Ecology of the intertidal pulmonate limpet Siphonaria diemenensis Quoy et Gaimard. I. Population dynamics and availability of food

115

J. Eq. Mar. B&l. .&of., 1988, Vol. 117, pp. 115-136 Elsevier

JEM 01047

Ecology of the intertidal pulmonate limpet Siphonaria diemenensis Quoy et Gaimard. I. Population dynamics and av~labi~ty of food G.P. Quinn Department

ofZoology. Univerdy of Me&oume,

Parkville, Victoria, Australia

(Received 1I August 1987; revision received 5 January 1988; accepted 8 January 1988) Abstract: Seasonal variations in the size structure, patterns of growth and mortality of the intertidal pulmonate limpet Siphonaria diemenensis Quoy et Gaimard were examined in two zones on a rocky intertidal shore. Food supply in the upper zone (Zone 1) showed strong seasonal variation whereas in the lower zone (Zone 2) food supply was more constant. Limpets in Zone 2 were larger, grew faster, and had smaller annual adult mortality rates than those in Zone 1. In Zone 1, reduced growth and increased mortality were correlated with the seasonal reduction in food supply. Field experiments demonstrated that the availability of food, particularly in Zone 1, was a major determinant of growth rate. Starvation was a likely cause of the great seasonal mortality in Zone 1, and the growth of shell and tissue were variable characteristics in these Iimpets, changing quickly in response to changes in food supply. Key words: Food availability; Growth; Intraspecific variation; Mortality; Siphonaria diemenensis; Starvation

&IXODUCTION

Intraspecific differences in demography and life history among populations of intertidal gastropods have been documented, on different shores (Frank, 1975; Roberts & Hughes, 1980) and within one shore (Sutherland, 1970; Fletcher, 1984; Moran et al., 1984). These studies are useful in examining the factors that might influence pop~ation dynamics, particularly in the case of species with planktonic larvae which can be dispersed over some distance and for which genetic variations are unlikely to explain intraspecific differences in demography from place to place. Variations in the av~ab~ty of food have often been inferred as a cause of differences in the structure and dynamics of populations of intertidal herbivorous gastropods (e.g., Paine, 1969; Sutherland, 1970; Fletcher, 1984). The amount of food available can be assessed by measuring the abundance of macroflora or microflora known or assumed to be part of the diet of these organisms {e.g., Underwood, 1984a; MacLulich, 1986). Seasonal and spatial variations in algal abundance have been used to exphrin aspects of behaviour (MacKay & Underwood, 1977; but see Underwood, 1988), morphology (Underwood & Creese, 1976) and population dynamics (Sutherland, 1970; Black et al., Correspondence address: G. P. Quinn, School of Biological Sciences, Carslaw Building, F07, University of Sydney, Sydney, New South Wales 2006, Australia. 0022-0981/88/$03.50 0 1988 Elsevier Science Publishers B.V. (Biomedical Division)

116

G.P.QUINN

1979; Creese, 1980; Parry, 1982) of intertidal gastropods. Underwood (1984a) showed that microalgal abundances on a rocky shore vary both spatially and seasonally, and the growth rate of at least one species of grazing gastropod was positively correlated with algal abundance (Underwood, 1984b). Comparisons of the degree of intraspecific competition for food can provide another estimate of differences in food availability - the greater the intensity of competition between individuals, the smaller the relative availability of food. Studies on intraspecific competition in gastropods in one area of the shore have often demonstrated that, at greater densities of grazers, growth is reduced and/or mortality is increased (see reviews by Branch, 1981, 1984; Hawkins & Hartnoll, 1983). Other workers have shown that the degree of intraspecific competition varies between different areas on one shore (Creese, 1980; Underwood, 1976; 1984~; Fletcher & Creese, 1985) and between different times of the year (Parry, 1982; Underwood, 1984c), although Underwood (1978) showed that the effect of increased density on tissue weights of grazing gastropods was similar at two times of the year. In this study, the population dynamics of the marine pulmonate gastropod Siphonaria diemenensis Quoy et Gaimard were examined at two different tidal heights on a rocky intertidal shore. The aim was to quantify seasonal and spatial changes in size structure, growth and mortality of, and availability of food to, S. diemenensis. Experiments in the field were used to determine the importance of various factors, particularly availability of food, in influencing the population dynamics of this species. Despite the large amount of information available on intertidal limpets (Branch, 1981), little work has been done on the population dynamics of Siphonaria. Olivier & Penchaszadeh (1968) and Black (1979) have examined the patterns of vertical distribution in S. lessoni and S. kurracheensis, respectively, and Ortega (1985) studied the effects of competition on S. gigas. Creese (1978, 198 1) compared the population dynamics of a number of species of prosobranch and pulmonate limpets in New South Wales, including S. denticulata and S. virgulata, and Creese & Underwood (1982) examined intraspecific and interspecific competition in these two species. Parry (1977) provided preliminary data on the dynamics of a population of S. diemenensis near the site of the present study.

MATERIALS STUDY

AND

METHODS

SITE

The rocky intertidal shore at Griffith Point, San Remo, Victoria, Australia, was used in this study. This shore has been described in detail by Parry (1982), and the present work was done in two zones on the more exposed southerly facing “ocean beach” (Parry, 1982). Zone 1, which represented the typical habitat of S. diemenensis atGrifIith Point, was a gently sloping section of the shore composed of grey feldspathic sandstone. It was defined as extending from the seaward edge of the rock platform (0.3 m above

POPULATION

DYNAMICS

OF SIPHONARIA

DIEMENENSIS

117

Chart Datum, CD) ~25 m up the shore to the lower limit of the grazing gastropods Bembicium nanum (Lamarck) and Austrocochlea constricta (Lamarck) (0.8 m above CD). The total area was % 300 m2. S. diemenensis occur in this zone at densities of up to 1000 * m - 2. The limpets Cellunu trumosericu (Sowerby) ( < 10 . m - 2, and Putelfoidu ulticostutu (Angas) (~2 * me2) are the only other common grazers. Three sites (1A - 0.396 m2, 1B - 1.205 m2, 1C - 1.545 m’), each 0.6 m above CD and surrounded by water tilled crevices which prevented movement of limpets in or out, were chosen for detailed study of S. diemenensis. Below the edge of the rock platform was an extensive boulder field of a variety of rock types. Some of these boulders, composed of a coarse granitic sandstone, had populations of S. diemenensis markedly different from those in Zone 1 and were designated Zone 2. Two of these boulders (Site 2A - 0.546 m2, Site 2B - 0.745 m’) were completely separate from other boulders, thus preventing the migration of limpets in or out. These were chosen for detailed study of S. diemenensis. The short period of emersion of Zone 2 during low tide prevented the use of more sites. Sites 2A and 2B were 0.5 and 0.4 m, respectively, below the level of Sites lA, 1B and 1C. As in Zone 1, C. trumosericu and P. ulticostutu were the only other grazers present in Zone 2 but both were uncommon.

POPULATION

DYNAMICS

The sizes of all individuals of S. diemenensis on each study site in each zone were measured to the nearest 0.1 mm with vernier calipers every 2 months from October 1979 to February 1981 and then at intervals of 2 to 4 months until December 198 1. Size-frequency distributions were constructed for each study site for each census date. Cohorts were extracted, and the numbers of individuals in, and mean size of, each cohort calculated, using Underwood’s (1975) probit modification of Cassie’s (1954) graphical method. Data were only used from cohorts, usually recruit and adult cohorts, that were clearly distinguishable in the size-frequency distributions. Mortality rates were determined for cohorts to which recruitment had ceased. Linear regressions of logarithm (base 10) of cohort numbers against time (months) were calculated for each study site in each zone and the slopes of these regressions provided instantaneous mortality rates (deaths * individual- ’ * month- ‘). Seasonal variations in mortality rates were determined by calculating instantaneous mortality rates between successive census dates. Annual mortality rates were calculated as both instantaneous mortality rates and percent mortality for a 12-month period. Growth rates (mm - month - ‘) were determined from the change through time of the mean size of each cohort on each study site. Also, limpets were marked individually in each zone with either a plastic tag and epoxy resin or with a marine paint and were measured to the nearest 0.1 mm every 2 months between January and August 1981. The very wet conditions and the thick covering of algae on the shells of the limpets after August caused many labels to be lost and prevented marking of new individuals.

118

G. P. QUINN

Growth rates (mm * month- ‘) were calculated for the marked individuals in each zone for the following periods in 1981: January-March (summer), March-May (aut~n) and May-July/A~st (winter). At monthly intervals between September 1979 and June 1981,20-25 S. diemenensis were collected from each zone, the shell length of each was measured, and the soft tissue dried at 55 “C and weighed to the nearest 0.01 mg. Linear regressions of logarithm (base 10) of dry tissue weight (g) against shell length (mm) were calculated for each sample date in each zone. AVAILABILITY

OF FOOD

The gut contents (stomach and intestine) of at least 10 actively feeding S. diemenensis collected from each zone in winter and summer over 2 yr were qualitatively examined. Algal abundance was estimated from colour photo~aphs of a permanently marked 0.25-m2 quadrat within each study site in each zone taken at monthly intervals from December 1979 to December 198 1. The percent covers of ah species of macroalgae were determined from the photographs using an image analyser (MOP 3, Carl Zeiss). EXPERIMENTS

Experiments which involved enclosing limpets used 15 x 15-cm fences (2 cm high) constructed of woven stainless steel mesh (20 gauge, 3 mesh * cm- ‘) attached to the substratum with screws inserted into Raw1 plugs. All resident limpets were removed from these areas before the experimental limpets were added. At 2-wk intervals during any experiment, the numbers of surviving limpets in each enclosure were counted and missing limpets were replaced by paint-marked individuals of similar size. These marked limpets were used solely to maintain experimental densities and were not used in the analysis.

An experiment was done to examine seasonal variations in intraspecific competition and the importance of starvation as a potential cause of mortality of S. diemenensis. Adult limpets from each zone (Zone 1: 9.5-10.4 mm; Zone 2: 19.5-20.4 mm) were enclosed within fences for 137 days between August and December 1980 (~ter/sp~ng) and then again (with new limpets) for 142 days between December 1980 and May 198 1 (summer/autumn). Experimental densities were 8, 15 (approximate natural biomass), 30 and 45 limpets per enclosure in Zone 1. In Zone 2, densities of 6 (approximate natural biomass), 12, and 24 limpets per enclosure were used. Three experimental areas, separate from the study sites, were chosen within each zone on the basis that each area possessed a uniform to~~aphy suitable for the erection of enclosures, and had an algal cover and composition representative of the zone. Each density was represented once in each area. In Zone 1, the same areas were used in both

POPULATION DYNAMICS OF SZPHONARZA

DZEMENENSZS

119

experimental periods, but the location of fenced enclosures within each area was changed. In Zone 2, the small size of boulders required that new areas be chosen for the second experimental period. All enclosures in each zone were covered by a 40 x 40 cm galvanized mesh (1 mesh +cm- ‘) cage to exclude predators. Predation could therefore not confound any conclusions drawn about density-dependent mortality in this experiment. At the end of each experimental period, five randomly chosen original individuals in each enclosure were collected, their shell lengths measured, their soft tissues dried at 55 ‘C and weighed to the nearest 0.01 mg. Instantaneous mortality rates, calculated from the slope of the regression of log density against time, were determined for each enclosure. Reduction of amount of food The effects of a reduced amount of food on growth of shell and tissue of S. diemenensis were examined experimentally in Zone 1. Fifteen adult limpets (9.5-10.4 mm) were placed within enclosures in two treatments: an area of substratum that had a natural cover of macroscopic algae, and a similar area of substratum from which all algae were removed with a wire brush. The reestablishment of algae within the latter treatment was prevented by rescraping (carefully avoiding damage to the limpets) every 2 wk. The experiment ran for 171 days between June and November 198 1 and there were four replicate enclosures for each treatment; original limpets from a fifth enclosure of each treatment were used to replace missing limpets (the density of limpets in this enclosure was maintained using limpets of similar size collected from Zone 1 and marked with paint), so all limpets in the four replicates were kept under the same conditions for the duration of the experiment. At the end of the experiment, live randomly chosen limpets from each of the four replicate enclosures in each treatment were collected, their shell lengths were measured, and their soft tissues dried at 55 “C and weighed to the nearest 0.01 mg. Transplants between zones A transplant experiment was done to separate the effects of local environmental differences and intrinsic genetic differences on shell growth of S. diemenensis. Limpets of 6.0-7.0 mm in shell length (the smallest that could be enclosed) were collected from each zone. Half (randomly chosen) were translocated into fenced enclosures in their zone of origin (controls) and half were transplanted into fenced enclosures in the other zone (transplants). Fine fly-screen mesh (10 mesh - cm- ‘) was attached to the fence walls to improve enclosure of these small limpets. An experimental density of 15 limpets per enclosure was used, there were two replicate enclosures of each treatment (Zone 1, Zone 1 + 2, Zone 2, Zone 2 --+l), and the experiment was run for 90 days between March and June 198 1 (“autumn”) and repeated for 90 days (with new limpets) between August and November 198 1 (“spring”). The shell lengths of all limpets in each enclosure were measured at the end of each experimental period.

120

G. P. QUINN

RESULTS POPULATIONDYNAMICS The size-frequency distributions for Sites 1C (Sites 1A and 1B were similar) and 2B (Site 2A was similar), using August 1980 (2-3 months after peak recruitment) and March 1981(9-10 months after peak remitment) as examples, are presented in Fig. 1. Adult individuals of 5’. diemenensisattained a much larger size (> 20 mm) on study sites in Zone 2 than did those on the study sites in Zone 1 (< 15 mm), and this pattern was consistent between seasons. Seasonal instantaneous mortality rates could be determined for the adult cohort in Zone 1 from October 1979 to February 1980 (excluding 1979 recruits), from December

r

400-

SITE1C AUG 1980 l7-

200-

SITE 28 AUG 1980

60-

SITE 2 B MAR1981

30-

10 SHELL

20 LENGTH (mm)

30

Fig. 1. Size-frequency distributions of S. diemenensison Sites 1C and 2B in August 1980 and March 1981.

POPULATION DYNAMICS OF SIP~O~~~~

DI~~E~~~SZS

121

TABLE I

Seasonal instantaneous mortality rates (deaths. individual - ’ . month - ’ x lo- 3, of S. diemenensis in Zone 1 and 2 from October 1979 to December 1981. Sites lA, B, C: * excluding 1979 recruits; remainder excluding 1980 recruits; * excluding 1981 recruits. Sites 2A, B: s excluding 1979 and 1980 recruits; remainder excluding 1980 and 1981 recruits. NLD, cohort no longer distinguishable. Site

Period

2A

2B

24.5* 65.2* 50.2

13.4s 12.1r 26.7

24.5” 8.9”

NLI)*

46.9”

27.5 7.9

28.9 27.4’ 4.6 2.4’ 19.3 - 12.8’ 3.7

11.5” 20.4 25.7s 2.1 44.99 26.4 _ 19.61 11.9

NLDl

NLDl

IA

1B

1C

7.4* 45.0* 23.5

Ott-Dee 1979 Dee 1979Feb 1980 Feb-Apr 1980

NLD*

Apr-Jun

1980

37.4 38.1

- 12.3* 48.8* 8.8 32.9* 21.8 26.3

Jun-Aug

1980

32.8

39.1

14.9

Aug-Ott

1980

18.7

13.6

35.8

Ott-Dee

1980

19.4

17.6

37.4

Dee 1980Feb 1981 Feb-May 1981 May-Jul 1981 Jul-Nov 1981 Nov-Dee 1981

15.2 16.2X 50.1 18.5” 13.3” 15.9” 12.6”

102.7 55.4* 80.1 44.4” - 6.2* 13.3” 24.6+

75.6 49.1” NLD

0.0” 31.5” -5.1” 19.8”

16.3 11.0

15.2 21.7

26.2

15.6

23.1 5.6 44.6

55.9 7.8 NLD

1979 to February 1981 (excluding 1980 recruits) and from December 1980 to December 1981 (excluding 198 1 recruits). Table I shows that mortality rates on all study sites in Zone 1 were generally greatest in summer and autumn (December-May) and least in winter and spring (June-November). Because the juvenile cohorts could be separated for longer periods after recruitment in Zone 2, mortality rates were determined for different periods of time in this zone compared with Zone 1 and more than one adult (i.e., non-remit) cohort.was often present. Mortality rates were determined for the adult cohort between October 1979 and December 1980 (excluding 1979 and 1980 recruits) and between February 1980 and December 1981 (excluding 1980 and 1981 recruits). No clear seasonal trends in mortality rates were apparent on either study site in Zone 2 (Table I), except that the greatest mortality was in winter on Site 2B in 1980 (June-August) and 1981 (May-July). Negative mortality rates of adults (Table I) represent inaccuracies in the separation of the recruit cohort in the size-frequency distributions. Annual mortality rates of adults on the study sites in Zone 1 were greater in 1980 than in 198 1 (Table II). In Zone 2, annual adult mortality was slightly greater in 198 1 (i.e.,

122

G.P. QUINN TABLE

II

Mean annual mortality rates ( + SD) of adult cohorts of S. ~~e~ene~ in each zone; * indicates “equivafent” cohorts (i.e., excluding 1980 recruits) appropriate for comparison between zones. Area

Period

Annual mortality rate Instantaneous (deaths &individual- ’ . month- r)

Zone 1 study sites

Dee 79-Dee 80 (excluding 80 recruits)

Zcne 1 study sites

Dee 80-Dee 81 (excluding 81 recruits)

Zone 2 study sites

Ott 79-Ott 80 (excluding 79, 80 recruits)

Zone 2 study sites

Dee 79 (ZA)/Feb 80 f2B) -Dee 80 (excluding 80 recruits) Ott 80-Nov 81 (excluding 80, 81 recruits)

0.0264* * 0.0034 n=3 0.0170 f 0.0029 n=3

Zone 2 study sites

0.0177 f 0.0004 n=2 0.0157* + 0.0~6 n=2 0.0191 it:0.0027 ?I=2

Percentage (%) 53.40* f 7.12 n=3 39.59 + 6.89 n=3

33.64 f 0.27 n=2

34,83* f 6.01 ?l=2 39.16 f 4.49 n=2

October 1980-November 1981) than in 1980 (i.e., October 1979-October 1980). The most approp~ate comparison of annual mortality rates between zones involves adults in 1980 (including the 1979 recruits) from each zone. This showed a significantly greater mortality rate in Zone 1 (Table II: t test, P < 0.05). The adult cohorts on the study sites in Zone 1 grew at 0.05 mm - month - ’ between June and December 1980 but growth was very slow from then until February or May 198 1 ( < 0.01 mm * month - ‘). The fastest growth rates of adult cohorts on the study sites in Zone 2 were in autumn and winter (April-August 1980,0.4-0.6 mm - month - * ; May-July 1981, 0.5-1.0 mm.month-‘). Linear regressions of growth increment (mm - month- ‘) against initial size (mm) of marked limpets in each zone for summer, autumn and winter were compared (nonlinear regressions, e.g., log-linear or log-log, did not improve the tit to the data). The slopes and intercepts of the seasonal regressions in Zone 1 were significantly different (ANCOVA; slopes: F = 10.3, df = 2,165, P < 0.001; intercepts: F = 14.9, df = 2,167, P < 0.001). The predicted growth rates of &mm and lo-mm individuals in Zone 1 were four times greater in winter than in summer (Table III). Only the intercepts of the seasonal regressions in Zone 2 were si~~c~tiy different (ANCOVA; slopes: F = 1.2, df = 2,183, NS; intercepts; F = 5.1, df = 2,185, P < 0.01). The predicted growth rates of lo- and 20-mm individuals in Zone 2 were greater in winter than in summer (Table III), although the difference for IO-mm limpets was less than for Zone 1. The predicted growth rates of lo-mm limpets were much greater in Zone 2 than in Zone 1 in all three seasons.

POPULA~ON

DYNAMICS OF S~PHOMA~A TABLE

~IE~ENE~S~S

123

III

Predicted size-specific growth rates of S. diemenensk calculated from regressions of growth rate against initial size for marked individuals in each zone. Growth rate (mm . month - ‘)

Season

Zone 1

Summer Autumn Winter

Zone 2

6mm

10 mm

10 mm

20 mm

0.20 0.38 0.73

0.04 0.09 0.19

0.59 0.56 0.64

- 0.07 0.11 0.19

The mean sizes of cohorts and the size-specific growth rates calculated from the data for marked individuals from January 1981 to July/August 1981 were used to construct approximate size-age relationships for S. d~rne~~i~, starting with the 1980 recruits in Zone 1 and the 1979 recruits in Zone 2. Most recruitment occurred in June each year in both zones (Quinn, 1985). These relationships were based on the assumption that the growth rates of cohorts were similar between years, and therefore that the curves in Fig. 2 represent continuous growth of individuals. Limpets in each zone grew at approximately the same rate for the first 12 months after recruitment. The m~um mean size of the cohort of adults in Zone 1 was reached at the start of summer in December (Fig. 2), 18 months after first recruitment. Mortality rates were greatest during summer and autumn in each year (Table I), and cohorts of adults disappeared from the sue-fr~uency dis~butions during these seasons. Thus, the average longevity of S. diemenensis in Zone 1 is probably between 18 months and 2 yr. The maximum mean sizes of the cohorts of adults on Sites 2A and 2B were reached between 3 and 4 yr after first recruitment (Fig. 2). As there were no clear seasonal trends in mortality (Table I), and there was no seasonal disappearance of cohorts of adults from the size-frequency distributions on either site, the average longevity of S. diemenensis in Zone 2 is difficult to estimate. It was, however, likely to be at least 3 to 4 yr; and the comparison of the annual mortality rates of the “equivalent” cohorts in Zone 1 and Zone 2 in 1980 (Table II) suggests that the longevity of S. diemene~i~ would be considerably greater in Zone 2 than in Zone 1. The predicted tissue weights of adult S. diemenensis (10 mm in Zone 1 and 20 mm in Zone 2), from the monthly regressions of log tissue weight against log shell length, showed strong seasonal variation (Fig. 3). Maximum tissue weights in both zones were found in spring (October) and minimum values in autumn (April), representing the beginning and end, respectively, of the egg mass laying period in both zones (Quinn, 1988).

124

G. I’. QUINN

f

i 1

2

3

4

YEARS

Fig. 2. Size-age relationships of S. diemenemh estimated from mean shell length (+ SD) on Site 1C in (Sites 1A and IB were very similar to 1C) iu Zone 1 and on Sites 2A (,--------) and 2B (-) Zone 2. Zone I: 0 1980 recruits, 0 predicted from 1981 marked limpets, c] 1981 adults; Zone 2: 0 1979 recruits, 0 predicted from 1981 marked limpets, 0 1981 adults, + predicted from previous 2 months rate (Site 2A only).

AVAILABILITY OF FOOD

The macroflora in both zones was dominated by encrusting brown algae, the most common species in both zones being Ralfsia verrucosa (Aresch) J. Ag., with R. clavata (Harvey) Crouan and Pseudolithoderma sp. also present. The foliose alga Scytosiphon iomentaria (Lyngb.) J. Ag. was abundant in Zone 1 in spring and the crust in Zone 2 contained considerable amounts of blue-green algae (e.g., Ca~uth~x sp.). The guts of S. diemenensis from each zone primarily contained pieces of encrusting brown algae, although only R. verrucosu was positively identified in the guts examined. Individuals

POPULATION DYNAMICS OF SIP~ONA~A

if

u

.lOO-

E

.080-

~IEMENENSIS

ZONE

1

ZONE

2

125

P

1

0 4

.060-

-04’’ ‘0’ 1979

’ 'J ’ ’ 'A' ’ 'J ’ ’ ‘6 ’ 'J ’ 1980

’

‘A 1981

t #

Fig. 3. Predicted dry tissue weights ( f SE) of S. dhnenensir from September 1979 to June 1981 for Zone 1 (lo-mm individuals) and Zone 2 (20~mm individuals).

in Zone 1 collected in the vicinity of S. lomentaria usually had large pieces of this alga in their guts; pieces of blue-green algae (Calothrix sp.) were common in the brown crust in the guts of individuals from Zone 2. A marked seasonal trend in the percent cover of encrusting algae in each study site in Zone 1 is apparent (Fig, 4) with the turn cover of algae in summer (January to March) and the maximum in spring (August to December), a pattern representative of the whole zone. S. lomentaria was present on Sites 1A and 1B from August to December 1980. In contrast, there was no seasonal difference in algal cover on the two study sites in Zone 2; both had 100% cover of encrusting brown algae at all times of the year, typical of the whole zone,

G.P. QUINN

126

1980

1981

Fig. 4. Percent cover of encrusting algae on three study sites in Zone 1 from December 1979 to December indicates S. lomentaria present in Zone 1. 1981; 0 Site lA, A Site lB, 0 Site 1C; I

EXPERIMENTS

Manipulationof adult density The loss of limpets in both zones early in each experimental period was small, and was unlikely to have been related to declining tissue weights. Therefore, the instantaneous mortality rate was calculated over the last 11 wk of each experimental period. The decline in the numbers of limpets within each enclosure was constant during this time. The data from each zone were analysed with a two-factor ANOVA (Period and Density both fwed), with each area as a replicate. In Zone 1, the mortality rate increased with density only in summer/autumn (Density x Period interaction; F = 10.9, df = 3,16, P < 0.01) and in Zone 2, mortality was significantly greater in summer/autumn (square root-transformed data; Period: F = 5.5, df = 1,12, P < 0.05; Density: F = 0.9, df = 2,12, NS; Density x Period interaction: F = 2.4, df = 2,12, NS). Dry tissue weights from each zone were analysed with three-factor ANOVAs (Density, Period, and Area). In Zone 1, Density and Period were fvred and Area was random; in Zone 2, Density and Period were fved and Area was random and nested within Period. Tissue weights in Zone 1 were significantly smaller at the end of summer/autumn than winter/spring (Fig. 5, Table IV) and the effect of density varied spatially in each zone (significant Density x Area interaction, Table IV). The interaction between Period and Density was not significant; but, because Area was a random factor, the test of this intera~~on had only 3 and 6 df and was not very powerful. It is apparent from Fig. 5 that the decline in tissue weight with increasing density was greater in summer/autumri than in winter/spring. Tissue weights in Zone 2 were also significantly smaller in summer/autumn than in winter/spring (Fig. 5, Table IV - Period significant) but, in contrast to Zone 1, the decline in tissue weight with increasing density was similar in both experimental periods (Fig. 5, Table IV).

POPULATION DYNAMICS OF SIPHONARIA DIEMENENSIS

127

.020-

.015-

1

ZONE

1

3 5 : 3 3 .OlOz F & CJ .005-

i

45

.lOO-

ZONE

2

38 !z

.080-

i? 3 s.

060-

3 = & cl

4 .040-

11

f 12

6 NUMBER

PER

t

24

ENCLOSURE

Fig. 5. Mean dry tissue weight ( f SD, n = 5) of S. diemenensis at end of each experimental period for Zone 1 and 2; closed symbols for winter/spring and open symbols for summer/autumn; difkrent symbols represent different experimental areas.

The relations~p between the rate of mortality and mean dry tissue weight of limpets from each enclosure was also examined. There was a significant negative correlation between mean dry tissue weight and the instantaneous mortality rate of limpets from enclosures in Zone 1 (Fig. 6; Spearman rank correlation coefficient, r, = - 0.68, df = 22, P < 0.001). It appears that mortaIity may occur when dry tissue weight drops below 0.01 g for 5’. diemenensisof 10 mm shell length (the starting size of limpets in the

df

1 3 2 3 2 6 6 96

Source

Period (P) Density (D) Area (A) PxD PxA DxA PxDxA Residual

31.6 8.1 6.6 1.2 0.7 0.8 0.6 0.3

Zone 1

51.9 10.5 23.1 1.9 2.6 2.7 2.1

F

NS

<0.05

NS

NS

<0.05 to.01
P

Period (P) Density (D) Area w/i P PxD A w/i P x D Residual

Source

1 2 4 2 8 72

df

63.2 30.1 2.9 3.9 3.1 0.6

Zone 2

21.4 9.1 5.0 1.3 5.3

F

< 0.001

NS

< 0.01 to.01 to.01

P

ANOVAs of dry tissue weight of S. diemenensis in Zone 1 and 2 at end of experiment in which adult density was manipulated at two times of year (w/i, within; df, degrees of freedom; MS, mean square; F, F ratio; P, probability).

TABLE IV

POPULATION DYNAMICS OF SIPHONARIA DIEMENENSIS

129

I

ZONE

0

1

1

?

0

a l* n

Ab

L

0

.ob5 5

0.15-

5 ZONE

$

2

0

s 0 Ly O.lOz 2

A

f !iJ

Z -

0

0.050

A

.020

.040

.060

.080

DRY TISSUE

.120

.lOO

WEIGHT

Fig. 6. Relationship between instantaneous mortality rate, over last dry tissue weight (see Fig. 5) of S. diemenensb at end of each period, combination in Zone 1 and 2; symbols as in Fig. 5; dotted line S. diemenensir of shell lengths 10 mm in Zone 1 and 20 mm in Zone * represents loss of one limpet Erom enclosure

.140

(g)

11 wk of each experimental period, and for each experimental area and density represents minimum tissue weight of 2 (see Fig. 3). In Zone 1, point marked with eight limpets.

experiment in Zone 1). The minimum dry tissue weights of adult limpets in Zone 1 (10 mm) in autumn (Fig. 3) were as small as those correlated with mortality in experimental enclosures (Fig. 6). There was no significant correlation between the mean dry tissue weight and the instantaneous mortality rate of limpets from enclosures in Zone 2 (Fig. 6; r, = - 0.36, df = 16, NS).

130

G.P. QUINN

Reduction of amount of food These data were analysed with two factor ANOVAs, Enclosures nested within Treatment (Table V). ~~0~ there was si~~c~t variation between replicate enclosures, the shell lengths and dry tissue weights of S. diemenensis at the end of the experiment were significantly greater in the normal food treatment than iu the reduced food treatment (Table V).

TABLE V

Mean (& SD, n = 5) shell lengths (mm) and dry tissue weights (g) of S. diemenensis in each replicate at end of experiment in which amount of food avaifabie iu Zone 1 was decreased. Symbols as in Table IV. A. Results Normal food Shell length

11.56 k 11.02 + 11.24 + 11.10 i:

Reduced food Shell length

Tissue weight (x 10-q

0.04 0.02 0.03 0.00

1.92 f 1.63 + 1.67 t 1.49 I

B. ANOVAs Source

0.36 0.26 0.13 0.07

10.14 & 0.02 10.48 + 0.02 10.52 * 0.04 10.56 i: 0.07

Shell length F

df

1 6

64.8 2.4

32

0.7

0.98 f 1.20 f 1.09 k 1.12 k

0.19 0.15 0.09 0.16

Tissue weights P

F

P

32.8 2.7


(XTbs-5,

(X7-3,

Treatment Enclosures w/i treatment Residual

Tissue weight (x 10-y

27.6 3.4


33.6 1.0 0.4

Transplants between zones These data were analysed with a three-factor ANOVA (Season, Original Zone and Transplant Zone all fmed). There were no significant interactions and the shell lengths of limpets at the end of the experiment were significantly greater in spring than in autumn (Table VI) and si~~c~~y greater in Zone 2 than in Zone 1, irrespective of which zone they came from (Table VI).

DISCUSSION

This study has demonstrated marked differences in the population structure of S. diemenensis in two zones on the shore. Such variations between populations of other

TABLE VI

Mean ( f SD with sample size in parantheses) shell lengths (mm) of S. diemenensis at end of experiment in which limpets (6.0-7.0 mm shell length) were transplanted between zones. Data from two replicates of each treatment. Symbols as in Table IV. All interactions were not significant in ANOVA (P> 0.05). A. Results

Zone 1-+ 1 Zone l-+2 Zone 2--, 1 Zone 242

B.

ANOVA Source

Season Original zone Transplant zone Enclosures w/i season and zones Residual

df

Autumn

Spring

7.6 t 0.4 (13) 8.6 f 0.5 (15) 10.0 f 0.7 (12) 9.8 + 0.7 (13) 8.4 + OS (15) 7.8 + 0.4 (15) 10.3 + 0.7 (13) 9.8 + 0.8 (12)

8.6 + 0.6 (14) 8.8 & 0.4 (11) 10.7 f 0.8 (7) 10.5 + 0.3 (10) 9.6 + 0.5 (12) 9.4 +_0.5 (13) 10.8 f 1.1 (12) 10.5 + 0.5 (11)

MS

1

F

1 1 8

29.2 2.8

22.1 2.2

143.1 1.3

111.1 3.3

184

0.4

P

io.01 NS

< 0.001
intertidal gastropods, on different shores and as shore-level size gradients, are well documented (Underwood, 1979; Branch, 1981) and presumably result, at least partly, from differences in the rates of mortality and/or growth. Ideally, estimates of mortality rates should come from records of marked individuals through time (e.g., Creese, 1981). U~o~unately, long term marking of S. die~~ens~ was not possible in either zone because of the very wet conditions and thick coating of algae on the shells during winter and spring, The alternative method of estimating mortality, by sampling the populations, cannot distinguish between mortality and migration as explanations for changes in abundance through time. This problem was overcome in this study by choosing study sites from which migration of S. diemenensis was not possible. The patterns of mortality of S. dienzenensis in Zone 1 were strongly seasonal, the fastest rates occurring during summer and autumn (December-April/May). By this time, most of the spawning had ceased and the minimum tissue weights of limpets of 10 mm shell length were as small as those tissue weights found to be correlated with high mortality in the experimental enclosures. The least mortality occurred in winter and spring (June-November), preceding or during spawning, when size-specilic tissue weights were greatest and there was little intraspecific competition. These demo~ap~c patterns in Zone 1 correlate strongly with the seasonal&y in algal abundance. The algal crust which the limpets consumed was most abundant in spring

132

G.P. QUINN

and disappeared in summer, probably due to the stresses of desiccation, when hot weather coincides with low tides in the middle of the day. During December, the algal crust completely dried out at low tide, and large sections of crust were observed lifting and flaking away from the substratum (pers. obs.); a similar mechanism for determining the seasonal occurrence of encrusting algae in the upper part of an intertidal shore was proposed by Sutherland (1970). The diet of S. diemenensis, the increased growth of limpets experimentally enclosed on encrusting algae compared with those on bare rock (Quinn, 1985) and the increased level of intraspecific competition in summer and autumn compared with winter and spring suggest that the seasonal variation in abundance of algae in Zone 1 represents seasonal variation in the availability of food to S. diemenensis. Sutherland (1970) and Parry (1977, 1982) have argued similarly for other species of intertidal limpets. Density-dependent food shortage resulting in starvation was the most likely cause of the negative correlation between tissue weights and rates of mortality of limpets from experimental enclosures in Zone 1. If this is correct, the increased mortality of S. diemenensis in Zone 1 in summer and autumn is apparently due to starvation. Starvation as a result of intraspecific competition has been shown to cause mortality at experimentally increased densities of other intertidal gastropods (see reviews by Underwood, 1979; Branch, 1981, 1984). Sutherland (1970) and Creese (1980) argued that food limitation restricted biomass, or caused mortality, of intertidal limpets in natural populations. Parry (1982) provided strong experimental evidence that the prosobranch limpet Cellana tramoserica dies from starvation over summer and autumn at a site nearby that of the present study for the same reasons as for S. diemenensis. Desiccation, even acting on individuals already stressed by shortage of food (e.g., Parry, 1982), was unlikely in the experimental enclosures in Zone 1 because the numbers of S. diemenensis declined steadily during summer and autumn, with no increase in mortality during periods when low tides were in the middle of very hot days. Nor was there any evidence (e.g., catastrophic mortality during hot weather; see Branch, 198 1) of desiccation in the natural population in Zone 1. The only important predators on S. diemenensis are the wrasses Pseudolabnrs fucicola and P. tetrikus(Parry, 1977 ; Quinn, 1985); Parry (1977) found that small (3-6 mm) individuals of S. diemenensis were most susceptible to predation by wrasses but that wrasses contributed little to the total mortality of adults in the population he studied. Some of the mortality of limpets in winter and spring may have been due to predation by wrasses since desiccation and starvation were unlikely at this time of the year; wrasses would have been able to forage longer because both zones were submerged during daylight for longer periods during winter and spring than at other times. This mortality in winter and spring may also be related to the patchy regrowth of macroalgae after the disappearance in summer of the algal crust in Zone 1 and some individuals may have starved after the end of the breeding season (i.e., winter) ifthey occurred in an area where the macroalgae were slow to grow back. The constant algal abundance and the absence of seasonal variation in the intensity

POPULATION

DYNAMICS

OF SIPHONARIA

DIEMENENSZS

133

of intraspecific competition in Zone 2 suggests that any seasonal variation in the availability of food to S. diemenenk in this zone is considerably less than in Zone 1. The rate of mortality of limpets in this zone also showed much less seasonal variation than in Zone 1. Seasonal variation in tissue weights in Zone 2 was not as pronounced as in Zone 1 and increased mortality when tissue weights were at a minimum was not evident, suggesting that starvation was an unlikely cause of mortality in Zone 2. Desiccation was also improbable in Zone 2 because of the short emergence period during low tide (< 3 h). While wrasses would have more access to Zone 2 than Zone 1 because of its greater submergence time, Parry’s (1977) data suggest that larger individuals (> 10 mm) would not be taken by fishes. Few conclusions, therefore, can be drawn concerning the causes of mortality in Zone 2. The rates of growth of cohorts of S. diemenensis in Zone 1 were also correlated with the availability of food and this was supported by the size-specific rates of growth of marked individuals. Similar correlations between seasonal variations in growth and food supply have been described for other limpets (Blackmore, 1969; Sutherland, 1970; Phillips, 198 1; Parry, 1982). The experiments in the present study in which adult density was manipulated or the amount of food was reduced demonstrate the importance of available food as a determinant of growth of S. diemenensis in Zone 1. No clear seasonal trends in the rate of growth of cohorts in Zone 2 were apparent. The size-specific growth of marked individuals showed the same pattern as in Zone 1 although the seasonal variation in Zone 2 was much less than in Zone 1. Even though there was no seasonal variation in algal cover in Zone 2, the higher growth rates of marked individuals in winter may be because the substratum remains damp during low tide, increasing the time available for foraging (pers. obs.). The faster growth rate of individuals of similar size in Zone 2 compared with Zone 1 in summer, autumn and winter is not surprising given the differences in the availability of food and the results of experiments discussed earlier. Sutherland (1970), Creese (1980), Workman (1983) and Fletcher (1984) have also correlated larger sizes and faster rates of growth of intertidal limpets with measures of availability of food, the latter author assuming that higher densities of limpets meant reduced food. Underwood (1984b) has shown experimentally that the growth of one species of intertidal gastropod is related to the availability of food. The differences in rates of growth between zones in the present study appear to be environmentally determined, because transplanted limpets from each zone grew the same amount as resident animals in either zone. The results from all experiments indicate that growth is not a fared characteristic in S. diemenensis and can change rapidly in response to variations in food supply. The conclusions of this study rely to some extent on the result of field experiments, particularly manipulating the densities of adults. One difficulty with such experiments is that the results from artificial enclosures may not be applicable to natural populations or communities. “Cage controls” are usually not possible and potential “cage effects” (small size of enclosures, altered current flow, etc.) are difficult to assess. In this study, limpets enclosed at natural density in Zone 2 (6 per enclosure) had tissue weights close

134

G.P. QUINN

to field values but limpets enclosed at natural density in Zone l(l5 per enclosure) were heavier and survived better than those in the field in summer and autumn. This latter result may be because the enclosures made the microenvironment more conducive to algal growth and survival, although increased algal growth was not apparent from macroscopic observations. Alternatively, the effect on S. diemenensis of interspecific competition from other grazers which were excluded from the enclosures may be important in natural populations. For example, Creese & Underwood (1982) showed that the prosobranch limpet, C. Z~~~u~e~cu, could adversely af&ct two species of Siphonaria by removing the available food. This was unlikely to be the case in either zone in the present study because the density of S. diemenensis was much greater than of other grazers, and C. tramoserica was obviously not able to keep areas in either zone clear of macroalgae. Nonetheless, it is important to be able to relate experimental situations to natural conditions, by having quantitative measures of food abundance (Underwood, 1984c) or by comparing tissue weights (Underwood, 1978; Fletcher & Creese, 1985; this study) inside and outside enclosures. The latter information also provides a very useful technique for estimating the likelihood of starvation as a cause of mortality in natural populations (see also Parry, 1982). This study demonstrated that the growth of S. diemenen& was very flexible in character, and that food availability was likely to be a major determinant of variations in growth and survival. This conclusion supports Branch (198 1), who commented that, for limpets, “the amount of food (and the variability in that amount) may be a key issue in determining the pattern and flexibility of growth displayed by each species”. Reproduction in this species is also strongly affected by food availability and the data presented here provide the background for interpretation of the reproductive patterns of S. die~ne~is (Quinn, 1988).

ACKNOWLEDGEMENTS

This paper is based on a Ph.D. thesis submitted to the University of Melbourne. I would like to thank my supervisor M. J. Littlejohn and R. W. Day, P. G. Fairweather, G. P. Jones, G.D. Parry, R.N. Synnot, A. J. Underwood and G. F. Watson for helping with the thesis and this manuscript, the latter benelitting from the comments of two anonymous referees, and all those who assisted in field work and contributed in other ways. This study was funded by a U~versity of Melbourne Post~aduate Research Award and logistic support was provided by the Department of Zoology, University of Melbourne (thesis) and the School of Biological Sciences, University of Sydney (typescript). REFERENCES BLACK,R., 1979. Competition between intertidal limpets: an intrusive niche on a steep resource gradient. .i. Anim. Ecol., Vol. 48, pp. 401-411.

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135

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