMENTS
GENERAL INTRODUCTION
vii
iii
vi.i
ix
xv
xviii
1
PART I MORPHOLOGY (Volume 1)
Chapter 1 THE MORPHOLOGY OF ADULT SCARIDS 5
1. 3.51. 3.61.3.7
1.1
1.2
1.3
Introduction
Materials, Methods and Terminology
A The Muscular and Skeletal System
Observations1.3.1 External appearance and integument1.3.2 Osteology1.3.3 Myology1.3.4 The 'sordidus' and 'frenatus' groups
1.3.4.1 The 'sordidus' group1.3.4.2 The 'frenatus' groupCe~oscarus btcoLorBoLbome~opon murtca~um
Htpposcarus Longtceps
5
6
11121238616163738696
Functional Interpretations1.41.4.11.4.21.4.31.4.41.4.5
'Sordidus' group species as 'bite~s'
'Prenatus' group species as 'scrapers'C. btcoLor and B. murtca~us
Htpposcarus LongtcepsThe pharyngeal apparatus
107107115120123123
1.5
1.6
1.7
B - The Visceral Anatomy
Observations
Functional Interpretations
Discussion
132
139
150
Chapter 2 THE MORPHOLOGY OF JUVENILE SCARIDS 153
2.12.22.32.42.5
IntroductionMaterials and MethodsObservationsFunctional InterpretationsDiscussion
153155155173178
PART II SYSTEMATICS (Volume ~)
viii
Chapter 3 SYSTEMATICS OF THE SCARIDAE:PHYLOGENY AND GENERIC CLASSIFICATION
Chapter 4 SYSTEMATICS OF THE SCARIDAE:ONTOGENY OF JUVENILE COLOUR PATTERNS
184
209
4.i4.24.3
4.4
IntroductionMaterials and MethodsResults4.3.1 Meristic data4.3.2 Field observations4.3.3 Colour patterns4.3.4 Species descriptionsDiscussion
209U3U42~4
21.5U7223277
PART III ECOLOGY (Volume 2)
Chapter 5 THE BEHAVIOURAL ECOLOGY OF ADULT SCARIDS
A Feeding Biology
290
5.15.25.35.4
5.55.65.75.8
IntroductionMaterials and MethodsResultsDiscussion
B General Biology
IntroductionMaterials and MethodsResultsDiscussion
29029629931.2
318321322330
Chapter 6 THE BEHAVIOURAL ECOLOGY OF JUVENILE SCARlDS
Part A - Feeding Biology
364
6.16.26.36.4
6.56.66.76.8
IntroductionMaterials and MethodsResultsDiscussion
Part B - General Biology
IntroductionMaterials and MethodsResultsDiscussion
364365369384
392394399423
CONCLUDING DISCUSSION
APPENDIX 1
APPENDIX 2
REFERENCES
434
454
455
461
Figure
1.1 A
1.1 B
1.2
1.3
1.4 A
1,4B
1.5 A
1.5 B
1.5 C
1.5 0
1.6 A
1.6 B
1.6 C
1.6 0
1.7 A
1.7 B
1.7 C
1.7 0
1.8 A
1.8 B
1.8 C
1.8 0
1.9 A
1.9B
ix
LIST OF FIGURES
Page
The external anatomy of the head of Scarus sordtdus .... 13
The external anatomy of the head of Scarus frena~us.... 13
The osteology of the head of Scarus sordtdus 15
The osteology of the head of Scarus frena~us 16
A lateral view of the suspensorium of S. sordtduS 18
A lateral view of the suspensorium of S. frena~us 18
A lateral view of the maxilla of S. sordtdus 22
A medial view of the maxilla of S. sordtdus 22
A lateral view of the maxilla of S. sordtdus 22
A medial view of the maxilla of S. frena~us..•......... 22
A lateral view of the premaxilla of S. sordtdus 25
A lateral view of the premaxilla of S. frena~us 25
A ventro-medial view of the premaxilla of S. sordtdus .. 25
A ventro-medial view of the premaxilla of S. frena~us .. 25
A lateral view of the articular of S. sordtdus 29
A medial view of the articular of S. frena~us 29
A lateral view of the articular of S. sordtdus 29
A medial view of the articular of S. frena1;us 29
A lateral view of the dentary of S. sordtdus ........... 32
A lateral view of the dentary of S. frena~us........... 32
A medial view of the dentary of S. sordtdus ............ 32
A medial view of the dentary of S. frena~us............ 32
An anterior view of the dentary cutting edge ofS. sordidus 33
An anterior view of the dentary cutting edge ofS. frena1;us 33
1. 10
1.11 A
1.1.1 B
1.J.2 A
1.J.2 B
1.B A
1.13 B
1.14 A
1.14 B
1.15 A
1.15 B
1.16
1.17 A
1.17 B
1.18 A
1.18 B
1.18 C
1.18 D
1.18 E
x
The head of scarus sordtaus with the integument, nasal,lacrymal, circumorbitals, A1a and part of A1~ removed,showing the shading conventions used in this section ... 39
The head of S. sordtaus with the integument andcircumorbitals removed 41
The head of S. soratd:u.s with the integument, nasal,lacrymal, circumorbitals, A1a and part of A1~ removed .. 41
The head of S. frenatus with the integument removed.... 45
The head of S. frenatus with the integument, nasal,lacrymal, circumorbitals and parts of Ala/A2 removed ... 45
A medial view of the upper jaw musculature ofS. sordtdus 46
A medial view of the upper jaw musculature ofS. frenai;us 46
A medial view of the lower jaw musculature ofS. sordtdus 47
A medial view of the lower jaw musculature ofS. frena1;us 47
A lateral view of the pharyngeal apparatus ofS. soratdus 51
A lateral view of the pharyngeal apparatus ofS. frenatus 51
The head of a 388 rom S.L. Cetoscarus btcoLor withthe integument, nasal, lacrymal, circumorbitalsand part of A1 removed 79
A lateral view of the neurocranium of BoLbometoponmurtcatum 80
A lateral view of the neurocranium of CetoscarusbtcoLor 80
A ventral view of the neurocranium of CetoscarusbtcoLor 81
A ventral view of the neurocranium of BOLbometoponmurtcatum 81
A ventral view of the neurocranium of HtpposcarusLongtceps 81
A ventral view of the neurocranium of Scarus sorataus .. 81
A ventral view of the neurocranium of Scarus frenatus .. 81
1.1.9
1.20
1.21 A
1.21 B
1.21 C
1.22 A
1.22 B
1.23
1.24
2.1 A
2.1 B
2.2
2.3
3.1
3.2
4.1
xi
The head of a 530 rom S.L. BoLbome~opon murtca~um wi~h
~he in~egument, nasal, lacrymal, circumorbitals andpart of Al removed 92
rrhe head of a 329 rom S.L. Htpposcarus "Longtceps withthe integument, nasal, lacrymal and circumorbitalsremoved 101
A lateral view of the neurocranium of Htpposcarustongtceps 102
A lateral view of the neurocranium of S. sorataus ..... 102
A lateral view of the neurocranium of S. frena~us..... 102
The dentary of S. soratdus showing the theoreticalforces acting upon the dentary during musclecontraction 110
A diagrama~ic figure describing ~he relationshipbetween the angle of a muscle and its mechanicalefficiency .............•.............................. 114
A diagramatic figure describing the properties ofmuscles wi~h weakly pinnate or strongly pinnatefibres .......................•........................ 114
The three types of intes~inal pattern found inscarue species 136
A lateral view of the anterior edge of thepremaxilla of a 9.0 rom S.L. S. sorataus 157
A lateral view of the anterior edge of thepremaxilla of a 8.7 mm S.L. S. frena~us 157
The head of S. sorataus at 25.0 rom S.L. with theintegument, nasal, lacrymal and circumorbitalsremoved 161
The head of S. frena~us at 26.5 mm S.L. with theintegument, nasal, lacrymal and circumorbitalsremoved 165
A cladogram showing the proposed phylogeny of thegenera in the subfamily Scarinae 188
The phylogeny of the genera in the family Scaridaeas proposed by schultz (1958) 194
A series of diagrams showing the ontogenetic changesin the colour pattern of juvenile Scarus speciesleading to the formation of the four primary stripesshown in Figure 4.2 218
xii
4.2 The 'typical' colour pattern of a juvenile Scarusspecies showing the position of the four primary darklongitudinal stripes and the six vertical bands 2~9
S. dt.mtdta1;us : 30.5 nun S. L ....•........•. 0 •• 0 0 0 •••••. 248
S. ~ongtptnnts : 75 1111II S.L .... 0.0 ••.••••...••. 0.0. 0" .249
S.~ongt.ptnnts : 39 1111II S.L 0.0 ••••••••••.•• 249
S. ovtceps 32 nun S.L. . . . 0 0 .248
S. ovt.ceps 73 nun S.L. 0 • 00 . .. .. .. . 0 .248
S. ghobban 53 mm S.L. I· •• . 0 . .. . ~ . • • ... II ,. .249
33 1111II S.L 0 •• 00 •• 0 .•••• 247
44 1111II S.L 0 .••••••• 0 •••••• 247
26 1111II S .L 0 ••• 0 •••••.•• 244
28.5 rom S.L .... 0 0 •..•••••••.• 0 •• 0. 0" .245
54 nun S. L 0 .•• 0 ••••••••••••• 245
55 1111II S.L ........•....•..•• 0 ••• o. 0 ••.• 245
31 nun S.L ...•................ o. 00.0 •.••. 246
22 mm S.L•..........•......•••..•..... 0 .246
55 mm S.L .... 0 ••.•.••••••••.•• 0 ••• 0 ••••• 247
10.5 nun S.L ...•.................•. 0 ••.•• 246
40 1111II S. L 0 0 • 0 ••••• 244
46 mm S .L ... 0 ••.• 0 •.••••. 0 • 0 • 0 .0 •••• 0 .•• 242
54 mm S. L 0 • 0 .•••• 0 0 .•• 242
24 mm S. L ....••.............. 0 • 0 •• 0 ••••••• 243
40 mm S. L ........................• 0 •...•• 0243
28.5 mm S.L .. 0 .•••••••.•.••.. 0 ••• 0000 ••.•• 243
25 mm S.L .•..............•. 0 ••• 0 •• 0 ••.•. 244
33 mm S.L...................•. 0" 0" 0.0.242
24 nun S .L " 0 •••••• 250
9.5 nun S.L 0 .•••••••.••. 0.0.250
S. b~ee1<.ert
S. b7,ee7<ert
S. b7,ee7<ert
S. gtbbus
S. gtbbus
S. gtbbus
S. sordtdus
S. sordt.dus
S. brevt.jt7,ts
S. brevt.jt~ts
S. brevt.jt~ts
S. brevt.jt7,ts
S. jrena1;us
S. jrena1;us
S. jrena1;us
S. jrena1;us
S. j~avtpec1;ora~ts
S. ntger
S. ntger
S. j~avt.pec1;ora~t.s
4.3 A
4.3 B
4.3 C
4.4 A
4.4 B
4.4 C
4.5 A
4.5 B
4.5 C
4.6 A
4.6 B
4.6 C
4.7 A
4.7 B
4.7 C
4.8 A
4.8 B
4.8 C
4.9 A
4.9 B
4.9 C
4.10 A
4.~0 B
4.~0 C
4.11 A
4.11 B
xiii
Ca101;omus caro1tnus 43 rom S.L .........•.•..••.••..•• 256
Ca101;omus caroLtnus 43 rom S.L 256
Ce1;oscarus btco7,or : 11 rom S.L 255
S. 1;rtco~or(cf. S. forS1;ent) : 61 nun S.L •.••.•....•••• 251
33 nun S.L ..•......•.•.••.••.•.• 255
10.3 rom S.L 255
38 nun S.L 254
22.5 nun S.L ..••..•....•••••••..•.. 254
18 mm S. L ....•..••.....•.•.••..... 254
34 nun S.L .•..........••..•..•..•••••.•••••• 250
57 nun S. L 251
S. rtvu7,a1;us 49 nun S.L. . . .. .. .252
S. sCh~ege7,t 37 nun S.L. ·. .. .. . .. .252
S. SC'h7,ege7,t 38 nun S.L. . ..· .. .. ·.. " . . . . .252
S. sptnus 20 nun S.L. . . ..... ... ·. . • iii ...... . . . .253
S. sptnus 22 nun S.L. . · . . . . . . . . .253
S. spt.nus 27 nun S.L. .. .. . . .. · • .... iii .. .. .. 253
A ventral view of the upper pharyngeal tooth rows ofa 128 rom S.L. S. rtvu1a1;us 260
S. rutlrovto7,aceus
S. rUbrovto1-aceus
S. rUbruvto~aceus
S. sp. ( ct· 7,unu1-a)?
S. sp. ( ct. 7,unu~a)?
A diagramatic figure of the three parametersmeasured when quantifying acarid feeding scars 298
A ventral view of the upper pharyngeal tooth rows ofa 128 rom S. L. S. g10tltceps .............•.••.•••.•••.•. 260
S. ntger
A diagramatic figure showing the disproportionateeffect of an increase in the bite length on theratio of H/L (bite height/bite length) 298
Ht-pposcarus 7,ongtceps 48 rom S.L .....••..••.•..•..••• 256
The location of the major study sites in thelagoon and at North Reef, Lizard Island 297
S. pstt;1;acus : 29.5 nun S. L ................•.....••.... 251
s. nt-ger4.~~ C
4.~2 A
4.~2 B
4.~2 C
4.~3 A
4.~3 B
4.B C
4.~4 A
4.14 B
4.14 C
4.15 A
4.~5 B
4.~5 C
4.16 A
4.16 B
4.~6 C
4.17 A
4.~7 B
4.17 C
4.U A
4.18 B
5.1
5.2 A
5.2 B
5.3 The foray sizes of two Scarus species 302
6.1 A
6.1 B
6.2 A
6.2 B
6.3
6.4
6.5
6.6
6.7
6.8
6.9 A
6.9 B
6.10
7.1 A
7.1 B
7.1 C
xiv
The mean feeding rates of three juvenile Scarusspecies between 20 and 120 mm T.L 370
The mean foray size of three juvenile Scarusspecies between 20 and 120 mm T.L 370
The intestinal contents of juvenile scarids;algae and sand , 382
The intestinal contents of juvenile scarids;crustacea. . . . . . . . . . . . . . . . . . 382
A summary of the ontogenetic changes in thebehaviour, diet and morphology of juvenile scarids .... 385
The relative abundance of juvenile scarids at theNorth Reef and lagoon study sites during the 1982-3and 1983-4 November-January recruitment periods 400
The relative abundance of juvenile scarids at threedepths in the North Reef study site and at two depthsin the lagoon study site, during the 1982-3 November-January recruitment period 401
The relationship between horne range/territoryarea and total length of juvenile scarids 406
The horne ranges of two juvenile S. sordtdusin the lagoon study site 407
A vertical profile of the primary study area at theNorth Reef study site, showing the distribution ofhorne ranges/territories of juvenile scarids inthe study area 412
The relative rates of aggression by pomacentridstowards juvenile scarids in the lagoon study site ..... 419
The relative rates of aggression by pomacentridsand Acan~hurus ttnea~us towards juvenile S. frena~us
in the lagoon study site 419
The feeding preferences of juvenile scarids: Themean number of juvenile scarids feeding on sixexperimental algal-covered substratum types 422
The proposed distribution of early scarids duringthe late Eocene period 448
The proposed distribution of the major scaridgroups approximately 4 million years ago.~ 448
The present di~tribution of the major scarid groups ... 448
Table
1.J.
1.2
1.3
1.4
1.5 A
1.5B
1.5 C
1.6
1.7
2.1
2.2
2.3
3.1
5.1
5.2
5.3
5.4
5.5 A
5.5 B
LIST OF TABLES
Page
A partial synonomy of the Scaridae of theGreat Barrier Reef 7
The morphology of adult scarids: Material examined .... 8
Abbreviations used in the figures 9
A comparative list of relative liver weights 134
The liver weights of two Scarus species 135
The intestinal length va. standard length of twoscarus species 135
The intestinal length vs. body weight of twosoar-us species 135
The distribution of intestinal types in Scarusspecies 138
Gut lengths of herbivorous reef fishes •............. 143
The morphology of juvenile scarids: materialexamined 156
Ontogenetic changes in the morphology of theintestinal tract of juvenile scarids 172
The functional morphology of juvenile scarids:a summary 179
The distribution of morphological charactersamong the scarid genera 189
Variability in the colour patterns of somejuvenile Scarus species 212
The feeding rates of six Scarus species 300
Observations of the feeding rates and the extentof scarring of the substratum by scarids 301
The size of substratum scars which result fromthe grazing activity of scarids 304
Patterns of substratum utilization byS. sordtdus and S. frena~us 307
An analysis of the curvature of the substratagrazed by S. sordtdus and S. frena~us 308
A comparison of the bite-scar lengths ofS. sordtdus and S. frena~us 308
xv
5.6
5.7
5.8 A
5.8 B
5.9
5.10
5.21 A
5.11 B
5.22 A
5.12 B
6.1
6.2
6.3 A
6.3 B
6.3 C
6.4
6.5
6.6
xvi
Coral species eaten by scarids 320
A summary of the morphological and behaviouralcharacteristics of 'sordidus' and 'frenatus'group species 323
Duration and size of home ranges/territories ofscarids: A - known individuals, at North Reef 323
Ouration and size of home ranges/territories ofscarids: B - permanent sites, unknownindividuals, at North Reef ... , .. ", " .... ,., , .. '" .. 323
Aggressive interactions between scarids .. ". "" .... 325
Differences in the extent of interspecificaggression by terminal and initial phaseS. jrenat;us 329
Estimated acarid bioerosion rates atNorth Reef, Lizard Island .....•................ , .... 353
Scarid abundances: a comparison betweenCaribbean and Indo-pacific reefs." ,., 353
Estimates of bioerosion by scarids: acomparison between the Caribbean and theGreat Barrier Reef 354
Rates of bioerosion: a summary 354
Functional interpretations of the morphologyof juvenile scarids 366
Size-related differences in the feeding ratesof three juvenile Scarus species between20 and 220 mm T.L 372
Changes in the bite rate and foray size ofS. sordtdus between 10 and 29.9 rom T.L 372
The feeding rates of S. sordtdus andS. frenatus between 20 and 120 rom T.L 372
The mean number of bites per foray of S. sordtdusand S. frenatus between 20 and 120 rom T.L 372
Qualitative observations of the feeding ratesof juvenile scarids between 40 and 120 rom T.L .... , .. 373
Size-related differences in the mean foraysize of three juvenile Scarus speciesbetween 20 and 120 rom T.L 374
The intestinal contents of juvenile scarids- A: Algae, sand and crustacea 380
6.1
. 6.8
6.9
6.10
6.12
6.13
6.1.4
7.1.
xvii
The intestinal contents of juvenile scarids- B: Crustacea 381
The intestinal contents of some juvenileherbivorous reef fishes other than scarids 383
Relative rates of recruitment at the lagoonand North Reef study sites during threesettlement seasons 403
A list of the acarid speies present as newrecruits and juveniles in the vicinity of thelagoon and North Reef study sites .................•. 404
The duration and nature of site attachmentin juvenile scarids 410
The size of early post-recruit scarids overvarious substratum types in the North Reef andlagoon study sites 415
Aggressive interactions of three Scarus species ..... 411
Aggressive interactions of juvenile scarids 41.8
The relative frequency of attacks uponjuvenile scarids by various damselfish speciesat the North Reef and lagoon study sites 420
A summary of the biological factors influencingthe three post-larval life stages of scarids 443
xviiiACKNOWLEDGEMENTS
Facilities for this study were provided by the School of
Biological Sciences, James Cook University, and I am grateful to the
former Head of the school, Professor C. Burdon-Jones, the present
Head of Zoology, Professor R.E. Jones, and other staff members for
their assistance.
I would like to thank my supervisor, Dr. N. E. Milward for his
support and guidance.
Most of the field work in this study was undertaken at Lizard
Island Research station, a facility of the Australian Museum. My
time at the Lizard Island was both pleasant and rewarding as a
result of the kindness, humour and fellowship of the people there.
In particular I wish to extend my gratitude to Hugh Sweatman, Bill
Gladstone, Jeff Leis, Jack Randall, Vicki Harriott, Lyle vail, Randy
Olson, Patrick Filmar-Sankey, John Chisolm, Geoff Smith and Roger
Steene. I am particularly endebted to Dr. J.H. Choat. His
encouragement and infectious enthusiasm was a source of much
inspiration. My visits to Lizard Island were both comfortable and
productive, primarily as a result of the thoughtfulness and
painstaking efforts of Lois and Barry Goldman.
specimens were kindly donated by: Drs G.R. Russ and
D.McB. Williams (Australian Institute of Marine science);
Dr. J.H. Choat (University of Auckland); Dr. P.O. Doherty (Griffith
University); Dr. J.E. Randall (Bernice P. Bishop Museum);
A. Cabanban (Silliman University); Dr. G. Denton, O.S. Perez,
L.L. Dolar, R.S. Smith and J. Chisolm (J.c.u.).
xix
I wish to thank the following people for their helpful
discussions and/or comments on various drafts of this thesist Drs
C. Alaxander, P. Arnold, P. Doherty, D.G. Reid, G.R. Russ,
D.HCB. Williams, Associate Professor R. Kenny, Professor R.E. Jones
and my collegues at J.C.U. and Lizard Island.
Some publications were kindly translated by Dirk Zeller and
Tomoko Yoda.
This project was supported by a scholarship from the Drapers'
Company London, to whom I am extremely grateful. Additional
financial support was kindly provided by the Great Barrier Reef
Marine Park Authority. The completion of this thesis would not have
been possibly without the timely financial assistance of my parents
who supported me during the latter part of my studies.
I wish to thank Orpha S. Perez for her friendship and
invaluable assistance in the preparation of this thesis.
Finally, I would like to thank the two people whose thoughts
and guidance throughout my studies have been so valuable. To June
and Roy, my parents, this thesis is as much yours as it is mine.
xx
DECLARATION
I declare that this thesis is my own work and has not been
submitted in any form for another degree or diploma at any
university or other institution of tertiary education.
Information derived from the published or unpublished work of
others has been acknowledged in the text and a list of
references is given.
D.R. Bellwood
December, 1985
1
GENERAL INTRODUCTION
The scaridae t is a distinctive group of perciform teleosts,
characterized by the possession of a pharYngeal mill and fused
teeth, which form dental plates. Scarid species have a tropical and
sub-tropical distribution and are typically associated with coral
reefs. They are predominantly herbivorous and form a conspicuous
part of the herbivorous reef fish community. At present, there are
69 recognised species in 12 genera (Schultz, 1969 and Randall &
Bruce, 1983).
Members of the scaridae are predominantly protogYnous
hermaphrodites, with two main colour phases, a drab initial phase
(IP) and a colourful terminal phase (TP) (Robertson & warner, 1978).
Initial phase individuals may be either male or female, whilst
terminal phase individuals are invariably male. Some individuals
are male throughout their life, during both initial and terminal
phases; these are referred to as primary males. Most males,
however, are secondary males and, as such, spend the initial phase
period as females before developing testes and exhibiting the
terminal phase colouration (Choat, 1966, Choat and Robertson, 1975,
Robertson and Warner, 1978 and Bruce, 1979). The common name for
the family, the parrotfishes, has arisen from the striking colours
of the terminal phase and the close resemblance of the dental plates
to a parrot's beak.
t The conventional nomenclature is utilized. The recently proposedfamilial synonomies are discussed in Chapter 3.
2
physiological
content of
Hussaini, ~945, ~947 and Gohar & Latif, 1959) and a range of
adaptations to the exceptionally high carbonate
the diet (Fontaine e~ a~., ~973 and Smith & Paulson,
parrotfishes have many unusual characteristics. These include
the secretion of a mucous cocoon at night (Winn, ~955, Winn &
Bardach, ~959, ~960 and Casimir, ~97~), a diet that includes live
coral (Hiatt & strasburg, ~960, Glynn 8~ a~., ~972 and Randall &
Bruce, ~983), a grinding pharyngeal mill (AI Hussaini, ~945 and
Board, ~956), an additional articulation point in the lower jaw
(Lubosch, ~923 and Gregory, 1933), an unusual sacculated intestine
(AI
~975). Parrotfishes have been implicated as important agents in
bioerosion (Gygi, ~975 and Frydl & stearn, ~978), sediment transport
(Bardach, ~96~) and in the regulation of benthic invertebrates
(Glynn 8~ a~., ~972, Kaufman, ~977, Brock, ~979 and wellington,
~982), as well as being an important component of the grazing reef
fish community (Stephenson & searles, ~960, Randall, ~965, Day,
1977, Ogden & LObel, 1978, Bouchon-Navaro & Harmelin-Vivien, 198~,
Hatcher, ~98~, Miller, 1982 and RUSS, ~984 a, b). The parrotfishes
form a significant proportion of the
tropical regions and include at
food fishes caught in many
least one highly prized species
(Alcala & Luchavez, ~98~ and Johannes, ~981).
Despite the recent increase in the number of studies on coral
reef fishes (Ehrlich, 1975), parrotfishes have received relatively
little attention, particularly in the Indo-Pacific region. One
aspect that appears to have deterred many prospective investigators
is that of identification. The identification of scarids in the
field and in preserved collections is difficult owing to the lack of
diagnostic morphological characters." Because of this, species
3
descriptions are frequently based on colour. patterns. This has
resulted in considerable confusion as colour patterns change with
size, sex, reproductive status and a variety of environmental and
behavioural factors. The colours also change during fixation. On
the Great Barrier Reef, there are about 26 scarid species with a
total of approximately 125 colour phases or patterns.
seven are shared by at least two species.
of these,
Recent studies (including Randall & ormond, 1978, Randall &
Choat, 1980, Randall, 1983, Randall & Bruce, 1983 and Choat &
Randall, pers. conun.) are contributing greatly to a more stable
scarid nomenclature. Detailed morphological analyses have revealed
useful characters that were previously overlooked. The initial and
terminal phase colour patterns of most species have now been linked
and the problems of synonomy, as a result of colour phases being
identified as different species, have been largely resolved.
The aim of this stUQy wa~ to investigate the
between the functional morphology and behavioural ecology of
parrotfishes. Parrotfishes are ideally suited for such comparative
studies as they have highly specialized morphological characters and
distinctive behavioural traits. Parrotfishes are also suitable
study species in that they are diurnally active, strongly reef
associated and numerous, and have a limited mobility.
This study includes analyses of both adults and juveniles. The
biology of adults and juveniles are clearly not independent,
although often different, and an investigation of the biology of a
species must therefore include both stages, if a broad understanding
of it is to be obtained. The biology of larval and juvenile
4
tropical marine fishes have received increasing attention in recent
years (eg. Sale et a~., 1980, Williams, 1980, Williams & Sale, 1981,
Leis, 1982, Brothers e~ a~., 1983, Doherty, 1983 and Shulman, 1984)
but integrated studies of several life history stages are limited.
This thesis is presented in three main parts: morphology
(Chapters 1 s 2 ) , systematics (Chapters 3 s 4) and behavioural
ecology (Chapters 5 & 6). Each part is further subdivided into
adult and juvenile chapters. The descriptions in Chapters 1 and 2
are detailed, but unavoidably so, as they form a prerequisite for:
a) the systematic considerations in Chapter 3 and b) the functional
analyses in Chapters 1 and 2, which form the basis for designing and
interpreting the ecological studies described in Chapters 5 and 6.
The lack of published information on the taxonomy of juvenile
scarids made the systematic analyses in Chapter 4 necessary, prior
to the studies of juvenile scarids in Chapters 2 and 6.
