distribution and population dynamics of three populations of siphonaria ...

/. Moll. Stud. (1994), 60, 431-443 © The Malacological Society of London 1994

DISTRIBUTION AND POPULATION DYNAMICS OF THREEPOPULATIONS OF SIPHONARIA ON ROCKY INTERTIDAL

SHORES IN HONG KONG

J .H. LIUThe Swire Marine Laboratory, The University of Hong Kong, Hong Kong

(Received 17 September 1993; accepted 16 June 1994)

ABSTRACT

The pulmonate limpets Siphonaria japonica andSiphonana sirius occur over a wide range of localhabitat types in terms of exposure to wave action andsalinity. This is a study of these two species on threedifferent shore types in Hong Kong, ranging from anextremely exposed, high salinity (32-35%o) shore atCape d'Aguilar to a sheltered, low salinity (16—33%o)shore at Tai Lam Chung. Both species are restrictedto the low shore, year round. 5. japonica is a winterbreeder and recruitment occurred between Octoberand January. The recruitment of 5. sirius could not berecognised from the size-frequency histograms. Thealgal standing crop at Tai Lam Chung was higher thanat Wu Kwai Sha during the winter period, i.e., be-tween October and April. Seasonal fluctuations ingrowth rate were recorded for both Siphonariaspecies with the time of fastest growth occurring inwinter. S. japonica grew faster at Tai Lam Chungthan at Wu Kwai Sha. Food availability is thought tobe an important factor affecting growth.

INTRODUCTION

Although much work has been done on thepopulation biology of prosobranch limpets (seereview by Branch, 1981), most studies onSiphonaria have focused on activity rhythmsand homing behaviour (Cook, 1969, 1971,1976; Thomas, 1973; Cook & Cook, 1975,1978,1981; Garrity & Levings, 1983; Verderber etal., 1983; Branch & Cherry; 1985; Branch,1988) and competition (Creese & Underwood,1982; Ortega, 1985; Sutherland, 1986; Lasiak &White, 1993). Ortega (1987) studied habitatsegregation and seasonal changes in density ofS. gigas Sowerby and S. maura (Sowerby).Johnson and Black (1982) studied the variationin four polymorphic enzymes of an undescribedspecies of Siphonaria, from a rocky shore atRottnest Island, Western Australia. Little in-formation is, however, available on the popula-tion biology of species of Siphonaria and this ismainly from temperate shores. For example,

Quinn (1988a, b) has studied the ecology of theintertidal pulmonate limpet S. diemenensisQuoy & Gaimard in terms of population dy-namics and food availability and reproductivepatterns and energetics. The population dy-namics of S. denticulata and S. virgulata havealso been studied by Creese (1981).

Siphonarid limpets are common on the rockyintertidal shores of Hong Kong but informationon them is restricted to a general study of theiroccurrence and vertical distribution (Morton &Morton, 1983). Three species occur, i.e.,Siphonaria japonica (Donovan, 1834), Sipho-naria sirius (Pilsbry, 1894) and Siphonaria atraQuoy & Gaimard, 1833 (Christiaens, 1980,1982). The present study investigates the distri-bution, abundance and population dynamics ofthe three Siphonaria populations on three HongKong shores at Cape d'Aguilar, Wu Kwai Shaand Tai Lam Chung (Figure 1). Such shoresexperience a variety of hydrographical con-ditions and this study aimed at determining howeach species responded to such differences interms of patterns of recruitment, growth andpopulation dynamics.

MATERIALS AND METHODS

Stations and species studied

Cape d'Aguilar is located on the south-eastern tip ofHong Kong Island. As predominantly easterly windsprevail throughout the year, the shore experiencesheavy wave action and is characterized by near-normal salinities (32-35%o). Wu Kwai Sha, located inthe embayment of Tolo Harbour, is protected fromheavy wave action and experiences salinities of be-tween 28-33%o. Tai Lam Chung is a moderatelysheltered shore located in the western estuarine re-gion of Hong Kong. Fresh water issuing from thePearl River affects salinity, causing it to vary over awide range (16-33%o).

The substratum at Cape d'Aguilar is a coarse darkgrey tuff. It forms thick massive, beds with no inter-nal stratification (Allen & Stephens, 1971). The

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Figure 1 A map of Hong Kong showing the three study sites.

shore, in this area, falls gently to the sea formingpools and crevices. The shore substratum whichSiphonaria inhabits at Wu Kwai Sha is granitic rocks(Allen & Stephens, 1971). The shore falls steeply tothe sea and comprises broken granitic rocks withmany crevices. The Sung Kong Granite of Tai LamChung is uniformly coarse-grained (Allen andStephens, 1971) and the shore falls smoothly andgently to the sea.

Siphonaria japonica occurs mainly on shelteredshores but a few were found at Cape d'Aguilar.Siphonaria sirius tends to be a species of near-normalsalinities, common at both Cape d'Aguilar and WuKwai Sha but, at the latter, not available in sufficientnumbers to be sampled and only a few were found atTai Lam Chung. Siphonaria atra occurs on bothexposed and sheltered shores, i.e., Cape d'Aguilarand Wu Kwai Sha but was present in insufficientnumbers to be sampled. S. atra and 5. sirius from WuKwai Sha were not studied.

Distribution and abundance

To investigate the distribution of the limpets, fieldwork was undertaken at Cape d'Aguilar, Wu KwaiSha and Tai Lam Chung (Figure 1) between August1987 and December 1988. The vertical distributionand limpet abundance were assessed using 0.25 m2

quadrats placed at 1 m intervals down transect lines

set from Extreme High Water Spring Tide (EHWST)to the waters edge (ELWST). Height (m) of thequadrats above Extreme Low Water Spring Tide(ELWST) were calculated from the profiles obtained.The distribution and abundance of limpets were re-corded monthly in terms of the numbers of limpets.0.25 m~2 along the transect.

Chlorophyll analysis was used to estimate theabundance of the algal assemblage present at eachsite, i.e., encrusting algae, microalgae and filamen-tous algae. Samples were obtained every threemonths. Usually, six randomly-chosen rock samples,each of about 10 cm2, were chopped from the rockbelow mid tide level (MTL) where the limpets occur-red. Samples were analysed within 24 hours of collec-tion, usually after overnight storage in an air-tightand light-sealed container placed in a refrigerator(4° C). Exposure to strong light and high tempera-tures were also avoided in transit. Chlorophyll wasextracted from each sample using the acetone extrac-tion technique of Parsons et al. (1984).

Size-frequency histograms

Limpets were sampled monthly, i.e., from August1987 to March 1989 for Siphonaria sirius at Caped'Aguilar; from August 1987 to December 1988 forSiphonaria japonica at Wu Kwai Sha and fromNovember 1987 to December 1988 for S. japonica at

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POPULATION BIOLOGY OF SIPHONARIA 433

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Figure 2 The vertical distribution and abundance of the population of Siphonaria sirius along the transect atCape d'Aguilar.

Tai Lam Chung. For each species, an area of 1 m2 wassampled by removing all the limpets from four 50 x50 cm squares positioned randomly in an area neigh-bouring the transect. The shell length of each indi-vidual was measured to the nearest 0.5 mm withvernier calipers. These data were used to constructmonthly size-frequency histogTams of the sampledpopulations using size class intervals of 1 mm.

Growth

Growth was estimated by analysing the sizes of thecohorts in the monthly size-frequency distributions,i.e., from the monthly change in the mean size ofeach cohort. Annual growth increments were calcu-lated for each cohort in the size-frequency classesobtained for each species.

Mortality

The mortality of individuals in the three populationswas estimated by the decrease in density of cohortsover time

RESULTS

Vertical distribution and abundance of the threepopulations

The distribution and abundance of Siphonariasirius along the transect at Cape d'Aguilar areshown in Figure 2. Individuals were found onthe lower shore, all year round.

At Wu Kwai Sha, Siphonaria japonica wasrestricted to a low position on the shorethroughout the year (Figure 3). The increase inpopulation density corresponded closely withthe numbers of juveniles present, i.e., a peak of33 individuals. 0.25 m~2 was recorded betweenNovember and January, when juvenile recruit-ment took place.

The distribution and abundance of Siphonariajaponica along the transect at Tai Lam Chung areshown in Figure 4. Individuals occupied themiddle to low shore between November andApril, disappeared in May, but occurred on theshore again from the following November.

Recruitment

Year-classes of the limpets were estimated bysize-frequency analysis of the histograms.

A definite season of recruitment into theSiphonaria sirius population at Cape d'Aguilarcould not be recognized from the size-frequency histograms (Figure 5). The reasonsfor this will be discussed below.

During winter, i.e., between December,January and February, there is a lack of dataconcerning the species from Cape d'Aguilar be-cause of heavy wave-action which preventedsampling.

At Wu Kwai Sha, recruitment of Siphonariajaponica occurred over a narrow period of time

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Figure 3 The vertical distribution and abundance of the population of Siphonaria japonica along the transect atWu Kwai Sha.

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Figure4 The vertical distribution and abundance of the population of Siphonaria japonica along the transect atTai Lam Chung.

between October and December (Figure 6). from the shore in May. The lifespan is thusThe population largely comprised one year- estimated to be approximately one year,class and the lifespan is thus estimated to beapproximately one year.

Recruitment of Siphonaria japonica at Tai (~'rowtn

Lam Chung occurred only from November to The growth of Siphonaria sirius from CapeDecember (Figure 7). The species disappeared d'Aguilar could not be estimated from the size-

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POPULATION BIOLOGY OF SIPHONARIA

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Shell length ( mm)Figure 5 Size-frequency histograms of the population of Siphonaria siriiis at Cape d'Aguilar. n is the totalsample size.

frequency histograms, for the animals could notbe divided into year-class cohorts.

Siphonaria japonica at Wu Kwai Sha grewrapidly from October to March, for a period of5-6 months, reaching a shell length of 18 mm.Figure 8 shows the estimated mean shell lengthof each cohort of the 5. japonica population.

Cessation of growth occurred during late springand summer, i.e., between April and August1988. Growth occurred, however, from Octoberto March. The annual growth increments ofSiphonaria japonica at Wu Kwai Sha were alsoestimated from the size-frequency histograms.The mean length of the population in October

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Figure 6 Size-frequency histograms of the population of Siphonaria japonica at Wu Kwai Sha. The numberabove each peak represents the year of birth of that size class and n is the total sample size.

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POPULATION BIOLOGY OF SIPHONARIA

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Figure 7 Size-frequency histograms of the population of Siphonaria japonica at Tai Lam Chung. The numberabove each peak represents the year of birth of that size class and n is the total sample size.

1987 was 7.2 mm and reached 19.5 mm in October1988. The annual growth increment was around12.3 mm.

Siphonaria japonica from Tai Lam Chunggrew from 10.9 mm in November to 20.8 mm inApril (Figure 9). It is not possible to estimatethe annual growth increment, as the species wasnot present on the shore between May andOctober 1988.

Mortality

Mortality was estimated from the changes inadult density. The mean adult mortality rate ofthe population of Siphonaria japonica at WuKwai Sha was estimated to be 89.2%.year"1.

It is not possible to estimate the annual mor-tality rates of the population of Siphonariajaponica at Tai Lam Chung and the populationof Siphonaria sirius at Cape d'Aguilar, becausethe former species was not present on the shore

from May to October 1988 while the lattercould not be divided into year-class cohorts.

The algae

Seasonal variations in the abundance of en-crusting algae, microalgae and filamentousalgae (mostly Brachytrichia maculans, Hilden-brandia prototypus, Ralfsia verrucosa, Entero-morpha spp. and Oscillatoria spp.), as reflectedin chlorophyll levels, are shown in Table 1. Thechlorophyll content showed a similar seasonalpattern at the three sites, i.e., chlorophyll read-ings were higher between December and March(2.53-6.57 jig. cm"2) and stayed at lower valuesbetween June and September (0.86-1.70 u,g.cm"2). The maximum value of 6.57 p.g. cm"2

was recorded in March, the minimum value of0.86 u.g. cm"2 was recorded in June. The valuesfrom Tai Lam Chung were the highest of the

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1987 1988Figure 8 The estimated mean shell length of each cohort of the population of Siphonaria japonica at Wu KwaiSha. The number represents the year of birth of each cohort.

three sites while those from Cape d'Aguilar andWu Kwai Sha were similar.

DISCUSSION

This study shows that Siphonaria japonica andSiphonaria sirius occurred over a wide range oflocal habitat types in terms of exposure to waveaction and salinity. They thus exhibit a widetolerance to differing physical, chemical andbiological environments. The vertical distribu-tions of S. sirius and 5. japonica were restrictedto the lower regions of the shore, year around.

Juveniles of Siphonaria japonica from bothWu Kwai Sha and Tai Lam Chung occurred lowon the shore. Each of the two S. japonica popu-lations demonstrated a single annual phase ofrecruitment. Recruits of S. japonica at Tai LamChung were first recorded in November, onemonth later than when recruits were first re-corded at Wu Kwai Sha. This may be because at

the former site, they were lower on the shore.The recruitment of juveniles of S. sirius at Caped'Aguilar could not be recognised from thesize-frequency histograms. This could be be-cause either the juveniles were not sampled, orbecause of their distribution on the lowest partof the shore. This is an area deserving of furtherstudy.

Recruitment of Siphonaria japonica occurredbetween October and January, when tempera-tures are low, algal availability is high and waveheights are, on average, 1 m higher than insummer (Apps & Chen, 1973). Under such con-ditions, juveniles are better protected from de-siccation, high temperatures and have abundantfood. Table 2 shows the pattern of mean airtemperature and relative humidity changes inHong Kong between 1987-1989 (RoyalObservatory, Hong Kong). Quinn (1988a) alsoshowed that recruitment of Siphonaria die-menensis occurred in winter (June) each year inboth upper and lower zones.

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Figure 9 The estimated mean shell length of each cohort of the population of Siphonaria japonica at Tai LamChung. The number represents the year of birth of each cohort.

Table 1. The chlorophyll content of rock samplestaken from the three sites, sampled betweenMarch 1988 and March 1989: mean ± SD chloro-phyll u.. cm"2; n = 6.

Sites Mar. Jun. Sept. Dec. Mar.1988 1989

Cape d'Aguilar 3.54 1.56 1.70 2.53 3.87(1.22) (0.68) (0.55) (1.22) (1.56)

Wu Kwai Sha 3.24 1.30 1.48 2.57 3.16(1.05) (0.65) (0.54) (1.04) (1.07)

Tai Lam Chung 5.5 0.86 1.08 6.17 6.57(1.19) (0.24) (0.24) (1.38) (1.02)

The population dynamics of a species can beexpected to differ at sites where different bioticand abiotic environments are encountered. Thegrowth and population dynamics of the samespecies of limpets may also be expected to varyamong different habitats (Sutherland, 1970,1972; Branch, 1975, 1976; Creese, 1980; Work-man, 1983; Fletcher, 1984). Lewis and Bowman

(1975) stressed the importance of biologicalhabitat upon growth and pointed out thatchanges in the surrounding species compositionwould produce corresponding changes in thelimpet populations. Estimates of growth bySiphonaria japonica indicate that the popula-tion at Tai Lam Chung grew faster than that atWu Kwai Sha (Figure 10).

On the shore at Wu Kwai Sha, the mostabundant herbivores were Patelloida pygmaea(Dunker), Siphonaria japonica and S. sirius.These three species characterize the middle andlower shore. Other grazing gastropods such asMonodonta labio (Linnaeus) and Nerita albi-cilla Linnaeus were also common on the middleand lower shore. The shore at Tai Lam Chungwas occupied only by 5. japonica, from Novem-ber to April, with other herbivores occurring inlow numbers. Liu (1992) has shown that thesiphonariid radula comprises numerous fineteeth of uniform size, capable of rasping macro-algae but not of scraping into rock. Competi-tion for food may lead to different growth rates

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Table 2. Mean air temperature and relativehumidity of Hong Kong between 1987-1989 (Datafrom: Monthly Weather Summary 1987-1989,Royal Observatory, Hong Kong).

Jan.Feb.Mar.Apr.MayJun.Jul.Aug.Sep.Oct.Nov.Dec.

1987

M.A.T.(C)

17.318.321.321.925.027.528.928.627.325.721.816.8

RH%

717886868982828179807960

1988

M.A.T.(C)

17.916.316.820.826.628.629.027.827.624.419.917.7

R.H.%

778184788678818577776668

1989

M.A.T.(C)

15.716.618.622.025.127.528.828.928.125.121.517.8

R.H.%

807475868683798077736974

in S. japonica occupying the two shores, asgrowth is affected by food intake (Paine, 1969;Bosman & Hockey, 1988). However, the foodresources available for S. japonica on the twoshores were also different. At Tai Lam Chung,from October to April, green filamentous algaeformed a thick, soft, layer which coveredalmost 100% of the rock surface from the low tomiddle shore. At Wu Kwai Sha, the encrustingalgae Hildenbrandia prototypus and Brachy-trichia maculans formed patches on the shoreand filamentous algae formed a thin film. Algalproduction at Tai Lam Chung was higher thanat Wu Kwai Sha during the winter period, i.e.,between October and April.

A variety of factors are known to affect thegrowth rate and ultimate size reached by inter-tidal gastropods. Much of the difference ingrowth rate has been attributed to food avail-ability on the shore (Stearns, 1976; Creese andUnderwood, 1982; Underwood, 1984a, b;

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1987 1988Figure 10 Growth curves of Siphonaria japonica at Wu Kwai Sha and Tai Lam Chung.

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Bosman and Hockey, 1988). Paine (1969) sug-gested that individuals of Tegula grew slowly athigh levels on the shore but, after reaching acertain adult size, moved downshore wherewith increased food availability, grew faster.Quinn (1988a) studied the population dynamicsof Siphonaria diemenensis Quoy & Gaimardand found that food availability was a majordeterminant of growth rate, i.e, limpets in thelower zone where food supply was more con-stant were larger and grew faster than those inthe upper zone where food supply showedstrong seasonal variation. It has also beenshown that growth rates of intertidal gastropodsincrease when densities are experimentally re-duced (Frank, 1965; Sutherland, 1970; Haven,1973; Underwood, 1976). Bosman and Hockey(1988) have studied on the influence of primaryproduction rate on the population dynamics ofPatella granularis Linnaeus in South Africa.They found that the most significant correlateof limpet growth was the rate of algal produc-tion. That is, there was more rapid growth bylimpets on nutrient-rich shores which, com-bined with the effects of predation by AfricanBlack Oystercatchers (Haematopus moquiniBonaparte), led to differences in size structureand life-history patterns of the populations in-habiting enriched and unenriched shores.

Food availability may be the limiting factoraffecting growth as density increases. Intra-specific competition at increased densities hasbeen shown to greatly affect the growth andmortality of species of Cellana (Underwood,1978; Creese and Underwood, 1982). Highdensities of other grazing gastropods have alsobeen shown to affect the growth and mortalityof species of Cellana (Underwood, 1978). Thus,increased intra- and inter-specific competitionmay be a factor responsible for the observedslow pattern of growth of the Siphonaria japon-ica population at Wu Kwai Sha.

Seasonal fluctuations in the rate of growthwere seen in the Siphonaria japonica popula-tions from both Wu Kwai Sha and Tai LamChung with the times of fastest growth beingrelated to the times when the weather is coolerand the primary production rate is higher, i.e.,the availability of food is higher, between Octo-ber and March.

In this study, the lifespans of Siphonariajaponica from both Wu Kwai Sha and Tai LamChung were estimated to be approximately oneyear. Quinn (1988a) showed that the averagelongevity of Siphonaria diemenensis from upperzone to be between 18 months and 2 years whilethose from lower zone likely to be at least 3 to 4

years. In Hong Kong, from October to Aprilwhen rocky intertidal habitats are relativelywet, cool and protected from intense sunlight,fast-growing algae (blue-green algae, diatoms,filamentous and membranous species of red andgreen algae) and macroalgae species coverthem. During the hot, dry and more sun-exposed summer, algae disappear, leaving themid and high shore encrusted with only patches.The radula of Siphonaria consists of numerousfine teeth of uniform size, capable of raspingmacroalgae but not of scraping into the rock(Liu, 1992). It seems that the lack of food insummer for Siphonaria may affect its lifespan.

Sources of mortality were not directly deter-mined in this study. Associated with harsh sum-mer conditions, temperature and desiccationare considered the most important physical fac-tors causing limpet mortality on the shore.Quinn (1988a) demonstrated that the annualmortality rates of Siphonaria diemenensis(adults) from upper shore were significantlygreater than those from lower shore and theseasons of maximum mortality for those in theupper shore were summer and autumn whilethere was no clear seasonal trends for those inthe lower shore. In summer, air temperatures inHong Kong may reach 36° C and temperaturesof 50° C have been recorded from rock surfacesin August (Liu & Morton, 1994). Many limpetswere observed dead on the bare rocks and inintertidal pools at Cape D'Aguilar during thesummers of 1988, 1989 and 1990.

Predation is also a source of mortality. Tong(1986) reported that local muricid gastropods,Thais clavigera and Morula musiva, feed onlimpets. The diet of Thais clavigera at Caped'Aguilar included Siphonaria spp. (9%)together with Cellana spp., Patelloida spp. andNotoacmea schrenkii (7.1%). The diet of Thaisclavigera at Wu Kwai Sha included Siphonariasp. (0.7%) and that of Morula musiva at WuKwai Sha also included Siphonaria sp. (2.1%).Taylor (1990) provides a table of T. clavigeraand M. musiva diets at Wu Kwai Sha with ahigher predation rate upon Siphonaria sp. beingrecorded for the latter species, i.e., 1.1% and12.9% respectively. Summer heat and preda-tion thus appear to be the major causes of deathof individual limpets on local shores.

ACKNOWLEDGEMENTS

I thank my supervisors, Dr I.J. Hodgkiss andProfessor Brian Morton for their advice on thisstudy and the latter for his critical reading of the

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first drafts of the manuscript of this paper. Thiswork forms a part of the thesis submitted to TheUniversity of Hong Kong for the degree ofDoctor of Philosophy.

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