Distribution Patterns of the Herbivorous Gastropods

Benthos Research Vol.57,No.1:1-10(2002) BENTHOS RESEARCH The Japanese Association of Benthology

Distribution Patterns of the Herbivorous Gastropods Chlorostoma lischkei and Omphalius pfeifferi pfeifferi(Trochidae)in Relation to the Algal Community on a Rocky Shore of the Oshika Peninsula, Northeastern Japan

Akiyuki Ishida•õ,Koichi Sasaki,Michio Omori and Kazuya Taniguchi

Graduate School of Agricultural Science,Tohoku University,

1-1Tsutsumidori-Amamiyamachi,Aoba,Sendai,Miyagi981-8555,Japan

Abstract:The distribution of the herbivorous gastropods Chlorostoma lischkei and Omphalius pfeifferi pfeifferi in relation to the algal community was investigated on a rocky shore of the Oshika Peninsula,north eastern Japan.Chlorostoma lischkei was distributed chiefly in a shallower cobble area all year round while .p.pfeifferi lived always in the Eisenia bicyclis forest. Detailed microhabitat surveys showed that smallerO C.lischkei individuals inhabited the undersides of cobbles and the bottom beneath cobbles ,and that larger ones migrated to more exposed places. Larger O.p.pfeifferi individuals inhabited the laminae of E.bicyclis, medium-sized ones the holdfasts of E.bicyclis,and smaller ones the sea bottom under cobbles .Avoidance of predation is probably why smaller individuals of both species commonly lived beneath cobbles .With growth,O.p. pfeifferi utilized E.bicyclis not only as food but also as the main living space,but C.lischkei did not form such a relationship with algae.This indicates a fundamental difference between the two species in their relationships with algae and algal vegetation.

Key words:algal zonation,Chlorostoma lischkei,distribution,habitat,Omphalius pfeifferi pfeifferi

They are arranged in order from inshore to offshore:a INTRODUCTION kelp forest of larger perennial brown algae such as laminarians and fucoids,a zone dominated by the The trochid gastropods Chlorostoma lischkei and smaller perennial brown alga Dilophus okamurae,and a Omphalius pfeifferi pfeifferi are common throughout the flat of crustose coralline red algae.The rocky shore off waters around Japan from the southern part of Hokkaido Tomari-hama on the Oshika Peninsula in Miyagi Prefec to Kyushu,inhabiting rocky intertidal to subtidal areas. ture has an arrangement of benthos communities corre Both are herbivorous and similar in adult size and exter sponding to the algal zonation.There,O.p.pfeifferi in nal features. habits a kelp forest of Eisenia bicyclis,and C.lischkei a Subtidal seabeds on rocky shores along the Pacific cobble area shallower than the kelp forest.Both gastro coast from the Sanriku to Joban districts of northeastern pods are dominant species in their respective zones,each Japan commonly show a series of distinct algal zones, having a larger biomass than other gastropod species each dominated by a different alga(Taniguchi1991). (Omori et al.2000). Kelp forests of E.bicyclis on rocky shores have a

Received July27,2001:Accepted January 28,2002 high annual productivity of20kg/m2wet weight and pro vide important habitats and food for herbivorous

Present address:Institute of Environmental•õ Ecology, benthos,including commercially valuable animals such METOCEAN Co.Ltd.,1334-5 Riemon,Ooigawa, Shizuoka as sea urchins and abalone(Taniguchi&Kito1988). 421-0212,Japan Ishida et al.

Seki(1997)showed that biological processes in rocky shore ecosystems include interactions among various or MATERIALS AND METHODS

ganisms,including algae,and that animal populations Study area there might depend on such interactions as the pass through successive developmental stages.These findings The study was conducted in a small bay off Tomari suggest that the mode of life of animals in rocky shore hama on the northern coast of the Oshika Peninsula, ecosystems can only be understood in relation to algal Miyagi Prefecture(Fig.1).The U-shaped small bay vegetation.Although C.lischkei,which dominates the opens northeastwards to the open sea. It is exposed di shallow cobble area,and O.p.pfeifferi,which dominates rectly to wave action from offshore because of the ab in the kelp forest,are both inferred to intensely affect the sence of any islands or rocky reefs in front.The seabed dynamics of the rocky subtidal ecosystem,little is known slopes gently,reaching a depth of about8m at a distance about their interrelationships with the algal community of about200m from the coastline.The seabed down to from the juvenile to adult stages. 2m deep accumulates cobbles up to15-20cm in inter This study examines changes in the gastropods'dis mediate diameter,with some patches of Sargassum tribution patterns as they grow from settled juveniles to yezoense growing on the surface of the underlying rock adults,in relation to the algal community and the various exposed in places.The seabed2to7.5m deep consists microhabitats of each algal zone.The selection of habitat of black muddy rocks with scattered cobbles.The brown is discussed in relation to the change of feeding habits alga Eisenia bicyclis dominates to a depth of5m,and with growth.The species names of the gastropods used crustose coralline red algae in the range from5to7.5m. in this paper follow the taxonomic nomenclature of Dilophus okamurae forms a narrow band about1m wide Okutani(2000). more-or-less spanning the boundary between them.A sandy bottom with scattered cobbles occupies the area deeper than7.5m,where no dominant algae are found.

Depth-related sampling The gastropods C.lischkei and O.p.pfeifferi were taken at intervals of about one to two months from August, 1997,through June,1998,in order to investigate their vertical distribution patterns and changes in size compo sition with depth.A transect150m long was set north eastwards from a starting point(St.0)at a depth of about1.5m.Sixteen stations were set along the transect at intervals of10m.The stations were designated St.0 to St.150in accordance with their increasing distance from the starting point.Apart from these stations,St.A was set in the cobble area1to2m deep,and St.B in a patch of S.yezoense,in order to collect C.lischkei from the shallower zone.

At each station,a1m•~1m quadrat was placed

and the snails within it were collected by hand from algal

thallis and the sea bottom,including surfaces of cobbles

as well as the sea bottom beneath cobbles.Then,another

Sargassum zone Eisenia zone Dilophus zone smaller quadrat of0.5m•~0.5m was randomly placed crustose coralline algal zone inside the larger one.Organisms inside the smaller

quadrat were scraped off the sea bottom and cobbles Fig.1.Bottom topography and profile of algal zonation in the with a metal scraper and collected by means of an air-lift study area,Tomari-hama,Oshika Peninsula,Miyagi Prefecture. sampler,which drew them upward through a suction

Italic numerals show depths in meters.Solid circles denote sam pipe into a collecting bag of 1-mm mesh.Dominant pling stations.Stations0to150are set along a transect,16sta algae and bottom features within a5-m radius at each tions at10m intervals. station were also recorded.Organisms collected were

140145E•_•_”n•E•A•A•T‚î•A1•_•E•A•A•A‹T•A•A”••A‹T‚ç•œ•A89•A•A•A”n7•A‹T_34•B•_“¯'•Aƒm•_•A;bl•_"•A6‚Öil‚±,,,./ƒ€/1•c•œ'ƒ^'•_•A36‚¢8'‚Äƒt‚®ƒm•A•A•_•_•_•_•E•E‡`•A•A•E•A•æ•A'•A1•A•E‚µ•E•A•_•_•AŠd‡`"48"‚®0‚¢•A——•E•E•A•_•A•_•_li’È:˜K‹¿•ø“«•øli‘’i‘áƒjƒ“‚¬)1•Yˆê‹\•A“åƒm/œW Distribution of trochid gastropods

immediately fixed in10%seawater formalin.Samples formalin solution in seawater.The length,width,and were not obtained at Sts.130and150in March of1998 height of each cobble were measured after the animals because of rough weather. had been removed from them,and the small algae grow Chlorostoma lischkei and O.p.pfeifferi were sorted ing on the cobble's surface were identified.The wet out and counted by species.The shell diameter(ShD)of weights of S.yezoense and E.bicyclis were recorded,and each individual was measured to the nearest0.01mm the number and arm length of lateral blades of E.bicyclis and the body weight was weighed to the nearest0.01g. were counted and measured.Both species of gastropod The smaller snails collected by air-lifting were sorted out were sorted out and measured in the same manner as for and their ShD was measured to the nearest0.01mm by the depth-related samples. using a stereo dissecting microscope equipped with an ocular micrometer. Other investigations

Two supplementary investigations were conducted in Microhabitat-related sampling June and September,1999.The investigation in June fo

To clarify and compare the micro-distribution of the gas cused on microhabitats in the Eisenia zone at Sts.3and tropods among zones exhibiting different conditions,six 4.At St.4,where E.bicyclis grew densely,a detailed stations(Sts.1to6)were established(Fig.1).Station distinction was made among three microhabitats:on

1was set in the cobble area1to2m deep,and St.2in algal laminae,around algal holdfasts,and on and beneath a patch of S.yezoense at a depth of about1m.Three sta cobbles.Collections of individuals of E.bicyclis and tions were set in the E.bicyclis zone:St.3in the cobbles,and drawing up of scraped-off organisms by the shoreward fringe about2m deep,St.4in the central part air-lift sampler were done in the same manner as for the

3-4m deep,and St.5 in the offshore fringe5-6m microhabitat-related samples.After the algae had been deep.Station6was in the crustose coralline red algal collected,a0.5m•~0.5m quadrat was placed on the zone at a depth of6-7m.Investigations were carried spot from which the algae had been cropped and organ out in September,November,and December of1998, isms were collected by the air-lift method.Then,three or when newly settled juveniles were expected to be ob four cobbles outside the quadrat were removed and the tained in the field. Larvae of the snails usually appear air-lift method was employed on the bottom surface be from mid-August to early September(Sasaki1994),and neath these cobbles.At St.3,with a sparse distribution the spawning season of O.p.pfeifferi lasts from May to of E.bicyclis(•ƒ2individuals/m2),organisms were ob

November(Horikawa&Yamakawa1982). tained from on and beneath cobbles,and these results

Organisms were collected from three microhabitats were compared with those from St.4. at each station:on algal laminae,surfaces of cobbles,and The investigation in September,1999,was carried the bottom beneath cobbles.At each station,three or four out at Sts.1,3,and4,focusing on the tops and under cobbles were collected randomly and shut into a plastic sides of cobbles and the bottom beneath cobbles.At each container.Then,a0.5m•~0.5m quadrat was placed on station,three or four cobbles were selected randomly and the spot from which the cobbles had been removed,and organisms on their tops were drawn up by the air-lift after scraping organisms inside the quadrat loose with a method.The cobbles were then enclosed in a plastic con metal scraper,the air-lift was used to draw them up into tainer in order to collect organisms adhering to their un a bag of1-mm mesh.Collections at Sts.1 and6were dersides.Organisms on the bottom beneath cobbles were made only from cobble surfaces and from beneath cob then collected by the air-lift method. bles,because no large algae grew there.At St.2,S. yezoense inside the quadrat was cropped at the holdfast Feeding habits and put in a collecting bag0.5m wide and2.5m long made of0.475-mm nylon mesh netting,in order to col Stomach content's of the gastropods were examined.For lect attached animals.At Sts.3,4,and 5,three individu C.lischkei,5snails collected from surfaces of cobble at als of E.bicyclis,regardless of age,were also cut at the St.A and five from rock surfaces in the S.yezoense holdfast and put in a collecting bag.Organisms that were patch at St.B were examined between August,1997,and shaken off the algae were also caught by the mesh net June,1998.The snails collected from cobbles ranged ting. from15.0to20.4mm in ShD with a mean and standard The cobbles,algae,and organisms were transported deviation of17.2•}1.81mm ShD,whereas snails col back to the laboratory and immediately fixed in10% lected from rock surfaces ranged from20.2to29.0mm

3 Ishida et al.

ShD(24.1•}3.04mm ShD).For O.p.pfeifferi20 image analyzing system(Quantimet600;Leica Cam snails collected in December,1998,and June,1999,from bridge Ltd.,Cambridge,England)that was connected to 3microhabitats at St.4were examined:those on algal a compound microscope.Sand grains were assumed to laminae,around the holdfasts of E.bicyclis,and on and have been taken in with food,because no attached dia beneath cobbles.The snails collected from these toms were detected on their surfaces.The category "other"included microorganisms such as copepods microhabitats ranged in size from11.0to27.4mm ShD ,ju

(19.4•}5.81mm ShD),from13.1to19.4mm ShD veniles of gastropods and bivalves,and foraminiferans,

(15.9•}2.31mm ShD),and from14.6to28.0mm ShD which were scarcely digested and were considered to

(19.3•}4.94mm ShD),respectively.In all cases the have been eaten accidentally. stomach contents were dissected out and mounted in glycerin on glass slides. Although fragments of algae in the stomach con RESULTS tents could not be identified to species level,they were Distribution of dominant algae and bottom substrata classified into three categories depending on color,cellu lar structure,and cell shape.Type1was similar in cellu Figure2shows the most dominant algal species and the lar structure to E.bicyclis,Type2to Sargassum spp., condition of the seabed at each station.At St.A,in the and Type3to smaller algae such as Neodisea yendoama,

Chondrus sp.,and Gelidium anansii.The stomach con Numbers of individuals O2040202020202020201997A•Ag.281•E204332000002030N•Bv.710248594407002030Dec.2210265707040020E301998•¸Jan.22='1023707000009Œd20Ž±•’30‚ÌMa,.1810370722002030ApŠÍ281•E020042002030June1‚è0907700072030St.ABO‚è020304050 tents were sorted into seven categories-algal fragments of Types1to3,crustose coralline red algae,unidentified digested algal fragments,sand grains,and other-and the area that each category occupied was measured by an

1997 Aug.28ab–Úš¢”®•‡•Ž•ß•ß•ß•ß”B•ß•ß•ßƒˆƒRNov.7a“å‘p“ï•c”X“ï“ï•c˜W– “ï”X˜W“ï•˜“ï“ï“ï“ï“ï’F“ï•˜"Š¶Ž¿"“UŽ¿’îŽ¿˜hŠ¶Š¶ƒ•Ž¿"Š¶Ž¿Ž¿Š¶ŠsŠ¶Š¶•rŠ¶,ƒ]""Ž¿Ž¿ƒ••rŽ¿Ž¿Œ[rŽ¿‰Q"‰¯b–ÚŽMƒˆ–|ŽM‘Á”®ŽM”®”±š£•ßƒˆƒRDec.22ab–ÚŽMŒœ”Ù–|ŽMŽFŒœŽF•ßât”®ŽFŒ®–ÚƒR1998Jan.22ab–ÚŽMŽMŽM”Ùi•ß—…–|ŽM”ÕŽF•ßŽŠƒRMar.i8ab–Ú1š£ŽM”®—…•©–|ŽM‹§•ßƒˆ=ƒRApr.28ab–ÚŽMŽM‹§•ß•ß•ß–|ŽMŒ—•ß•ßƒˆƒRJunelab–ÚŽMi•ß•ßƒˆŽM‹§•ßƒˆŽMŽM•ß1•k=St.ABO1050100150a=š™Sa’_ss"mye‡SeƒÅseš —Õ”•b’¤•Žš£ƒÏ•V•EƒÏ‰Ás•EƒÈamu˜ú•E•¡•E–ã•Et•Esec•B•Ealline•Eed•Elgae• •E•Ed•Emi•Eant•Elgaeb=Ž©•E•Bbb‡sˆÍ•E•B•EkŽM•ckwi‡qsca‡q•Eed•E•BbblesŒûsandwi‡qsca•›•Eed•E•Ebbles

Fig.3.Seasonal changes in the distribution of shell diameter of Fig.2.Dominant algal species(a)and status of seabed(b)at Chlorostoma lischkei by station.Italic numerals denote sample each station along the transect in Fig.1. sizes.

4 Distribution of trochid gastropods

Numbers of individuals

Fig.4.Seasonal changes in the distribution of shell diameter of Omphalius pfeifferi pfeifferi by station.Italic numerals denote sam ple sizes.

cobble area about1m deep,crustose coralline red algae The seabed along the transect consisted of an intricate and smaller thalloid algae such as Gelidium vagum and mixture of rocky-bottom and cobble areas,where S.

G.amansii were attached to the surfaces of cobbles.At yezoense dominated in shallower zones1to2m deep, St.B,in a rocky bottom area about1m deep, the bottom Eisenia bicyclis in areas1.5to5m deep,and crustose surface was thickly covered with Sargassum yezoense. coralline red algae in areas deeper than5m in all

0202020202020202020202020202002019971075502689743244422727007Aug.28207223010038772896244276750000Nov•E7“†•E’U20‚¨‚À3080•¸••Dec.22”Ë10957607879322326077`‚Ì203047751998107237272753700007Jan.2220307343338St.ABO10203040506070809010011014002020202020202020202020202020199810830442369333475700Mar.1820•s3036•¸ƒÃ‚Æ3107747i787754744750400Apr.28‚À•¸.920”ûŠÅ308232022‚¨10582i7707766422000007June120305St.ABO102030405060708090100110 Ishida et al.

seasons.Sargassum yezoense was the second most domi snails smaller than this did not occur except for four col nant alga in the Eisenia zone.In January of1998,S. lected at St.A in June of1998. yezoense extended to a depth of about3m, and the Omphalius pfeifferi pfeifferi was distributed densely shoreward margin of the Eisenia zone correspondingly in the Eisenia zone at depths of2to5m(Sts.20-80) retracted somewhat offshore.During and after November (Fig.4).Its population density decreased in the marginal of1997,Dilophus okamurae formed a narrow zone at the parts of the Eisenia zone,where the proportion of other boundary between the zones of Eisenia and crustose algae increased.In contrast to C.lischkei,the density coralline red algae,or inside the latter zone,at a depth of was lower at Sts.A and B than at the stations in the about5m.The seabed seaward of St.150was composed Eisenia zone.The Eisenia zone contained snails of vari of intermingled sand and cobbles, where few epiphytic ous sizes,but snails larger than about25mm ShD were algae grew. scarce at Sts.A and B and only a few small snails were found at the stations seaward of St.70or80in the Dilophus zone and in the crustose coralline red algal area Shell diameter distributions by habitat at depths greater than6m(Sts.90-140).Thus,al Figure3shows the seasonal changes in the distribution though smaller individuals of O.p.pfeifferi were widely of shell diameter(ShD)of C.lischkei along the transect. distributed,larger ones tended to be concentrated in the Snails were dense at St.A.Although some were also col Eisenia zone. lected at St.B and Sts.0to50,the population densities there were considerably lower than that at St.A,and no snails were found at stations seaward of St.50.The den Size distribution according to microhabitat sity at St.A was high in August and November of1997 Figure5shows the ShD distributions of C.lischkei by and fell during and after December of that year. Snails microhabitat at Sts.1to6.In September of 1998,snails larger than10mm ShD dominated at all stations, and were collected at Sts.1to3.At St.1,a single small snail of less than5mm ShD was obtained from beneath a cob ble.At St.2,larger snails of about20mm ShD were found on the bottom under cobbles,and one smaller one on a lamina of S.yezoense.One small snail was collected from a cobble at St.3.In November,large snails were caught at Sts.1and2,all from beneath cobbles,and snails of less than15mm ShD were not found at all.In December,snails were found only at Sts.1and2:many larger snails of greater than15mm ShD and a few smaller ones below10mm ShD at St.1,and only larger snails at St.2,all beneath cobbles.In both cobble areas and Sargassum patches, most snails inhabited the bottom beneath cobbles;few lived on the surfaces of cobbles or on algal laminae.No snails were collected at Sts.4,5, and6.Small snails were very uncommon throughout the investigations. Figure6compares the ShD distribution of O.p. pfeifferi among microhabitats at Sts.1to6.In September of1998,snails occurred at all stations except St.3.Al- though one snail was obtained from the surface of a cobble at St.1,and one from a lamina of S.yezoense at St. 2,all other snails were found beneath cobbles,and small snails of less than5mm ShD dominated.In November, almost all snails were caught beneath cobbles and were smaller than10mm in ShD;two snails found on laminae Fig.5.Shell diameter distributions of Chlorostoma lischkei by of E.bicyclis at Sts.3and5were larger than10mm in microhabitat at Sts.1to6.Open circles denote individuals ob ShD.In December,various sized snails from below10 tained from the bottom surface beneath cobbles,triangles from algal laminae,and squares from the cobbles themselves. mm to over20mm ShD were found beneath cobbles at

05101520251998St.1;ep.2923456St.1-ˆêˆêˆêˆêˆêˆêˆêˆê{ˆêˆêˆêˆê10V.1123456St•E1-ˆêˆêˆêˆê)ec.112-ˆêˆêˆêˆêˆêˆêˆêˆêˆêˆêˆêˆêˆê345 Distribution of trochid gastropodsShelldiameter(mm)0510152025301998St.1Sep.292-ˆê•uˆê‚çˆêˆêˆêˆêˆêˆêˆêˆêˆêˆêˆêˆêˆê34-oo-G-ˆêˆêˆêˆêˆêˆêˆêˆêˆêˆêˆêˆêˆê5ˆê“Ô•@ˆêˆêˆêˆêˆêˆêˆêˆêˆêˆêˆêˆêˆêˆêˆêˆêˆêˆêˆê6St.1-ˆêˆêˆêˆêˆêNov.1123’Ïˆêˆêˆêˆêˆêˆêˆêˆêˆêˆê4•vˆêˆêˆêˆê5-ˆêˆêˆê6St.1Dec.1123-O-ˆêˆêˆêˆêˆêˆêˆêˆêˆêˆêˆê4•vˆêƒg5•vˆêˆê6

Fig.7.Shell diameter distributions of Omphalius pfeifferi

pfeifferi by microhabitat on and around the algal body of Eisenia bicyclis.Circles denote individual snails.Shelldiameter(mm•t051015202530C‚í'omsfOma"sc‚îƒÈe'St•E1{9-ˆêˆêˆêˆêˆê340mƒÏha'ŒŒJSƒÏfe'ŒÞefƒSƒÏ•le'•v‹íefƒSSt.134-ˆêˆê

Fig.6.Shell diameter distributions of Omphalius pfeifferi pfeifferi by microhabitat at Sts.1to 6.Open circles denote indi viduals obtained from the bottom surface beneath cobbles,tri angles from algal laminae,and squares from the cobbles them selves.

St.2,and a smaller one at St.6.At Sts.3,4,and5in the Eisenia zone,snails were found both beneath cobbles Fig.8.Shell diameter distributions of Chlorostoma lischkei and on algal laminae,mainly smaller snails in the former and Omphalius pfeifferi pfeifferi by microhabitat around cob bles at Sts.1,3,and4.Triangles denote snails obtained from case,larger snails in the latter. Although smaller individuals of O.p.pfeifferi were the topsides of cobbles,squares from the undersides of cobbles, and circles from the bottom surface beneath cobbles. found beneath cobbles at nearly all stations, they were more abundant at stations in the Eisenia zone than at other stations.Larger snails,which were caught in De cember,1998,were abundant on algal laminae at Sts.3 St.3,where the density of the algae was low,smaller to5,especially at St.4in the central part of the Eisenia snails of below3mm ShD and larger ones of over 25 zone. mm ShD occurred on the surfaces of cobbles and on the Figure7shows the ShD distributions of O.p. bottom beneath them,but no snails of medium size oc pfeifferi by microhabitat on and around the thallus of E. curred;the results at St.4were similar. bicyclis.At St.4,where E.bicyclis grew densely,the Figure8shows the ShD distributions of the species algal laminae were occupied mainly by larger snails of by microhabitat around cobbles.Chlorostoma lischkei over20mm ShD.Snails of various sizes from smaller was distributed mainly at St.1in the cobble area.Small than5mm ShD to larger sizes occurred around the individuals of less than8mm ShD inhabited the under holdfasts.While some snails of below5mm and over20 sides of cobbles and the bottom beneath cobbles,and mm ShD were found on the surfaces of and under cob larger snails occupied the uppersides of cobbles,but bles,most snails of medium size from10to20mm in snails of10to20mm ShD were not found.Smaller ShD were found around the holdfasts of E.bicyclis.AtShe61diameter(mm•t051015202530St.30nalgallaminaeAroundalgalholdfastsO•Eandb•E•Eeath•E•Ebbles•¨•‘ƒg•[ˆêˆêˆêˆêˆêˆêˆêˆêˆêˆêˆê(d‚àO--St.40•Eal9•Ell•Emi•Eae-ˆêˆêˆêˆê‚Âˆêˆêˆêˆê•Z-Aroundalgalholdfasts-ˆêˆê•s)ˆê}ˆêˆêˆêˆê()ˆêˆêˆê•B•Eandb•E•Eeath•E•Bbblesˆêsnails of O.p.pfeifferi at St.4were concentrated on the

7 Ishida et al.

bottom beneath cobbles,and few were found on either contents of snails obtained around algal holdfasts and on the tops or undersides of cobbles.At St.3, where E. the bottom beneath cobbles,the proportion of Type1 bicyclis grew sparsely,large snails of greater than25mm was lower,and those of Types2and3higher.The pro

ShD inhabited the tops of cobbles.In sum,larger snails portion of crustose coralline red algae was very low. of both species inhabited mainly the tops of cobbles,me dium-sized snails of10to20mm ShD of both species did not occur at all,small C.lischkei inhabited the under DISCUSSION sides of cobbles and the bottom beneath cobbles,and small O.p.pfeifferi also mainly lived beneath cobbles. The gastropod Chlorostoma lischkei inhabits mainly shallow cobble areas where few large perennial algae

Feeding habits grow,showing little or no change in its range throughout the year.Smaller snails are distributed on the undersides Figure9shows the stomach content compositions of the of cobbles and on the bottom beneath cobbles,and they

gastropods inhabiting different microhabitats.If the cate move to open areas such as the tops of cobbles when

gories of•gunidentified digested algal fragments•h, they grow to over20mm ShD.In the muricid gastropod other•h,and•gsand grains•hare excluded,algae •g of Types Nucella emarginata,juvenile snails live in three 2and3comprised about80%of the stomach contents of dimensionally complex structures such as filamentous C.lischkei obtained from the surfaces of cobbles;Type algae and beds of the mussel Mytilus californianus, 3in particular constituted a high proportion.In•@ contrast, while larger snails invulnerable to predation by hermit the proportion of algae of Type2in the stomach contents crabs inhabit open surfaces(Gosselin1997).Although of C.lischkei living on rock surfaces in the Sargassum its predators are unknown,we infer that C.lischkei also

patch was higher,while that of Type3algae was lower. moves to exposed areas such as the tops of cobbles when In both habitats, the proportions of Type1algae and vulnerability to predation becomes reduced due to crustose coralline red algae were distinctly low. growth.The feeding habits of C.lischkei change along More than70%of the stomach contents of O.p. with the shift in microhabitat.Smaller snails living on pfeifferi living on laminae of Eisenia bicyclis were algae cobbles feed on both small algae and Sargassum, of Types1and3,especially the former. In the stomach whereas larger snails inhabiting open rock surfaces eat more Sargassum.The turbinid gastropod Lunella coronata coreensis was reported to shift from eating at tached diatoms to macroalgae as it grows;smaller adult snails of less than20mm ShD inhabit the upper intertidal zone,grazing on diatoms,while larger snails of more than20mm ShD feed chiefly on macroalgae in habiting the middle and lower intertidal zones(Yukihira- et al.1995).This demonstrates that the change in feed ing habit with growth is closely related to the shift in microhabitat,and a similar relationship may be inferred for C.lischkei. All sizes of Omphalius pfeifferi pfeifferi chiefly in habited the kelp forest of Eisenia bicyclis all year round, with a higher density in the more central part of the kelp forest than in the periphery,which suggests that the mode of life of the snail is specifically connected with kelp forests.On the other hand,the snail changed its microhabitat in the kelp forest depending on stage of growth;smaller snails,including juveniles,lived on the bottom under cobbles,medium-sized snails of10-20 mm ShD gathered around the holdfasts of the kelp, and Fig.9.Stomach content compositions of Chlorostoma lischkei larger snails of greater than20mm ShD lived mainly on and Omphalius pfeifferi pfeifferi by microhabitat.N denotes the algal laminae.Some larger snails that were found on sample size. the tops of cobbles and on rock surfaces may have been

C‚î'o'osfoma•Vscˆè•ye'OncobblesN=50nr‡tkSlinŽReSa‹rmp‘Œ1020406080100%OmƒÏha•V"sƒÏfO'f–Æ11•uƒÏ7b“se7‚¸‹È•»1—ji“å”®“å“åAroundho—Êdfas‹TsofƒÃ'seƒÅ'ab'{yc•VSN=4•Enandbeneathc•E’û•“020406080100%š£TyI˜NZIType2ˆÍType3š£c•Eu•Jš•c•E‘Ÿlline•EedalgaeŒûuniden‰¿‰¿eddige•Ýedalgal’¡agmen‡s•¡•Ether–Ú“cndgŠ×ins Distribution of trochid gastropods

shaken off the laminae by physical factors such as Acknowledgments.This work was supported in part by waves.This species of snail also had different feeding a Grant-in-Aid for Scientific Research from the Ministry habits depending on microhabitat,which shows that of Education,Science,Sports and Culture of Japan.The changes in microhabitat and feeding habit are authors are greatly indebted to Dr.Kazunori Hasegawa interlinked. of The National Science Museum for his help and valu Tegula funebralis,a relative of O.p.pfeifferi,in able advice in identifying juvenile gastropods. habits the upper intertidal zone,where few predators exist,up to the age of sexual maturation at6years,and then shifts toward the lower zones(Paine1969).Articu REFERENCES lated coralline algae,which grew densely to form a tight mat,provide juveniles of Batillus cornutus not only with Gosselin,L.A.1997.An ecological transition during juvenile essential feeding grounds of abundant attached diatoms, life in a marine snail.Marine Ecology Progress Series,157: but also effective hiding places that allow juveniles to 185-194. obtain higher survival rates by avoiding predation by car Horikawa,H.and H.Yamakawa1982.Ecological study of nivorous animals such as starfish(Yamazaki&Ishiwata Omphalius pfeifferi Phillipi(Gastropoda:Prosobranchia) 1987).The undersides of cobbles and the bottom be Bulletin of the Nansei. Regional Fisheries Research Labora neath cobbles seem to provide safety to smaller C. tory,14:71-81(in Japanese with English summary). lischkei and O.p.pfeifferi and decrease the predation Okutani,T.(ed.)2000.Marine Mollusks in Japan.Tokai Uni pressure on them.Larger O.p.pfeifferi utilize E.bicyclis versity Press,Tokyo,1173pp.(in Japanese). directly as their main living space while at the same time Omori,M.,K.Taniguchi,K.Shiraishi and T.Seki2000.Distri feeding on it.By contrast,although C.lischkei inhabits bution of benthic invertebrates in relation to zonal structure the surfaces of cobbles and rocks while feeding on S. of algal communities in a rocky sublittoral area,Tomari yezoense and smaller thalloid algae such as Gelidium hama,Oshika Peninsula, northern Japan.Benthos Research, amansii and Chondrus ocellatus,it does not live on the 55:69-83. algae,especially the larger seaweed.This is a fundamen Paine,R.T.1969.The Pisaster-Tegula interaction:prey tal differences between C.lischkei and O.p. pfeifferi in patches,predator food preference and intertidal community their relationships with algae and algal vegetation. structure.Ecology,50:950-961. The two species of gastropods differ in their large Sano,M.,M.Omori,K.Taniguchi,T.Seki and R.Sasaki1998. scale patterns of distribution with respect to algal Distribution of the sea urchin Strongylocentrotus nudus in zonation.Settlement and metamorphosis of some marine relation to marine algal zonation in the rocky coastal area of invertebrates are known to be induced by chemical sub the Oshika Peninsula,northern Japan.Benthos Research,53: stances emitted from or contained in coralline algae. 79-87. Sano et al.(1998)reported that larvae of the sea urchin Sasaki,R.1994.Some attempts to investigate larval recruit Strongylocentrotus nudus settle in the crustose coralline ment processes of Ezo abalone,Haliotis discus hannai,in red algal zone and stay there during the first year,then the adjacent water of Kesennuma Bay,Japan.Bulletin of gradually move toward the kelp forest.Taniguchi et al. Kesennuma Miyagi Prefectural Fisheries Experimental Sta (1994)showed that dibromomethane,a secondary me tion,9:1-17(in Japanese with English summary). tabolite of coralline algae,induces sea urchin larvae to Seki,T.1997.Biological studies on the seed production of the settle in the coralline algal zone and metamorphose.Seki northern Japanese abalone,Haliotis discus hannai Ino.Bul (1997)found the substance to have the same action on letin of Tohoku National Fisheries Research Institute,59:1 the abalone Haliotis discus hannai.However,the differ 71(in Japanese with English summary). - ent modes of life of C.lischkei and O.p.pfeifferi cannot Taniguchi,K.1991.Marine afforestation of Eisenia bicyclis be explained by this mechanism.To clarify the full rela (Laminariaceae:Phaeophyta).NOAA Technical Report tionship between their life histories and the algal com NMFS,102:47-57. munities,attention must be directed to their early stages, Taniguchi,K.and H.Kito1988.Age composition in the popu from larvae to immediately settled juveniles,in relation lation of Eisenia bicyclis(Laminariaceae:Phaeophyta). to the algae,including larval distribution in and around Nippon Suisan Gakkaishi,54:1583-1588(in Japanese with the kelp forest and differences in survivorship of juve English summary). niles settling in the kelp forest and the coralline algal Taniguchi,K.,K.Kurata,T.Maruzoi and M.Suzuki1994. zone. Dibromomethane,a chemical inducer of larval settlement and metamorphosis of the sea urchin Strongylocentrotus

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