This file is part of the following reference:

Reid, David Gordon (1984) The systematics and ecology

of the mangrove-dwelling Littoraria species (Gastropoda:

Littorinidae) in the Indo-Pacific. PhD thesis, James Cook

University.

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http://eprints.jcu.edu.au/24120/

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THE SYSTEMATICS AND ECOLOGY

OF THE MANGROVE-DWELLING LITTORARIA SPECIES

(GASTROPODA: LITTORINIDAE)

IN THE INDO-PACIFIC

VOLUME I

Thesis submitted by

David Gordon REID MA (Cantab.)

in May 1984

. for the Degree of Doctor of Philosophy in

the Department of Zoology at

James Cook University of North Queensland

STATEMENT ON ACCESS

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 uses

consulting this thesis will have to sign the following statement:

'In consulting this thesis I agree not to copy or

closely paraphrase it in whole or in part without the

written consent of the author; and to make proper

written acknowledgement for any assistance which I have

obtained from it.'

David G. Reid

May 1984

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published or unpublished work of others has been acknowledged in the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.

David G. Reid

May 1984

ACKNOWLEDGEMENTS

For fostering my enthusiasm for molluscs, and for his continued

support and interest during this study, I thank Dr J. D. Taylor of

the British Museum (Natural History). During visits to the

Australian Museum I have benefitted greatly from the stimulating

discussion and advice of Dr W. F. Ponder, without whose

encouragement the taxonomic work could not have been completed. By

his numerous publications on the family Littorinidae, Dr J.

Rosewater has laid all the foundations for my systematic work; I

wish to thank him for enabling me to visit the National Museum of

Natural History in Washington, and for generously making available

his own unpublished material and specimens.

At James Cook University I thank Prof. C. Burdon -Jones for his

support during my stay, and my supervisor, A.Prof. R. P. Kenny, for

his help during the preparation of this thesis. For invaluable

advice on statistical matters I thank Dr R. E. Jones, and for

patiently teaching me to use a computer, J. Oliver. I am grateful to

Dr J. Lucas for the identification of crab species. My friends and

colleagues amongst the PhD students in the School of Biological

Sciences have been a constant source of inspiration, sympathy and

fellowship. For assistance with techniques of electron microscopy

and histology, I thank J. Darley and L. Winsor respectively, and for

German translation A. von Wallenstern.

For permission to study the collections in their care, I thank:

the curators and staff of BMNH, AMS, USNM, Prof. K. Boss (MCZ), Dr

C. Christensen (BPBM), Dr G. M. Davis (ANSP), Ms C. M. Yang (NUS)

and the Linnean Society of London. I am grateful to the following

for the loan of specimens: Dr P. Bouchet (MNHNP), S. Boyd (NMV), Dr

E. Gittenberger (RNHL), Dr R. N. Kilburn (NM), Dr T. Okutani (NSMT),

Dr G. Oliver (NMW), T. SchiOtte (Zoologisk Museum, Copenhagen), Dr

J. Stanisie(QM), Dr N. V. Subba Rao (ZSI), Dr C. Vaucher (MHNG) and

11

Dr F. E. Wells (WAM). Additional specimens were received from: D. R.

Bellwood, K. Fujiwhara, S. T. Garnett (all James Cook University),

Prof. B. S. Morton (University of Hong Kong), Dr M. Nishihira (Kyoto

University) and Dr Z. Wang (Institute of Oceanology, Academia

Sinica).

Laboratory facilities were provided by: Dr J. Hylleberg (Phuket

Marine Biological Center, Thailand), Prof. E. A.'Kay (University of

Hawaii), Dr J. E. Ong (Universiti Sains Malaysia, Penang) and Dr A.

Sasekumar (Universiti Malaya, Kuala Lumpur). For help in the field I

am grateful to M. Gilham (Darwin, N.T.), S. Pripanapong

(Kanchanadit, Thailand) and N. Sarti (Department of Fisheries and

Wildlife, Broome, W.A.).

In addition to many of the above, I am indebted to Dr R. Cleevely

(BMNH), Dr V. Fretter and Prof. A. Graham (University of Reading),

Dr R. S. Houbrick (USNM), Dr N. J. Morris (BMNH), Dr W. B. Rudman

(AMS), Prof. R. D. Turner (MCZ), Dr A. J. Underwood (University of

Sydney) and A.Prof. G. J. Vermeij (University of Maryland) for

useful discussion.

This study was made possible by the award of a scholarship for

postgraduate research from the Drapers' Company of London, to which

charitable institution my deepest gratitude. I thank the Trustees of

the Australian Museum for the Keith Sutherland Award, which financed

my travel around Australia. Financial support was also received as a

grant from the Short Term Visitor Programme of the Smithsonian

Institution.

My coverage of the literature was made more complete by the use

of the bibliography of the family Littorinidae by C. W. Pettitt

(1974a, b, 1979), and by access to the looseleaf system of the

Department of Malacology, AMS, compiled by Dr W. F. Ponder and the

late Dr C. Hedley.

FRONTISPIECE

Shell colour polymorphism of Ltttorarta species. From top:

Row 1: L. ftLosa, Cockle Bay, Magnetic Island, Queensland;

colour forms: YO, Y2, B4, P0.

Row 2: L. at:WI:pp -Lana, Cockle Bay, Magnetic Island,

Queensland; colour forms: Y0, Y2, B5, P0.

Row 3: L. paLLescens, Ao Nam-Bor, Phuket Island, Thailand;

colour forms: Y0, Y3, B5, P0.

Row 4: L. LuteoLa, Kurnell, Botany Bay, New South Wales;

colour forms: Yl, Y3, B4, P0.

Row 5: L. aLbtcans, Santubong, Sarawak; colour forms: Y0, Y2,

Y3, PO.

V

ABSTRACT

The supposed species PLittortna scabra (L.)' has been noted for

its extreme variability in shell form and colouration. The project

was undertaken with the aim of investigating this variability and

its possible adaptive significance.

Recent taxonomic treatments of the 'scabra group' (comprising the

members of the family Littorinidae associated with mangroves in the

Indo-Pacific) have recognized three species. Using material

personally collected and specimens from fourteen museums, the

taxonomy of the scabra group was revised, demonstrating the

existence of 20 species and one subspecies. Initially, species were

defined by the diagnostic morphology of the penis and sperm nurse

cells. The form of the pallial oviduct is described in detail,

demonstrating that some species are ovoviviparous while others

produce egg capsules. In addition, the radula, alimentary system,

pallial complex and colouration of the head-foot are described,

although less useful for taxonomic purposes than the reproductive

anatomy. Once species were defined by anatomical criteria,

characters of the shell such as shape, sculpture, columella and

protoconch were shown to be rather uniform and adequate for the

identification of species in most cases. Systematic descriptions and

full synonymies are given for each species.

For comparative purposes, the anatomy of 42 other littorinid

species was examined. Employing the method of cladistic analysis,

the anatomical data were used to construct a tentative phylogeny of

the family Littorinidae. The scabra group is classified in the genus

Littorarta, which is shown to be the sister group of NodiLittortna.

A cladogram of the 36 Recent species of Littoraria is presented, and

four subgenera are recognized.

Distribution maps are given for each species in the scabra group,

vi

and were compiled from a total of 1900 museum collections. The

biogeography of the group is discussed. The species can be divided

into two classes, characteristic of continental and oceanic habitats

respectively, and the members of the latter group show the greatest

geographical ranges. The form of the protoconch and data in the

literature suggest that both oviparous and ovoviviparous species are

widely dispersed as planktotrophic veligers. It is suggested that

speciation may be occurring in the peripheral regions of the

Indo-Pacific, and that species have accumulated in the central

region of highest diversity.

The zonation and abundance of Ltttorarta species were quantified

on transects through mangrove forests at 14 localities in- Australia,

South-east Asia and Hawaii. Species were found to show

characteristic patterns of vertical and horizontal zonation,

although the degree of overlap between sympatric species was

considerable. There was a clear distinction between species dwelling

on bark and those on foliage. Densities of Ltttorarta species were

very low, except on the trees at the outermost edge of the forest.

It is suggested that landward limits of horizontal zonation may be

determined by physiological tolerance, and vertical distribution by

behavioural responses.

Detailed ecological investigations were carried out at Cockle

Bay, Magnetic Island, Queensland. Here five Ltttorarta species were

common. From lowest to highest, the order of vertical zonation of

these species on Rhtzophora trees was: L. arttcuLata and L.

tntermedta, L. scabra, L. phtttpptana, and on Avtcennta trees: L.

arttcuLata, L. ftlosa, L. phti.tpptana.

The snails were highly mobile, those from the lower levels (L.

arttctaata, L. tntermedta, L. scabra) migrating vertically with each

tidal cycle, to avoid submersion. Those from the higher levels (L.

ftLosa, L. phtLipptana) periodically moved down to the water surface

at high tide, and were active during the night,, early morning and

during light rain. All species occupied higher tidal levels during

vii

spring tides, and those from higher levels occurred further up the

trees during rain. All species showed a vertical size gradient, with

smaller individuals at the lower levels. Intense predation pressure

at low levels during high tides is believed to have been the

selective force responsible for the vertical migration behaviour.

At Cockle Bay the three species from lower levels were found to

be reproductively mature throughout the year, and spawning probably

occurred each month. The two species from higher levels were

reproductively mature only during the wet summer months. There was

no correlation between the method of development (release of either

pelagic egg capsules or planktotrophic veligers) and the habitats of

the species. Phylogenetic patterns of method of development and of

breeding season in the Littorinidae are discussed.

Population dynamics of L. tntermedta, L. scabra, L. phtlipptana

and L. ftLosa were investigated by a multiple mark and recapture

technique. Despite probably continuous spawning, recruitment of L.

tntermedta and L. scabra was only significant following the peak

spawning period in January and February. In contrast, recruitment of

L. ftLosa was highly successful, perhaps because this species

settled on foliage, out of reach of predatory crabs. The subsequent

survivorship of L. ftLosa, under more rigorous microclimatic

conditions, was relatively low. Survivorships of all species were

lowest in the smallest size classes and in the summer months, and

all showed a marked drop in survivorship during three weeks of

monsoonal rain.

Growth rates, as measured on the individually numbered snails,

are the highest recorded for the family. Values of the instantaneous

size-specific growth rate (k in the von Bertalanffy growth equation)

ranged from 0.05 to 0.25 per month. L. tntermedta and L. scabra

attained a size of 6 mm in the first month of growth following

settlement, and reached the minimum size for sexual maturity in 3

to 4 and 6 to 8 months respectively. Growth rates were highest

during the summer months, with the exception of L. ftLosa, in which '

viii

the season of maximum growth followed that of spawning. These

patterns are related to the zonation and feeding behaviour of the

species. Few individuals survived to reach 2 years of age, but

maximum longevity may be 6 years.

The major predators of the post-larval stages of Ltttorarta

species at Cockle Bay were crabs of the genus Metopograpsus and the

species ThaLamtta crenata. Direct estimates of the causes of death

of snails were obtained for artificial populations of L. ftlosa in

exclusion cages. Crabs caused 57% of the total loss, or 86% of the

total mortality, of L. ftLosa in the size range 7 to 12 mm,

accounting for the loss of 19% of the population per month. Bird

predation appeared to be insignificant. The severity of crab

predation on Ltttorarta species was supported by an analysis of the

repaired breakages of the shell, which indicated sublethal damage by

crabs. The average numbers of repairs per adult shell were between

0.7 and 3.5 in the five species at Cockle Bay. The rate of sublethal

damage (repairs per whorl per month) was highest in 2 to 5 mm shells

of L. tntermedta, L. scabra and L. phtIetpptana, although in L.

ftlosa the rate was highest in adult shells (23 mm). This pattern is

explained by the much lower resistance of the thin-shelled L. ftLosa

to attack, as demonstrated in laboratory predation trials. The

distribution of crabs on the trees at Cockle Bay suggested a

gradient of increasing intensity of predation at lower tidal levels.

A corresponding interspecific' gradient of increasing shell thickness

in the species typical of lower tidal levels was shown at nine out

of ten of the localities where zonation was recorded on transects,

and this is interpreted as an adaptive trend. Interspecific trends

of increasing shell size, stronger sculpture and narrower shells at

higher tidal levels are interpreted as adaptations to the more

rigorous microclimatic conditions at higher levels.

Within the scabra group, nine species show a phenotypically

similar colour polymorphism, with yellow, pink or brown shells,

while the remaining species are merely variable in the degree of

shell pigmentation. The degree of colour variation was greatest in

ix

Ltttorarta species typically found on foliage at the higher tidal

levels, while species from bark substrates at lower levels were

brown. In some species there was a suggestion of a direct influence

of the substrate upon shell colour. This was not the case in L.

ftLosa; in this species the polymorphism was presumed to have a

genetic basis, and the mechanisms maintaining the polymorphism were

investigated. Evidence is presented for the action of visual

selection on L. ftlosa on backgrounds of different colour, although

the predators involved were not identified. Climatic selection did

not appear to be operating. The shell colour forms did not show

significant behavioural differences. Manipulation of the colour

proportions of L. fttosa on isolated trees showed that disappearance

of colour forms was frequency-dependent. On the basis of this

evidence and the persistent rarity of the conspicuous pink colour

form, it is concluded that the polymorphism is maintained by

apostatic selection.

CONTENTS

ACKNOWLEDGEMENTS

ABSTRACT

LIST OF TABLES xiv

LIST OF FIGURES xviii

1 GENERAL INTRODUCTION 1

PART I SYSTEMATICS

2 INTRODUCTION AND AN HISTORICAL REVIEW 4

3 MATERIALS AND METHODS 11 3.1 Material, types and synonymies 11 3.2 Methods 13

3.2.1 Shell characters 13 3.2.2 Anatomical characters 17

3.3 Zonation and distribution 20 3.4 Abbreviations 21

4 SHELL CHARACTERS 23 4.1 Shape, size and thickness 23 4.2 Sexual dimorphism 28 4.3 Protoconch 30 4.4 Shell sculpture 32 4.5 Shell colour 36 4.6 Operculum 39

5 ANATOMICAL CHARACTERS 40 5.1 Colouration of head—foot 40 5.2 Male reproductive tract 41 5.3 Sperm cells 52 5.4 Female reproductive tract 58 5.5 Egg capsules 80 5.6 Radula 86 5.7 Alimentary system 91 5.8 Pallial complex 94

6 REPRODUCTIVE ISOLATION 97 6.1 Introduction 97 6.2 Copulatory behaviour 97 6.3 Possibility of hybridization 101

7 BIOGEOGRAPHY 102 7.1 Patterns of distribution 102 7.2 Dispersal 108 7.3 Variation and speciation 111 7.4 Regional diversity 112

8 PHYLOGENY AND GENERIC CLASSIFICATION

117 8.1 Status of the genus Ltttorarta 117

xi

8.1.1 Synonymy of the genus Ltttorarta 119 8.1.2 List of recognized Recent taxa of Ltttorarta 120

8.2 Relationships of the genus Ltttorarta 122 8.3 Subgeneric classification 127

9 SYSTEMATIC DESCRIPTIONS 132 9.1 Key to shells 132 9.2 Genus Ltttorarta Griffith & Pidgeon 136

9.2.1 Subgenus Ltttorarta Griffith & Pidgeon 136' 9.2.1.1 L. vespacea n. sp. 137

9.2.2 Subgenus LameLltLttortna Tryon 148 9.2.2.1 L. aLbtcans (Metcalfe) 148

9.2.3 Subgenus Ltttortnopsts March 160 9.2.3.1 L. scabra (Linnaeus) 160 9.2.3.2 L. Lutea (Philippi) 177 9.2.3.3 L. paLLescens (Philippi) 188 9.2.3.4 L. phtLtpptana (Reeve) 205 9.2.3.5 L. tntermedta (Philippi) 217 9.2.3.6 L. subvtttata n. sp. 238 9.2.3.7 L. ftLosa (Sowerby) 249 9.2.3.8 L. ctnguLata ctnguLata (Philippi) 262 9.2.3.9 L. ctngulata prtsttsstnt n. subsp. 272 9.2.3.10 L. LuteoLa (Quoy & Gaimard) 285 9.2.3.11 L. ardoutntana (Heude) 297 9.2.3.12 L. deLtcatula (Nevill) 306

9.2.4 Subgenus PaLustortna n. subgen. 314 9.2.4.1 L. meLanostoma (Gray) 314 9.2.4.2 L. fLammea (Philippi) 325 9.2.4.3 L. contra (Philippi) 332 9.2.4.4 L. cartntfera (Menke) 343 9.2.4.5 L. suLcuLosa (Philippi) 355 9.2.4.6 L. arttcuLata (Philippi) 366 9.2.4.7 L. strtgata (Philippi) 383

PART II ECOLOGY

10 COCKLE BAY, THE PRINCIPAL STUDY AREA 399

11 HABITAT AND ZONATION 407 11.1 Introduction 407 11.2 The mangrove habitat 409 11.3 Methods 411 11.4 Patterns of zonation and abundance 443

11.4.1 Horizontal zonation 443 11.4.2 Vertical zonation 445 11.4.3 Effect of leaf or bark substrate and of

tree species 446 11.4.4 ,Occurrence in habitats other than mangroves 449 11.4.5 Continental and oceanic distributions 450

11.5 Discussion 452 11.5.1 The control of vertical distribution 455 11.5.2 The control of horizontal distribution 457 11.5.3 Continental and oceanic distributions 461

12 BEHAVIOUR 463 12.1 Introduction 463

12.2 Methods

12.3 Observations 12.3.1 Daily tidal migrations 12.3.2 Influence of synodic cycle upon distribution 12.3.3 Effect of rainfall upon distribution 12.3.4 Effects of shell size, sex and tree species 12.3.5 Substrate and attachment

12.4 Discussion

xii

467 470 470 485 492 493 503 509

12.4.1 Vertical migration 509 12.4.2 Rhythms of activity 514 12.4.3 The maintenance of zonation 516 12.4.4 Long term changes in zonation pattern 518 12.4.5 The mucous holdfast 520 12.4.6 Shell size gradients • 521

13 REPRODUCTION, POPULATION DYNAMICS AND GROWTH 524 13.1 Introduction 524 13.2 Methods 527

13.2.1 Reproduction 527 13.2.2 Population dynamics 530 13.2.3 Growth 534

13.3 Results 537 13.3.1 Reproduction 537 13.3.2 Population dynamics 547

° 13.3.3 Growth 583 13.4 Discussion 603

13.4.1 Developmental type 603 13.4.2 Seasonality of breeding 608 13.4.3 Larval settlement and recruitment to the

population 612 13.4.4 Mortality 616 13.4.5 Longevity 621 13.4.6 The form of the growth curve 622 13.4.7 Rate of growth 623 13.4.8 Summary of life history characteristics 627

14 PREDATION AND SHELL MORPHOLOGY 632 14.1 Introduction 632 14.2 Methods 635

14.2.1 Occurrence and distribution of potential predators 635

14.2.2 Caging experiments using L. ftlosa 636 14.2.3 Laboratory predation trials 638 14.2.4 Analysis of repaired shell breakages 638 14.2.5 Shell morphology and the zonation of species 640

14.3 Results 642 14.3.1 Field observations of potential predators at

Cockle Bay 642 14.3.2 Sources of mortality of L. ftLosa 647 14.3.3 Laboratory predation trials 651 14.3.4 Incidence of repaired shell breakages 655 14.3.5 shell morphology and the zonation of species 662

14.4 Discussion 668 14.4.1 Potential predators and other sources of

mortality of Ltttorarta species at Cockle Bay 668

14.4.2 The intensity of predation by crabs 671

14.4.3 The interpretation of repaired shell breakage data 676

14.4.4 Microenvironmental gradients and trends in shell morphology 684

15 SHELL COLOUR POLYMORPHISM 694 15.1 Introduction 694 15.2 Description and classification of the colour

polymorphism 697 15.3 Methods 699 15.4 Results 707

15.4.1 Polymorphism and habitat 707 15.4.2 Geographical distribution of colour'forms 713 15.4.3 Variation between microhabitats in the

proportions of colour forms 718 15.4.4 The distribution of colour forms of L. ftLosa

on Avtcennta trees at Cockle Bay, and evidence of natural selection 724

15.4.5 Observations on the behaviour, loss rate and sex of the colour forms of L. ftLosa 728

15.4.6 Temperature effects and seasonal differences in proportions of colour forms of L. ftLosa 730

15.4.7 Frequency-dependent selection in L. ftLosa 734 15.5 Discussion 738

15.5.1 The basis of shell colour variation: genetic or environmental? 738

15.5.2 The agents of natural selection 742 15.5.3 The maintenance of the polymorphism 748

16 CONCLUDING DISCUSSION 763

REFERENCES 770

xiv

LIST OF TABLES

Table

4.1 Summary of sexual dimorphism in the shells of the

Page

Ltttorarta scabra group 29

5.1 Nomenclature of the glandular components of the pallial oviduct in the family Littorinidae 60

6.1 Pairs of Ltttorarta species in copulation position, recorded at Cockle Bay, Magnetic Island, Queensland 99

6.2 Pairs of Ltttorarta species in copulation position, recorded at Broome, Western Australia 100

7.1 Comparison of distribution of species of the Ltttorarta scabra group with the subdivisions of the Indo-Pacific province proposed by Macnae (1968) on the basis of mangrove faunas 103

8.1 Character states in the family Littorinidae 125

8.2 Character states in the genus Ltttorarta 129

9.1 Dimensions of Ltttorarta (Ltttorarta) vespacea 140

9.2 Dimensions of Ltttorarta (LametltLitortna) aLbicans 152

9.3 Dimensions of Ltttorarta (Ltttortnopsts) scabra 169

9.4 Dimensions of Ltttorarta (Ltttortnopsts) Lutea 183

9.5 Dimensions of Ltttorarta (Ltttortnopsts) paLLescens 195

9.6 Dimensions of Ltttorarta (Ltttortnopsts) phtttpptana 210

9.7 Dimensions of Ltttorarta (Ltttortnopsts) tntermedta 227

9.8 Dimensions of Ltttorarta (Ltttortnopsts) subvtttata 242

9.9 Dimensions of Ltttorarta (Ltttortnopsts) fttosa 254

9.10 Dimensions of Ltttorarta (Ltttortnopsts) ctnputata ctnpuLata 266

9.11 Dimensions of Ltttorarta (Ltttortnopsts) ctnguLata prtsttsstnt 276

9.12 Dimensions of Ltttorarta (Ltttortnopsts) tuteola 289

9.13 Dimensions of Ltttorarta (Littortnopsts) ardoutntana 301

9.14 Dimensions of Ltttorarta (Ltttortnopsts) dettcatuta 310

XV

9.15 Dimensions of Ltttorarta (PaLustortna) meLanostoma 318

9.16 Dimensions of Ltttorarta (Palustortna) fLammea 330

9.17 Dimensions of Ltttorarta (PaLustortna) contca 336

9.18 Dimensions of Ltttorarta (PaLustortna) cartntfera 348

9.19 Dimensions of Ltttorarta (PaLustortna) sulcuLosa 359

9.20 Dimensions of Ltttorarta (PaLustortna) arttcuLata 372

9.21 Dimensions of Ltttorarta (PaLustortna) strtaata 388

10.1 Dimensions of trees in three main study areas at Cockle Bay, Magnetic Island, Queensland

406

11.1 List of mangrove localities visited

412

12.1 Distribution of Ltttorarta arttcuLata on AVtcennta trees at Cockle Bay 494

12.2 Distribution of Ltttorarta tntermedta on Rhtzophora trees at Cockle Bay 495

12.3 Distribution of Ltttorarta scabra on Rhtzophora trees at Cockle Bay 496

12.4 Distribution of Ltttorarta ftLosa on Avtcennta trees at Cockle Bay 497

12.5 Distribution of Ltttorarta phtLtpptana on Avtcennta trees at Cockle Bay 498

12.6 Distribution of Ltttorarta phtLtpptana on Rhtzophora trees at Cockle Bay 499

12.7 Comparison of levels of Ltttorarta phtLtpptana on Avtcennta and Rhtzophora trees at Cockle Bay 502

12.8 Analysis of variance of effects of tide (spring or neap) and rain (wet or dry weather) on proportions of Ltttorarta ftLosa and L. phtLtpptana found on leaves at Cockle Bay 505

12.9 Comparison of distribution of Ltttorarta ftLosa on upper and lower surfaces of Avtcennta leaves during wet and dry weather at Cockle Bay 506

13.1 Stages of reproductive maturity of male Ltttorarta species 529

13.2 Stages of reproductive maturity of female Ltttorarta species 529

13.3 Sex ratios and minimum sizes at maturity for five species of Ltttorarta at Cockle Bay 546

xvi

13.4 Details of the mark and recapture experiment at Cockle Bay 546

13.5 Survivorships and instantaneous loss rates for cohorts and size classes of four Ltttorarta species, averaged over the year of observations at Cockle Bay 567

13.6 Functions relating monthly growth increment to initial size in Ltttorarta tntermedta at Cockle Bay, from August 1980 to August 1981

584

13.7 Functions relating monthly growth increment to initial size in Ltttorarta scabra at Cockle Bay, from August 1980 to August 1981

585

13.8 Functions relating monthly growth increment to initial size in Ltttorarta phtLtpptana on Avtcennta trees at Cockle Bay, from October 1980 to September 1981

586

13.9 Functions relating monthly growth increment to initial size in Ltttorarta ftLosa at Cockle Bay, from August 1980 to August 1981 587

13.10 Frequency of varices in Ltttorarta species from Cockle Bay 602

13.11 Breeding age and longevity of Ltttorarta species at Cockle Bay 602

14.1 Birds seen in mangrove forest at Cockle Bay 646

14.2 Comparison of mean numbers of repaired breakages per shell in Ltttorarta species on Avtcennta and Rhtzophora

- trees at Cockle Bay 656

14.3 Proportions of shells of Ltttorarta species at Cockle Bay showing one or more repaired breakages on the last two whorls 656

14.4 Regressions of shell height on whorl number for Ltttorarta• species at Cockle Bay 657

14.5 Shell shape parameters for species of Ltttorarta on mangrove transects 663

14.6 Spearman rank correlation coefficients between shell shape parameters and three measures of zonation level on mangrove transects with two or more Ltttorarta species 664

15.1 Correlation coefficients between index of shell colour variation (E) and three measures of zonation level on mangrove transects with two or more Ltttorarta species 710

15.2 Comparisons of shell colour proportions of Ltttorarta species on Avtcennta and Rhtzophora trees 719

xvii

15.3 Comparison of shell colour proportions of Ltttorarta paLtescens in different habitats at Ao Nam-Bor, Phuket Island, Thailand

721

15.4 Comparison of shell colour proportions of Ltttorarta LuteoLa in different microhabitats at Bonna Point, Kurnell Peninsula, Botany Bay, N.S.W. 721

15.5 Shell colour proportions of Ltttorarta ftLosa, on Avtcennta trees classified by relative area of leaves and bark and by exposure to sunlight, at Cockle Bay on 8 February 1981 725

15.6 Shell colour proportions of Ltttorarta ftLosa on Avtcennta trees classified by relative area of leaves and bark, at Cockle Bay on 11 July 1981 726

15.7 Changing shell colour proportions of Ltttorarta ftlosa on Avtcennta trees classified by relative area of leaves and bark, over four month interval, at Cockle Bay 727

15.8 Comparisons of shell colour proportions between the sexes of Ltttorarta ftLosa at two localities 727

15.9 Comparison of shell colour proportions of Ltttorarta ftLosa on leaves and bark of Avtcennta trees at Cockle Bay 729

15.10 Comparison of shell colour proportions of Ltttorarta ftLosa in sun and shade on Avtcennta trees at Cockle Bay 729

15.11 Surface temperatures of empty shells of Ltttorarta ftLosa in full sunlight 731

15.12 Shell surface and body temperatures of Ltttorarta ftLosa on Avtcennta trees at Cockle Bay 731

xviii

LIST OF FIGURES

Figure Page

Frontispiece: Shell colour polymorphism of Ltttorarta species iv

3.1 Shell dimensions 15

4.1 Examples of columellar types in Ltttorarta species 27

5.1 Ltttorarta (Ltttortnopsts) scabra: male reproductive tract 42

5.2 Penes of Ltttorarta species other than those described in Chapter 9 49

5.3 Spermatozeugmata of Ltttorarta species 55

5.4

Schematic diagram explaining the form of the pallial oviduct in oviparous Ltttorarta species 64

5.5 Ltttorarta (PaLustortna) meLanostoma: female reproductive tract

66

5.6

Ltttorarta (PaLustortna) meLanostoma: serial sections of pallial oviduct

68

5.7 Ltttorarta (Ltttortnopsts) scabra: female reproductive

tract

73

5.8 Ltttorarta (Ltttortnopsts) scabra: serial sections of

pallial oviduct

74

5.9

Diagrammatic representations of the pallial oviducts of some genera of Littorinidae, arranged in morphological sequence, showing how progressive elaboration of the path of the egg groove may have occurred

76

5.10 Egg capsules of Littorinidae, arranged to show possible derivation of the forms characteristic of several genera from a simple pelagic capsule 83

5.11 Ltttorarta (Ltttortnopsts) scabra: dissection of alimentary system and foregut 92

5.12 Ltttorarta (Ltttortnopsts) scabra: stomach dissected away from digestive gland 93

7.1 Worldwide contour map of species richness in the genus Ltttorarta 113

7.2 Contour map of species richness of the 20 members of the Ltttorarta scabra group in the Indo—Pacific 115

ixx

8.1 Cladogram representing an hypothesis of phylogenetic relationships amongst ten genera of Littorinidae 124

8.2 Cladogram of species of Ltttorarta 128

9.1 Ltttorarta (Ltttorarta) vespacea: shells 139

9.2 Ltttorarta (Ltttorarta) vespacea and Ltttorarta (Ltttortnopsts) Lutea: shell microsculpture and radulae 142

9.3 Ltttorarta (Ltttorarta) vespacea: anatomical characters 144

9.4 Distribution of Ltttorarta (Ltttorarta) vespacea 146

9.5 Ltttorarta (LameLLtLttortna) albtcans: shells 150

9.6 Ltttorarta (LamelLtLttortna) aLbtcans: shell microsculpture and radula 154

9.7 Ltttorarta (LameLLtLttortna) aLbtcans: anatomical characters 156

9.8 Distribution of Ltttorarta (LameLLtLttortna) aLbicans 158

9.9 Ltttorarta (Littortnopsts) scabra: shells 168

9.10 Ltttorarta (Ltttortnopsts) scabra: shell microsculpture and radula 171

9.11 Ltttorarta (Ltttortnopsts) scabra: anatomical characters 173

9.12 Distribution of Ltttorarta (Ltttortnopsts) scabra 175

9.13 Ltttorarta (Ltttortnopsts) Lutea: shells 182

9.14 Ltttorarta (Ltttortnopsts) Lutea: anatomical characters 185

9.15 Distribution of Ltttorarta (Ltttortnopsts) Lutea 186

9.16 Ltttorarta•(Ltttortnopsts) paLLescens: shells 192

9.17 Ltttorarta (Littortnopsts) paLLescens: shells 194

9.18 Ltttorarta (Ltttortnopsts) paLLescens: shell microsculpture 197

9.19 Ltttorarta (Ltttortnopsts) paLLescens: anatomical characters 199

9.20 Distribution of Ltttorarta•(Ltttortnopsis) paLLescens 201

9.21 Ltttorarta (Littortnopsts) phtLtpptana: shells 208

9.22 Ltttorarta (Ltttortnopsts) phtLtpptana: shell microsculpture and radula 212

9.23

9.24

9.25

9.26

9.28

9.27

232

9.29 Distribution of Ltttorarta (Ltttortnopsts) tntermedta 233

9.30 Ltttorarta (Ltttortnopsts) subutttata: shells 241

Ltttorarta (Ltttortnopsts) phtltpptana: anatomical characters

Distribution of Ltttorarta (Ltttortnopsts) phiLtpptana

Ltttorarta (Ltttortnopsts) tntermedta: shells

Ltttorarta (Littortnopsts) tntermedta: shells

Ltttorarta (Ltttortnopsts) tntermedta: shell microsculpture and radula

Ltttorarta characters

(Ltttortnopsts) tntermedta: anatomical

229

214

215

224

226

XX

9.31 Ltttorarta (Ltttortnopsts) sublitttata: shell microsculpture and radula; Ltttorarta (Ltttortnopsts) angzatfera: shell microsculpture 245

9.32 Ltttorarta (Ltttortnopsts) subutttata: anatomical characters 246

9.33 Distribution of Ltttorarta (Ltttortnopsts) subutttata 248

9.34 Ltttorarta (Ltttortnopsts) ftlosa: shells 253

9.35 Ltttorarta (Ltttortnopsts) paLLescens and Ltttorarta (Ltttortnopsts) filosa: shell microsculpture and radulae 256

9.36 Ltttorarta (Ltttortnopsts) filosa: anatomical characters 258

9.37 Distribution of Ltttorarta (Ltttortnopsis) ftLosa 260

9.38 Ltttorarta (Ltttortnopsts) ctngulata ctnguLata: shells 264

9.39 Ltttorarta (Ltttortnopsts) ctnguLata ctnaulata: shell microsculpture and radula; Ltttorarta (Ltttortnopsts) deLtcatzaa: shell microsculpture 268

9.40 Ltttorarta (Littortnopsts) ctnguLata ctngzaata: anatomical characters 269

9.41 Distribution of Ltttorarta (Ltttortnopsts) cinguLata ctnauLata 271

9.42 Ltttorarta (Ltttortnopsis) ctnguLata prtsttsstnt: shells 275

9.43 Ltttorarta (Ltttortnopsts) ctnazaata prtstisstnt: shell microsculpture and radula 278

9.44 Ltttorarta (Ltttortnopsts) ctnguLata prtsttsstnt: anatomical characters

9.45 Distribution of Ltttorarta (Ltttortnopsts) ctnguLata prtsttsstnt

9.46 Ltttorarta (Ltttortnopsts) LuteoLa: shells

9.47 Ltttorarta (Ltttortnopsts) LuteoLa: shell microsculpture and radula

9.48 Ltttorarta (Ltttortnopsts) LuteoLa: anatomical characters

9.49 Distribution of Ltttorarta (Ltttortnopsts) LuteoLa

9.50 Ltttorarta (Ltttortnopsts) ardoutntana: shells

9.51 Ltttorarta (Ltttortnopsts) ardoutntana: anatomical characters

9.52 Distribution of Ltttorarta (Ltttortnopsts) ardoutntana

9.53 Ltttorarta (Ltttortnopsts) deLtcatuLa: shells

9.54 Distribution of Ltttorarta (Ltttortnopsts) deLtcatuLa

9.55 Ltttorarta (PaLustortna) meLanostoma: shells

9.56 Ltttorarta (PaLustortna) meLanostoma: shell microsculpture and radula; Ltttorarta (PaLustortna) fLammea: shell microsculpture

9.57 Ltttorarta (PaLustortna) meLanostoma: anatomical characters

9.58 Distribution of Ltttorarta (PaLustortna) meLanostoma

9.59 Ltttorarta (PaLustortna) fLammea: shells

9.60 Ltttorarta (PaLustortna) contca: shells

9.61 Ltttorarta (PaLustortna) contca: shell microscuipture and radula 338

9.62 Ltttorarta (PaLustortna) contca: anatomical characters 340

9.63 Distribution of Ltttorarta (PaLustortna) contca 342

9.64 Ltttorarta (PaLustortna) cartntfera: shells 346

9.65 Ltttorarta (PaLustortna) cartntfera: shell microscuipture and radula 350

xxi

280

282

288

291

293

295

299

303

304

309

312

317

320

322

324

329

335

9.66 Ltttorarta (PaLustortna) cartntfera: anatomical characters 352

9.67 Distribution of Ltttorarta (Palustortna) cartntfera 354

9.68 Ltttorarta (PaLustortna) suLcuLosa: shells 358

9.69 Ltttorarta (PaLustortna) suLcuLosa: shell microsculpture and radula; Ltttorarta (PaLustortna) articuLata: radula 361

9.70 Ltttorarta (PaLustortna) suLcuLosa: anatomical characters 363

9.71 Distribution of Ltttorarta (PaLustortna) suLcuLosa 365

9.72 Ltttorarta (Palustortna) articulata: shells 371

9.73 Ltttorarta (PaLustortna) arttcuLata: shell microsculpture 374

9.74 Ltttorarta (Palustortna) articuLata: anatomical characters 376

9.75 Ltttorarta (PaLustortna) arttcuLata: anatomical characters ,378

9.76 Distribution of Ltttorarta (PaLustortna) articuLata 380

9.77 Ltttorarta (PaLustortna) strtgata: shells 386

9.78 Ltttorarta (Palustortna) strtgata and Ltttorarta (Ltttortnopsts) ardoutntana: shell microsculpture and radulae 390

9.79 Ltttorarta (PaLustortna) strtgata: anatomical characters 392

9.80 Distribution of Ltttorarta (PaLustortna) strtgata 393

9.81 Ltttorarta (Ltttorarta) unduLata, Ltttorarta (Ltttortnopsts) anguttfera, Ltttorarta (Ltttorarta) zebra and Littorarta. (Littorarta) cingultfera: shells 398

10.1 Map of Magnetic Island and Cleveland Bay, Queensland 401

10.2 Map of the study area at Cockle Bay, Magnetic Island, Queensland

401

10.3 The exclusion cages at Cockle Bay, Magnetic Island, Queensland

404

10.4 Aerial view of study area at Cockle Bay, Magnetic Island, Queensland 404

11.1 Transect, Cockle Bay, Magnetic Island, Queensland 416

11.2 Transect, 2 km north of Cockle Bay, Magnetic Island, Queensland 418

11.3 Transect, Pioneer Bay, Orpheus Island, Palm Islands, Queensland

420

11.4 Transect, 1 km north of St. Paul's Mission, Moa Island, Torres Strait Islands, Queensland

422

11.5 Transect, Bonna Point, Kurnell Peninsula, Botany Bay, New South Wales 424

11.6 Transect, Little Lagoon, Denham, Shark Bay, Western Australia 426

11.7 Transect, just south of Lookout Hill, Broome, Western Australia 428

11.8 Transect, Ludmilla Creek, 6 km north of Darwin, Northern Territory 430

11.9 Transect, creek opposite East Woody Island, Gone Peninsula, Northern Territory 432

11.10 Transect, Ao Nam-Bor, Phuket Island, south-west Thailand

434

11.11 Transect, Kanchanadit, 15 km south-east of Surat Thani, south-east Thailand 436

11.12 Transect, Batu Maung, Penang, Malaysia 438

11.13 Transect, Santubong, Sarawak, Borneo 440

11.14 Transect, Coconut Island, Kaneohe Bay, Oahu, Hawaiian Islands 442

12.1 24 hour record of the vertical migratory behaviour of ten marked individuals of Ltttorarta articuLata on a Rhtzophora tree at Cockle Bay 472

12.2 24 hour record of the vertical migratory behaviour of ten marked individuals of Ltttorarta tntermedta on Rhtzophora"trees at Cockle Bay 474

12.3 24 hour record of the vertical migratory behaviour of ten marked individuals of Ltttorarta scabra on Rhtzophora trees at Cockle Bay 476

12.4 24 hour record of the vertical migratory behaviour of ten marked individuals of Ltttorarta ft Lose on Autcennta trees at Cockle Bay 478

12.5 24 hour record of the vertical migratory behaviour of ten marked individuals of Ltttorarta phttipptana on Rhtzophora trees at Cockle Bay 480

12.6 Records of temperature and relative humidity during 24 hour observations of vertical migratory behaviour of Ltttorarta species, measured at 2 m above the ground in

xxiv

the Rhtzophora forest at Cockle Bay 482

12.7 Mean zonation level of Ltttorarta arttcuLata on Avicennta trees at Cockle Bay, recorded during low tide at spring and neap tide periods 487

12.8 Mean zonation level of Ltttorarta tntermedta on Rhtzophora trees at Cockle Bay, recorded during low tide at spring and neap tide periods. 487

12.9 Mean zonation level of Ltttorarta scabra on Rhtzophora trees at Cockle Bay, recorded during low tide at spring and neap tide periods 489

12.10 Mean zonation level of Ltttorarta ftLosa on Avtcennta trees at Cockle Bay, recorded during low tide at spring and neap tide periods 489

12.11 Mean zonation level of Ltttorarta phtLtpptana on Avtcennta trees at Cockle Bay, recorded during low tide at spring and neap tide periods 491

12.12 Mean zonation level of Ltttorarta phtLtpptana on Rhtzophora trees at Cockle Bay, recorded during low tide at spring and neap tide periods 491

13.1 Annual reproductive cycle of adult males of five Ltttorarta species at Cockle Bay 539

13.2 Annual reproductive cycle of adult females of five Ltttorarta species at Cockle Bay 541

13.3 Frequency of copulation in five Ltttorarta species over the year of observation at Cockle Bay 545

13.4 Size frequency histograms for Ltttorarta tntermedta on Rhtzophora trees at Cockle Bay, from August 1980 until , September 1981 549

13.5 Size frequency histograms for Ltttorarta scabra on Rhtzophora trees at Cockle Bay, from August 1980 until September 1981

551

13.6 Size frequency histograms for Ltttorarta phtLtpptana on Rhtzophora trees at Cockle Bay, from August 1980 until September 1981

553

13.7 Size frequency histograms for Ltttorarta phtttpptana on Avtcennta trees at Cockle Bay, from October 1980 until October 1981

555

13.8 Size frequency histograms for Ltttorarta ftLosa on Avtcennta trees at Cockle Bay, from August 1980 until September 1981

557

13.9 Seasonal patterns of estimated recruitment of four Ltttorarta species at Cockle Bay 560

XXV

13.10 Seasonal variation in estimated population density of four Ltttorarta species at Cockle Bay 563

13.11 Survivorship curves for 'juvenile' and 'adult' cohorts of four Ltttorarta species at Cockle Bay 566

13.12 Seasonal variation in monthly survivorships of size classes of Ltttorarta tntermedta on Rhtzophora trees at Cockle Bay 572

13.13 Seasonal variation in monthly survivorships of size classes of Littorarta scabra on Rhtzophora trees at Cockle Bay 574

13.14 Seasonal variation in monthly survivorship of one size class of Ltttorarta pht/tpptana on Rhtzophora trees at Cockle Bay 576

13.15 Seasonal variation in monthly survivorships of size classes of Ltttorarta phtLtpptana on Avtcennta trees at Cockle Bay 578

13.16 Seasonal variation in monthly survivorships of size classes of Ltttorarta ftLosa on Avtcennta trees at Cockle Bay 580

13.17 Monthly temperature and rainfall for the period July 1980 until October 1981, recorded by Bureau of Meteorology at Townsville airport, 12 km from Cockle Bay 582

13.18 Growth curves for Ltttorarta tntermedta on Rhtzophora trees at Cockle Bay 590

13.19 Growth curves for Ltttorarta scabra on Rhtzophora trees at Cockle Bay 590

13.20 Growth curves for Littorarta phtLtpptana on Avtcennta trees at Cockle Bay 592

13.21 Growth curves for Ltttorarta ftLosa on Avtcennta trees at Cockle Bay 592

13.22 Seasonal variation in the instantaneous size-specific growth rate (k) for Ltttorarta scabra and L. tntermedta, on Rhtzophora trees at Cockle Bay

596

13.23 Seasonal variation in the instantaneous size -specific growth rate (k) for Ltttorarta phtLtpptana and L. ftlosa, on Avtcennta trees at Cockle Bay 598

13.24 Seasonal variation in the percentage of individuals of Ltttorarta ft/03a and L. phtLtpptana with a flared and thickened (non-growing) apertural lip to the shell, in samples of adult snails with at least one varix 601

14.1 Vertical distribution of Metopograpsus species in

xxvi

Rhtzophora forest at Cockle Bay over 24 hours 644

14.2 Design and results of the exclusion cage experiment at Cockle Bay, to determine sources of mortality of Ltttorarta ftLosa on Avtcennta trees 649

14.3 Results of laboratory predation trials in which Ltttorarta ftLosa and L. articuLata were preyed upon by eight Metopograpsus Lattfrons of various sizes

654

14.4 Distribution of repaired shell breakages per whorl on five species of Ltttorarta from Rhtzophora and Avtcennta trees at Cockle Bay 659

14.5 Rate of sublethal damage (repaired breakages per whorl per month) plotted against shell size, for four species of Ltttorarta from Rhtzophora and Avtcennta trees at Cockle Bay 661

14.6 Relationships between index of shell thickness and vertical zonation of Ltttorarta species above the ground, at localities in Australia, South-east Asia and Hawaii 666

15.1 Ltttorarta ftLosa arranged on foliage of Avtcennta at Cockle Bay, showing range of colour forms 709

15.2 The three common bark-dwelling species of Ltttorarta at Cockle Bay, on Rhtzophora trunk 709

15.3 Relationships between index of shell colour variation (E) and vertical zonation of Ltttorarta species above the ground, at localities in Australia, South-east Asia and Hawaii

712

15.4 Geographical variation in proportions of shell colour classes in samples of Ltttorarta ftLosa from Australia and the Arafura Sea 715

15.5 Geographical variation in proportions of shell colour classes iri samples of Ltttorarta paLLescens from the Indo-Pacific 717

15.6 Annual variation in proportions of shell colour classes of Ltttorarta ftLosa on Avtcennta trees at Cockle Bay 733

15.7 Correlation between index of shell colour variation (E) and estimated population density in Ltttorarta ftLosa on Avtcennta trees at Cockle Bay 733

15.8 Evidence for apostatic selection acting on Ltttorarta ftLosa on Avtcennta bushes at Cockle Bay 736