Benthos Research Vol.54,No.2:71-80(1999) BENTHOS RESEARCH

The Japanese Association of Benthology

Activity Patterns and Habitat Preferences of Two Herbivorous Gastropods

(Gibbula umbilicaris and Jujubinus exasperatus)on Leaves of the

editerranean Seagrass Posidonia oceanica M

Yoshitake Takada1),Giovanni F.Russo2)and Lucia Mazzella1)•õ

Laboratory of Benthic Ecology,Stazione Zoologica•eAnton 1)Dohrn•fdi Napoli,

Punta S.Pietro,I-80077Ischia(Napoli),Italy 2)Department of Animal Biology ,University of Catania,Sicily,Italy

Abstract:Laboratory experiments were carried out to observe the day/night activity patterns and habitat preferences of two gastropods,Gibbula umbilicaris and Jujubinus exasperatus,on leaves of the seagrass Posidonia oceanica.Both G.umbilicaris and J.exasperatus preferred old(apical)parts of leaves to young (basal)ones,and vertically oriented leaves rather than horizontal ones.Four types of behavior(rest, shaking epipedalic tentacles without any other motion,directional movements ,and shell twisting mainly for foraging)were observed.Also,interspecific differences in the day/night activity pattern were recog nized;G.umbilicaris mainly rested during the day and actively moved and foraged at night ,whereas J. exasperatus continued to move about and forage during both day and night,resulting in a less marked day/night pattern.These results partly explain the observations of previous studies ,in which both species were more abundantly sampled on seagrass leaves at night than by day.

Key words:day/night activity,epiphytic snail,habitat preference,Posidonia seagrass

(Russo et al.1984b;Russo et al.1991).Most of these INTRODUCTION snails,including Gibbula(Tumulus)umbilicaris (Linne1758)and Jujubinus exasperatus(Pennant, Epiphytic snails on seagrass leaves are one of the most 1777),showed variation in abundance on leaves between important components of the structural(Mazzella et day and night observations(Russo et al.1984a).Both al.1989;Edgar1990;Gambi et al.1992)and functional G.umbilicaris and J.exasperatus belong to the family (van Montfrans et al.1982;Orth&van Montfrans Trochidae and are the dominant herbivores on the epi 1984;Klumpp et al.1992;Mazzella et al.1992; phytic algae that grow on P.oceanica.Their abundance Jernakoff et al.1996)organization of the seagrass eco on leaves is higher at night than by day(Russo et al. system.In seagrass beds of Posidonia oceanica(L.) 1984a).Russo et al.(1984a)suggested that this day/ Delile,several studies have been carried out on the spe night variation in abundance was due to the vertical cies composition and distribution of epiphytic snails migration of the snails along the seagrass leaves,but there has been little direct observation on the behavior

Received August16,1999:Accepted November12,1999 of these snails(Mazzella&Russo1989).In this study,

*Corresponding author .Present address:Ishigaki we hypothesize that the vertical migration of the snails Tropical Station,Seikai National Fisheries Research is related to their day/night feeding on the epiphytic Institute,Fukai-Ota148-446,Ishigaki907-0451,Japan. algae. Epiphytic snails graze mainly on epiphytic algae •õDeceased June 1999

71 Takada et al.

both the leaf age and the shoot structure.Older,apical parts of leaves carry a diverse and well-grown cover of algae,while younger,basal parts have only a primary cover.This spatial variation in algal cover may induce spatial variation in the feeding activity of herbivorous snails,because the snails may encounter different types of food while grazing.Spatial variation in abundance of some species of snails,including Gibbula umbilicaris and Jujubinus exasperatus,indicates their preference for certain types of epiphytic algae(Spada1971; Kitting 1985;Peduzzi1987;Mazzella&Russo1989). However,it is necessary to ascertain the snails'prefer ence by a selection experiment between leaf fragments with different kinds of epiphytic algae.Otherwise,al Fig.1.Experimental aquarium(12cm diameter and6cm depth).Each aquarium contained one snail(Gibbula ternative explanations for this phenomenon,such as umbilicaris or Jujubinus exasperatus).Filtered seawater geotaxis and/or phototaxis,may be confounded with was flowing into the bottom of the aquarium from a preference for any particular type of epiphytic algae.In siphonal tube fixed by a clothes peg.Four fragments of addition,G.umbilicaris and J.exasperatus are rarely Posidonia oceanica leaves were placed vertically in the found on dead leaves that accumulate horizontally on center of the aquarium in the first experiment. the sea bottom(Russo unpubi.).It should be tested whether this is due to the snails'lower preference for epiphytic algae on dead leaves,for horizontally posi (=periphyton,i.e.microalgae and macroalgae growing tioned leaves,or both. on leaves of seagrasses(van Montfrans et al.1982; The present study included laboratory experiments Peduzzi1987;Mazzella&Russo1989;Klumpp et al. to evaluate the effect of epiphytic algae and the spatial 1992;Mazzella et al.1992)).Seagrass shoots carry sev arrangement(vertical or horizontal)of Posidonia eral kinds of epiphytic algal communities(Jacobs et al. oceanica leaves on the day/night feeding activity of 1983;Mazzella&Russo1989;Mazzella&Spinoccia Gibbula umbilicaris and Jujubinus exasperatus.The re 1992;Mazzella et al.1995),primarily depending on sults are discussed in relation to the vertical variation of algal cover and the day/night migration patterns of the snails.

Table1.Source and epiphyte cover of the five types of leaf fragments.Four types(A,B,C,and D)of leaf fragments were used in the first experiment,three types(C,D,and MATERIALS AND METHODS E)in the second experiment. Snails(Gibbula umbilicaris and Jujubinus exasperatus)

LeaffragmentSourceEpiphytes and seagrass(Posidonia oceanica)were collected in No

ABasalpartoftheNomacroscopic vember1995from two localities,Lacco Ameno and youngestleafalgae Castello(Island of Ischia,Gulf of Naples;Colantoni et BIntermediatepartNomacroscopic al.1982),from a depth of3m.Seagrass shoots were ofthesecondandalgae kept in an aquarium with flowing seawater after re thirdyoungest leaves moving all the mobile animals from the leaves.One

CApicalpartofthePrimarycover snail was placed in each small(12cm diameter and6cm secondandthirdofmacroscopic depth)aquarium with flowing seawater(Fig.1).After youngestleavesencrustingalgae 2-5days of acclimation,snails did not escape from

DApicalpartofDiverseand their aquariums and their behavior was observed.The olderleaveswellgrowncover ofmacroscopic quariums were maintained under natural a thermal con enCrUStingalgae ditions(13.0-17.6•Ž). EDeadleafDiverseand According to the development of the epiphytic wellgrowncover algae on Posidonia leaves(Mazzella&Russo1989; ofmacroscopic enCrUStingalgae Mazzella et al.1989;Mazzella&Spinoccia1992;

72 Activity patterns of epiphytic gastropods

Mazzella et al.1995),five types of leaf fragments The natural light from the window of the laboratory (6cm long)were used in the experiments(Table1).De was not altered.During the night observations,a flash

velopment of the algal cover on the leaf fragments was light was used.In preliminary observations,it was

categorized,in increasing order,as‘A'<‘B'<‘C'<‘D' found that a dimmed flashlightcould be used for sev =‘E' .Macroscopic algae on the leaf fragments of types eral seconds to observe the behavior of the snails with ' ‘C ,‘D',and‘E'were mainly composed of encrusting out disturbing them.All the leaf fragments were re coralline algae.Width of the leaves(9.9mm±0.5SD, placed daily with new leaves in the morning(9:30- =96)was homogeneous among n the five types . 11:00h),without touching any snails.Ifa snailwas at We recorded four phases of behavior of the two tached to a leaf fragment,we waited until it moved off snail species:‘rest'involved resting in a place without the fragment before we replaced the fragment.

any motion;‘tentacle shake'involved shaking the

epipedalic tentacles slowly without any other motion; Second experiment move'involved moving straight(1.6-5.5cm/min) ‘

from one place to another without twisting the shell; In the second experiment,one group of leaf fragments

twist'involved twisting the shell and shifting the‘ ce was placed vertically as in the first experiment and an

phalic part around while moving slowly(0.1-0.9cm other group was placed horizontally on the bottom of

/min).Thus,two‘inactive'phases(‘rest'and‘tentacle the aquarium.The natural curve of the leaf fragments

shake')and two‘active'phases(‘move'and‘twist') allowed snails to use both sides of the fragments.In

were recognized.These behaviors were common to the this experiment,three types of leaves(‘C',‘D',and‘E')

two species and were clearly distinguishable.Snails fed were used for each group;thus,six leaves were offered

rarely during the‘move'phase,and most often during in each aquarium.Leaf fragments were replaced with

the‘twist'phase. new ones every day,as in the first experiment.Observa

Two experiments were carried out.Interspecific tions on the position and the behavior of the snails were

differences in the activity pattern and preference carried out as described above daily at12:00h,18:00h,

among the leaf fragments(epiphytic algae)were ob and0:00h.In total,23snails(9specimens of G. served in both of the experiments.In addition,the day ,mean shell width=8.38mm,range=6.30 umbilicaris

/night activity of snails and their preferences among -13 .00mm;14specimens of J.exasperatus,mean shell living leaf fragments was observed in the first experi height=9.21mm,range=8.20-9.85mm)were ob ment,and the snails'preferencein spatialarrangement served in the second experiment. (verticalvs.horizontal)of leaves,including dead leaf fragments,was examined in the second experiment. Statistical analyses

Repeated-measure ANOVAs and Scheffe's multiple con First experiment trasts were carried out on the proportions of certain

In the first experiment,four fragments of living leaves behaviors or occurrence on certain leaf types by the

(one from each type,‘A',‘B',‘C',and‘D')were placed snails.Each individual was regarded as a block factor, vertically in the center of each aquarium(Fig.1). and the two species(G.umbilicaris and J.exasperatus)

Snails(11specimens of G.umbilicaris,mean shell were regarded as a between-block factor.Data were width=11.75mm,range=8.65-13.40mm;9speci arcsin(square root)-transformed before the analysis. mens of J.exasperatus,mean shell height=9.52mm, When we analyzed the behavior of snails observed only range=8.60-10.90mm)were placed individually in the on the leaves,we pooled the data for the days and/or aquariums.Observations were carried out7times a day the hours to increase the number of records.Snails that at3hrs interval over four days.Observations at9:00h, did not occur on the leaves were excluded from the

12:00h,and15:00h were in the daytime,and those at analyses.Preferences in the type(‘A'and‘B'vs.‘C'and

18:00h,21:00h,0:00h,and6:00h were at night.Dur D')and spatial arrangement(vertical‘ vs.horizontal) ing each observation,the position of each snail(i.e.on of leaf fragments were examined by two-tailed t-tests which type of leaf fragments it was found)and its be against null hypotheses of equal preference. havior were recorded6times,with5minutes between each record.The number of a certain position(or be havior)divided by6records was used as the proportion of this position(or behavior)during an observation.

73 Takada et al.

Gibbula sumbilicari showed a clear behavioral pat

tern over the course of a day(Fig.2a).It tended to be

inactive'during the day and‘active'at nlght‘ RESULTS First experiment (Scheffe's multiple contrasts,df=1,F=34.16,P

In the first experiment,the repeated-measure ANOVA 0.0001).The proportion < of different behaviors changed

(Table2)exhibited statistically significant(P<0.05) during the day,with maximum‘rest'in the morning

differences in the proportion of‘active'(‘move'and (9:00h)and maximum‘move'in the evening(21:00h).

twist')behavior in relation to‘ three sources of vari By only considering the behavior of snails observed on

ance:species,hours of observation,and the interaction the leaves(Fig.2b),and excluding observations of

between these two factors. snails on the glass(bottom and wall)of the aquarium,

the percentage of‘twist'increased and the percentage

of‘move'decreased.In fact,most‘twist'behavior was Table2.Repeated-measure ANOVA of the proportion of observed on the seagrass leaves(97.1%;total number active'phases(‘twist'and‘move')of the snails in the‘ of observed‘twist'=209),and most‘move'behavior first experiment.Two‘within'factors are the hour and was observed on the glass of the aquarium(86.8%,n= the day of the observations.One‘between'factor is the 450).The proportion of‘twist'on the leaves increased species(Gibbula umbilicaris number of individuals=11, to a maximum at18:00h,then gradually decreased and Jujubinus exasperatus number of individuals=9). (Fig.2). The data were arcsin(square root)-transformed before Although Jujubinus exasperatus showed a less the analysis. marked behavioral pattern over the course of a day

SourcedfMSFP (Fig.3)than G.umbilicaris,overall it had a similar be

Species(S)121.37414.0840.002 havioral pattern,with the maximum proportion of

1ndividuals(Group)(1)181.518 rest'in the morning(9:00h)and the maximum pro‘ Day(D)30.1510.7670.517 portion of‘move'in the evening(18:00h).On the D×S30.5432.7500.052 leaves alone(Fig.3b),‘twist'behavior was more fre D×1540.197 quent and‘move'behavior less frequent compared with Hour64.22511.2230.0001 the combined observations on both the leaves and the H×S61.1342.9920.010 glass(Fig.3a),as was also noted above for G. H×11080.379 Overall,J.exasperatus were more activeumbilicaris. D×H180.1951.1710.284 than G.umbilicaris. D×H×S180.1941.1690.285 Apparently,the percentage occurrences of snails on D×H×13240.166

(a)(b) n=264n=1161551281421227973 100100

(

.§ 〉 」= Φ OD

6912151821069121518210 TimeofdayTimeofday

[コtwist物m・vei:i:i=tentacleshake■rest

Fig.2.Pattern of behavior(pooled over4days)of Gibbula umbilicaris(11specimens)in the firstexperiment.(a)Total records,including snails observed on both the Posidonia oceanica leaf fragments and the glass of the aquarium.(b) Records only concerning snails onthe Posidonia leaf fragments;n=number of records.

74 Activity patterns of epiphytic gastropods

(a) (b) n=216100 n=5672 101 107 76 61 89 100

( 80 80

」60 60 ・睾

歪40 40 畠 20 20

0 」0 6 9121518210 69121518 21 0 Timeofday Timeofday

[]twist㎜m・ve tentacleshake■rest

Fig.3.Pattern of behavior(pooled over4days)of Jujubinus exasperatus(9specimens)in the first experiment.(a)Total records,including snails observed on both the Posidonia oceanica leaf fragments and the glass of the aquarium.(b) Records only concerning snails on the Posidonia leaf fragments;n=number of records.

Table3.Repeated-measure ANOVA of the proportion of Table4.Repeated-measure ANOVA of the proportion of snails on leaf type•eD•famong the four types of leaf frag snails on leaf fragments observed in(a) the•emove•fphase ments in the first experiment.One•ewithin•ffactor is the and(b)the•etwist•fphase in the first experiment.One hour of the observations and one•ebetween•ffactor is the within•ffactor is the leaf type and one•ebetween•ffactor•e is species(Gibbula umbilicaris number of individuals=7, the species(Gibbula umbilicaris number of individuals= and Jujubinus exasperatus number of individuals=7). 7,and Jujubinus exasperatus number of individuals=9).

The data were pooled for the four days and were arcsin The data were pooled for the four days and the seven

(square root)-transformed before the analysis. hours and were arcsin(square root)-transformed before

the analysis. Source df MS F P Species(S) 1 0.660 1.2870.279 Source df MS F P

Individuals(Group)(1) 12 0.513 (a)`move'

Hour(H) 6 0.148 0.5510.768 Species(S) 1 0.169 0.652 0.433

H×S 6 0.288 1.0680.390 Individuals(Group)(1) 14 0.259

H×1 72 0.269 Leaf(L) 3 0.389 3.578 0.022

L×S 3 0.160 1.473 0.236 L×1 42 0.109

(b)`twist'

Species(S) 1 1.970 20.029 0.0005 the four types of leaf fragment varied between species Individuals(Group)(1) 14 0.098 and among the times of observation(Fig.4),but occur Leaf(L) 3 0.446 5.478 0.003 rence on leaf type•eD•fdid not significantly differ be L×S 3 0.037 0.433 0.731 tween the species,the hours of observation,or the in L×1 42 0.085 teraction of these two factors(Table3).Considering the data averaged for a whole day,the percentage oc currences on leaf fragment types•eD•fand•eC•fwere46.3% and33.0%,respectively,in G.umbilicaris,and47.7% varied depending on the type of fragment(Table4,Fig. and26.7%,respectively,in J.exasperatus.Both species 5).The proportion of•emove•fbehavior was greater on preferred older leaf fragments(•eC•fand•eD•f)to younger the younger leaf fragments than on the older ones ones(•eA•fand•eB•f)(t-tests,P<0.01for both species). (Scheffe•fs multiple contrasts,df=1,F=9.419,P=

The behavior of the two species on leaf fragment 0.0038),but the proportion of•etwist•fbehavior was

75 Takada et al.

(a》 αbbσ1au・mb〃car15 (b)」 乙〃硬ノわ1ησsθxa5ρera如s n・=116155128142 122 79 73 n=5672101107 76 61 89 100 100 ( ) 80 80 の ⊆ Φ 60 E 60 o 仁 40 40

2 20 20

0 0 6 9 121518 21 0 6 9 121518 21 0 Timeofday Timeofday [コA 吻B C ■D

Fig.4.Patterns of occurrence(pooled over4days)of two species of snails on different types of leaf fragment in the first

experiment:•eA•f,basal part of the youngest leaf;•eB•f,intermediate part of the second and third youngest leaves;•eC•f,apical

part of the second and third youngest leaves;•eD•f,apical part of older leaves.(a)Gibbula umbilicaris.(b)Jujubinus

exasperatus.n=number of records,including only snails on leaf fragments.

(a)αbbσ1aαmb1〃oarls (b)」 乙〃更の1ηαsexasρera如5 n=59110269 327 n=6975150 268 100 100 「

( 80 80

と .Ω 60 60 焉誌 40 40 m

20 20

0 0 ABCD ABCD

Typeofleaffragment Typeofleaffragment [==コtwist物move :tentacleshake■rest

Fig.5.Behavior on the four different types of leaf fragments(•eA

periment.(a)Gibbula umbilicaris.(b)Jujubinus exasperatus.n=number•f,•eB•f,•eC•f,and•eD•f,as of defined in Table1)in the firstrecords,including ex only snails on leaf frag

ments.larger on the older leaf fragments than on the younger Second experiment ones(Scheffe's multiple contrasts,df=1,F=15.626,

P=0.0003).Jujubinus exasperatus showed more•etwist•f In the second experiment,the behavioral patterns of the

behavior than G.umbilicaris(Table4b). snails were similar to those of the first experiment at

corresponding times;however,the proportion of

twist•fbehavior was generally higher,and that of•erest•f •e

76 Activity patterns of epiphytic gastropods

Table5.Behavior observed in the second experiment Table7.Repeated-measure ANOVA of the proportion of

(Gibbula umbilicaris number of individuals=9,and snails on leaves observed in(a)the•etwist•fphase and(b) jubinus exasperatus number of individuals=14,pooled the•etentacle shake•fphase in the second experiment.One over4days):(a)both on the Posidonia oceanica leaf frag within factor is the leaf type and one•ebetween•ffactor is ments and on the glass of the aquarium and(b)only on the species(Gibbula umbilicaris number of individuals= the Posidonia leaf fragments. 6,and Jujubinus exasperatus number of individuals=11).

The data were pooled for the four days and the three hours

α わδぬ μmわ`伽rεsJ吻'め 伽sθ καsρ2r伽s and were arcsin(square root)-transformed before the

12:0018:000:0012:0018:000:00 analysis.

(a)

Numberofrecords(tota1) SourcedfMSFP

216216216336336336 (a)`twist'

Behavior(%) Species(S)11.57615.6090.001 `rest'61 .117.623.647.97.423.5 1ndividuals(Group)(1)150.101 `tentacleshake'19 .426.430.19.510.79.8 1」eaf(L)20.3362.0590.145 `move'4 .634.325.011.629.527.7 LxS20.1560.9590.395 `twisゼ14 .821.821.331.◎52.439.0 L×1300.163

(b) (b)tentacleshake

Numberofrecords(onleaffragments) Species(S)11.54924.3960.0002

81101121142235198 1ndividuals(Group)(1)150.064

Behavior(%) Leaf(L)20.1231.2980.288 `resゼ29 .614.922.316.97.314.6 LxS20ユ291.3630.271 `tentacleshake'27 .223.828.96.39.48.6 L×1300.095 `move'3 .714.910.73.58.510.6 `twisポ39 .546.538.073.274.966.2

Table8.Behavior of Gibbula umbilicaris and Jujubinus exasperatus and occurrence on the differently arranged Table6.Occurrence of Gibbula umbilicaris and Jujubinus leaf fragments(vertical and horizontal)within each of exasperatus on the three types of Posidonia oceanica leaf three types of Posidonia oceanica leaf fragments(defined fragments(defined in Table1)and on differently ar in Table1)in the second experiment;n=total number of ranged leaves(vertical and horizontal)in the second ex records on the leaf fragments. periment;n=total number of records on the leaf frag ments. α δわぬ 配mbεZεCαrεsJm勉 わ伽Sθ καSρθrα加S

CDECDE α わわ蜘 μ励`砒 αrεsJm幅 わ伽sε κ卿 εrα伽 η492114352411112 12:0018:000:0012:0018:000:00 Behavi◎ で(%) η,81101121142235198 `rest'20 .426.12.30.013.413.4 Leaftype(%) `te ntacleshake'42.927.07.05.88.88.0 C23.59.916.50.713.210.1 `mo ve'8.26.232.626.93.416.1 D63。072.371.978.273,664.1 {twisゼ28 .640.858.167.374.562.5 E13.617.811.621.113.225.8

Position(%) Position(%) Vertica197.574.377.788.086.872.7 Vertica183.788.248.871.282.785.7 Horizo捻ta12。525.722.312.013.227.3 Horizonta116.311.851.228.817.314.3

lower,in the second experiment(Table5).Among the two species was similar.Jujubinus exasperatus showed three leaf-fragment types,most individuals of both more•etwist•fand less•etentacle shake•fbehavior than G. species occurred on•eD•f(Table6).Although J. umbilicaris(Tables7,8).Although statistical analysis exasperatus rarely occurred on leaf type•eC•fat 12:00h, did not show any significance(Table7),the behavior of in general,the proportion of leaf types exploited by the the two species appeared different on the different leaf

77 Takada et al.

Table9.Repeated-measure ANOVA of the proportion of the basal(younger)part of the leaves(Mazzella& snails on the vertically positioned leaf fragments against Spinoccia1992;Mazzella et al.1995).At least for win all records on leaf fragments.One•ewithin•ffactor is the tertime,the present results agree with the previous ob three differently epiphytized leaf fragments and one•ebe servation of Peduzzi(1987),that G.umbilicaris prefer tween•ffactor is the species(Gibbula umbilicaris number microalgae as food.In summertime,with the addition of individuals=6,and Jujubinus exasperatus number of in the periphyton of a well-developed layer of macro individuals=11).The data were pooled for the four days algae,both encrusting and erect,the food items of G. and three hours of observations,and were arcsin(square umbilicaris become more varied(Mazzella&Russo root)-transformed before the analysis. 1989).

Both G.umbilicaris and J.exasperatus preferred: SourcedfMSFP

Species(S)10.0510.1460.707 (ú@)living leaves to dead ones,and(úA)vertically posi

1ndividuals(Group)(1)150.346 tioned leaves to horizontal ones.The first point sug

Leaf(L)20。1881.2590.299 gests a feeding selection for fresh material,the second,

L×S20.7334.8930.015 a sort of geotaxis,which requires further investigation.

Lxl300.150 In any case,these results well explain the natural distri

bution of these species;that is,few grazing snails occur

on dead leaves that accumulate on the bottom of

seagrass beds(personal observation).

types(Table8):J.exasperatus behaved almost identi This study also demonstrated an interspecific dif

cally,mainly displaying•etwist•f,on all three types of ference in the activity pattern between G.umbilicaris

leaf fragment,but G.umbilicaris displayed•etentacle and J.exasperatus;the former species was predomi

shake•fmore frequently on•eC•f,and•emove•fmore fre nantly active during the night,while the latter showed

quently on•eE•f.Both species preferred the vertically po a less clear day/night pattern.Active phases were more

sitioned leaves to the horizontal ones(Table8)(t-tests, frequent in J.exasperatus than in G.umbilicaris.When

P<0.005for both species),but the occurrence of G. snails occurred on the less preferred leaf fragments,the

umbilicaris was not affected by the leaves•fspatial ar younger parts of the leaves,G.umbilicaris rested there

rangement when it was on a dead leaf(•eE•f).This while J.exasperatus moved,presumably searching for a

interspecific difference was reflected in the statistically better place to feed.

significant interaction between the types of leaf frag The higher proportion of•etwist•fbehavior of both

ment and the species(Table9). species in the second experiment than in the first may

have been due to some difference in the leaf fragments

or acclimation regimes adopted in the experiments.In

DISCUSSION any case,this small difference in results does not affect

any of the conclusions derived from this study.

Both Gibbula umbilicaris and Jujubinus exasperatus The observations that G.umbilicaris was active at

mostly occurred on the apical fragments of Posidonia night and foraged mainly on the apical fragments of

oceanica leaves,which are the oldest parts of living seagrass leaves partly explain the observation of Russo

leaves,and the parts covered with the largest amount et al.(1984a)that both G.umbilicaris and J.

of epiphytes.On the older leaf fragments,both species exasperatus are more abundantly sampled on seagrass

displayed•etwist•fbehavior,which represented the feed leaves at night than by day.The present study suggests,

ing behavior of the snails,more often than on the at least for G.umbilicaris,that the snails migrate up

younger leaf fragments.This suggests that they are ward and forage on the apical part of leaves because of

able to select an appropriate feeding substrate on which a nighttime preference for a diverse and well-grown

to forage.This preference is independent of any possible cover of epiphytic algae.By day,the snails rest,but the

tendency to climb towards the apical part of the leaf, present results do not explain why they migrate down

because all the experimental leaves were set at the same ward as suggested by Russo et al.(1984a).

height in the aquarium in order to remove any possible Nocturnal activity has also been demonstrated in

factor of height.Therefore,this preference must be re other species(Kitting1985;Klumpp et al.1992),so

lated to the distribution of epiphytic algae on the this behavior pattern seems to be frequent among epi

leaves.In winter,most epiphytic algae are microalgae, phytic grazing snails.Although Russo et al.(1984a)

which are more abundant on the apical(older)than on concluded that J.exasperatus predominantly occurs on

78 Activity patterns of epiphytic gastropods

leaves at night,the present results show that this spe duction and growth dynamics in Posidonia oceanica. cies tends to move and forage on the apical parts of Pubblicazioni della Stazione Zoologica di Napoli I:Ma leaves over the whole day.This inconsistency of results rine Ecology,13:2-16. may be due to qualitative and quantitative variation of Colantoni,P.,P.Gallignani,E.Fresi and F.Cinelli1982 epiphytes(food)with the seasons(Mazzella&Ott Patterns of Posidonia oceanica(L.)Delile beds around 1984;Buia et al.1991).The observations by Russo the island of Ischia(Gulf of Naples)and in adjacent wa (1984a)were made in summer,while the present study ters.Pubblicazioni della Stazione Zoologica di Napoli was done in winter. I:Marine Ecology,3:53-74. Gibbula umbilicaris and J.exasperatus in nature Edgar,G.J.1990The influence of plant structure on the both forage on Posidonia leaves.However,their feeding species richness,biomass and secondary production of ability is different.Peduzzi(1987)reported that G. macrofaunal assemblages associated with Western umbilicaris can graze on seagrass debris and macro Australian seagrass beds.Journal of Experimental Ma epiphytes,but has a higher absorption efficiency when rine Biology and Ecology,137:215-240. ingesting diatoms and films of reen algae.Mazzella& Gambi,M.C.,M.Lorenti,G.F.Russo,M.B.Scipione Russo(1989)also demonstrated the feeding ability of and V.Zupo1992Depth and seasonal distribution of G.umbilicaris on erect macroepiphytes.Arico(unpubl. some groups of the vagile fauna of the Posidonia doctoral thesis)reported that J.exasperatus feeds on oceanica leaf stratum:Structural and trophic analysis. diatoms and encrusting macroalgae.Little(1989)sug Pubblicazioni della Stazione Zoologica di Napoli I:Ma gested the importance of food supply on the activity rine Ecology,13:17-39. pattern of grazers and hypothesized that where compe Jacobs,R.P.W.M.,P.M.Hermelink and G.van Geel tition for food is low,nocturnal feeding should pre 1983Epiphytic algae on eelgrass at Roscoff,France. dominate;where competition is high,daytime or con Aquatic Botany,15:157-173. tinuous feeding should predominate.Future studies Jernakoff,P.,A.Brearley and J.Nielsen1996Factors af need to investigate the effects of food supply and com fecting grazer-epiphyte interactions in temperate sea petition on the day/night activity pattern of G. grass meadows.Oceanography and Marine Biology:an umbilicaris and J.exasperatus. Annual Review,34:109-162. In conclusion,this study demonstrated a day/night Kitting,C.L.1985Adaptive significance of short-range activity pattern and a preference among leaves in two diel migration differences in a seagrass-meadow snail species of epiphytic herbivores.These results generally population.Contributions in Marine Science,27:227- explained the spatial and temporal variations in the 243. snails'natural distribution patterns.However,this is Klumpp,D.W.,J.S.Salita-Espinosa and M.D.Fortes only a preliminary explanation,because day/night ac 1992The role of epiphytic periphyton and macro tivity patterns may be affected by other factors,such invertebrate grazers in the trophic flux of a tropical as temperature,wave action,and predation,besides the seagrass community.Aquatic Botany,43:327-349. previously outlined seasonality in the quality and quan Little,C.1989Factors governing patterns of foraging ac tity of the food supply(Kitting1985;Bronmark1989; tivity in littoral marine herbivorous molluscs.Journal Little1989). of Molluscan Studies,55:273-284. Mazzella,L.,M.C.Buia,M.C.Gambi,M.Lorenti,G.F. Acknowledgments.Thanks are due to M.Lorenti and A. Russo,M.B.Scipione and V.Zupo1992Plant-animal Rando for helping with the underwater sampling and C. trophic relationships in the Posidonia oceanica ecosys Norman for comments on the manuscript.YT was fi tern of the Mediterranean Sea:a review.In,Plant nancially supported by the Italian CNR and the Japan Animal Interactions in the Marine Benthos Society for the Promotion of Science(JSPS). (Systematics Association Special Volume46),John, D.,S.J.Hawkins and J.H.Price(eds.),Clarendon Press,Oxford,U.K.,pp.165-187. REFERENCES Mazzella,L.,M.C.Buia and L.Spinoccia1995Bio diversity of epiphytic diatom community on leaves of Bronmark,C.1989Interactions between epiphytes,macro Posidonia oceanica.In,Proceedings of the Thirteenth phytes and freshwater snails:a review.Journal of International Diatom Symposium,Marino,D.and M. Molluscan Studies,55:299-311. Montresor(eds.),Biopress Limited,Bristol,U.K.,pp. Buia,M.C.,V.Zupo and L.Mazzella1991Primary pro 241-251.

79 Takada et al.

Mazzella,L.and J.A.Ott1984Seasonal changes in some 8:359-370. features of Posidonia oceanica(L.)Delile leaves and Russo,G.F.,E.Fresi,D.Vinci and L.A.Chessa1984a epiphytes at different depth.In,International Workshop Mollusk syntaxon of foliar stratum along a depth gra on Posidonia oceanica Beds,1.Boudouresque,C.F.,A. dient in a Posidonia oceanica(L.)Delile meadow:diel Jeudy de Grissac and J.Olivier(eds.),GIS Posidonie variability.In,International Workshop on Posidonia Publishing,Marseilles,France,pp.119-127. oceanica Beds,1.Boudouresque,C.F.,A.Jeudy de Mazzella,L.and G.F.Russo1989Grazing effect of two Grissac and J.Olivier(eds.),GIS Posidonie Publish Gibbula species(Mollusca,Archaeogastropoda)on the ing,Marseilles,France,pp.303-310. epiphytic community of Posidonia oceanica leaves. Russo,G.F.,E.Fresi,D.Vinci and L.A.Chessa1984b Aquatic Botany,35:357-373. Mollusk syntaxon of foliar stratum along a depth gra Mazzella,L.,M.B.Scipione and M.C.Buia1989Spatio dient in a Posidonia oceanica(L.)Delile meadow:sea temporal distribution of algal and animal communities sonal variability.In,International Workshop on in a Posidonia oceanica meadow.Pubblicazioni della Posidonia oceanica Beds,1.Boudouresque,C.F.,A. Stazione Zoologica di Napoli I:Marine Ecology,10:107- Jeudy de Grissac and J.Olivier(eds.),GIS Posidonie 129. Publishing,Marseilles,France,pp.311-318. Mazzella,L.and L.Spinoccia1992Epiphytic diatoms of Russo,G.F.,D.Vinci,M.Scardi and E.Fresi1991 leaf blades of the Mediterranean seagrass Posidonia Mollusc syntaxon of foliar stratum along a depth gradi oceanica(L.)Delile.Giornale Botanico Italiano,126: ent in a Posidonia oceanica bed:3.A year's cycle at 752-754. Ischia Island.Posidonia Newsletter,4:15-25. Orth,R.J.and J.van Montfrans1984Epiphyte-seagrass Spada,G.1971Contributo alla conoscenza della relationships with an emphasis on the role of micro malacofauna della biocenosi a Posidonia oceanica(L.) grazing:a review.Aquatic Botany,18:43-69. lungo le coste Italiane.Conchiglie,7:125-135(in Ital Peduzzi,P.1987Dietary preference and carbon absorp ian). tion by two grazing gastropods,Gibbula umbilicaris van Montfrans,J.,R.J.Orth and S.A.Vay1982Prelimi (Linne)and Jujubinus striatus(Linne).Pubblicazioni nary studies of grazing by Brittium varium on eelgrass della Stazione Zoologica di Napoli I:Marine Ecology, periphyton.Aquatic Botany,14:75-89.

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