Growth of the pulmonate limpet Siphonaria lessoni (Blainville) in a rocky intertidal area affected by sewage pollution

JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY J. Exp. Mar. Biol. Ecol. 175 (1994) 211-226

Growth of the pulmonate limpet Siphonaria lessoni (Blainville) in a rocky intertidal area affected by sewage pollution” A. Tablado, J. J. Lttpez Gappa*, N. H. ~aga~di MuseoArgerrrirx~de Ciencias

Natwales

“‘Bemordiw Riwdu Go “, A. Guihdo

4711,(1405j Buertor A iws.

Argembw (Received

2 February

1993; version received

23 July 1993; accepted

24 September

1993)

Abstract of Siphonaria lessani (Blainville) was studied at two rocky intertidal sites near Quequen (38” 35’ S, 58”42’ W), Argentina. One of them was severely affected by sewage pollution and the other was located in a natural area without visible signs of organic enrichment. Results obtained through periodical sampling, recapture of marked specimens and controlled reciprocal translocations between both areas demonstrated increased growth (9.7 mm after one year) and low densities in the vicinity of the outfall. This area is characterized by an abundance of cyanophytes, diatoms and opportunist, ephemeral green algae, and also by the total absence of the mytilid Brachidantes radriguezi (d’orbigny). On the other hand, in unpolluted areas monopolized by B. rodriguezi at mid-intertidal levels, densities were high and growth was slower (6.2 mm after two years). Growth was also increased in specimens experimentally transported or swept by waves from the mussel community to tide-pools dominated by the green alga Ulvu lu~ru~a L. Growth in the natural environment or in enriched areas was remarkably lower than values rcported in a previous study on floating substrata within Mar de1 Plata (38” 03’ S, 57” 33’ W) harbour (19.5 mm after one year). A positive correlation between growth and mortality rates was observed. Due to considerable habitat-induced variations in growth rate, estimation of age as a function of size in this species may be unreliable without taking into account the sl~rroundi!l~ environment. Results obtained in the present study emphasize the influence of primary) production and of the presence of other sessile organisms on the population dynamics of S. le.c.ro~i. Growth

Key wards: Siphonaria lessani; Growth;

’ Dedicated to the memory * Corresponding author. 0022-098 1/94~$7.00 SSDI 0022-098

of Norman

0 1994 Elsevier 1(93)EO143-M

Sewage pollution;

Rocky intertidal;

H. Magaldi.

Science B.V. All rights reserved

Argentina

1. Introduction Several studies have reported that domestic sewage discharges cause profound changes in benthic community structure (Littler & Murray, 1975) and energetic pathways (Littler & Murray, 1978), as well as in patterns of algal succession (Murray & Littler, 1978) on rocky intertidal areas. Intertidal primary production is also enhanced by higher nutrient concentrations in areas influenced by seabird guano (Bosman ct al.. 1986). Higher rates of algal production modify growth rates and life-history patterns of limpets, and also produce indirect effects at higher trophic levels of the intertidal community (Bosman & Hockey, 1988a,b.c). In previous studies (Lcipez Gappa et al., 1990, 1993), we have analyzed the impact of sewage pollution on the rocky intertidal zone at Queyuin (38” 35’ S, 58” 42 W), Argentina. The community around the outfall was characterized by crusts of blue-green algae and diatoms and the almost complete disappearance of the mytilid Brcrchi&&c vodriguezi (d’orbigny), the dominant primary space occupier in natural areas. The overall objective of this study was to analyze the effect of changes produced by scwage pollution on the growth rate of the pulmonate limpet Sip~io~z~ri~zkrsoni (Blainvillc). Although S. lessotri is the dominailt herbivore and also the only limpet species in the intertidal zone of Buenos Aires Province, Argentina. relatively little is known about it. Observations on its anatomy, development and spatial distribution have been reported from natural areas of rocky shore at Mar de1 Plats (38” 03’ S, 57” 33’ W), Argentina (Olivier & Penchaszadeh, 1968); while its growth and feeding habits were studied in populations growing on rafts within Mar de1 Plata harbour (Bastida et al.. 197 11. Although many life-history features of S. Iessnni are poorly understood. the absence of homing behaviour (Olivier & Penchaszadeh, 1968) distinguishes this species from most other known members of the genus Siphonnricr (Cook, 1971; Thomas. 1973; Branch, 19X1; Creese & Underwood, 1982; Garrity & Levings, 19X3: Vcrderbcr et al.. 1983; Hulings, 1985; Branch & Cherry, 1985). The present study explores the influence of the surrounding community on growth rate and mean size (Fischer-Piette, 1948; Lewis & Bowman, 1975). as well as the importance of other primary space occupiers (Choat, 1977; Thompson, 1980; Creese, 1982; Hawkins & Hartnoll, 1982; Dungan, 1986) on the demographic characteristics of limpets, in the presence and absence of enrichment by sewage.

2. Material and methods 2.1. SlU& nren Field work was carried out in a site located 4 km eastward of QuequPn harbour (Fig. 1). The intertidal zone consists of loess platforms with shallow grooves lying perpendicular to the shoreline. The whole area is exposed to heavy wave action. Around 14 million 1 of untreated sewage produced by ca. 42000 inhabitants of Necochca and Quequt?n are discharged daily into the intertidal zone. A more detailed description of the study area, as well as physico-chemical characteristics of the water along the pollution gradient, can be found in a previous paper (L6pez Gappa et al., 1990).

,

20 km I ’

Samples of S. lessoni were obtained at approxim~~tely monthly intervals, from October 1985 to September 1989, in order to compare size-frequency distributions at two sites with contrasting characteristics. One of the sampling sites was located in the vicinity of the outfall (hereafter referred to as “polluted area”), a zone heavily impacted by organic enrichment where the Brachidontes rodriguezi community was completely absent. The other site was located 300 m to the SW of the outfall, in an area without visible signs of pollution and normal development of the B. rodriguezi community (hereafter referred to as “clean area”). A detailed description of both zones is given in Lopez Gappa et al. (1990). All the limpets sampled in four or five 12.5 x 12.5 cm quadrats (total surface 625781 cm’) were fixed in formalin, measured with a nlicrometer eyepiece, and grouped in 1 mm length intervals. Size-frequency distribLItions in both areas were compared each month using Kolmogorov-Smirnov two-sample tests (Sokai & Rohlf, 198 I). Density differences between both sites were estimated by counting all limpets found in four 2.5 x 25 cm quadrats randomly thrown in each area on five dates from March to September 1989. Density data were transformed using log,,,(x + 1) and processed by two-lvay ANOVAs (sites x dates) with 4 replications. 2.3. Recapture experiment Comparison of size-frequency showed that modal displacement

distributions obtained during preliminary sampling was not an adequate method for growth rate analysis

in S. lessorli (see Results). Therefore, growth was estimated by painting shell surfaces with an epoxy enamel (Alcurnia S.A.). Specimens from the numerically dominant cohort were chosen in order to lninin~ize length variance of marked limpets in clean and polluted areas. Shell length of each marked (or recaptured) limpet was measured in situ with dividers. Each length was recorded by scratching paper with the sharp ends of the dividers. These marks were measured in the laboratory with a stereomicroscope fitted with a micrometer eyepiece. Thus, manipulation stress was completely avoided, since limpets were not removed from the substratum. Recaptures (i.e., recovery and measurement of marked limpets at later dates) were carried out at ~lpproximately quarterly intervals. New limpets were painted whenever recaptured specimens of a cohort were too scarce. In order to keep variances as low as possible, new specimens were chosen within a very narrow range ( f 0.5 mm) around the mean of recaptured limpets. Mean size of the newly marked limpets was never significantly different from that of the previously recaptured sample. Heights of mark and recapture (and also translocation, see below) sites were measured with a sighting level and are given in metres over Quequtn Harbour zero datum. The clean site was slightly higher than the polluted one (1.87 and 1.68 m, respectively). Differences in mark loss and mortality rates between both areas were quantified by the following method: on 2nd December 1990, 100 empty shells were glued to the substratum with fast-drying epoxy cement and painted with epoxy enamel in the clean and polluted sites. Simultaneously, 500 S. Iessoni specimens living in surrounding areas were also painted at each site. On the next day, live limpets were counted in order to allow for losses due to failures in paint attachment to the shell surface. In February, April, and August 1991, the live-marked limpets were counted, as well as the proportion of painted and non-painted shells still fixed to the substratum. Both areas were always thoroughly surveyed as far as 2 m beyond the last recaptured iimpets. Monthly rates of mark loss in both sites were used to calculate monthly mortality rates from recapture data. Recapture data (corrected using rates of mark loss) were compared by two-tailed Fisher’s Exact Tests.

On 25th November 1991, 300 S. lessoni from the clean area were measured and painted. Of these, 100 were transported to the polluted area, 100 were carried to nearby tide-pools dominated by the green alga U/vu lactuca I,. and the remaining 100 were re-settled on the original area as controls. A reciprocal translocation experiment was carried out using S. lessoni from the polluted area. In this case, 100 limpets were transported to the B~~c~~~o~tes rodriguezi community in the clean site, 100 were located in Cf. lactuca tide-pools, and the remaining 100 were re-settled in the polluted area as controls. Different colours were used to distinguish each group of limpets. On 1st March 1992, limpets remaining in both areas were recaptured and measured. Nonparametric Mann-Whitney U tests (Sokal & Rohlf, 198 1) were used to compare mean lengths in translocated and control groups due to lack of normality andjor homogeneity of variances, even after applying different transformations.

315

1. Ttrhlndo et al. i J. Esp. Mnr. Biol. Ecol. I7.r (1994) 21 1-226

1

Percentage

Sire (mm) Fig. 2. Relative size-frequency 1989 in polluted months (Kolmogorov-Smirnov

to September

q

distributions of ~~~~~J~?~~~~~ fe.wni from samples obtained from October 198S and clean areas. Differences between both areas were highly significant in all two-sample tests, 17
Table 1 Density of Siphonurirr jessuni in the polluted performed on log,,,(.x + I)-transformed data

and clean areas. Two-way

Date

Density

(sites x dates)

Total

analysis

of variance

(ind,m-‘)

Poluted

3~~~3~~9 3 l/05:89 14,,07%9 13:08~89 03;09:89

Polluted

Clean

Mean

SD

Ii

Mean

SD

11

556 1048 424 348 524

778 611 320 310 408

4 4 4 4 4

1384 2012 732 1712 1912

1407 815 437 978 x02

4 4 4 4 4

550

525

20

1574

970

20

ANOVA Source

Sum of squares

Sites Dates Sites x dates Error

4.3994 2.5102 1.2639 15.2924

Table

Degrees of freedom 1 4 4 30

Mean square

F-ratio

I’

4.3994 0.6275 0.3160 0.5097

8.631 1.231 0.620

< 0.01 > 0.05 > 0.05

Substratum heights were similar in the polluted, clean, and tide-pool sites chosen for the translocation experiments (1.73, 1.87 and 2.01 m, respectively). Density of 5’. lessoni in these three areas was estimated by counting all specimens in five randomly located 12.5 x 12.5 cm quadrats. Community structure was quantified by estimating percentage cover of macrobenthic species using 5 replicated 45 x ‘15 cm quadrats provided with a grid of 100 evenly spaced points (see Lopez Gappa et al.. 1990).

3. Results

A total of 1946 specimens with mean monthly lengths ranging were collected in the polluted area, while 3543 limpets between sampled in the clean area. Size differences between both sites nificant (Kolmogorov-Smirnov two-sample tests, p < 0.00 1

Clean M M,‘R M,‘R R M R M R hl R

6.33 8. I5 8.30 0.73 0 .I3;. 0.82 0,8h 0.68 9.61 9.41

from 7.76 to 13.3 1 mm 4.63 and 8.06 mm were were always highly sigin all months). Size-

0.533 0.5% 0.358 0.5J2 0.103 0.173

24:02/90 22/04:90 23,:04:90 10/09;90 11:09,90 05: 12,YO Otv12:90 25;01:91 27’02/91 13;04/91

I000

13’12%9 23/0?;;‘90 11?;04/90 10~09,190 12109!90 05,‘12/90 06/ IQ90 24X)2/9 1 25/o&,91 qo3i91

iooo

0.265

440

0.594

178 53 73 29 129 38 89 58

0.572 0.501 0.452 1.006 0.597 0.7% 0.626 0.656

30 131 I8 II8 55 745 57 107 39

0.357 0.598 0.514 0.520

0.96 0.31 II 00 _ 0.07 .. 0. I?

0.37 (I.09 Cl.07 0. I5 0.13 0.02

A. Tahlmh et al. i J. Exp. Mur. Rid. Ed

217

I75 (1994) 21 l-226

frequency distributions were not useful for growth rate measurement due to extensive overlapping and absence or irregular modal displacements through time (Fig. 2). Mean density of S. lessoni was 580 ind.m -2 in the polluted site and 1574 ind.m ’ in the clean area. Differences between areas were highly significant but temporal variations and the interaction term were non-significant (Table 1). Field observations indicate that, in the polluted zone, the new cohort of S. le.sso~li can be distinguished in December, when it has reached ca. 1.5-2.0 mm after 2-3 months of benthic existence. 3.2. Recqmre

experiment

In the polluted area, 1000 limpets with a mean length of 6.33 mm were marked on February 1990. After several consecutive paintings and recaptures, 39 limpets with a mean length of 9.44 mm were obtained in April 1991 (Table 2, Fig. 3). Therefore, this group had a growth rate of 2.53 mm.year-’ (after subtracting differences introduced by adding new marked limpets to the original cohort). The original 1000 marked individuals on December 1989 in the clean area had a mean length of 4.83 mm. A group of 53 specimens with a mean length of 6.20 mm were retrieved in September 1990. After successive paintings and recaptures, 58 limpets measuring 7.49 mm on average were recovered in April 1991 (Table 2, Fig. 3). Therefore, growth rate in this group reached 1.63 mm.year-’ ( a 11owing for differences due to additions of new individuals). Monthly rates of mark loss were low in both areas, ranging from 0 to 5”,, (Table 3). Differences in mortality rates showed a clearly seasonal pattern during three Shell length hn) 11 10 c 9 8 7 6 6 10 9 1

Polluted

t

Clean

II

Ill

I

1

I

j,

/

)

,I

(

,j

JASONDJFMA

DJFMAMJ 1990

I m

Marked

1991

I I=I

Fig. 3. Relative size-frequency distributions of marked and recaptured December 1989 to April 1991 in polluted and clean areas.

Recaptured specimens

of Siphontrria k.wmi

from

21X

A. Tuhlado et al.

: J. E.rp. Mar. Biol. Ecol. 17.5 ilY94) 211-226

Table 3 Number of painted shells and of shells that have lost their marks attached tures of live Siphonun’ct lessoni specimens in the polluted and clean areas

to the substratum,

Clean

Polluted

Date Attached Paint present

Paint lost

100 78 45 4

12 4 1

03:12,‘90 24/02,‘91 23/04!‘9 1 30/08/91

Live limpets

shells

Attached

Monthly loss ram (“,,)

4.x 4.2 4.7

Mean

and rccap-

452 112 49 0

Pamt prcscnt

Paint lost

lO(~ 75 61 47

12 2 0

shells

Live IlmpCls

Monthly

.

5.0 1.7 0

4.57

loss

riltc (I’,,) 490 97 12 I3

2.23

different field experiments encompassing a period of over two years (Table 4). Nonsignificant differences between both areas were found during spring and summer. Mortality was, however, significantly higher in the polluted area than in the clean area during autumn and winter. Successive recaptures in the Brachidontes rodriguezi community indicate that most individuals remain in the vicinity of the site where they were marked. So far, we have not observed population migrations towards upshore areas of lower density. NeverTable 4 Monthly mortality rates of marked limpets. RE: Recapture Translocation experimenl (controls). Rates were calculated in a Fisher’s Exact Test. ns: non-significant Period

Season

experiment. MLE: Mark loss experiment. TE: from data in Tables 2, 3 and 7. ,I: probability

Monthly

mortality

rate”

Polluted

Clean

I’

RE Feb/90-Apr,!90 Apr/90-Sep/90 Sepi90-Dee/90 Dee/90-Feb;91 Feb/91-Apr/91

autumn winter spring summer autumn

0.51 0.18 0.20 0.27 0.33

0.30 0.14 0.21 0.26 0.18

< 0.00 1 0.0 1s 1.000 ns 0.4X7 ns 0.029

MLE Dee/90-Feb/91 Feb/91-Apr/91 Aprl91-Aug/91

summer autumn winter

0.26 0.27 I .oo

0.29 0.12 0.19

0.065 ns 0.033 0.002

TE Novi9 1-Mar/92

summer

0.23

0.18

0.090 ns

,‘: Corrected

using mean monthly

rates of mark loss for each area (see Table III).

1 I9

A. Trrhlado et al. /J. E.up. MNT. Biol. Ecol. I75 (1994J 21 l-226 Table 5 Statistical comparisons tion experiments

of Si~~horwiu lessorzi natural

densities

(ind’m

Polluted Mean I,

for transloca-

Tide-pools

MUSSelS

3981 1160 5

SD

‘) in 3 areas selected

18419 3682 5 Mann-Whitney’s

Mussels-polluted Mussels-tide pools Polluted-tide pools

7010 1293 5

U test U

I’

25 25 20.5

< 0.0 I < 0.0 I > 0.05

theless, two limpets “escaped” from the mussel community in December 1990 and grew to remarkably higher sizes than the others (3 mm over mean size). They arc shown as outliers in Fig. 3. Shells of limpets living among mussels usually had dark colours and a worn out periostracum. On the other hand, the two fast-growing limpets swept to U/W Immca pools had a clear, intact margin which could be easily distinguished from the darker, central area. 3.3.

Tramlocation experiment

Density of S. lessoni in the Brachidontes rodriguezi community was significantly higher than either in Ulvu 1actuc.a tide-pools or in the polluted area. The number of limpets per

Table 6 Percentage cover of macrobenthic organisms and percentage deviation) in 3 areas selected for translocation experiments

of unoccupied substratum (mean and standard (mussels, tide-pools, polluted)

Mussels

Tide-pools

Mean

SD

28.2 55.6 13.6 0.2 0.7 2.1 _

14.2 13.5 4.0 0.4 0.3 1.2 _

Mean

Polluted SD

Mean

SD

26.2

14.0

59.4

31.0

48.4

17.0 3.1 5.0 10.4 5.7 2.4 1.3

4.0 9.2 13.2 2.8 2.X 0.7

_

3.2 24.6

0.2

1.1

Il.3 0.3

_

_

11.0 2. I

14.7

0.2

2.0 0.3

220

A. Tdhdo

rr ul.

J. Exp. Mar. Bid.

Ed.

17-i iI 994~ 21 I-226

unit area living among mussels was more than four times higher than that measured in the vicinity of the outfall, and double that registered in pools. Differences in density between tide-pools and the polluted site were non-significant (Table 5). Community structure differed markedly in these three experimental areas (Table 6; SW also Lopez Gappa et al., 1990). Brachidorztes vodriguezi was the dominant spaccoccupier both in the unpolluted rocky substratum and in pools, but was completely absent from zones heavily impacted by sewage pollution. UO’LIhctuca reached highest densities in tide-pools. Crusts of blue-green algae and diatoms together with the filamentous chlorophytc Cladophova sp. were abundant in the polluted area, but absent or rare in zones dominated by mussels. The proportion of unoccupied substratum ~~1s highest in the vicinity of the outfall. Growth of translocated and control limpets is shown in Fig. 4 and Table 7. Controls marked and retrieved at the polluted area showed significant growth. Limpets transported from the polluted area to tide-pools or to the mussel community showed. however, negative growth rates. Analysis of size-frequency distributions of marked and recaptured limpets (Fig. 4) indicated that this was due to higher mortality rams in the largest size classes. Limpets transferred from clean to polluted areas showed highly significant differcnccs

L-6

;5

1’3

Size (mm)

Fig. 4. Size-frequency distributions of marked and recaptured spccimcns of S@horrcrrrtr komi in a reciprocal translocation experiment among the Lhchidmrev rodrigwri community (mussels). tide-pools and the polluted area.

Table 1 Mean length (mm) of marked and recaptured specimens of Si~~hon~ritr /e.tsor~ after 97 d translocation expcrimcnts to the polluted area, tide-pools, and the Bmchidorm\ rzdr@e;i community (100 specimens ~crc translocatcd to each area). SD: standard deviation; ,I: sample sire: I>: probability in Mann-Whitnq II test, Marked

Recaptured

I’

Grovvth rate

(ml,, mo ’ ) Mean

SD

Mean

SD

II

0.64 0.61 0.79

9.72 8.31 7.83

0.70 0.79 0.52

72 ‘0 15

< (1.001 > 0.05 < 0.01

(1.33 0.03 0.16

Limpets from the mussel communit) Control 6.09 0.58 Tldc-pools 6.07 0.62 Polluted 6.04 0.56

6.17 6.45 9.05

0.68 0.63 0.71

3x 50 26

> 0.05 < 0.00 I
0.02 0.I2 0.93

I.impcts from the polluted Control X.64 Tidepools 8.38 Muascls 8.38

area

between means, growth rate being three times higher than in controls from the polluted area. On the other hand, controls which remained in the mussel community showed almost no growth. Limpets from the Brachidontes rodriguezi area translocated to C//VU Iuctucct tide-pools showed intermediate but significant growth.

4. Discussion Results obtained by recapture of cohorts clearly demonstrated that growth of S. lessoni in rocky intertidal areas dominated by Bvachidontes rodriguezi is remarkably lower than on floating substrata at Mar de1 Plats harbour, where it attained 19.5 mm after one year, and 23.8 mm after two years (Bastida et al., 1971). According to field observations, the cohort that was marked in the clean area on December 1989 (mean size: 4.8 mm) was already present in September 1989. Maximum spawning frequency in the study area occurred during September (unpublished observations), and peak recruitment presumably took place during October-November. The smallest recruits observed among B. rodriguezi valves had a size of ca 0.8 mm. Therefore, it can be concluded that limpets marked on December 1989 were around 13-14 months old, and attained scarcely 6.2 mm after 2 years. This means that in the B. rodriguezi community, S. lessmi reaches less than 30”,, of the growth observed on floating substrata within a harbour located at a similar latitude (Bastida et al, 1971). Remarkable differences have also been found in Prltelka vulgata L., in which some populations reached equal or greater sizes in a 3-year period than in other habitats after 8-10 years (Lewis & Bowman, 1975). The increased growth rate observed within the harbour environment may be accounted for by the abundance of phytobenthos and limited trophic competition (Bastida et al.. 1971). The growth equation calculated by these authors should be therefore regarded as describing the potential growth capacity of the species, which is rarely, if ever, attained in natural populations inhabiting the intertidal zone.

Both recapture and translocation experiments demonstrated that growth of S. I<.s,~ot?i is increased in the vicinity of the outfall. After one year, mean size was double than that observed in the clean area, but was still 50y0 lower than the size attained by limpets from Mar de1 Plata harbour (Bastida et al., 197 1). Higher growth rates in zones afl’ected by organic enrichment have been previously reported for Patella vulgcm (Hatton, 1938; Fischer-Piette, 1948) and QI/z~~IUY~(~ pectinafa (L.) (Voss, 1959). Differences in primary productivity are also known to affect growth rates of other intertidal herbivorous gastropods (Underwood, 1984). Similarly, it has been shown that nutrient enrichment due to guano produced by seabird colonies stimulates both primary productivity (Bosman ct al., 1986), and consequently, growth of Putelk g~~~~l~~~fI~is L. in South Africa (Bosman & Hockey, 1988a,b,c). Algal cover and biomass of hcrbi~~orous limpets in regions of upwclling off the Chilean coast were significantly greater than in other regions of Chile where upwelling did not occur (Bosman et al., 1987). Biuc-green algae, diatoms and opportunist, ephemeral chlorophytes such as Clrrdophortr sp. and Etlterornovpha spp. increased their abundance in the vicinity of the outfall (Table 6; L6pez Gappa et al., 1990. 1993). Most of these algae are included in the diet of S. ks.soni, which is composed mainly of diatoms, green (Ijl~/, E}ztero/ncjrl,h~l) and red algae (Bastida et al., 197 1). Feeding habits of S. lessoni arc apparently difrcrent on the Chilean coast, where the main food item is the red alga Iriden hov,~lnn (Setch. et Gardn.) Skottsb. (Jara & Moreno, 1984). Field observations made during the present study confirm the absence of homing behaviour in S. /essoni in exposed areas of the shore, as already reported for this species by other authors (Olivier & Penchaszadeh. 1968). The available evidence suggests that juveniles and small-sized individuals of S. lessom have a very limited home range. In a few cases, we detected some specimens in upshore pools dominated by clvn Iuctuw, several mctres away from their original location; they had presumably been swept away by waves, since distances were too large for normal locomotion. These limpets, as well as specimens experimentally translocated from the mussel community to Ii;. I~~mccr tide-pools (Table 7, Fig. 4), had a significantly faster growth than those which remained among mytilids. A similar colour change to that observed in shells of recaptured S. les.so/li limpets was experimentally obtained in Lotticr asmi (Middendorff) and L. digitalis (Rathkc) by translocatioll of specimens between different substrata (Lindberg & Pearsc, 1990). Preferential predation by oystercatchers on tr~~nsitional ecophenotypes of L. p&a (Rathke) has been mentioned in a recent paper (Sorensen & Lindberg, 1991), and higher mortality rates due to predation of limpets mismatched to their background has also been reported in L. digitalis and L. pelta (Mercurio et al., 1985). S. lessmi shows a characteristic gradient of increasing size towards higher intertidal levels (Olivier & Penchaszadeh, 1968; Vermcij, 1972). Although the present study was not intended to elucidate the factors producing this phenomenon, the decreased growth rates of limpets living at mid-intertidal levels dominated by mytilids can be proposed as one of its causes. The same kind of size gradient in Notoacrne~t petterdi (TenisonWoods) is reportedly related to higher growth rates at upper intertidal levels, where density and intraspecific competition is lower (Creese, 1980). Another mechanism producing size gradients is the gradual and progressive lnigration toward upper levels

during the course of their life (Lewis, 1954; Branch, 1975b; Frank, 1965). Our data suggest that the home range of S. fessoni is fairly restricted. A small proportion of the population, however, may undergo transportation by waves. This passive transportation seems to be more frequent upshore than seaward, but our observations on this subject are insufficient. The influence of the surrounding community in determining the growth rate and mean size of individuals in limpet populations has been pointed out by several authors (Fischer-Piette, 1948; Lewis & Bowman, 1975). Growth of S. lessoni was negligible in areas where available space was mostly monopolized by Brurhidontes rodriguezi. Barnacles, like mytilids, are important occupiers of intertidal primary space and have been freqnelltly reported as producing a decrease in growth rates and mean sizes of limpets (Fischer-Piette, 194X; Lewis & Bowman, 1975; Branch, 1976; Choat, 1977; Thonlpson. 1980; Hawkins & Hartnoll, 1982). The longevity of S. /essoni can only be conservatively estimated as at least 2 years. The extreme variability in growth rate recorded in this study suggests that most estimations of age as a function of size may be unsound. The method of modal displacement in size-frequency distributions could not be employed in the present case. due to remarkable habitat-induced variations as well as low growth rates; although it proved to be useful in previous studies (Underwood, 1975; Crecse, 1981). The phenotypic plasticity of S. lessnni was clearly demonstrated during the translocation experiment. in which individuals rapidly responded to improved conditions of the new habitat. Simiiar results were obtained in reciprocal translocations of Patek g~fl~zz~i{7~i.~ in South Africa (Bosman & Hockey, 1988c). Higher mortality rates in the polluted area were clearly shown during the recapture. translocation and mark loss experiments (Table 4). Mortality was significantly higher around the outfall than in the clean area during autumn and winter, and this fact presumably accounts for the lower densities observed in the former. A negative correlation between growth rate and longevity has been frequently reported in limpets (reviewed in Branch, 1981: pp. 302-304). This correlation was not only found among different species, but also among populations of the same species growing in different habitats, in the case of Patella vulgata (Fischer-Piette, 1948; Lewis & Bowman, 1975; Thompson, 1980). It has been suggested that rapid growth and early sexual maturity may exhaust body reserves, so that any subsequent food shortage would not be tolerated (Branch, 1981). Decreased mean sizes observed in the polluted area in February and April 199 1 (Table 2) suggest differential mortality of the largest specimens. which can bc clearly seen in the size-frequency graphs of limpets translocated from the polluted site to tide-pools and the mussel community (Fig. 4). Lower energetic requirements of smaller individuals could enable them to tolerate food shortages better than adults. as has been reported in another intertidal gastropod (Underwood. 1976). A hypothesis to test in future studies is the possibility that the higher mortality in the polluted area is due to increased predation rates by fish or birds. Important predators are absent in this community (Lopez Gappa et al., 1990), but we have observed groups of gulls (Larus dominicanus Lichtenstein), sheathbills (Chionis albu (Gmelin)) and schools of Mugil lka Valenciennes around the effluent discharge area. Predation by fishes on benthic intertidal organisms seems to be rare in the study area. as well as in

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A. Tahlado et al. ! J. Erp. Mar. Biol. Ecol. I75 (1994~ 21 l-226

other temperate regions (Bertness et al., 198 1). The fact that some species of the genus, such as Siphonaria capensis Q. & G. and S. thersites Carpenter, are not eaten by fishes that usually consume other limpets (Branch & Cherry, 1985; Branch, 1988) is noteworthy. These species are unpalatable (Branch, 1988), presumably because they contain polypropionates, which were also found in S. Iessoni (Capon & Faulkner. 1984). Only a few specimens of S. lessoni have been found among the food items of a common sea anemone at the study area (Zamponi, 1979). In the Chilean intertidal, S. /e.s.ro/~i is included in the diet of the omnivorous fish S?.vc/.ses snrzguineusMtiller & Troschel (Paine & Palmer, 1978). An alternative hypothesis explaining the accelerated growth in the polluted area and also in tide-pools may be a decreased level of intraspecific competition due to lower densities. In several limpet species it has been shown that growth rate, mean size or weight decrease with increasing densities (Jones, 1948; Sutherland, 1970; Branch, 1975a. 1976; Black, 1977; Choat, 1977; Underwood, 1978; Creese, 1980; Ortega, 1985; Fletcher & Creese, 1985; Quinn, 1988). Both a higher primary productivity and a lower intraspecific competition may produce higher growth rates, although the relative importance of these factors could not be assessed in the prcscnt study. Nevertheless, organic enrichment can be regarded as the direct or indirect cause of the enhanced growth rate observed in S. lessorli: in the first case as a consequence of higher primary productivity, and in the second due to changes produced by pollution in removing the interaction of this species with the major space-occupier, the mussel B. rodvigue:i.

Acknowledgements We thank the authorities and staff of the Argentine Museum of Natural Sciences “Bernardino Rivadavia”, Puerto Quequtn Hydrobiological Station and its Supporting Cooperative Association. Technical assistance by Maria Luisa Marin and Claudio Lemus is gratefully acknowledged. Alcurnia S.A. provided the epoxy enamels and Maria Amelia Lluch performed monthly sampling. Nestor Cazzaniga and two anonymous referees made useful comments and Victoria Lichtschein improved the English version ofthe manuscript. This research was supported by a PID grant No. 0351’88 from the National Council of Scientific Research and Technology (CONICET).

References Bastida, R., 4. Capezzani & M.R. Torti, 197 I. Fouling organisms in the port of Mar del Plats (Argentina). 1. Siphonaria lessoni: ecological and biometric aspects. Mar. Biol.. Vol. 10, pp. 297-307. Bertness, M.D., S.D. Garrity & S.C. Lcvings, 1981. Predation pressure and gastropod foraglng: a w>p~caltemperate comparison. Evolution, Vol. 35, pp. 995-1007. Black, R., 1977. Population regulation in the mtertidal limpet Parelloida alticosrara (Angas. 1865). Oecolo~~o (Berlitz), Vol. 30, pp. 9-22. Bosman, A.L., J.T. Du Toit, P.A.R. Hockey & G.M. Branch, 1986. A field experiment demonstratmg the influence of seabird guano on intertidal primary production. Estuar. Coast. Sher Sci., Vol. 23. pp. 2X3294.

Bosman, A.L. & P.A.R. Hockey, 1988a. Life-history patterns of populations of the limpet Putelln g~ffttz{~~t~j~: the dominant roles of food supply and mortality rate. Oecohgiu (Berlin), Vol. 75, pp. 412-4 19. Bosman, A.L. Rr P.A.R. Hockey, 1988b. The intluencc of scabird guano on the biological structure of rocky intertidal communities on islands of the west coast of Southern Africa. S. .4fi. ./. A4nv. Sci., Vol. 7. pp. 61-68. Bosman. A.L. & P.A.R. Hockey, 1988~. The influcncc of primary production rate on the population dynamics of Pcze/lN ~rc~rtu[ari.s, an intertidal limpet. P.S.%.N.l.: Mm. Em/., Vol. 9. pp. 181-198. Bosman, A.L.. P.A.R. Hockey & W.R. Siegfried, 1987. The influence of coastal upwelling on the functional structure of rocky intertidal communities. Oec,ok@fiitri&r/i@. Vol. 72, pp. 226-232. Branch, G.M.. 19753. Intraspecific competition in f’uteI1~~ctjchienr Born. J. Auim Em/.. Vol. 43. pp. X282. Branch, G.M., 1975b. Mechanisms reducing intraspecific competition in Pat& spp.: migration, ditfcrcntiation and territorial behaviour. f. At7irn. Ecd., Vol. 44, pp. 575-600. Branch. G.M.. 1976. Interspecific coxnpetition experienced by South African ~~i~e~1~1 spccics. J. .Initn. Gi~i.. ‘i’ol. 45. pp. 507-529. Branch. G.M.. 1981. The biology of limpets: physical factors, energy flow. and ecological mteractions. &P(oIO~~)..Mnr. Bioi. Apiir. Rev., Vol. 19, pp. 235-380. Branch. G.M., 1988. Activity rhythms in Siphor7trriu rhemira.r. In, Behoviord crdqxrrriwr to intertidd Me. cditcd by G. Chelazzi & M. Vannini, Plenum Press, New York, pp. 27-44. Branch. G.M. & M.I. Cherry, 1985. Activity rhythms of the pulmonatc limpet Siphomrict cupemis 0. 6i G. LISan adaptation to osmotic stress, predation and wave acti0n.J. E.y[). MU. Biol. Ecol.. Vol. 87. pp. 153-16X. Capon. R.J. & D.J. Faulkner, 1984. Mctabolites of the pulmonate S@J/KUINY~O /essorri. J. Or,?. Chrw.. Vol. 49. pp. 25(36-250X. Cheat, J.H.. 1977. The influence of sessile organisms on the population biology of three spccics of acmaeid limpets. .I. Exp. Mar. Biol. EA., Vol. 26, pp. 1-X. Cook, S.B.. 197 1. A study of homing behavior in the limpet ~i~~~~~~t~tu aitenwta. Bioi. Bull.. Vol. lli, pp. 449-457. Crecsc, R.G.. 1980. An analysis of distributi~~ll and abundance of populations of the high-shore limpet. ~~~Jt~ff~nte~~ petrerdi (Tenison-Woods). Oec&& ~Beriirr~, Vol. 45, pp. 252-260. Creesc, R.G.. 1981. Patterns of growth, longevity and recruitment of intertidal limpets in New South W’alcs. ,/. E.yip, M0r. Bi0/. E&.. Vol. 5 1. pp. 145-17 I. Crcese, R.G.. 1982. Distribution and abundance of the acmaeid limpet Pure/l&r lutistri~e~rcr and its intcractions with barnacles. Oecokogicr (Berh,J, Vol. 52, pp. 85-96. Crccsc. R.G. & A.J. Underwood, 1982. Analysis of inter- and intraspecific competition amongst intertidal limpets with dificrcnt methods of feeding. Oecolo@ jBer/iui. Vol. 53. pp. 337-346. Dungan, M.L., 1986. Three-way interactions: barnacles. limpets. and algae in a Sonoran dcscrt rocky intertidal zone. A~Jz. Nat., Vol. 127, pp. 292-316. Fischer-Picttc, E.. 1948. Sur les elements de prosperit& des Patelles ct sur lcur spCcificitC. ./. Cox/tj,i.. Vol. 88. pp. 45-96 Fletcher, VV.J. & R.G. Creese. 1985. Competitive interactions between co-occurring herbivorous gastropods. :ittrr. &ill.. Vol. X6, pp. 183-191. Frank. P.W.. 1965. The biod~mog~~phy of an intertidal snail population. Ecoi<>gr, Vol. 46, pp. X3 l-844. Garrity. S.D. C S.C. Levings, 1983. Homing to scars as a dcfonse against predators in the pulmonute iinpet S@/~OIZN~~N &~s (Gastropoda). ;Mur. Bioi., Vol. 72, pp. 3 1Y-324. Hatton. H., 1938. Essais de bionomie explicative sur quelques especes intcrcotidales d’algucs ct d’animaux. A/?rll.\. Imt. O~~earwgr. .~onaco,Vol. 17, pp. 24 l-348. Hawkins, S.J. & R.G. Hartnoll, 1982. The influence of barnacle cover on the numbers, growth and behaviour of PcrteNu wlgmt on a vertical pier. J. Mar. Biol. Ass. U.K., Vol. 62. pp. 855-867. Hulings, N.C., 1985. Activity patterns and homing in two intertidal limpets, Jordan Gulf of Aqabn. Xmtrh. Vol. 99, pp. 75-80. Jara H.F. & C.A. Moreno, 1984. Herbivory and structure in a midlittoral rocky community: a case in southern Chile. Ecology, Vol. 65, pp. 28-38. Jones, N.S., 1948. Observations and experiments on the biology of Pmelk vztlgutcrat Port St. Mary. Isle of Man. Prtrc. 7’mn.r. Liverpoof Bioi. SK.. Vol. 56, pp. 60-77.

226

A. Tahlado et al. i J. Ewp. Mar. Biol. Ecol. 175 11994) 21 l-226

Lewis, J.R., 1954. Observations on a high-level population of limpets. J. Anim. Ecol., Vol. 23. pp. 85-100. Lewis, J.R. & R.S. Bowman, 1975. Local habitat-induced variations in the population dynamics of PareNo vulgatu L. J. Exp. Mar. Biol. Ecol., Vol. 17, pp. 165-203. Lindberg, D.R. & J.S. Pearse, 1990. Experimental manipulation of shell color and morphology of the limpets Lottia asmi (Middendortf) and Lottia digifalis (Rathke) (Mollusca: Patellogastropoda). J. Eup. Mar. Biol. Ecol.. Vol. 140, pp. 173-185. Littler, M.M. & S.N. Murray, 1975. Impact of sewage on the distribution. abundance and community structure of rocky intertidal macro-organisms. Mar. Biol., Vol. 30, pp. 277-291. Littler. M.M. & S.N. Murray, 1978. Influence of domestic wastes on energetic pathways in rocky intertidal communities. J. Appl. Ecol., Vol. 15, pp. 583-595. L6pcr Gappa, J.J., A. Tablado & N.H. Magaldi, 1990. Influence of sewage pollution on a rocky intertidal community dominated by the mytilid Brachidontes rodrigur;i. Mar. Ecol. Prog. Ser., Vol. 63, pp. 163- 175. Lopez Gappa, J.J., A. Tablado & N.H. Magaldi, 1993. Seasonal changes in an intertidal community afTcctcd by sewage pollution. Environ. Pollut., Vol. 82, pp. 157-165. Mercurio, K.S., A.R. Palmer & R.B. Lowell, 1985. Predator-mediated microhabitat partitioning by two species of visually cryptic, intertidal limpets. Ecolog_r,, Vol. 66. pp. 1417-1425. Murray, S.N. & M.M. Littler, 1978. Patterns of algal succession in a perturbated marine intertidal ccimmunit). J. Phwol., Vol. 14, pp. 506-512. Olivier, S.R. & P.E. Pcnchaszadch, 1968. Observaciones sobre la ecologia y biologia de Siphowria (Pw/IA..xiphonuriaj lessoni (Blainville, 1824) (Gastropoda. Siphonariidae) en el litoral rocoso de Mar dcl Plats (Buenos Aires). Cah. Biol. Mar., Vol. 9, pp. 469-491. Ortega. S.. 1985. Competitive interactions among tropical intertrdal limpets. .I. Etp. Mur. Biol. Ecol., Vol. 90, pp. I l-25. Paine, R.T. & A.R. Palmer, 1978. SicJ.crse.7 .tcmguineus: il unique trophic generalist from the Chilean intcrtidal zone. Copeia, Vol. 1978, pp. 75-81. Quinn. G.P., 1988. Ecology of the intertidal pulmonate limpet Siphonaricr diernenensrc Quo) ct Gaimnrd. I. Population dynamics and availability of food. J. Eup. Mu. Biol. Ecol., Vol. 117, pp. 115-136. Sokal, R.R. & F.J. Rohlf, 1981. Biometry. Second edition. W.H. Freeman & Co., San Francisco. 859 pp. Sorensen. F.E. & D.R. Lindberg, 1991. Preferential predation by American black oystercatchers on transitional ecophenotypes of the limpet Lnttia pelta (Rathkc). J. E\p. Mar. Biol. Eu~l.. Vol. 154, pp 123136. Sutherland, J.P., 1970. Dynamics of high and low populations of the limpet. Acnww rcuhnr (Gould). Eeol. Morwgr.. Vol. 40. pp. 169-188. Thomas. R.F., 1973. Homing behavior and movement rhythms in the pulmonate limpet, Siphorwrrr~ pectiwrtr Linnaeus. Pm. Malac. SK. Land., Vol. 40, pp. 303-31 1. Thompson, G.B., 1980. Distribution and population dynamics of the limpet Prrtellu vulgurrr L. in Bantry Bay. J. Ewp. Mu. Biol. Ecol.. Vol. 45. pp. 173-217. Underwood. A.J.. 1975. Comparative studies on the biology of j%‘eriraufranwntom Reeve. Be~~~hicium~UU~UIII (Lamarck) and Cellana tramoserica (Sowerby) (Gastropoda: Prosobranchia) in SE. Australia. ./. E\/I. Mu. Biol. Ecol., Vol. 18, pp. 153-172. Underwood. A.J., 1976. Food competition between agc-classes in the intertidal neritaccan :C’erirtl~mmnemm Reeve (Gastropoda: Prosobranchia). ./. E.\-l,. Mar. Bwl. Ewl.. Vol. 23, pp. 145-154. Underwood. A.J., 1978. An experimental evaluation of competition between three species of intertidal prosobranch gastropods. Oecologia iBrrlini, Vol. 33, pp. 185-202. Underwood, A.J., 1984. Vertical and seasonal patterns in competition for microalgac bctwccn mtcrtidal gastropods. Oecok~gicr iBerliuj, Vol. 64, pp. 21 l-222. Vcrdcrbcr. G.W.. S.B. Cook & C.B. Cook, 1983. The role of the home scar in reducing water loss during aerial exposure of the pulmonate limpet S@honaria nlrenuta (Say). Veliger, Vol. 25. pp. 235-333. Vermcrj. G.J.. 1972. Intraspecific shore-level size gradients in intertidal molluscs. Ecok~~~~..Vol. 53. pp. 693700. Voss, N.A., 1959. Studies on the pulmonate gastropod Siphonuria pectimta (Linnaeus) from the southeast coast of Florida. Bull. Mar. Sci. Czdf Curihh., Vol. 9. pp. 84-99. Zamponi, M.O., 1979. Sobre la alimentacihn cn Actiniaria (Coclcnterata Anthozoa). .‘Veowo>/wc/.Vol. 25. pp. 195-200.