M 1 ? VMS Ro IV; v/v ISSN 0043-33111 THE A Quarterly published by CAUFORNIA MALACOZOOLOGICAL SOCIETY, INC. Seriteley, California VOLUME 24 OCTOBER 1, 1981 NUMBER 2 CONTENTS A Method for Artificially Protracting Gastropod Radulae and a New Model of Radula Function. (1 Plate; 2 Text figures) TOM E?MORRIS &. CAROLE S. HICKMAN , . . . 85 Crystalline Style Cycling in Ilyandssa obsolete (Say) (Mollusca: Neogastropoda) : Further Studies. (1 Text figure) LAWRENCE A, CURTIS & L. E. HURD ................ 91 Spatial Segregation of Four Species of Turban Snails (Gastropoda: Tegula) iii Central California. (4 Text figures) .,_. MARIANNEL.RIEDMANJ AN SON H. HINES &. JOHN S. PEARSE ....... 97 Diet and Reproductive Biology of the Rocky Intertidal Prosobranch Gastropod Tricolia pulloides. (5 Text figures) MARY G. MOOERS 103 Growth Rates of Penitella penita (Conrad, 1837), Chaceia ovoidea (Gould, 1851) (Blvalvia : Pholadidae) and Other Rock Boring Marine Bivalves in Monte- rey Bay. (3 Plates) E. C. HADERUE 109 Shell Shape Changes in the Gastropoda: Shell Decollation in Rumina decollata (Pulmonata: Subulmidae). (1 Plate; 3 Text figures) PIETERW. KAT 115 Two New Cryptobranch Dorid Nudibranchs from California. (1 Plate; 1 a Text figures). DAVID W BEHRENS & ROBERT HENDERSON .............. 120 CONTENTS ? Continued Distributed free to Members of the California Malacozoological Society, Inc. Subscriptions, by Volume only, payable in advance to Calif Malacozocl. Soc, Inc. Volume 24: $37.50 plus mailing charges $1.50 U. S. A; ?5.- for all foreign addresses Single copies this issue $20.-. Postage additional. Send subscription orders to California Malacozoological Society, Inc. 1584 Milvia Street, Berkeley, CA 94709, U.S. A Address all other correspondence to Dr. R. STOHLER, Editor, Department of Zoology University of California, Berkeley, California 94720, U.S.A. Second Class Postage Paid at BciVtlcy, California Vol. 24; No. 2 THE VEL1CER Page 97 Spatial Segregation of Four Species of Turban Snails (Gastropoda: Tegula) in Central California BY MARIANNE L. RIEDMAN, ANSON H. HINES' AND JOHN S. PEARSE Center for Coastal Marine Studies, University of California, Santa Cruz, California 95064 (4 Text figures) INTRODUCTION FOUR, SPECIES OF GRAZING TURBAN SNAILS of the genus Tegula are abundant in central California (ABBOTT & HADERUE, 1980). Two of these species, Tegula ftmebralis (A. Adams, 1855) and Tegula brunnea (Philippic 1848), are common in rocky intertidal communities; T. fiinebralis h abundant from mean lower low water {MLLW) to 1.5 m above MLLW, and T. brunnea is common below 0.5 m above MLLW. In addition, Tegula pulligo (Gmelin, 1791) and Tegula montereyi (Kiener, 1850) are common sub- tidally in kelp forests. LOWRY, MCELROY & PEARSE (1974) studied the distribution of the 3 subtidal species at one location within the middle of a kelp forest off Pacific Grove, California; the snails were associated with specific algae on the bottom as well as throughout the water col- umn on fronds of giant kelp plants {Macrocystis pyrifera). In the present paper, we describe the horizontal and ver- tical distribution of all 4 species of Tegula, from the inter- tidal zone to the seaward edge of a kelp forest, at the same location as the LOWRY, MCELROY & PZARSE (1974) study. Distributions of the snails in early spring, when kelp bio- mass and canopy are minimal, are compared with their distributions in late summer, when kelp biomass and can- opy development are maximal. METHODS Our study was conducted at Hopkins Marine Life Refuge in Monterey Bay off Pacific Grove, California. The habitat is very heterogeneous with a granite substrate interspersed with sand channels, pinnacles, cracks, and boulders. The substrate is covered with a lush understbiy of Cystoseim osmundacea, many species of red algae, and a dense algal- invertebrate turf of coralline algae, tunicate;, bryozoans, solitary corals, sponges, vermetids, and many other en- crusting organisms. The dominant, canopy-forming plant is the giant kelp Macrocystis pyrifera. A detailed descrip- tion of the study area is provided in PEARSE & LOWRY (1974)- Samplmg was done using SCUBA in March 1977 and again in August 1977 along a 300m transect that ex- tended from the intertidal zone seaward, through the kelp forest to a depth of about 13 m (Figure 1). Nine stations were established along the transect at about 1.5 m incre- ments of increasing depth beginning at the intertidal level Present address: Chesapeake Bay Center for Environmental'. Studies, Smithsonian Institution, R O. Box 28, Edgewater, Mary- land 31037 Figure 1 Hopkins Marine Life Refuge, Pacific Grove, California, showing the nine sampling stations transecting the intertidal zone, shallow subtidal zone and lelp forest (hatched). Drawn from an aerial photograph taken on June 14, 1978 Page 98 THE VEL1GER Vol. 24; No. 2 of 1.5m above MLLW. Populations of Tegula spp. were sampled at each station in two ways, depending on whether they occurred on giant kelp plants or on the "bottom" which included algal-invertebrate turf and understory plants as well as rock and sand. At each station, approxi- mately 200 individuals of Tegula spp. were collected from the bottom. Giant kelp plants were present only at sta- tions 3 to 9; at these stations, snails were collected from the nearest giant kelp plant that extended up the water column to the surface. All snails were removed from the selected kelp plants in 1.5 m increments of increasing depth from the surface to the bottom; snails from each sample level were placed in a separate plastic bag. The snails were identified, counted and measured to the nearest mm in the laboratory. The data were analyzed for relative frequency and size distribution of each species on the bottom and on kelp plants at each station. The relative frequencies of each species on kelp plants at each station also were calculated for each 1.5 m depth interval in the water column. Our sampling design did not provide estimates of the densities of each species along the transect because determining densities requires additional labor-intensive estimates of the number of snails per unit bottom area, per kelp frond and the density of kelp fronds at each station. MARCH (Tegula brunnea -a -4 ~6 -8 Depth (m) 10 -is -14 EESULTS In March each of the 4 species of Tegula showed a distinct zone of abundance on the bottom from the intertidal zone to the seaward edge of the kelp forest (Figure 2). Tegula junsbralis was restricted to the intertidal region from about 1.5 m above MLLW to 0.5 m below MLLW. Tegula brunnea occurred between 0,5 m to 7 m below MLLW. Near the shoreward edge of the kelp forest, at a depth of 3m, nearly 90% of the turban snails on the bottom were comprised of TV brunnea. Tegula montereyi had a broad zone of distribution across the kelp forest, and except for a peak relative frequency of 50% at the 6 m depth, TV mon- tereyi did not exhibit a clear dominance in relative fre- quency at any location. The relative abundance of T. putligq on the bottom increased rapidly in the middle of the kelp forest at depths of 4 to 7 m. This species predom- inated in the seaward half of the kelp forest, with relative frequencies of 70% at a depth of 7m to 100% at the 13m depth. The distribution of turban snails on giant kelp plants along the transect was similar to that of the snails on the bottom (Figure a). Tegula brunnea was dominant on plants at the shoreward edge of the kelp forest. T. pulligo Figure a Distribution of four species of Tegula on the bottom and on giant kelp plants along the transect in March, 1977. The relative frequen- cies that each species comprised are plotted for each station. Snails on the bottom were sampled separately from: snails on kelp plants. At each station, about sop snails were collected ??m the bottom, and all snails were collected from single large kelp plants present at stations between depths from 3 to ra m. Sample sizes for snails on kelp plants are shown in Figure 4 predominated on plants at the seaward portion, and T. montereyi occurred at low relative frequencies on plants throughout the middle of the kelp forest The pattern of zonation along the transect in August was remarkably similar to that in March for all 4 species, both on the bottom and on kelp plants (Figure 3). How- ever, at 0.5m depth Tegula funebralis occurred with higher relative frequency in August than in March and TV brunnea occurred at correspondingly lower frequency. TV brunnea was present at higher relative frequencies in August than in March at the 4 to 6 m depths, both on the bottom and on kelp plants. Tegula montereyi did not Vol. 24; No. 2 THE VELIGER Page 99 80 60 AUGUST ) -^Tegula brunnea ' ' -*Tegula pulligo Tegula- on MacTOcystis pyrifera Tegula montereyi ii 1 1 i>*y4 1 Figure 3 Distribution of four species of Tegula on the bottom and on giant top plants in August, 1977. Sampling procedures as explained in Figure a attain relative frequencies in the middle of the kelp forest as high in August as in March. The distribution and rela- tive abundance of Tegula pulligo remained similar during both sampling periods. The vertical distributions of turban snails on giant kelp plants did not show patterns of zonation that were as dis- tinct as the horizontal distributions (Figure 4). Tegula brunnea in the shoreward part of the kelp forest showed a shift in relative abundance from the deeper portions of the plants in March up into the canopy in August. At the seaward stations, TV brunnea was generally evenly dis- tributed throughout the water column at both sampling periods. Tegvla montereyi occurred at about equal relative frequencies throughout the water column on kelp plants during both sampling periods. Similarly, T. pulligo was found at all depths on kelp plants with little apparent vertical zonation. However, in the middle of the kelp for- S"3 >v ^ Tegula montereyi ^ -6 -9 N. i a i A i Tegula pulligo Femttt Sole "*--sZJiB** 10O O ICO I (1 1 t > 1 1 Station, i^ 2 3 4 56 7 8 "9 March n = 24 39 65: 281 281 50 ? August n = no8 8~7 114 219 9a 17 54 Figure 4 Vertical distributions of four species of Tegula on giant kelp plants at stations along the transect in March 1977 (open polygons} and August >977 (solid polygons). The relative frequencies that each species comprised in the total number of snails collected from one large kelp plant at each station are shown for each 1.5 m interval of increasing depth from the surface to the bottom. Sample ??-* for each sampling period and scale of relative frequency in per- cent are indicated est, there were proportionately fewer individuals of T, pulligo near the top of the plants in August than in March. The size distribution of snails on the plants were similar to those found by LOWRY, MCELROY & PEAKSE (1974); individuals of Tegula brunnea, T. montereyi and T. pul- Page ioo THE VEL1CER Vol. 24; No. 2 Hgo were smaller on the bottom, and in the lower portions of the kelp plants, than on the upper portion of the kelp plants. DISCUSSION Kelp forests are complex structural communities (PEARSE & GERARD, 1977) and closely related species often exhibit zonal patterns of distribution from the intertidal zone to increasing depths, e.g., abalones (Tursc-HUtTE, 1976); bryozoans (BERNSTEIN & JUNG, 1979); scorpaenid fish (HAUUVCHER, 1977; LARSON, 1980}; and spider crabs (HiNJjs, 1981). The 4 sympatric species of Teguta in the present study similarly exhibited a well-defined pattern of spatial segregation in the Hopkins Marine Life Refuge. Tegula funebralis occurred exclusively in the intertidal zone. Tegula brunnea was dominant from the low inter- tidal zone through the shoreward portion of the kelp forest while Tegida pulligo dominated the seaward portion of the kelp forest. Tegula montereyi usually occurred at low relative frequencies throughout the kelp forest, with the highest relative abundance near the middle of the forest. Thisjiattern of zonation was consistent both on the bottom and on the giant kelp plants, and it changed little sea- sonally. The vertical distribution of the three species of Tegula oh fronds of Macrocystis pyrifera showed no clear pattern of zonation in either March or August However, in the shoreward portion of the kelp forest individuals of T. brunnea were more frequent and individuals of T. pulligo were less frequent in the kelp canopy in August than in March. LOWSY, MCELROY & PEARSE (1974) also found a vertical stratification with T. brunnea predominating in the canopy and T. pulligo predominating near the bottom. Their study was done near the center of the kelp forest {6-9 m depth) during August. Our more extensive sampling across the forest in March and August indicates that ver- tical stratification between these two species is very un- stable. Considering the marked seasonal changes in biomass and density of kelp plants in the Hopkins Marine Life Refuge (GERARD, 1976), the lack of substantial seasonal changes in the relative distribution of the different species of turban snails is surprising. Proliferation of kelp fronds in summer results in a tremendous increase in available substrate area at the sea surface, whereas winter storms greatly reduce the canopy cover. Moreover, winter storms probably knock many snails off the kelp fronds. The effect of the winter storm swells is most pronounced in shallower water, and may account for the seasonal shifts of Tegula brunnea on the plants of the shoreward portion of the forest. The mechanisms maintaining the zonation pattern of the 4 species of Teguta in the Hopkins Marine Life Refuge are not apparent. The upper distributional limits of many intertidal species may be determined by physical factors or behaviors that avoid adverse physical factors (e.g., WOLCOTT, 1973). In this respect, Teguta funebralis may be able to withstand temperature and desiccation stresses encountered in the intertidal area better than the other 3 species, thereby partially accounting for the near com- plete dominance of 7\ funebralis in the intertidal zone. However, such a physiological mechanism would not ac- , count for the observed lack of T. funebralis subtidally, or the zonation of the subtidal species. Gradients of water turbulence and light could be impor- tant in determining the zonation patterns of. the subtidal species. If, for example, individuals of Tegula brunnea were better able to maintain a grip on substrates in strong surge than those of T. pulligo, they might be expected to predominate in high-energy areas of the shallow subtidal zone and inner edge of the kelp forest. The zonation pat- tern of the snails also might be the result of pronounced dietary preferences for particular algal species limited to particular depths by specific light requirements. However, LOWRY, MCELROY & PEARSE (1974) found that all 3 sub- tidal species were widely distributed on different species of algae in the middle of the kelp forest, and all were found most frequently on giant kelp plants. Moreover, all 4 species have a high preference for Macrocystis pyrifera for food (unpublished observations; James M. Watanabe, pers, Cornm.). Considering the enormous abundance of giant kelp, both as attached plants and as pieces of plants on the forest floor (GERARD, 1976), competition among these snails for a limited food resource is unlikely, and differences in food preferences and availability probably cannot account for the subtidal zonation pattern. Further- more, we have not observed any behavior in the field or laboratory that could be categorized as interference com- petition (sensu COLWELL & EUENTES, 1975) among any of these species. Predation often limits the lower distribution of inter- tidal organisms, and in some areas predation by sea stars and whelks may determine the lower limit of Tegula funebralis (PAINE, 1969; B. MENCE, 1972; J. MENGE, 1974). Predation by rock crabs, Cancer antennarius, also could be important. These crabs cannot crack the shells of Tegula brunnea as easily as those of T. funebralis (ABBOTT & HADERLIE, 1980), and their presence in the low Vol. 24; No. 2 THE VELIGER Page i0i intertidal area might provide an explanation for the re- placement of T.funebralis by T. brunnea in the shallow sub tidal zone. However, individuals of C. antennarius are very scarce in the Hopkins Marine Life Refuge (Hines, in press), and the small number of crabs there is unlikely to have much impact on the large snail populations. Sea stars are important predators in the subtidal kelp forest of the Hopkins Marine Life Refuge, and Tegula spp. are highly preferred prey of Pbaster giganteus in par- ticular (HARROLD, 1981). WATANABE (1980) found that high w?ter movement and dense cover of red algae in the shallow subtidal area provided turban snails with some refuge from sea star predation. Snails within the kelp for- est also may escape sea star predation by crawling up - fronds of giant kelp plants (HARROLD, 1981). However, sea otters, Enhydra lutris, in the Hopkins Marine Life Refuge eat large numbers of turban snails collected from the kelp fronds (COSTA, 1978). The distributions and foraging patterns of all these different predators arc not understood well enough to explain whether and how they might influence the distribution patterns of the subtidal species of Tegula in the Hopkins Marine Life Refuge. Recruitment patterns may reflect and partly determine the distributions of the adult snails. Recruitment of Tegula funebralis, for example, is restricted to the intcrtidal zone (PAINE, 1969). Moreover, Watanabe (pers. comm.) found distributional patterns of juvenile turban snails in the Hop-. kins Marine Life Refuge that were strikingly similar to those of the adults. Small juveniles (<$ mm diameter) of JT. brunnea were most abundant on solid rock surfaces at depths less than 3 m, those of T. pulligo were mainly oh shell fragments in the seaward portion of the kelp forest, and those of T. montereyi, were on shell fragments dis- tributed throughout the forest. However, turban snails probably live at least for several years (FRANK, 1975), and they are very mobile, More knowledge of the movements and life history of these snails clearly is needed before the mechanisms that maintain their distinct patterns of dis- tribution will be revealed. SUMMARY *' Three species of turban snails display distinct patterns of zonation between the intcrtidal area and the sea- ward edge of the giant kelp forest in the Hopkins Marine Life Refuge, central California. Tegula fune- bralis is exclusively intcrtidal, Tegula brunnea is mainly shallow subtidal (0.5 to 7 m depth) in the shore- ward portion of the kelp forest, and Tegula pulligo is mainly deeper (7 to 13 m depth) in the seaward por- tion of the kelp forest. 2. A fourth species, Tegula montereyi, occurs subtidaUy throughout the kelp forest, but does not dominate any particular zone. 3. The 3 subtidal species of Tegula are distributed snails in the Hopkins Marine Life Refuge were very throughout the water column ori giant kelp plants, Macrocystis pyrifera, from the surface canopy to the bottom holdfasts, in the same pattern as their bottom distributions. Tegula brunnea is mainly on plants in the shoreward portion of the forest, T. pulligo is mainly on plants in the seaward portion of the forest, and T. montereyi is distributed more or less evenly on the plants. There is little distinct pattern of vertical distribution on the plants of any of the species of Tegula. 4. The patterns of distribution of the 4 species of turban ? similar in March and August, 1977, except that in August Tegula brunnea was most frequent in the can- opy and T. pulligo was most frequent near the bottom ??? of the plants. 5. Although recruitment patterns of juveniles reflect adult distributional patterns, the mechanisms main- taining these distributional patterns remain unclear. Tolerance to aerial exposure may permit Tegula-fune- bralis to thrive in the intcrtidal zone, and lack of such tolerance may exclude the other species from this zone. Effective defense from predation and tolerance to high water turbulence may permit T. brunnea to dominate in the shallow subtidal, while T. montereyi and T. pulligo may escape predation in ^?cper waters by crawling up kelp fronds. ACKNOWLEDGMENTS We thank Yusef Fadlajlah and Valle Thompson Sprinkle for diving assistance, Donald P. Abbott and the staff at Hopkins Marine Station of Stanford University for pro- ; viding diving facilities, Christopher Harrold and David R. Lindberg for comments on the manuscript, and James M. Watanabe for sharing his unpublished information. This work was supported by NGAA Office of Sea Grant, U.S. Department of Commerce, under Grant No. 04-7-158-44121 to John S. Pearse. Literature Cited ABBOTT, DONALD PUTNAM t EUOEKE CUHTOH HADZKUX i960. Prcnobr&nchia; marine snails, pp. 930-307. In; Robert H. Morrii, Donald P. Abbott and Eugene C. Haderlie, Intcrtidal invert*. bratet of California. Stanford Univ. Freu, Stanford, Calif xiv+ 690 pp.; 300 colored pit*.; 1 text fig. {** November 1980} Page 102 THE VELICER Vol. 24; No. 2 community m Ann. Rev. Ecol. Syst. 6; BERNSTEIN, BROCK B. fc NANCY JONO '979- ScjccUve pressures and convolution In a kelp southern California. Ecol. Monogr. 49: 335*355 COLWJSLL, ROBERT K~ a. 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