Patterns of growth, longevity and recruitment of intertidal limpets in New South Wales

J. esp. mar. Biol. Ecol., 1981, Vol. 51, pp. 145-171 0 Elsevier/North-Holland Biomedical Press

PATTERNS

OF GROWTH,

OF INTERTIDAL

LONGEVITY

LIMPETS

R. G. Zoology Department,

School of Biological Sciences,

AND RECRUITMENT

IN NEW SOUTH

WALES

CREESE University

of Sydney,

Sydney, N.S. W. 2006, Australia

Abstract: Six species of limpets, representing the families Acmaeidae, Fissurellidae, and Siphonariidae, were investigated. Size-frequency distributions were obtained regularly for each species, and provided data on rates of growth and mortality of age cohorts, and on the time and intensity of recruitment of juveniles into the population. Where possible, rates of growth and mortality were also obtained from individually marked animals, and data on recruitment were obtained by regular monitoring of permanently marked out quadrats. The usefulness of information gained by the two methods for determining rates of growth and mortality is compared. All species showed indeterminate growth and great variability in mortality and recruitment. The possession of iteroparity and early reproductive maturity may partially compensate for this variability and unpredictability in growth, longevity and recruitment. The differences between species within the same genus can be as great as the differences between families, however, and it is not meaningful to consider further generalisations concerning life history characteristics.

INTRODUCTION

The ecological implications of life history characteristics in benthic marine invertebrates are poorly understood (Cole, 1954; Frank, 1968; Vance, 1973; Underwood, 1979). Lack of detailed empirical data is still a major drawback in improving the predictions of the present diffuse theories about life histories (Stearns, 1976). Background data on growth, mortality, recruitment and reproduction are also valuable

in any analysis

of the structure

nities (Underwood, 1979). Intertidal limpets are a convenient

group

and dynamics in which

of biological to examine

commupopulation

dynamics and life history characteristics. They live in a readily accessible often occur in large numbers, and are easy to sample, mark and relocate. tions

of limpets

exhibit

great

plasticity,

and environmental

conditions

habitat, Populaon a very

local scale often influence their dynamics (Ward, 1967; Giesel, 1969; Sutherland, 1970; Lewis & Bowman, 1975; Bowman & Lewis, 1977). Comparative studies of a group of congeneric species inhabiting the same shore have also revealed great variability in life histories (Branch, 1974a,b; Choat, 1977). Few attempts have been made, however, to compare the population dynamics of co-existing limpets from different families (Parry, 1977; Creese, 1978). The species investigated here are from different phylogenetic origins, have different modes of reproduction, and spawn at different, although often overlapping, times (Creese, 1980a,b). Yet their shells are 145

146

R. G. CREESE

morphologically similar, they have similar requirements for space, and several have overlapping diets and distributions on the shore. It is therefore of interest to determine to what extent the life history characteristics of this group of limpets have converged, what range of life histories can operate under very similar environmental conditions, and how these life histories relate to the continued co-existence of the species. Apart from the work on the patellid limpet Cellana tramoserica (Sowerby) by Underwood (e.g. 1975a,b), there have been no detailed studies of the population dynamics or life history characteristics of intertidal limpets in New South Wales. A detailed study of six species of limpet from three families was therefore carried out between 1975 and 1978 at Cape Banks, on the northern headland of Botany Bay, Sydney. The species were: Notoacmea petterdi (Tenison-Woods), Patelloida latistrigata (Angas) and Patelloida alticostata (Angas), (Family Acmaeidae); Mon!fortula rugosa (Quoy & Gaimard), (Family Fissurellidae); Siphonaria denticulata Quoy & Gaimard, and Siphonaria virgulata (Hedley), (Family Siphonariidae). Notoacmea petterdi is restricted to vertical surfaces in the upper littoral, and Mon@rtula rugosa is usually found in damp areas in the lower littoral or in pools. The remaining four species co-occur in the mid-littoral (Dakin et al., 1948) although their distributions are often patchy (Creese, 1978). This paper describes the growth, longevity and recruitment of each species. This information, together with data on their reproductive cycles and fecundities (Creese, 1980a,b), allows a preliminary discussion of the life histories of these species. Three main techniques have been used to investigate the growth of limpets. First, growth lines laid down on the shell can sometimes be used to determine the rate of growth and age of individual animals (Abe, 1932; Hamai, 1937; Kenny, 1969; Parry, 1978). Limpets in New South Wales, however, do not show clearly distinguishable growth lines on their shells. Secondly, populations may be sampled periodically and the mean sizes of the individuals within distinct age cohorts calculated from the polymodal size-frequency distributions (Ward, 1967; Underwood, 1975a; Choat, 1977). Finally, by marking individuals and measuring their sizes periodically, direct measurements can be obtained (Frank, 1965a,b; Seapy, 1966; Ward, 1967; Branch, 1974b; Black, 1977). The assumptions underlying the estimation of rates of growth and mortality from size-frequency data are rarely met (e.g. Yamaguchi, 1975). In the present study, therefore, rates calculated by this method were supplemented where possible by measurements of the growth and survival of marked individuals. This allowed the results from the two methods to be compared critically.

GROWTH.LONGEVITYANDRECRUlTMENTOFLlMPETS MATERIALSAND

147

METHODS

Size-frequency data were collected on a regular basis during 1976 and 1977, although the period over which samples were taken and the interval between samples differed for each species (Table I). The size of the limpets was determined by measuring the length of the shell with vernier callipers, as this allowed limpets to be measured in situ on the shore. As rates of growth often show intraspecific variability (e.g. Frank, 1965b), sampling was deliberately restricted to populations in a typical habitat. For Notoacmea petterdi, however, rates of growth were measured for two small subpopulations, one at a high level on a vertical surface, and the other at a level z 1.5 m below it. For each population, all the individuals in a number of randomly chosen quadrats (Table I) were measured to the nearest TABLE I Number

analyses:

and size of random quadrats sampled, and the sampling interval used for size-frequency within a species, the size of quadrat was the same for both the random sampling programme and for the three permanent quadrats.

Species

Size of quadrdts (cm)

No. of random quadrats

M. rugosa

50 x 50

10

P. latistrigata

25 x 25

10

P. alticostata

50 x 50

IO

N. petterdi (at both levels) S. denticulata

25 x 25

5

50 x 50

10

S. virgulata

50 x 50

10

Sampling interval Monthly between Nov. 1976 and Nov. 1977 Alternate months between Sept. 1975 and Sept. 1977 Alternate months between Jan. and Sept. 1976; monthly between Nov. 1976 and Dec. 1977 Alternate months between Sept. 1975 and Sept. 1977 Alternate months between Jan. 1976 and Nov. 1977 Alternate months between Jan. 1976 and Nov. 1977

0.5 mm. Subpopulations for each population sampled were separated using probability paper (Cassie, 1954), as modified by Underwood (1975a), and their mean shell lengths plotted against time of sampling. The size-frequency data were used to estimate rates of mortality of particular cohorts, and to indicate the time and intensity of recruitment of juveniles. Instantaneous rates of mortality were calculated from the slope of the regression of log density (within a cohort) on time (Deevey, 1947; Underwood, 1975a). Additional data on recruitment were obtained from three quadrats permanently marked on the shore in the centre of the vertical

R.G. CREESE

148

range of each species. The numbers of juvenile recruits in these quadrats were recorded monthly between September 1975 and December 1977. For each species, all adult limpets within the three permanent quadrats were individually marked in situ with non-toxic marine paint using a dot code. Additiona animals were chosen from the rock surrounding these quadrats so that several size classes were adequately represented in the growth analyses, and so that the total number of marked animals was at least 60. When a marked animal was lost, it was replaced at the next sampling time with another of approximately the same size. Individuals were measured to the nearest 0.1 mm at monthly intervals between January 1976 and April 1977. Increments in shell length were used to calculate individual rates of growth and to test for seasonal patterns in growth. For each species, mean monthly increment decreased with increasing size, the relationships being more similar to an exponential decay curve than to a linear one. Regressions of log increment on initial length were thus calculated for four seasons of the year. The rate of decline in the density of marked adult limpets within these quadrats was also used to estimate rates of mortality, using the same procedure as for the size-frequency data.

RESULTS MONTFORTULA

RUGOSA

This species has a spawning season extending over 9 months of the year (Underwood, 1974; Creese, 198Ob). Juvenile M. rugosu are therefore present in large numbers throughout the year, especially in shallow pools and areas dominated by erect coralline algae in mid-littoral regions of the shore. It is virtually impossible, therefore, to obtain discrete age cohorts from size-frequency data. Lower on the shore, however, it is often possible to obtain meaningful results (Fig. 1). Here the size of adult animals (cohort B) could be followed throughout the year, and of juveniles (cohort C) after March when the intensity of recruitment in this region decreased (Fig. 2). Cohort C increased from a mean size of 6.9 (+ 1.3 SD) mm in March 1977 to 12.2 (k2.5 SD) mm in November 1977, a rate of growth of 0.7 mm/month. Cohort B grew at 0.55 mm/month, during this period. Cohort A disappeared from the population in December 1976. Because of the continual recruitment of juveniles over a large part of the year, it was not possible to calculate the rate of growth of newly-recruited juveniles {cohort D), as there was no increase in the mean size of this cohort during the period of investigation. It is difficult to mark individual M. rugosa because they occur low on the shore in damp microhabitats. Loss of paint marks occurred frequently, and no estimates of individual rates of growth are available.

GROWTH.

se

u_

FEB 77’-

_

LONGEVITY

C

AND

RECRUITMENT

B

- JUL.11 -0

r

IO-

OF LIMPETS

_--c,

r 20- MAR.77.

,C

B_

-

CC

_ SEP.77.

7

IOI 5

I IO

I 20

15

5

I 20

I 15

IO

SIZE (mm) Fig. 1. Size-frequency distributions for Montfortula rugosa: A, B, C, D are the age cohorts, in this and subsequent figures showing size-frequency distributions, not all data are presented, only those samples that serve to illustrate the features of the annual cycle are figured.

I

N

I

0

1976

hi

Fig. 2. Growth

I

F

I

M

I

Ap

of age cohorts

I

My

I

J

I

I

JY A 1977

I

S

of Monifortula rugosa.

I

0

I

N

150 PATELLOIDA

R. G. CREESE LATISTRIGATA

Juveniles of this species (cohorts D and E) grew at a rate of 0.6 mm/month between March and the following September (Fig. 4). One-year-old animals (cohort C in 1975-1976, cohort D in 19761977; Fig. 3) grew at a rate of

5

10

IS

lb

IS

SIZE (mm) Fig. 3. Size-frequency

distributions

for Pff~el~#i~a ~u~is~rig~fu.

0.4 mm/month during a 1-yr period. The growth of marked individuals agreed well with these rates (Fig. 4). The oldest cohorts disappeared from the population during their third (or possibly fourth) year on the shore at a mean size of 14 mm (cohorts A, B, C respectively). Marked individuals, however, rarely grew > 12.5 mm (Fig. 4). To test if there were differences in the growth of juveniles depending on when

GROWTH.

LONGEVITY

AND

RECRUITMENT

they were recruited

to the population,

recruitment

at the end of 1976. Twenty

period

two separate

OF LIMPETS

151

groups were marked

individuals

were marked

during

the

at the end

14pc$o$3 z

6-

5 F4 2c

111111111111111111~111~

S N 1975 Fig. 4. Growth

Ja

M

My

Jy S 1976

N

Ja M “r,?:y

s

of Purelloidu laristrigara determined from the mean size of age cohorts and from groups of marked individuals ( x and ----).

(0

of August, and a further 20 in December (Fig. 4). There was no significant between the rates of growth of these two groups (analysis of covariance, PATELLOIDA

and ---)),

difference

P > 0.05).

ALTICOSTATA

The estimation of the growth of this species was complicated by the fact that there were two distinct peaks in the recruitment of juveniles, and because of the low density of adult limpets at the study site (Fig. 5). In January of each year there were four cohorts B + C, D, E, F in 1977). These

cohorts

do not,

present however,

(A, B, C, D in 1976 ; correspond

precisely.

Cohorts C, D and F of 1977 correspond to cohorts B, C and D of 1976, and represent 2-yr-old, I-yr-old, and juvenile limpets respectively (Fig. 6). No size-group equivalent

to cohort

E was present

in 1976, presumably

due

to the failure

of

settlement of juvenile limpets in the first few months of 1975. Cohort A, made up of the largest animals, was not represented in January 1977. The members of cohort B, which might have been expected to grow and replace this cohort of large animals, had virtually disappeared by July 1976, the few remaining individuals having merged with cohort C. Cohort A was absent after September 1976, and cohort B + C after November 1977 (Fig. 5). The rate of growth of marked animals was generally less than that predicted from the size-frequency data (Fig. 6). Large numbers of mature eggs were present in the gonads of adult limpets from January until May, but some individuals sampled during this time had spent gonads (Creese, 1980b). This suggests that partial spawnings may occur during this period,

152

R. G. CREESE

DEC.16.

FEB.17.

SIZE (mm) Fig. 5. Size-frequency

distributions

for Patelloida

alticostata.

201816g4-12K =10-

4-

,

1IIIll1IIIIIIIIIllllll

Ja

M

My

Fig. 6. Growth

Jy 1976

S

of Patelloida

N

Ja

alticostata:

M

My

symbols

Jy 1977

S

as in Fig. 4

N

GROWTH,

LONGEVITY

AND RECRUITMENT

OF LIMPETS

1.53

and Creese (1980b) identified a secondary peak in spawning activity in February to March. The major spawning occurred between May and July. The appearance of juveniles on the shore supports these conclusions. Cohorts D, F and H probably resulted from the major mid-year spawnings of 1975, 1976 and 1977 respectively. Spawnings early in 1976 and 1977 would have given rise to cohorts E and G respectively. Cohorts of juveniles grew at different rates (mm/month) during their first 6 months on the shore (D = 0.92, E = 0.75, F = 1.08, G = 0.65). Juveniles marked in April 1976 grew slower than the rate estimated from the size-frequency data for cohort E, but those marked in December 1976 had similar growth to the members of cohort F (Fig. 6). Cohort E suffered a dramatic decline in numbers between November and December 1976 (Fig. 5) and was indistinguishable from the faster growing cohort F after February 1977. NOTOACMEA

PETTERDI

In both populations of this limpet, adults (> 10-12 mm) were slow growing. For this reason discrete cohorts were impossible to distinguish, and cohorts A and A’ simply represent adult animals (Fig. 7). Juveniles (cohorts B, B’, C, C’, D, D’) grew rapidly and merged with the adult subpopulations within their first year. The rapid growth of cohort B (Fig. 8) is not reliable as it contained only 7-10 animals. The rate of growth obtained from cohort C, made up of 34-45 limpets, agrees well with the rate of 0.6 mm/month obtained from marked juveniles. Marked adult limpets in both populations grew at rates of only 0.05 to 0.2 mm/month. Thereafter, they grew increasingly slower and the rate of growth was negligible for individuals > 17 mm in shell length. An analysis of covariance was done to test for differences in the rates of growth of marked juveniles at the two different levels on the shore. The regressions of log increment on initial length for these two groups of limpets for the period July to December 1976 showed a significant difference between slopes (F,.,2 = 23.06, P < 0.001). Juveniles at the upper levels grew significantly faster (0.48 mm/month, SE = 0.03, II = 18) than juveniles at the lower level (0.24 mm/month, SE = 0.03, IZ= 10). There was no significant difference in the initial lengths of the limpets in the two groups.

154

R. G. CREESE

SEP. 75. 20 10

1

20IO20-

MAY 76.

-A

IOi-i-k_, 201

A

IO-

(a)UPPER LEVEL.

SIZE (mm)

(b) LOWER

Fig. 7. Size-frequency distributions for two populations of Notoacrnea

LEVEL.

petter-di.

GROWTH.

LONGEVITY

AND

RECRUITMENT

OF LIMPETS

155

UPPER LEVEL

Fig. 8. Growth

SIPHONARIA

of Noroacmeape/rerdi:

symbols

as in Fig. 4.

DENTICULATA

As with Notoacmea petterdi, it was impossible to distinguish discrete age cohorts for adult Siphonaria denticulata. Cohort A in Fig. 9 merely represents adult animals. Juveniles (cohorts B and C) grew relatively slowly (0.4 mm/month), the data for marked individuals agreeing well with those from the analysis of size-frequencies (Fig. 10). Data from marked adults gave a rate of growth of x 0.25 mm/month for limpets with initial sizes between 10 and 13 mm. and a rate of 0.2 mm/month for animals between 13 and 16 mm. Individuals longer than 17 mm had negligible growth during the 2 yr of investigation.

156

R. G. CREESE

20 10 z 5 20 ZI g IO

10

SIZE (mm) Fig. 9. Size-frequency

distributions

for Siphonaria

dmticulara

1816-14EE -12d
21 I I I I I I I I I I I I I I I I I I I I I I I Ja M My Jy S N Ja M My Jy S N 1916 1977 Fig. 10. Growth

of Siphonaria

denticulara:

symbols

as in Fig. 4

GROWTH, SIPHONARIA

LONGEVITY

AND

RECRUITMENT

157

OF LIMPETS

VIRGULATA

Cohorts of juvenile S. virgulata were estimated to grow at 0.5 to 0.6 mm/month between March and November (cohorts B and C in Figs. 11, 12). Adult animals (cohort A in 1976 and cohort A+ B in 1977) grew at an apparent rate of 0.2 mm/month over the entire year. No more than two cohorts were ever present in the population sample, although the presence of a number of large animals ( > I5 mm) often suggested a third cohort (Fig. 11). Marked individuals generally grew at rates considerably faster than those predicted from the size-frequency data. Marked juveniles grew at a mean of 0.9 mm/month between March and November 1976 and 1.4 mm/month for the same period in 1977. Adults had a mean rate of growth of 0.5 mm/month for sizes

NOV. 76.

IO-

l-t-l" =S_

20 IO IO

5

5

IO

for Siphonaria

virgulara.

15 SIZE (mm]

Fig.

Il. Size-frequency

distributions

15

158

R. ‘3. CREESE

between 9 and 13 mm, although there were obvious seasonal trends in the rate of growth of these marked individuals (Fig. 12).

I I I I I I

Ja

M

My Jy

I I I I I I I I I I I I I I I I I 5

N

Ja

1976 Fig. 12. Growth

SEASONAL

of Siphonaria

virgulata:

M

My Jy S / 1977

symbols

N

as in Fig. 4

VARIATION

Regressions of log increment on initial length were calculated for each species except Montfbrtula rugosa at different seasons of the year (Table II). Analyses of covariance showed that there were no significant differences between the slopes of these regressions for the different seasons. This indicates that the relationship between increment and initial length does not vary significantly with time. Because rate of growth decreases with increasing age, it was necessary to have animals of the same size at the start of each season, so that the effects of season and age (i.e. size at the start of the season) were not confounded. Any evidence of seasonal variation is, therefore, independent of the relationship between rate of growth and size (or age). The comparison of intercepts showed significant differences (P < 0.05) for Notoacmea petterdi, Siphonaria denticulata and S. virgulata (Table II). These differences among intercepts indicate seasonal changes in rate of growth after adjustment for the starting sizes of the limpets in the sample. Patelloida Iatistrigata and P. alticostata showed no such differences (Table II). Notoacmea petterdi grew faster in the winter and spring than in the autumn and summer, while the two species of Siphonaria grew fastest, at all sizes, during autumn.

TABLE II

P. latisrrigara P. alricosrata N. perrerdi S. denriculara s. vir&ua

SpXkS

F+$j) = 1.3 ns F4,36 = 0.6 ns

Fd,Jj = 1.7 ns Fj,23 = 2.8 ns F& = 1.3ns

___-among slopes

F4.3, = F3,26 = F4.39 = F4+ = F4,40 =

Common

Y=I-0.21x Y=I-0.14x Y=I-0.22x Y=I-0.13x Y=I-0.16X

x.4**+ 16.2”*” 48.2*‘*

regression equation

2.1 ns 2.1 ns

among intercepts

F-ratios

1.0 _

1.9 _

Summer 1976

1.1 2.3 3.4

1.3 I.5

Autumn 1976

1.9 1.4 1.8

3.3 1.7 1.8

Spring 1976 2.x 2.2

1976

1.9 1.5

Winter

1.5 1.3 1.9

1.5 2.0

Summer 1977

2.3 3.4

Autumn

1977

Y = If bX, where Y = In Summer is December to

Intercepts (I) for each season (monthly increment, mm)

Analyses of covariance for seasonal growth of five species at Cape Banks over four or five seasons: regression equations are in the form (mean monthly increment), I = intercept, b = slope, X = initial size; for all regressions 0.69 < rz < 0.92; Spring is September to December, March, Autumn is March to June, Winter is June to September; ***, P < 0.001; ns, P :, 0.05.

R. G. CREESE

160 MORTALITY

AND

LONGEVITY

Rates of mortality for all species except Montfortula rugosa were estimated for selected age cohorts (Table III). For Patelloida alticostata, Siphonaria denticulata and S. virgulata, rates of mortality were greater for juveniles than for adults (Table III). The two species of Siphonaria, however, differed in their patterns of TABLE III Instantaneous rates of mortality calculated from the decrease in density of limpets within a particular age cohort: rates are expressed as deaths individual’ month - ’ ; Ad, Adult; Juv, Juvenile.

Species P. latistrigata

Cohort designation D(Juv) E(Juv) C(Ad) D(Ad) B(Ad) C(Ad)

P. alticostata

D(Juv) E(Juv) C(Ad) E + F(Ad)

N. petterdi

(upper)

C(Juv)

(lower)

B(Ad) A’ + B’(Ad) B’ + C’(Ad)

S. denticulata

B(Juv) C(Juv) A(Ad)

S. virgulata

B(Juv) C(Juv) A(Ad) A + B(Ad)

Time period

Rate of mortality (x l@)

Mar.-Nov. 1976 Jan.-Sept. 1977 Aug. 19755July 1976 Nov. 1976Sept. 1977 Aug. 1975%July 1976 July 19766May 1977

3.4 2.0 3.1 2.2 34.0 54.5

Jan.-Nov. 1976 July 1976Feb. 1917 Jan-Sept. 1976 Mar.-Dec. 1977

12.5 14.8 8.5 6.0

Sept. 1976-May 1977 Mar. 1976May 1977 Mar.-Nov. 1976 Jan.-Sept. 1977

2.3 1.7 8.4 5.8

May 19766Jan. 1977 May-Nov. 1977 Jan. 1976May 1977

17.2 13.4 3.8

May-Nov. 1976 May-Nov. 1977 Mar. 1976Jan. 1977 Mar.-Nov. 1977

15.5 19.0 10.5 11.0

mortality: S. denticulata had relatively great juvenile mortality but little adult mortality, whereas S. virgulata had very fast rates for both adults and juveniles. Rates of adult and juvenile mortality for the high-shore species, Notoacmea petterdi, were both slow but were greater for adults at the low level compared to those higher on the shore. Patelloida latistrigata also had slow rates of adult and juvenile mortality. In their third year on the shore, however, P. latistrigata died rapidly after reaching a size of % 12 mm (cohort B after August 1975 and cohort C after July 1976). The pattern described above for P. latistrigata illustrates the point that mortality

GROWTH,

LONGEVITY

AND

RECRUITMENT

OF LIMPETS

161

of a cohort may not continue at the same instantaneous rate throughout life. Similarly, for both P. alticostata (cohorts B+ C, D and E between November and December 1976) and Siphonaria virgulata (cohort A after November 1976) there were periods when adult mortality was considerably greater than the “typical” rate. The periods used to estimate the rates of mortality in Table III were deliberately chosen, therefore, to correspond to periods when the numbers in a particular cohort decreased in an approximately logarithmic way. Another estimate of the mortality of adult limpets was made from the losses of marked individuals (Table IV). These animals could not be separated into age cohorts because of the small numbers involved. For this reason, and because data were collected over different periods of the year, the results in Tables III and IV are not strictly comparable. Despite this, the results of the two methods are similar, and show the same trends. Adult Notoacmea petterdi die faster at lower levels on the shore than at high levels. The mortality at high levels was remarkably constant over the 2-yr period. In contrast, both species of Siphonaria showed significant differences in mortality between time periods (Table IV). For each of the time intervals investigated, however, S. virgulata suffered greater mortality than its congener (Tables III and IV). TABLE

IV

Instantaneous rates of mortality calculated from the decrease in numbers of individually marked limpets: rates are given as the mean (+ SE) of the three permanent quadrats, and are expressed Table III.

Species

Mean rate of mortality (+ SE) X Id

Time period

P. laiistrigata

Sept. 1975Mar. 1976 Mar. 1976-Apr. 1977 Apr.-Sept. 1917

9.9(0.9) 6.0(0.8) 4.7(2.0)

P. alticostata

Jan.-June 1976 June 1976June 1977 June-Dec. 1977

7.9(4.1) 4.1U.3) 6.9(2.1)

N. petterdi

Sept. 1975%Mar. Mar. 1976-Apr. Apr.-Sept. 1977 Sept. 1975-Feb. Feb. 1976Mar. Mar.-Sept. 1977

(upper)

1976 1977

1.2(0.2) 1.3(0.1)

l.l(O.2) 1976 1977

7.7(0.7) 5.5(0.6) 5.1(0.8)

S. denticulata

Jan.-Aug. 1976 Aug. 19766Aug. 1977 Aug.-Dec. 1977

7.6(0.8) 2.2(0.7) 3.4(2.0)

S. virgulata

Jan.-Sept. 1976 Sept. 1976Sept. 1977 Sept. 1977-Feb. 1978

lKO(2.9) 17.5(1.4) 9.3(2.3)

(lower)

adult as in

162

R. G. CREESE

Because many cohorts showed unpredictable fluctuations in density, it was not appropriate to estimate longevity using size-frequency data, and the more accurate data on the growth and mortality of marked individuals were used instead. Marked adults of Siphonaria virgulata, Patelloida alticostata and P. latistrigata often died at a size corresponding to the maximum size found at the study site. The age of these limpets could be accurately estimated from the known rates of growth of marked individuals. For example, P. latistrigata marked in January 1976 at sizes > 11 mm had died by January 1977 at a mean size of 13.6 mm (SE = 0.39, n = 6). These individuals had all maintained recognizable home scars throughout the study (Creese, in prep.), indicating that they had died rather than merely lost their paint marks. During this period animals marked at 4 mm grew to a size of 9.5 mm, and animals marked at 10 mm grew to an average of 12 mm (Fig. 4). The largest P. fatistrigata found at the Cape Banks site was 15.1 mm, but animals > 14.5 mm were rare. From these data it was calculated that animals were disappearing from the population at a size of 13-14.5 mm, corresponding to an age of x 3 yr. Similarly, it was possible to estimate the longevity of Siphonaria virgulata as 2-3 yr, and of Patelloida alticostata as 5-6 yr. The disappearance of adult cohorts was observed for each of these three populations, and confirms the estimates of average longevity. Rates of growth for adult Notoacmea petterdi and Siphonaria denticulata were very slow, and mortality of the largest marked individuals was also negligible over a 2-yr period (Table IV). The individuals that did die had shown negligible growth during this time. The disappearance of cohorts of adult limpets from the population was not observed because adult animals were not separable into discrete age cohorts. From a consideration of the calculated rates of growth given earlier, however, it would take an average N.petterdi 10 yr to reach a size of 18 mm. There were several 18-20 mm animals that stayed alive throughout the 2 yr of observation. These animals must, then, have been at least 10 yr old. Similarly, the largest S. denticulata at Cape Banks would be at least 6 yr old, and the largest Montfortula rugosa at least 3 yr old. RECRUITMENT

The appearance of juvenile cohorts in the size-frequency graphs is not the actual time of settlement of juveniles on the shore. Newly-settled juveniles (< 3 mm) were often cryptic and hidden in inaccessible places; underneath turfs of coralline algae or on the insides of empty barnacle shells. Consequently, small juveniles could not be counted accurately, were generally impossible to measure, and were often difficult to classify. For these reasons, the densities of juvenile M. rugosa, Patelloida alticostata, Siphonaria denticulata and S. virgulata (Figs. 1, 5, 9, 11) underestimate the actual densities on the shore. As the study populations of Notoacmea petterdi and Patelloida latistrigata were located in areas where there were few other organisms present, juveniles of these two species could be identified, counted and

GROWTH,

LONGEVITY

AND

RECRUITMENT

163

OF LIMPETS

measured (but not marked) at sizes < 3 mm. Size-frequency data were collected every second month (except for Montfortula rugosa and Patelloida alticostata during 1977), and juveniles may have been present on the shore for well over a month before being recorded. Although these data cannot, therefore, be used to define the start and finish of periods of settlement, it is possible to identify periods of recruitment (defined as the time when limpets >3 mm appear in large numbers in the population). Juvenile P. lutistrigata began to recruit in October 1975, September 1976 and September 1977. In each year, large numbers of juveniles were present for 4-5 months, and no new recruits were found after March (Fig. 3). Notoacmea petterdi settled in July-August 1976 and July-September 1977 (Fig. 7). Juvenile Putelloida alticostata were recorded in two distinct peaks starting in December/ January and March/May (Fig. 5). Juvenile Montfortula rugosa were found throughout the year, and both species of Siphonaria recruited between March and July in both 1976 and 1977, although small individuals were occasionally found earlier in the year (Figs. 9 and 11). TABLE

Mean number

(f

V

SE) of juveniles (< 4 mm) present in the three permanent quadrats: * indicates greatest recruitment that was subsequently used in several analyses (see text).

the month

of

Month

1975 s 0 N D 1976 J F M A M J J A s 0 N D 1977 J F M A M J J A S 0 N D

M. ru,qosa

22.0( 1.7) 28.7( I .8) 26.3(2.9)* 26.3(4.1) 33.3(3.9) 33.7(4.5) 40.3(3.3) 36.7(2.8) 23.3(2.8) lO.O(l.6) 12.7(2.0) 16.0(2.1) 76.7(4.1) 92.3(4.7)* 81.3(10.0) 72.3(6.3) 54.1(7.3) 61.5(10.7) 30.7(5.5) 18.4(2.1) 13.3(5.1) 8.3(3.6) 15.9(5.0) 26.4(5.8) 19.1(2.3) 28.7(4.0) 51.3(6.7)*

P. lalblrigata

6.3(2.0) 20.0(1.6) 24.0(3.0)* 23.0(3.5) 18.7(2.0) 13.012.7)

16.3(2.6) 23.0(9.1) 43.7(7.0) 54.3(4.0)* 35.7(2.7) 30.0(3.6) 23.7(3.3) 22.7(3.2)

P. allicostatu

13.7(0.9) 18.0(1.7)* 14.3(1.4) 16.7(1.2) 21.3(2.7)* 20.7(2.4)

5.7(2.8) 9.0(3.5) 18.3(5.0) 17.7(4.5) 27.7(4.5)* 24.7(U) 29.7(3.5)* 17.3(2.9)

1.3(1.3) 0.3(0.3) 7.3(2.2)

N. perterd~

N. prtterdi

(upper)

(lower)

0.3(0.3) 0.3(0.3) 0.3(0.3) 0.3(0.3) 0.3(0.3)

3.0(0.6)* 3.0(0.6) 2.3(0.3) 2.3(0.3) 2.3(0.3) 2.3(0.3)

2.0(0.6) 4.7( 1.4) 7.7(2.0)* 6.3(1.2) 6.7(0.3) 6.3(0.3) 6.3(0.3) 6.0(m)

l.O(l.0) 3.0(-) 6.7( I .2) 7.0(2.0)*

7.7( 1.8) 22.0(3.2)* 18.7(1.2) 12.0(1.7) 9.0(1.7) 8.3(1.2) 8.3(1.2) 8.0(1.1)

1.3(1.3) 3.0(1.1) 18.7(1.2)* 17.3(2.9)

S

0.3(0.3) 4.7(0.9) 8.0(2.7)* 7.0(3.2) 7.0(3.5) 6.3(2.7)

0.3(0.3) 9.3( I .4) 17.3(1.4) 18.0(2.3)* 14.7(2.7)

0.7(0.9)

7.0(0.6) IS.O(2.5) 16.7(3.0)* 16.3(4.3) 15.7(3.2) 14.3(3.2) 12.3(2.7)

0.3(0.3) 0.3(0.3) 17.0(2.1)* 15.7(1.8) 13.0(1.6) 12.0(1.2) lO.O(l.2) 8.7(0.9)

164

R. G. CREESE

More precise information on the intensity of recruitment of juveniles was gained from the three permanent quadrats, which were searched regularly and intensively for the presence of juveniles (Table V). For each species and period of recruitment, the month that had the largest mean number of recruits was selected. These values (Table V) were compared by analyses of variance followed by Student-NewmanKeuls comparisons of means. Significant differences (P < 0.05) between years were obtained for Patelloida latistrigata (greater in 1976 than in 1975), Notoacmea petterdi (greater in 1976 and 1977 than in 1975), Siphonaria denticulata (greater in 1977 than in 1976) Montfortula rugosu (greater in 1977 than in 1975, greater in 1976 than in 1977), and Patelloida alticostata (greater in 1977 than in 1976). No differences in numbers of juveniles present were found between 1976 and 1977 for Siphonaria virgulata. Analysis of variance also showed that recruitment of Notoacmea petterdi was greater at the low level on the shore than at the high level. DISCUSSION THE DETERMINATIONOF GROWTH,LONGEVITYAND MORTALITY Analyses of size distributions have been used extensively to estimate rates of growth and mortality for populations of marine invertebrates. There are several problems with this procedure. The first problem arises from an inability to separate discrete age classes. The first couple of age classes are often distinct and can be separated by using probability paper (Cassie, 1954; Underwood, 1975a), but older individuals often form a single mode at the right side of the distribution, making the separation of size- or age-classes impossible. This applies to Notoacmea petterdi and Siphonaria denticulata, and probably to all long-lived species. Secondly, separation is usually impossible when there is prolonged recruitment (e.g. Montfortula rugosa). When recruitment occurs during a period of 3-4 months, as in Patelloida alticostata, P. latistrigata, Siphonaria denticulata and S. virgulata, the mean size of cohorts of juveniles will be depressed for several months and variance will increase because of the continued addition of large numbers of small individuals to the population during this time. This leads to an under-estimation of rates of growth during the period of recruitment, and makes it impossible to estimate the mortality of newly-recruited juveniles. Various models have been proposed to minimize or eliminate these and other problems (e.g. Ebert, 1973; Van Sickle, 1977). All these models assume constant rates of mortality, a stationary age distribution, constant recruitment confmed to a small interval of the year, and most also assume a theoretical growth model of the Von Bertalanffy type. These assumptions are rarely met in natural populations (Yamaguchi, 1975) and the models are of limited value, especially when a detailed study of the dynamics of a given population is required. Size-frequency distributions have also been used to estimate the longevity of

GROWTH,

LONGEVITY

AND

RECRUITMENT

OF LIMPETS

165

members of a population (e.g. Moore, 1937). These procedures assume that mortality occurs at a constant rate throughout life and that the number of individuals in corresponding cohorts is approximately the same from year to year. Because these assumptions are often tenuous, and because the separation of adults into discrete cohorts is impossible for long-lived species, estimates of longevity based on the history of marked individuals are likely to be more accurate than estimates made from size-frequency data. It has often been stated that rapid growth is directly related to rapid mortality (Ebert, 1975) and longevity has been shown to be inversely related to rate of growth for several limpets (e.g. Frank, 1965a; Lewis & Bowman, 1975). Collisella scabra appears to be an exception to this generalisation (Sutherland, 1970; discussion in Choat, 1977). Of the species studied here, Notoacmea petterdi grows slowest and lives longest, whereas Siphonaria virgulata grows fastest and has the shortest lifespan. Patelloida latistrigata, however, grows slowly but lives for only 3-4 yr, whereas its congener, P. alticostata, grows faster and lives longer. The apparently anomalous case of P. latistrigata may be the result of its close association with barnacles, which may limit the maximum size to which it can grow and hence its growth and longevity (Creese, in prep.). The relationship between growth and mortality within populations of a single species also has important implications for the use of size-frequencies. Adult cohorts of both P. alticostata and Siphonaria virgulata suffered great and variable mortality. The data from marked S. virgulata suggested that it was the fastest growing individuals that were suffering the greatest mortality. Such a pattern of differential mortality within a cohort could lead to an underestimation of rates of growth. This would apply in particular to short-lived species which are sampled at widelyspaced intervals (e.g. S. virgulata). Such a mechanism might explain why rates of growth calculated for marked individuals were faster for this species than those obtained from size-frequency data. Many more data using larger numbers of marked individuals are necessary, however, to clarify the relationship between growth and mortality. The above considerations argue that size-frequency analysis is most applicable to short-lived species (< 5 yr, say) with relatively restricted periods of recruitment and rapid enough growth so that age cohorts can be confidently distinguished over long periods of time, preferably until they disappear from the population rather than merge with faster growing cohorts. Ideally, mortality within a cohort should be slow and relatively constant over most of the lifespan of that cohort. In the present study, Patelloida latistrigata is the only species that is well suited to the use of size-frequencies in calculating rates of growth and mortality. The estimates obtained for animals of all ages closely corresponded to the estimates obtained from marked individuals. Furthermore, a few size distributions constructed at widely spaced intervals are of limited value when considered in isolation, and independent supporting data should be simultaneously collected from marked

166

R. G. CREESE

individuals wherever possible. This applies particularly to those benthic organisms that are easy to mark and relocate (e.g. sessile species and predominantly sedentary species such as limpets). For all species studied here, rates estimated from marked individuals are considered to be more accurate than those obtained from sizefrequency analyses. LIFE HISTORY

CHARACTERISTICS

Data on the growth, mortality and recruitment of the six species of limpets were collected primarily as a basis for further ecological studies involving manipulative experiments (Creese, 1980~ and in prep.). They can also be used, however, to compare the life-history characteristics of these species. Such a comparison can only be considered as preliminary, because the data were collected from only small areas (50-100 m’) on one shore. Information from populations in other places is needed before any comprehensive statement about their “life-history strategies” can be made. TABLE VI

Summary

of the growth,

Period of

longevity

and recruitment

AS

Size at

Species

recruitment

(yr)

age (mm)

rugosa

Continuous

P. latisrrigata

Nov.-March

P. alticosta1a

Dec.-March & April-May

I 2 3 1 2 3 1 2 4 6 1 2 5 IO I 2 4 6 1 2 3

M.

N. prtterdi

S. denticulata

July-Sept.

March-July

March-July

212 z IS 20 9 12 14 l&l2 15 19 21 10 12 15 17 9 12 16 18 12 16 18

Max. size found (mm) 22

of six species of limpet. Estimated longevity (yr)

Season of max. growth

>3

Unknown

15.1

3

NolIe

22.3

5-6

NOIK

19.9

>lO

Winter and spring

21.8

26

Autumn

18.0

2-3

Autumn

Several patterns of growth, longevity and recruitment are apparent for the limpets studied here (Table VI). Notoacmea petterdi grows rapidly during its first year on the shore, but very slowly thereafter, and is long lived (Table VI and Parry, 1977). Little mortality is found at high levels on the shore, although occasional “catastrophic” mortality may occur (Creese, 1980~). Mortality is greater at low levels

GROWTH,

because

of increased

LONGEVITY

intraspecific

ment to these levels (Creese,

AND RECRUITMENT

competition

1980~). Putelloidu

which

OF LIMPETS

is a result

alticostata

167

of greater

grows reasonably

recruitrapidly

and was estimated to live 5-6 yr. This species has a similar rate of growth in Victoria, but attains a larger maximum size, and therefore lives longer (Parry, 1977). Black (1977) has reported

faster rates of growth

and a larger maximum

size for members

of this species in Western Australia. At Cape Banks, the lowest regions of the intertidal zone are characterized by an extensive belt of macroalgae which results in the absence of most grazers (Underwood & Jernakoff, 1981). Although the largest P. alticostuta found intertidally was only 22.3 mm, larger individuals (up to 40 mm) are found subtidally below this belt of algae. The dynamics of these subtidal populations are unknown. P. latistrigata is a small limpet which grows slowly and reaches a size of only 13-14 mm after 3 yr. Great mortality occurs during its third year. The two pulmonate limpets show different patterns of growth and mortality. Siphonaria virgulata grew faster at all sizes than S. denticulata, had greater rates of adult mortality and was short-lived compared to its congener. Data for Montfortula rugosa are scarce, but it appears that growth is reasonably rapid, that juvenile mortality is great, and that the largest individuals in the population are > 3 yr old. The rates of growth of all species presented here are average rates only. The sizefrequency analyses indicate that rate of growth may vary from year to year for cohorts of corresponding age. Results from marked individuals also showed that limpets of similar sizes had significantly different rates of growth between years and that limpets of the same age showed considerable variability in growth even over the same time period. Patterns of growth and longevity are obviously plastic within these species. Many factors, both physical and biological, can influence the rate of growth of limpets (Branch, 1974b; Lewis & Bowman, 1975). The most frequently recognized of these is availability of food. Absolute abundance of microalgal food may vary on a seasonal

basis or between

different

microhabitats,

as suggested

by Sutherland

(1970) Branch (1974b) and Parry (1977). The time available for feeding may also influence the amount of food available to feeding limpets (Frank, 1965a; Sutherland, 1970). The density of other grazers (either of the same or another species) in the immediate vicinity of a limpet may determine the relative amount of food available to it. Experimental studies have shown that an increase in the density of grazers can reduce the rate of growth of individual limpets and may ultimately cause an increase in mortality (e.g. Choat, 1977; Haven, 1973; Sutherland, 1970; Underwood, 1979). This relationship has been established, by experimental manipulations, for two of the species studied here: Patelloida alticostata (Black, 1977) and Notoacmeapetterdi (Creese, 1980~) and is probably important in the other species as well. N. petterdi shows a seasonal pattern of growth, with growth being slowest between December and June. This period of depressed growth corresponds to the period prior to spawning (Creese, 198Ob), and it is possible that these limpets are channeling

R. G. CREESE

168

all available species

energy

into

of Siphonaria

occurring

(Creese,

seasonal

variations

gonadal

grew fastest

production

1980a). It is very difficult, in rates

at this time.

in autumn,

of growth.

Such

a period however, variations

In contrast,

when

to ascribe can

the two

spawning

is also

precise causes to

be correlated

with

changes in availability of food (e.g. Sutherland, 1970) changes in temperature (Seapy, 1966; Blackmore, 1969), or changes in the condition of the gonad (Notoacmea petterdi in this study, and Ward, 1967). All these factors are usually highly correlated, and have been examined only in terms of energy budgets (e.g. McMahon, 1975; Parry, 1978). No experimental studies have yet been devised to examine the cause-and-effect relationships between these seasonal components. Differences in the structure of the habitat (e.g. the presence or absence of sessile organisms) may also result in variable population structures and patterns of growth on a very local scale (Giesel, 1969; Branch, 1976; Bowman & Lewis, 1977; Choat, 1977). Local differences may be important for the populations at Cape Banks, especially for Patelloida latistrigata which generally lives in association with barnacles (Creese, in prep.). Patterns of recruitment of juveniles also differed among the six species. Unfortunately, these estimates of recruitment apply only to individuals >4 mm (except for Notoacmea petterdi and Patelloida latistrigata), and are restricted to a very limited part of the shore where adults of a given species were well established. Newly-settled juveniles (< 4 mm) of all species except Notoacmeapetterdi were often found scattered over the entire shore, but could not be sampled accurately. In areas other than the “typical” habitats of the adults, very few juveniles survived, and most newly-settled juveniles persisted for only a few months in these areas. Contingency tables were constructed using the data for the months indicated in Table V to test for associations between the densities of adults and the density of juvenile recruits in each of the permanent quadrats. For Patelloida alticostata, Siphonatia denticulata, S. virgulata and Notoacmeapetterdi, there were no significant differences (P > 0.05) in the proportions of juveniles with respect to adults in any of the quadrats, suggesting that areas with large numbers of adults were also areas where recruitment was more successful (see also fatistrigata there was a significant inverse relationship and

the numbers

apparent, Although

of recruits

(Creese,

in prep.).

however, in areas of exceptionally few quantitative data are available,

Black, 1977). For Patelloida between the densities of adults This

relationship

only

became

great densities (>2000 adults/m’). it appears, therefore, that settlement

of the larvae of these species is haphazard (except for Notoacmea petterdi; Creese, 198Oc), and that rates of mortality of newly-settled limpets are very high except in those patches on the shore where adults of that species are well established. Even within these favourable patches, the intensity of recruitment varies from year to year, as has been reported for other species of limpets (e.g. Frank, 1965a; Bowman & Lewis, 1977). The foregoing considerations lead to the conclusion that all six species, in

GROWTH. LONGEVITY AND RECRUITMENT

OF LIMPETS

169

common with most other limpets that have been investigated, are characterised by indeterminate growth, and highly variable patterns of mortality and recruitment. Aspects of the reproduction of these six species of limpets have been reported elsewhere (Creese, 1980a,b). All are iteroparous and show reproductive maturity within 1 yr after recruitment to the shore regardless of the rate of growth of the juveniles. For instance, all N. petterdi which settled during the winter of 1976 had mature gametes in May 1977 even though those at the high-shore level had attained a mean size of > 10 mm whereas those lower on the shore were considerably smaller. This means that all species can begin breeding at an early age, although these small limpets may not contribute very much to the total reproductive output. All species have dispersive larvae, although the mode of reproduction differs between species (Creese, 1980a,b). The three species of acmaeid limpet and Mon!fortulu rugosa are broadcast fertilizers, producing large numbers of short-lived lecithotrophic larvae (Anderson, 1965). The two pulmonate limpets have internal fertilization and produce either benthic egg ribbons (Siphonaria denticulata) or pelagic egg capsules (S. virgulata). Their veligers are planktotrophic and are potentially able to spend long periods in the plankton, and therefore these species have potentially greater powers of dispersal than the other four species. Because fecundity increases with size (Branch, 1974a; Creese, 1980a,b), it is advantageous to grow as large and as quickly as possible. Growth, however, is generally indeterminate, and rates of mortality of both adults and juveniles and the rate of recruitment are variable and unpredictable. The ability to reproduce at an early age and the adoption of iteroparity in these species act to insure against complete failure as a result of these unpredictable fluctuations. This form of “bethedging” is not unusual amongst marine invertebrates (see review by Stearns, 1976). The two species of Siphonaria provide the basis for an interesting comparison, as both occur over the same geographic range, live in the same region of the shore and eat the same food (Creese, 1978). S. dent&data is relatively sedentary, is long lived, has slow growth and lays benthic egg ribbons, whereas S. virgulata is more mobile, is short lived, has rapid growth and produces pelagic egg capsules. The reproductive output of S. virguluta is potentially as great as that for S. denticulata (Creese, 1980a). Although further data are needed, this situation suggests that more than one life history pattern is possible under the same set of environmental conditions (e.g. Calow & Woollhead, 1977). It also illustrates the point that there may be at least as much variability within a genus as there is between widely separated taxa such as the three families of limpets studied here.

ACKNOWLEDGEMENTS

This work was carried out whilst in receipt of an Australian Postgraduate Research Award, and was supported by a University of Sydney Research Grant.

170

R. G. CREESE

I am indebted to Dr. A. J. Underwood for his advice and encouragement throughout the work, and to him, Dr. P. W. Frank and Dr. G. D. Parry for critically reading the manuscript. REFERENCES ARE, N., 1932. The age and growth of the limpet (Acmaea doorsuosa). Scienr. Rep. Tohuku imp. Univ., Vol. 7, pp. 347-363. ANDERSON, D.T., 1965. The reproduction and early life histories of the gdstropods Notoacmaea prtterdi, Chiazacmaea flammen and Patelloida alticostata. Proc. Linn. Sot. N.S. W., Vol. 90, pp. 106-l 14. BLACK, R., 1977. Population regulation in the intertidal limpet Patelloida alticosrata (Angas. 1865). Oecologia (Beri.), Vol. 30, pp. 9-22. BLACKMORE, D. T., 1969. Studies of Pate/la vuigata (L.) I. Growth, reproduction and zonal distribution. J. exp. mar. Biol. Ecol.. Vol. 3, pp. 200-213. BOWMAN, R.S. & J.R. LEWIS, 1977. Annual fluctuations in the recruitment of Put&z wdgata L. J. mar. biol. Ass. U.K., Vol. 51, pp. 793-816. BRANCH, G. M., 1974a. The ecology of Pate/la L. from the Cape Peninsula, South Africa. 11. Reproductive cycles. Trans. R. Sot. S. Afr., Vol. 41, pp. 11 l-160. BRANCH, G. M., 1974b. The ecology of Parella L. from the Cape Peninsula, South Africa. III. Growth. Trans. R. Sot. S. Afr., Vol. 41, pp. 161-193. BRANCH, G. M., 1976. Interspecific competition experienced by South African Parella species. $1. Anim. Ecol., Vol. 45, pp. 507-530. CALOW. P. & A.S. WOOLLHEAD, 1977. The relationship between ration, reproductive effort and age specific mortality in the evolution of life history strategies ~ some observations on freshwater triclads. J. Anim. Ecol., Vol. 46, pp. 765-782. CASSIE, R. M., 1954. Some uses of probability paper in the analysis of size frequency distributions. Aust. J. mar. Freshwat. Res., Vol. 42, pp. 783-794. CHOAT, J. H., 1977. The influence of sessile organisms on the population biology of three species of acmaeid limpets. J. exp. mar. Biol. Ecol., Vol. 26, pp. l-26. COLE, L.C.. 1954. The population consequences of life history phenomena. Q, Rev. Biol.. Vol. 29, pp. 103-137. CREESE, R. G., 1978. Ecology and reproductive biology of intertidal limpets. Ph.D. thesis, University of Sydney, 384 pp. CRCESK, R. G., 1980a. The reproductive cycles and fecundities of two species of Siphonuria (Mollusca, Pulmonata) in south-eastern Australia. Aust. J. mar. Freshwat. Res., Vol. 31, pp. 37-47. CREESE, R.G., 1980b. The reproductive cycles and fecundities of four common eastern Australian archaeogastropod limpets (Mollusca : Gastropoda). Aust. J. mar. Freshbvar. Res., Vol. 3 1. pp, 49-59. CREASE, R.G., 1980~. An analysis of distribution and abundance of populations of the high-shore limpet, Notoacmeaperterdi (Tenison-Woods). Oecologia (Berl.J, Vol. 45, pp, 252-260. DAKIN, W. J.. I. BENNETT & E. C. POPE, 1948. A study of certain aspects of the ecology of the intertidal zone of the N.S.W. coast. Aust. J. scienr. Res., Vol. BI, pp. 176-230. DEFVEY, E. S., 1947. Life tables for natural populations of animals. Q. Rev. Biol., Vol. 29, pp. 283-314. EBERT, T. A., 1973. Estimating growth and mortality rates from size data. Oecologia (Ber/.), Vol. 11. pp. 281-298. EBER.r, T. A., 1975. Growth and mortality of post-larval echinoids. Am. Zool., Vol. 15, pp. 755- 777. FRANK, P. W., 1965a. The biodemography of an intertidal snail population. Ecology, Vol. 46, pp. 83 l-844. FRANK, P. W., 1965b. Growth of three species of Acmaea. Veliger, Vol. 7, pp. 201-202. FRANK, P. W., 1968. Life histories and community stability. Ecology, Vol. 49, pp. 355-357. GIESEL. J.T., 1969. Factors influencing the growth and relative growth of Acmuea digitalis, a limpet. Ecology, Vol. 50, pp. 10841086. HAMAI. I., 1937. Some notes on relative growth, with special reference to the growth of limpets. Scient. Rep. Tohuku imp. Univ., Vol. 12, pp. 71-95.

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LONGEVITY

AND

RECRUITMENT

OF LIMPETS

171

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