Polymorphism in Marine Mollusksand Biome Development

ARTHUR H. CLARKE

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SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY • NUMBER 274

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S M I T H S O N I A N C O N T R I B U T I O N S T O Z O O L O G Y • N U M B E R 2 7 4

Polymorphism in Marine Mollusksand Biome Development

Arthur H. Clarke

SMITHSONIAN INSTITUTION PRESS

City of Washington

1978

ABSTRACT

Clarke, Arthur H. Polymorphism in Marine Mollusks and Biome Develop-ment. Smithsonian Contributions to Zoology, number 274, 14 pages, 5 figures,1978.—Many arctic marine mollusks exhibit much greater intraspecific variationin shell shape and sculpturing and greater interspecific morphological overlapthan temperate or tropical species of the same families. Tropical marine mollusksordinarily exhibit more pronounced interspecific morphological distinctness inmixed-species communities and more remarkable intraspecific polychromatismin single-species dominated communities than their temperate or arctic relatives.A number of groups do not exhibit any variability shifts with latitude but shiftsopposite to those here described have not been observed. Changes in the natureand intensity of natural selection, which are deemed to occur with increasedbiome maturation, appear to account for these morphological trends .

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

Library of Congress Cataloging in Publication DataClarke, Arthur Haddleton, 1926-Polymorphism in marine mollusks and biome development.(Smithsonian contributions to zoology ; no. 274)Bibliography; p.1. Mollusks—Arctic regions. 2. Mollusks—Tropics. 3. Polymorphism (Zoology) 4. Animal so-

cieties. 5. Marine ecology. I. Title. II. Series: Smithsonian Institution. Smithsonian con-tributions to zoology ; no. 274.

Q1.S54 no. 274 [QJL429] 591'.08s [594'.09'28] 77-16821

Contents

Page

Introduction 1Acknowledgments 1

Variability in Arctic Marine Mollusks 1Variability in Tropical Marine Mollusks 5The Diversity Maturation Hypothesis 7

Phase I: Initial Occupancy 7Phase II: Early Biological Selection 8Phase III: Biome Maturation 9

Discussion 9Conclusions 11Summary 12

Phase I: Initial Occupancy 12Phase II: Early Biological Selection 12Phase III: Biome Maturation 12

Literature Cited 13

HI

Polymorphism in Marine Mollusksand Biome Development

Arthur H. Clarke

Introduction

This paper examines aspects of variation in shellshape and shell coloration among marine mollusks.Some previous generalizations about patterns ofintra- and interspecific morphological variability inarctic, temperate, and tropical mollusks are stated,pertinent data are compiled and presented, and ahypothesis is formulated to partially account forthese patterns in terms of altered responses to chang-ing selective pressures.

Viewed from the perspective of experience gainedinitially with New England marine mollusks andlater enriched through several field expeditions inthe Canadian arctic and others to the West Indiesand Panama, the nature and extent of variation inarctic and in tropical marine mollusks appearsquite different from each other and from those intemperate latitudes. Of course it is well known thatarctic mollusks are dull in color and conservativein sculpture and that tropical mollusks are oftencolorful and flamboyant in sculpture. More detailedexamination of these features reveals interestingcorrelations and trends, however, which presumablyare attributable to changes in the nature and inten-sity of natural selection.

The literature citations in the text are includednot only to document the statements made but toprovide additional bases for the generalizationspresented. Readers who desire additional informa-

Arthur H. Clarke, Department of Invertebrate Zoology, Na-tional Museum of Natural History, Smithsonian Institution,Washington, D. C. 20560.

tion, for example about the variability of arctic ortropical mollusks, are invited to refer to that litera-ture.

ACKNOWLEDGMENTS.—P. Beland, R. S. Houbrick,E. Alison Kay, Vida Kenk, E. G. Munroe, J. Rose-water, E. Yochelson, and R. Zusi read preliminarydrafts of this paper and provided useful suggestions.The photographs are by Smithsonian Institutionstaff photographer V. E. Krantz and the statisticalresults were provided by the Smithsonian Com-puter Services Department through Mrs. Lee AnnHayek. Laboratory assistance was provided by CathyLamb, Raye Germon, and Amr Mounib. The workwas conceived and begun while the author was astaff member of the National Museum of NaturalSciences, National Museums of Canada, but princi-pal support came later from the National Museumof Natural History, Smithsonian Institution. I amgrateful for all of this help.

Variability in Arctic Marine Mullusks

An approximation of the relative taxonomiccomplexity of the families of marine bivalve andprosobranch gastropod mollusks in the arctic maybe achieved by ranking them in order of the num-ber of arctic species they contain. No overall re-visions for the entire arctic exist but the regionalstudies by Ockelmann (1958) for East Greenlandbivalves and by Macpherson (1971) for Canadianarctic prosobranchs treat what appear to be typicalarctic faunas. Their data indicate that the mostimportant arctic families of these groups are asfollows:

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Bivalves (57 species): Nuculanidae (11), Astarti-dae (5), Mytilidae (5), Thyasiridae (4), Tellinidae(4), Cuspidariidae (4), Arcidae (3), Pectinidae (3),Cardiiae (3), Thraciidae (3), Limidae (2), Saxicavidae(2), and 8 families each with 1 arctic species.

Prosobranchs (102 species): Buccinidae (36), Tur-ridae (15), Trochidae (9), Lamellariidae (7), Ris-soidae (5), Naticidae (4), Muricidae (4), Lacunidae(3), Trichotropidae (3), Acmaeidae (2), Littorinidae(2), Turritellidae (2), and ten families each with 1arctic species.

The extreme and sometimes baffling phenotypicdiversity of form in some arctic species of Buccinum,Neptunea, Admete, Bathyarca, Mytilus, Astarte,Mya, and Hiatella, among others, and the conse-quent difficulty in distinguishing species in severalof these genera has been commented upon by sev-eral authors (e.g., Thorson, 1944; Ockelmann 1958;MacGinitie, 1959; A. Clarke, 1960, 1963; Macpher-son, 1971; Petersen, 1977). (Variation in color withinarctic species is not extreme and most species arewhite or some shade of brown.) In some publishedreports, however, and even in some museum col-lections, the fact that certain species are variablein shell shape within populations has been ob-scured by the segregation of various "varieties" and"forms."

MacGinitie (1959:65) has expressed well thesituation pertaining to marine mollusks:

Perhaps nowhere in the world do shells consistently exhibitsuch marked and confusing variations as do the Arcticspecies. Among the gastropods the genera Buccinum,Boreotrophon, Neptunea, Beringius, and Diaphana andamong the pelecypods Musculus, Astarte, and Liocyma areparticularly subject to variation. Because of these great varia-tions, species of some of these genera are extremely difficultto identify and in order to resolve these problems it will benecessary to make intensive studies at the specific level.

A. Clarke (1963) briefly commented on the ex-treme diversity seen in mollusks dredged from theChukchi Sea (Arctic Ocean). In Bathyarca frielei(Friele), for example, in addition to great variationin shell shape, some species have short taxodonthinge teeth which are nearly perpendicular to thehinge line whereas many others possess only elon-gate hinge teeth which are roughly parallel to thehinge line. All intergrades also occur. The speci-mens with lamellate hinge teeth are almost iden-tical, in fact, to the Ordovician species Cyrtodontagrattanensis Wilson (Steele and Sinclair, 1971, pis.

1-3) except that C. grattanensis is four times aslong.

In the following table (Table 1) arctic specieswhich exhibit marked variability within popula-tions are compared with other taxonomically re-lated and approximately ecologically equivalentspecies from the same climatic region and fromother regions. The families examined have beenselected because they are epifaunal and subject tovisual predation and because there are enoughspecimens within single lots available in museumcollections to enable diversity to be estimatedwith some confidence. All are important arcticfamilies. The Buccinacea, in fact, are the dominantgroup of arctic marine gastropods and constituteabout 35% of the gastropod species there. Relativediversities in particular morphological characteris-tics of population samples have been assessed bycomparing their coefficients of variability (CV).This is the standard deviation expressed as a per-

SD X 100centage of the mean (CV = ).

It is clear from Table 1 that in the superfamiliesArcacea, Astartacea, and Buccinacea, within popu-lations of some arctic species, variation in shellshape is unusually great. Not all arctic species inthese (or other) superfamilies show such prominentpolymorphism (pers. obs. and Petersen, 1977). Pre-sumably these groups are genetically more con-servative. Within the three superfamilies consid-ered, however, no species samples were found incollections in the Smithsonian Institution or theNational Museums of Canada from shallow tem-perate or tropical waters that exceeded, equalled, oreven approached the intrapopulation variabilityof the most variable arctic species samples. In someother superfamilies (e.g., Trochacea: Molleria cos-tulata (M0ller); Veneracea: Liocyma fluctuosa(Gould); Myacidae: Mya truncata L.), however,substantial variation also appears to exist, but suffi-cient material is not available to statistically dem-onstrate it. An estimated 35% to 40% of all arcticmarine mollusk species appear to be significantlymore variable than their closest temperate rela-tives. The other arctic species appear to be approxi-mately equally as variable as their closest tem-perate relatives.

Morphological distinctness between sympatricspecies appears to be substantially less in some