Intraspecific Shore-Level Size Gradients in Intertidal Molluscs

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<ul><li><p>Intraspecific Shore-Level Size Gradients in Intertidal MolluscsAuthor(s): Geerat J. VermeijReviewed work(s):Source: Ecology, Vol. 53, No. 4 (Jul., 1972), pp. 693-700Published by: Ecological Society of AmericaStable URL: .Accessed: 26/10/2012 11:03</p><p>Your use of the JSTOR archive indicates your acceptance of the Terms &amp; Conditions of Use, available at .</p><p> .</p><p>JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range ofcontent in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new formsof scholarship. For more information about JSTOR, please contact</p><p> .</p><p>Ecological Society of America is collaborating with JSTOR to digitize, preserve and extend access to Ecology.</p><p> </p></li><li><p>INTRASPECIFIC SHORE-LEVEL SIZE GRADIENTS IN INTERTIDAL MOLLUSCS' </p><p>GEERAT J. VERMEIJ Department of Zoology, University of Maryland, College Park, Maryland 20742 </p><p>Abstract. A synthesis of new data and literature observations indicates that, within rocky intertidal gastropod species (1) shell size tends to increase in an upshore direction in species characteristic of the littoral fringe and in high intertidal limpets, and (2) shell size often decreases in an upshore direction in species typical of lower intertidal levels. These size gra- dients are considered to be a response to gradients in the intensity and nature of postlarval prereproductive mortality on the shore. In gastropods whose size gradients are of type 1, mortality generally resulting from physical extremes operates from above and is most effec- tive against small individuals. Among snails with size gradients of type 2, mortality often in the form of predation or other biotic interaction is most intense at low levels. Sedentary species can become graded according to size with shore level only through differential mor- tality of one size group relative to another over the entire vertical range of the species, while mobile forms may become size segregated by active migration of one size group relative to another. </p><p>INTRODUCTION </p><p>The physical partitioning of different growth stages in different parts of the niche is typical of many an- imal species and, like morphological lines, can often be correlated with and considered to be a response to environmental gradients in space or time. In the ma- rine intertidal zone, the separation of postlarval life stages is often in the form of a gradient in body size along a vertical transect of the shore. Although many such gradients have been described, very few are adequately understood; and little attempt has been made to correlate the nature and direction of the size gradients with mode of life and habitat. </p><p>In conjunction with a study of morphological pat- terns among high intertidal rocky-shore gastropods (Vermeij, in preparation), samples of species were collected from different shore levels in several lo- calities and were examined for possible shore-level size gradients. In this paper, a summary of these gra- dients together with those recorded in previous lit- erature is presented, and an interpretation of patterns relating nature and direction of the gradients with mode of life and habitat of the species is suggested. </p><p>OBSERVATIONS AND RESULTS </p><p>Tables 1 and 2 summarize known size gradients from personal observations and from previous liter- ature in rocky-shore gastropods, based on maximum linear shell dimension. Only those size gradients are considered where juvenile specimens were included in the populations sampled. Size gradients reported for the first time in this paper were observed at all localities in the geographic area indicated where the species in question was found. </p><p>Not all gastropods exhibit shore-level size gra- dients, and many size gradients are likely to have been </p><p>1Received December 23, 1971; accepted February 8, 1972. </p><p>overlooked. Segal (1956) states that there are no significant size differences between low-level and high- level populations of the limpet Acmaea limatula in southern California, and Abe (1942) failed to find a size gradient in populations of the mangrove snail Littorina scabra in Palau. Size gradients also appear to be lacking in many forms of L. saxatilis in Britain (James 1968). </p><p>Some caution is to be exercised in the interpreta- tion of the present data. Allometric changes during ontogeny may slightly alter the correspondence be- tween maximum linear shell dimension and volume or weight. In most limpets there is an increase in cone height relative to major basal diameter (the max- imum linear dimension) during growth; hence size data based on the major diameter will tend to under- estimate differences in volume or weight between two samples. On the other hand, data based on the max- imum linear dimension of littorinids (distance from apex of shell to farthest point on outer lip) will tend to overestimate weight or volume differences because of allometric increase of spire height relative to aperture length and shell width during ontogeny. I feel, however, that maximum dimension is an ad- equate, if somewhat crude, measure to determine the presence and nature of size segregation. Shotwell's (1950) data on size gradients in two Californian limpets of the genus Acmaea (see Table 2) are based on volume. </p><p>A second, perhaps more serious, difficulty may arise because of differences in growth rate between low-level and high-level individuals of the same spe- cies. Newcombe (1935), Seed (1968), and others have shown that growth rate in the mussel Mytilus edulis is much lower at high shore levels than in lower shore habitats; yet high-level individuals, de- spite their small size, are often the oldest members of the population. In the sand-dwelling bivalve Tel- </p></li><li><p>694 GEERAT J. VERMEIJ Ecology, Vol. 53, No. 4 </p><p>TABLE 1. Gastropods increasing in size in an upshore direction </p><p>Species Vertical range Area References </p><p>Acmaeidae Acmaea digitalis high intertidal Oregon, California Frank 1965, Haven 1971 A. scabra high intertidal California Sutherland 1970, Haven 1971 Notaocema mayi high intertidal Tasmania Bennett and Pope 1960 </p><p>Patellidae Patella vulgata low to high intertidal Great Britain Orton, 1928 Lewis 1954, Blackmore </p><p>1969 Fissurellidae </p><p>Fissurella barbadensis low to high intertidal Barbados Ward 1967 Trochidae </p><p>Gibbula umbilicalis mid to high intertidal Wales, Brittany Bakker 1959, Williams 1964b Neritidae </p><p>Nerita quadricolor high intertidal Aldabra Atoll Hughes 1971 N. ascensionis deturpensis mid intertidal to lit- Ilha Fernando de No- Vermeij 1970 </p><p>toral fringe ronha, Brazil Littorinidae </p><p>Littorina angulifera high intertidal, lit- Florida, West Indies Lenderking 1954, GJV toral fringe </p><p>L. neritoides high intertidal, lit- Mediterranean Palant and Fishelson 1968, Star- toral fringe mtihlner 1969 </p><p>L. punctata high intertidal, lit- Mediterranean, Ghana Evans 1961, Palant and Fishelson toral fringe 1968, GJV </p><p>L. ziczac brasiliensis high intertidal, lit- Brazil Vermeij and Porter 1971 toral fringe </p><p>L. peruviana high intertidal, lit- Peru Vegas 1963 toral fringe </p><p>L. africana high intertidal, lit- South Africa Eyre and Stephenson 1938 toral fringe </p><p>L. saxatilis rudis high intertidal Great Britain James 1968 L. unifasciata unifasciata high intertidal, lit- New South Wales, Vic- Dakin, Bennett, and Pope 1948, </p><p>toral fringe toria, Tasmania Bennett and Pope 1953, 1960 L. u. antipodum high intertidal, lit- New Zealand Morton and Miller 1968 </p><p>toral fringe L. praetermissa high intertidal, lit- Victoria, Tasmania Bennett and Pope 1953, 1960 </p><p>toral fringe L. coccinea littoral fringe Society Islands Fischer 1952 L. planaxis high intertidal, lit- California North 1954 </p><p>toral fringe L. littoreaa low to high intertidal Great Britain Smith and Newell 1955, Williams </p><p>1964a Nodilittorina helenae ssp. high intertidal, lit- Ilha Fernando de No- GJV </p><p>toral fringe ronha, Brazil N. tuberculata high intertidal, lit- West Indies Lewis 1960, GJV </p><p>toral fringe N. miliaris high intertidal, lit- Sierre Leone, Ghana GJV </p><p>toral fringe N. millegranaa low intertidal to Ceylon Atapattu 1968 </p><p>littoral fringe Tectarius muricatus littoral fringe West Indies de Jong and Kristensen 1965 </p><p>Muricidae Thais distinguenda low to mid intertidal Queensland Endean, Kenny, and Stephensen 1956 Dicathais aegrota subtidal to mid West Australia Phillips 1969 </p><p>intertidal Siphonariidae </p><p>Siphonaria gigass mid to high intertidal west coast Panama GJV S. lessoni high intertidal, lit- Argentina Olivier and Penchaszadeh 1968 </p><p>toral fringe S. picta mid to high intertidal southern Brazil Marcus and Marcus 1960 </p><p>aComplex gradient; see text under Obervations. </p><p>lina tennis, growth rate is inversely related to pop- ulation density (Stephen 1928, Trevallion, Edwards, and Steele 1970); since density decreases from low to high shore levels, there is an apparent increase in body size in an upshore direction but no correspond- ing increase in average age (Stephen 1928). Suther- land (1970) has similarly found an inverse relation- ship between growth rate and population density in </p><p>the limpet Acmaea scabra, but in this case an up- shore decrease in density and corresponding increase in growth rate merely reinforce an upshore increase in mean age (Sutherland 1970, Haven 1971). The growth rate of high-level A. scabra was found to be slower than that of low-level individuals when kept at the same population density (Sutherland 1970). Judging from the number of growth rings on the </p></li><li><p>Summer 1972 SHORE-LEVEL SIZE GRADIENTS 695 </p><p>TABLE 2. Gastropods decreasing in size in an upshore direction </p><p>Species Vertical range Area References </p><p>Acmaeidae Acmaea peltaa low to mid intertidal Oregon Shotwell 1950 A. testudinalis testudinalis low to mid intertidal Nova Scotia Stephenson and Stephenson 1954 A. s. scutuma low to mid intertidal Oregon Shotwell 1950 A. noronhensis low to high intertidal Ilha Fernando de No- GJV </p><p>ronha, Brazil Patellidae </p><p>Patella argenvillei low intertidal west South Africa Stephenson, Stephenson, and Day 1940 </p><p>P. intermedia mid intertidal Senegal GJV Trochidae </p><p>Cittarium pica subtidal to mid West Indies Lewis 1960, GJV intertidal </p><p>Tegula funebralis low to mid intertidal Washington Paine 1969, 1971 T. atra low to mid intertidal central Chile GJV Monodonta lineata low to high intertidal Great Britain Desai 1966 Trochus niloticus subtidal to low Guam GJV </p><p>intertidal Neritidae </p><p>Nerita undata mid to high intertidal Singapore GJV N. scabricosta high intertidal to lit- west coast Panama Vermeij, in prep. </p><p>toral fringe N. sanguinolenta low to mid intertidal Red Sea Safriel 1969 </p><p>Littorinidae Littorina scutulata high intertidal California Bock and Johnson 1967 L. Iittorea low intertidal to Connecticut GJV </p><p>littoral fringe L. littoreab low to high intertidal Great Britain Smith and Newell 1955, Williams </p><p>1964a Planaxidae </p><p>Planaxis planicostatus mid to high intertidal west coast of Panama GJV Muricidae </p><p>Morula granulate low to mid intertidal Hawaii GJV Drupa ricina subtidal to mid Hawaii GJV </p><p>intertidal Thais haemastoma subtidal to high Senegal GJV </p><p>intertidal Ocenebra crassilabrum low to mid intertidal central Chile GJV </p><p>aJuveniles throughout vertical range; adults restricted to lower part of range. bComplex gradient; see text under Observations. </p><p>shell, size is positively correlated with age in all spe- cies in Tables 1 and 2. </p><p>Inspection of Tables 1 and 2 reveals two patterns among mobile rocky-shore gastropods: (1) shell size tends to increase in an upshore direction in species characteristic of the littoral fringe and in high inter- tidal limpets-that is, the largest and oldest indi- viduals are found near the upper limit of vertical distribution of the species; and (2) shell size often tends to decrease in an upshore direction in species typical of lower intertidal levels. </p><p>Among Littorinidae, a large number of supratidal species fall into pattern (1), while the high intertidal Littorina scutulata (see Bock and Johnson 1967) exemplifies pattern (2). Littorina littorea in Con- necticut, ranging from below low water to the lower- most littoral fringe, exhibits decreasing mean shell size toward high shore levels (Vermeij, unpublished). The same species on the coast of Kent in Britain exhibits a complex gradient with juveniles apparently living subtidally and adults inhabiting low and mid intertidal levels below second-year individuals (Smith </p><p>and Newell 1955). Still another pattern is shown by L. littorea in Wales (Williams 1964a), where juve- niles congregate near M. L. W. N., larger and older individuals occurring both above and below this level. This pattern is similar to that described by Atapattu (1968) for "Nodilittorina granularis" (= N. mille- grana), a species ranging throughout the intertidal to the lower littoral fringe on the west coast of Ceylon. </p><p>The only apparent exception to the rule that inter- tidal littorinids should conform to pattern (2) was observed by Bakker (1959), who found that the European intertidal L. obtusata increased in size in an upshore direction. Sacchi (1969a), however, could not detect any size gradient in this species, and points out that Bakker's material actually consisted of two species, the smaller low intertidal L. mariae and the larger mid intertidal L. obtusata. </p><p>In limpets (Acmaeidae, Patellidae, Siphonariidae), an intraspecific size decrease toward high shore levels is limited to low and mid intertidal species, while high intertidal species tend to exhibit the opposite size gradient. Most trochids in which size segregation </p></li><li><p>696 GEERAT J. VERMEIJ Ecology, Vol. 53, No. 4 </p><p>has been described exhibit an intraspecific size de- crease in an upshore direction. </p><p>DISCUSSION </p><p>The transitional nature of the intertidal habitat from fully marine to fully terrestrial conditions is reflected in the increase in rigor of the physical en- vironment (desiccation, extremes in temperature and salinity) from low to high shore levels. Not only does this gradient result in a pattern of distinct zones of plants and animals at different shore levels, but it may also lead to differences in the degree of inter- specific competition, food availability, and predation in different parts of an animal's vertical range (Con- nell 1961a, b, 1970, Paine 1969). We may therefore expect causes of mortality to be different and to act with varying intensities in different parts of the ver- tical range of a given species. </p><p>Suppose now that the intraspecific shore-level size gradients are a response to shore-level gradients in the nature and intensity of mortality. If the mortality gradients have any predictable component, any re- sponse to them might be expected to have adaptive significance. Postlarval prereproductives might, be- cause their survival is necessary to the maintenance of the population as a whole, he expected to inhabit the zone of minim...</p></li></ul>