Growth and mortality of the predatory intertidal whelk Morula Marginalba Blainville (Muricidae): The effects of different species of prey

J. Exp. Mar. Biol. Ecol., 1984, Vol. 75, pp. 1-17 Elsevier

JEM 206

GROWTH

AND MORTALITY

MORULA

OF THE PREDATORY

INTERTIDAL

Blainville (MURICIDAE):

MARGZNALBA

WHELK

THE EFFECTS OF

DIFFERENT SPECIES OF PREY

M. J.

MORAN’,

P. G.

Department of Zoology,

FAIRWEATHER

and A. J.

UNDERWOOD*

University of Sydney, Sydney, N.S. W. 2006. Australia

Abstract: Morula marginalba Blainville is a common predatory gastropod on rocky shores of southeastern Australia. Mean size of Morula varied in accordance with the species of prey present, both within a shore where a variety of prey were available, and among shores each dominated by a single species of prey. Growth of tagged whelks varied among populations both with respect to the asymptotic size reached by the adult whelks, and the rate of approaching this size. Sampling and short-term experiments on growth in an area with a mixed assemblage of prey confirmed these trends. Mortality also varied significantly among populations, but independently of the pattern of growth. The size structure of a population can be understood as an interaction of the mean and variance of the asymptotic size, and the rate at which animmals in any population approach this size, in comparison with the rate of mortality. Since these can vary independently in relation to different species of prey, a great range of size structures is possible in different habitats. Recruitment ofMorula can vary greatly from year to year, and the success of recruitment into any one population apparently bears no relationship to success in others. These findings are discussed with regard to generalizations about population models, life-histor) characteristics, and predator-prey interactions.

INTRODUCTION

In rocky intertidal communities, the effects of predators on aspects of the population biology of prey organisms have been well documented (e.g. Connell, 1961, 1970; Dayton, 1971; Paine, 1976). While it is recognized that the distribution, abundance, and size of predators may be important influences on their effects on prey (Menge, 1978a,b; Paine, 1976), discussion has centred on those components of the environment that influence the predators themselves (Connell, 1970; Butler, 1979). Feder (1970) and Paine (1976), however, have shown that the size of the starfish Pisaster ochraceus is related to the type of prey available, and Spight (1982) has correlated the population structure and local abundance of predatory thaid gastropods in two small patches of intertidal habitat with temporal changes in the abundances of their prey. Nevertheless, small populations of Thais showed no synchrony in population structure (Spight, 1982). Some intertidal herbivores, in contrast, have attracted attention because of intraspecific differences in abundance and size between populations associated with different levels of food. Sutherland (1970) and Creese (1980) found that growth- and mortality ’ Present address: Marine Research Laboratory, ’ Address for reprints and correspondence. 0022-0981/84/$03.00

0

1984 Elsevier

Science

West Coast Highway,

Publishers

B.V

Waterman,

W.A. 6020. Australia.

2

M.J.MORANET

AL

rate of acmaeid limpets differed between high- and low-shore populations. Lower, dense populations grew more slowly and suffered greater rates of mortality, purportedly because of smaller standing stocks of food at lower levels on the shore. McKillup (1983 ! has also demonstrated that populations of Nussarius pauper&us had different behaviours, recruitment, and mortality depending upon the availability of different types 01‘ food. The type and amount of food is also known to influence the size structure ‘tf urchin populations (Ebert, 1968). Sizes of whelks of the family Muricidae evidently vary from locality to locaht) (Phillips et al., 1973; Menge, 1978a). Taylor (1976) found distinctly different sir
MATERIAL

AND

METHODS

To measure sizes, whelks were collected during August 1978 from areas with different prey on the sandstone rock-platform at Green Point (see Underwood, 1981). Coilections were also made between 1976 and 1978 on shores along the New South Wales coast, from Port Stephens (32”38’S) to Twofold Bay (37”8’S; see Table II). These shores were sampled because they were dominated by different species of potential prey. The prey considered in the present study are hugely sessile species capable or‘ dominating sections of the shore at particular heights, and are readily eaten by Mot&. At least 100 whelks were collected during low tide from haphazardly placed 0.25-m”.

GROWTH

quadrats. nearest

OF WHELKS ON DIFFERENT

The length of the aperture 0.5 mm with Vernier calipers,

butions. Tagged populations near Sydney.

were monitored

3

PREY

of the shell of each whelk was measured to allow comparisons on four sandstone

Each of these shores was chosen

because

of size-frequency

to the distri-

shores in the Botany Bay area it was dominated

by a single

species of prey. Sites dominated by tube-worms, Galeloariu caespitosa (Lamarck) or oysters, Saccostrea commercialis (Iredale & Roughley) were rocks isolated from other rocky areas by deep water and sand. No such isolated areas could be found dominated by the barnacles Chumuesipho columnu Spengler or Tesseropora roseu (Krauss). Apparently isolated populations of Morulu were, however, studied in large areas dominated by each of these barnacles. There was an abundance of prey in all four sites (a cover of 50-80% throughout the study). In each area, every whelk that could be found during two consecutive low tides during June 1977 was collected and measured. All whelks in each OS-mm size-class were individually tagged, unless there were > 20 in that size class, when only a total of 20 was tagged. Small tags of paper marked with Indian ink were placed on the spire of the dry shell and covered with quick-drying epoxy resin. For 2 yr (June 1977 to June 1979), all tagged and untagged whelks were re-measured at z 3-monthly intervals. Sufficient extra whelks of the appropriate sizes were then tagged to make up the required number in each size-class. Whelks were returned to crevices and splashed with water until they had re-attached to the substratum; this procedure ensured that whelks were not dislodged by the next incoming tide. In a previous study (Moran, 1980), linear regressions of monthly and seasonal growth increments on initial size were significant; the same analysis was done here. Sainsbury (1980) has shown that if there is variability among the rates of growth of individuals that reach the size at which growth ceases, plots of growth increment against initial size include a substantial “tail” of large animals that do not grow any more. This causes large biases in the estimation of rates of growth from such data. In our calculations of regressions, therefore, large whelks that had an annual rate of growth within 0.5 mm of zero were omitted. Negative growth was, however, possible where the rate of growth was less than the rate of any erosion of the shell. It was possible that any differences in growth among the four tagged populations might actually be due to the difference in location rather than differences due to diet. The four sites varied in height, wave-action, and other uncontrollable variables (some of which might have caused the different patterns of occupancy by the different types of prey). Although the patterns of final size of the whelks were found to be consistent over several shores dominated by each type of prey (see Table II), the uncontrolled, confounded effect of different sites was a problem in the interpretation of the results. We therefore decided also to test the effects on growth of different types of prey on a single shore. A population of Morula was sampled during March 1980 in a 10 x 10 m area with a mixed assemblage of prey on a shore in the Cape Banks Marine Scientific Research

M.J. MORAN ET AL.

4

Area (Botany Bay). No a highly-preferred prey, Underwood, 1983) was were collected randomly

oysters were present in this area at the time of sampling, but the limpet Putelloidu latiwigatu (Angas) (see Fairweather & plentiful, and was included in place of oysters. Fifty whelks from those eating each of the four prey in the area (Patelloida. Galeolaria, Chamaesipho, and Tesseropora), and measured. Furthermore, two short-term experiments were done in this area to determine the growth of whelks on different types of prey. Fifteen whelks of known starting size were enclosed in stainless-steel mesh cages of 20 x 20 cm and, 3 cm high. To test the hypothesis that diet affects rate of growth, the prey beneath each cage were manipulated so that only one species, or a chosen “mixed” assemblage, was available inside each cage. Re-measurement of the whelks after a known time provided a relative measure of rate of growth on the different diets. Initial densities of prey were great and experiments were terminated before all prey were consumed in any cage. The initial sizes c!l’ the whelks were balanced so that they did not differ among treatments. In the first experiment, in March 1980, the diets examined were the four individual prey species and a complete mixture. Three different size-classes of Moruh, with means of z 10.3, 14.2, and 16.8 mm were included as a second factor. The experiment ran for 18 days, but there was only one cage for each treatment, and thus no estimates of spatial variation were possible. In the second experiment, in July 1980, only small Moruiu (11 .Omm mean) were used. Four cages of each diet were randomly placed on the shore over a total vertical range of some 45 cm (the tidal amplitude at this site is some 1.8 m). Juvenile Tesseropora were examined in place of Chamaesipho, to test for any differences in growth of Morula feeding on different sizes of this barnacle (as the whelks take different amounts of time to eat juvenile and adult Tesseropora, see Fairweather bi Underwood, 1983). After 21 days, the whelks were measured again, and their wet weights determined. These experiments had to be of short duration because it wah important that no whelks ran out of food during the period of measured growth. RESULTS

SAMPLING

OF NATURAL. POPULATIONS

At Green Point, differences in the mean size of Morufa eating each of seven sampled prey species were highly significant (P < 0.005; analysis of variance of means in Table I). The mean size of whelks was positively correlated with the mean weight and maximum weight of prey (Spearman’s rank correlation coefficients 0.96 and 0.78. respectively; both significant, P -=I0.02). Thus, on one shore, small prey (Galeolaria and Chamaesipho) were eaten by the smallest whelks; large prey such as adult Tesseroporu and oysters were eaten by the largest snails. This result is not merely due to the possible bias dealt with by Fairweather & Underwood (1983) (i.e. the increased frequency ol. observation of predators on prey with long handling times) because all of these species of prey have relatively long handling times and there was no correlation between the

GROWTH

OF WHELKS

ON DIFFERENT

PREY

5

sizes of the whelks on each prey and the handling times of the prey (Fairweather, unpubl.) . Sampling on a greater geographic scale revealed a similar trend. The mean size of predatory whelks was associated with the type of prey available (analysis of variance of means in Table II; P < 0.005). Adult size of whelks was larger on shores where large prey species predominated. TABLE I Mean ( i SD) sizes of Morula marginalba feeding on different species of prey on a single shore (Green Point. N.S.W.): n = 50 in each sample; the mean and range of dry flesh weights of prey of each species is shown. sampled over the sizes eaten by Morulu (n > 20 for each species).

Mean size of whelks (mm)

Prey species (Lamarck) - worm Spengler - barnacle Tetruclitelia purpurascens (Wood) - barnacle Brachydonres hirsutus (Lamarck) - mussel Chthamalus antennatus (Darwin) - barnacle Tesseropora rosea (Krauss) - barnacle Saccostrea commercialis (Iredale & Roughley) Galeolaria

10.7 11.6 12.6 14.0 14.4 14.6 15.2

coespitosu

Chamaesipho

columna

- oyster

(1.7) (1.8) (1.7) (3.0) (2.0) (2.8) (3.3)

Mean (range) dry flesh wt (mg) of prey 4 5 13 69 18 9’) I87

(0.3-15) (0.5-6) (1.5-40) ( I .O-260) (1.0-25) (0.9-200) (1.0-500)

TABLE I1 Sizes of Morula

Dominant

prey

Galeolaria

Chamaesipho

on shores

dominated

by different

types of prey.

Shore

Date sampled

Mean (+ SE) size (mm)

No. measured

Bondi Maitland Bay Bundeena

Nov. 1976 Feb. 1977 Oct. 1977

12.42 (0.13) 11.03 (0.10) 11.84 (0.07)

172 450 509

Greenpatch

June

1976

12.88 (0.13)

200

(Jervis Bay) Cronulla Ulladulla

Dec. 1976 Jan. 1977

12.18 (0.15) 12.75 (0.18)

35x 204

Jan. Oct. Oct.

1976 1976 1978

13.80 (0.22) 13.65 (0.11) 14.57 (0.07)

102 204 452

Boydtown

June 1976

15.14 (0.10)

478

(Twofold Bay) Port Stephens Turmiel Point

Nov. 1976 Dec. 1976

13.89 (0.25) 14.97 (0.14)

160 445

(sheltered) Tesseropora

Newcastle Huskisson Ulladulla (exposed)

Saccosfrea

(Port Hacking)

w

onj

6”f

77

’

!

2zix

77;

Il. i-78

1576

ll.iv.78

/ 1510

ll.Vll.

78

j 124

31.x.78

] !

4

152

2.11.79

0

I 2.ii.79 1

/

1

-;

941

23.4~. 79

555

23.~79

GROWTH TAGGING

OF WHELKS

ON DIFFERENT

PREY

EXPERIMENTS

The means and ranges of sizes of adult whelks in each of the four tagged populations were quite consistent

throughout

the 2 yr of sampling

(Fig. 1). The numbers

and sizes

of juvenile whelks were, however, quite variable from time to time, reflecting periods of recruitment, rapid growth and mortality of these smaller snails. The general trend was for a reasonably distinct mode of sizes representing the younger snails, but older size-classes merged together to form a single, coalesced adult group, with an approximately normal distribution in each population (Fig. 1). Some periods of recruitment were obvious; for example, the numerous small snails that appeared in the population on Galeolaria after July 1978. A very conspicuous feature of the data was the reduction or absence of Morda from the areas where they were feeding on barnacles (Chamaesipho and Tesseropora) during the October 1978 and February 1979 censuses. This was due to a temporary migration of whelks to lower areas on the shore, where an exceptionally abundant spatfall of Tesseropora had occurred (see Underwood et al., 1983). The populations eating Chamaesipho and Tesseropora were not isolated, and the tagged whelks in these two areas were clearly part of larger, continuous populations. The data from these two populations are still useful and valid for estimations of rates of growth. They are of no value for estimates of mortality of the whelks, which clearly could and did migrate to other areas at some times. Many of the regressions of growth-increment on initial size were significantly nonlinear in confusing ways (Fig. 2). Therefore, statistically reliable seasonal comparisons of growth on each diet could not be made. Averaged over all four populations, however, the general trend was for markedly seasonal growth, with least growth occurring during the winter-spring (June-October). Moran (1980) has related this seasonal pattern to sea-water temperatures, and the breeding period of the whelks. Growth-increments for the whole year, rather than for each season, were plotted against initial size, and showed linear relationships (Fig. 3). The slopes of these regressions were significantly different among the four populations (analysis of covariance in Table III; P < 0.005). Thus, whelks feeding on different kinds of prey have quite different patterns of growth, and reached different asymptotic sizes after a given period of growth. Survival could be reliably estimated for the two marked populations on isolated rocks with oysters and Galeolaria. In all populations sampled, the recapture rate of tagged juvenile whelks was much less than that of adults. At least in part, this was due simply to their smaller size (i.e. they were more difficult to find and extract from crevices). Consequently, only the rate of survival of non-juvenile whelks was calculated for each of the two years studied, by the regression of the logarithm of the number of adult whelks against time (see also Underwood, 1975). In both years, the slope of this regression was significantly greater for whelks eating Gafeolaria than for those eating oysters (P < 0.05, analysis of covariance; Fig. 4). During 1977-1978, the proportion of Mot-da that had survived for one year on a diet of Galeolaria was 0.41; during

ET AL

M.J. MORAN

. l* . ‘A

OCT-JAN

0‘3

L.

JAN -APR 0.3

. .

.

APR

0

.

I

-1

Jilt

- JUL

-0CT

.

1

-I J

STARTING

SIZE

(mm)

Fig. 2. Growth increments during three months for individual tagged whelks during each Jason, plotter against initial size (aperture length) ofthe straits: all increments are corrected to a total of 90 days ofgrowth. to compensate for slight variations in the interval between sampling the different populations; 3, whclhs feeding on the oyster Succosrrea; 0. on the worm Galeolariu; A, on the barnacle 7’esserapom: A. on ttx barnacle Chamaesipho.

‘I’ABLt

Analysis

of covariance

111

of regresstons of annual growth increments on initial size for tagged Morulu on different species of prey (see Fig. 3). Intercept

Prey

(mm

Guieolaritr Chamaesipho Tessetoporcr

960 4.87 7.N

SlICl~OWtYI

8.10

1

Regression coefficient -~0.74 0.26 0.51 0.50

r’

Cl.1:

O.6 1 0.36 0.66 0.49

26

Deviations Source

of variation

ss _

From individual regressions From common regression Among regression coefftcients

69.56 78.67 9.1 1

~~

from regression MS ~_

140 143

0.50 0.55 3.04

3

(I’

27 25 62

d.f. ._~..

populations

f-ratill

(1 I

P -2:o.oo:,

GROWTH

OF WHELKS

ON DIFFERENT

9

PREY

1978-1979, the proportion was 0.49. This represents a fast rate of mortality, with more than half the adults dying during each year. In contrast, the whelks eating oysters showed no measurable mortality during the 2 yr (Fig. 4). Rates of mortality showed no seasonal trends, and whelks apparently died at similar rates throughout the year, in contrast to Spight’s (1982) demonstration of marked seasonal variability in mortality of Thais emarginata and T. lamellosa.

10 INITIAL

SIZE

20

15

OF WHELKS

(mm)

Fig. 3. Annual growth increment of tagged whelks on different prey: each point represents the mean increment of all tagged Morulu of a given initial size that were still present in samples taken 1 yr later; arrows indicate the asymptotic size calculated from the regressions for each population (see Table III for details).

M. J. MORAN

IO

ET AL.

1978 -79

1977-78

On 0

m

Soccostrea 0

n

0 q

6

------h_ On Galeolariti

4

I 0

I

I 05

I

1 1.0 TIME

I

I

I

I

0.5

0

I

1.0

(Years)

Fig. 4. Rates of survival of whelks older than one year at the start of the study feeding on oystc~-h (Saccostrea) and worms (Galeoluriu): data are presented separately for two years of study; whelks WC’K tagged some weeks before the tirst sample; increases in numbers are due to recovery of previously mis\,t,ii animals.

CAGING

EXPERIMENl-S

On a single stretch of shore, whelks eating Tesseropora rosea or the limpet Putellodtr latistrigata were significantly larger than those eating Galeolaria and Chamaesipho (analysis of variance of datain Table IV; P -c 0.00 1). As described earlier, larger whelks tended to be found on larger prey. In the first caging experiment, growth decreased with increasing initial size (Fig. 5 1. Because a few small snails escaped from cages, the data will be considered separately for each size-class. The largest size of whelks investigated grew very little during the experiment. Thus, the final sizes (and, therefore, the growth-rates) did not show any difference among the different diets (analysis of variance, P > 0.10). Differences in TABLE IV

Sizes of whelks

feeding on different

prey in experimental prey).

areas

at Cape Banks (n = SO whelk& on WC:! ----.---.

Mean size ( + st) Species

of prey

Galeolariu caespitosu Chamaesipho columna Tesseropora rorea Patelloida latistrigata

(mm) 12.12 11.78 15.46 16.06

(0.21) (0.20) (0.15) (0.18)

-

GROWTH

OF WHELKS

mean growth due to diet were, however, even though

the experiment

ON DIFFERENT

detected

11

PREY

in the smaller two sizes of whelks,

was only of 18 days’ duration

(analysis

of variance,

P < 0.05). Notably, for small snails (initial aperture length 10.3 mm), there was relatively little growth on a diet of Patelloida, Galeolaria or Chamaesipho (which did not differ significantly; SNK tests, P > 0.05). There was significantly greater Eyowth on a mixed diet or when eating Tesseropora (again, these were not different;

SNK tests). The

regressions of growth for snails on different diets (Table III) also predict greater growth for 10.3-mm snails on a diet of Tesseropora than on diets of Chamaesipho or Galeolaria. In contrast, Tesseropora, Patelloida, and Chamaesipho provided the greatest growth for medium-sized snails (initially 14.2 mm). There was no difference among these three diets (SNK tests, P > 0.05). Growth of medium-sized whelks was less on a mixed diet or when eating Galeolaria (see Fig. 5). For these medium snails (aperture length 14.2 mm), the regressions in Table III also predict greater growth on a diet of Chamaesipho or Tesseropora than on a diet of Galeolaria.

EzlMIXED

cl GALEOLARIA q CHAMAESIPHO

DIET

PATELLOIDA

q TESSEROPORA

5 g

1.0

2 ; 05

z 3

12

10

INITIAL

14 SIZE

OF WHELKS

16 (mm)

Fig. 5. Mean growth increment (+ SE) during 18 days in experimental cages at Cape Banks: three sizes of Morulu were enclosed with each of five different diets; brackets indicate mean starting sizes of the three groups (10.3, 14.2, and 16.8 mm, respectively); there was no difference in the amount of growth of the largest size of whelk on any diet; other differences are discussed in the text.

TABLE V Mean growth ( + SE) of whelks on different diets during 21 days of the second experiment at Cape Banks: data are mean increments (mm) for small whelks (I 1.0 mm mean); n = 32 snails pooled from 4 replicate cages; horizontal line underlies means not significantly different at P = 0.05, by SNK tests.

Diet

Mean growth

Mixed

Galeolaria

Patelloida

0.58 (0.12)

0.44 (0.09)

- 0.01 (0.05)

Tesseropora

Tesseropora

(adult)

(juvenile)

- 0.12 (0.02)

- 0.18 (0.03)

12

M.J. MORAN ET AL.

Growth in the second experiment (in mid-winter) was less than for similar-sized whelks during the first expdent (early autumn; compare the results in Fig. 5 and Table V). This was to be expected given the seasonal differences demonstrated by the tagged populations (Fig. 4). Growth increments again differed during the second experiment (analysis of variance, P -c 0.01). Growth varied from diet to diet in a similar manner to that in the previous experiment, except that the ranked growth of whelks eating F~~~~i~~~ and T~~~~r~~~~~were reversed. Juvenile ~~ss~~~~or~yielded less growth than did adult barnacles of this species (Table V). Weights of the whelks did not, however, show any significant difference with respect to diets (P > 0.05).

DISXJSSION

In other studies, comparisons have been made among the life-histo~es of different muricid species (e.g. Spight et ul., 1974). In the present study, we have demonstrated that one species can exhibit quite different life-history characteristics under different conditions. For example, our results indicate that Mot& eating oysters have a stable. long-lived adult population, with only a trickle of recruits into it. Whelks eating Galealuriu, in contrast, die at a rate of > 50”/, of adults per year and the population is accordingly dominated by juveniles. Our studies of growth in natural populations of whelks on different diets are not unequivocal. Differences in rates of growth or mortality from one population to another may, as suggested, be due to the different diets. It is, however, impossible to eliminate the alternative, confounded hypothesis that rates of growth differ from site to site simply because the whelks are in different places. Site-&ects could be due to differences in such factors as time available for foraging, wave-action, desiccation, etc., or even dur to genetic differences in the populations of whelks that recruited to the different sites. The concIusions about growth were to a great extent validated by the caging experiments. These demonstrated conclusively that diKerences in diet caused differences III growth within a single site. The differences in growth of caged whelks were of sufftcient magnitude, albeit over a short period, to reinforce the interpretation of differences among natural populations being due to diet rather than site-effects. In addition, the patterns of sizes of whelks were found to be consistent over several widely-spaced sets of shores, each set dominated by a different species of prey (Table XI). This, again. suggests that differences in size from shore to shore are more likely to be caused by Merent prey than to be simply the result of variations from shore to shore in the rate of growth. Spight (198 1) examined seasonal rates of growth of three species of T&is that occup> different levels of the shore, and therefore encounter different types and abundances of available prey. He found asynchronies in the patterns of growth among the species. In the seasonal data presented here for different populations of Monrlu (see Fig. 2), it 1s clear that whelks on all four species of prey showed greatest growth during autumn

GROWTH

OF WHELKS ON DIFFERENT

PREY

13

(January to April), and little or no growth during spring (July to October). There was some asynchrony among the tagged populations, for example whelks on Saccostrea and Galeoluria increased their rates of growth earlier than those on other prey (Fig. 2). Thus, related species in one place (Spight, 1981), or different populations of a single species in different places can show variations in seasonal patterns of growth. This suggests that factors governing growth are more complex than just the nutritive value of different types of prey, or the effects of seasonal factors on the rate of feeding. Growth may, for example, be interrupted by breeding activity. In the tagged populations of the present study, non-linearities in the regression of growth-increment on size were most marked from October to January. During this period, whelks were breeding, and virtually no whelk > 12.5 mm aperture length showed positive growth. This and other factors that affect the rate of feeding and/or foraging activity (e.g. height on the shore, abundance or nutritive value of prey) may interact with the time of year to influence growth. Two interacting processes seem sufficient to produce the observed pattern of different size of whelks on different types of prey. These were the growth and survival of the whelks. Our conclusions for Mordu marginalba parallel in many respects those reached by Spight (1972) for Thais lumellosa. From the present study, two different aspects of growth proved to be important determinants of final size of the whelks. These were the asymptotic size reached by adult whelks (as determined by the point where a regression of growth increment on initial size intercepts the abscissa, see Figs. 2 and 3), and the rate at which animals approach this asymptote (i.e. the slope of the regression, see Fig. 3, Table III). There is variance associated with each of these variables, due to individual variations in growth. If a large proportion of animals in a population survive long enough to grow to their asymptotic size, there will be an accumulation of animals around this size. These adult whelks have a range of sizes above and below the mean asymptotic size; this is related to the variance within each population. For example, whelks in a population eating Galeolaria grew rapidly towards their asymptotic size, but there was little accumulation of snails at this large size because of the low survival. For whelks on a diet of oysters, however, the rate of mortality was so small that a very large proportion of the whole population was scattered around the asymptotic size (Fig. 3), despite a relatively slower rate of growth. The size-frequency distribution of adults can, therefore, be understood as an interaction of three factors: mean asymptotic size, its variance, and a complex factor consisting of the rate of approach to asymptotic size compared with the rate of mortality. Rates of mortality of whelks eating Chamaesipho or Tesseropora could not be measured reliably. Examination of the available size-frequency distributions may, however, provide some clues. For instance, there were similar sharp decreases in the number of whelks larger than the asymptotic size (Fig. 3) in the two populations eating Tesseroporu and Galeolaria. This suggests a more similar relationship between rate of mortality and the rate of approach to asymptotic size in whelks on diets of Tesseropora and Galeolaria than between whelks on diets of Tesseropora and oysters. Mortality of whelks eating Tesseroporu may, therefore, be expected to be less than the rate of those eating Galeolaria,

14

M. J. MORAN ET AL

because the former whelks approached their asymptotic size at a slower rate than did the latter population. The rate at which Morula on a diet of Chamaesipho approached their asymptotic size was much slower than that for other diets (Fig. 3). The absence of an accumulation of‘ whelks around the asymptote was evidence that rates of mortality, or emigration to areas with better supphes of food, were not correspondingly reduced. Chamaesipho anti Galeolaria are less-preferred prey for Morula than are oysters, Pateifoida and the larger barnacles (Moran, 1980; Fair-weather & Underwood, 1983). As discussed above, however, whelks grew rapidly on Gaieobria and slowly on Chamaesipho. Thus, there is no simple relationship between rate of growth and preference for particular prey. While it would have been desirable to measure the effect of different diets on reproductive output of Mu&a, it was not possible to do so in the present study. For many marine invertebrates, however, the annual reproductive output of an individuai female of a given species is dependent on body-size (e.g. Barnes & Barnes, 1968; Spight et al., 1974). Other potential advantages of large adult size include access to a widet range of types and sizes of prey (Fairweather, unpubl.), and escape from certain causes of death (e.g. desiccation, predation; see Connell, 1975). Recruitment of Morula is quite variable and apparently independent of the numbers or sizes of the adult breeding population on any shore (see the changes in juvenile size-classes of whelks in Fig. 1). Such variations in recruitment have been documenteci for other muricids (Spight, 1974, 1982) and local invertebrate species (e.g. Denley & Underwood, 1979; Creese, 1980; Underwood & Denley, in press; Underwood &L McFadyen, 1983). The various prey species in the present study have similar irregularities in recruitment: oysters (in 1976) and Tesseropora (1975 and 1978) have had years of very intense recruitment into some shores during the last ten years. Chamaesipho recruited densely at Green Paint in 1974, but has had insignificant recruitment on most shores examined since 1979 (Underwood, unpubl.). Where the relative proportions of different prey change over time, the population dynamics of Morufa will not be related to the total abundance of all types of prey, but rather to the abundance of the most highly-preferred prey species present. Accomodation to any decline in the abundance of the most highly-preferred prey wili not occur by a rapid decline in the abundance of the predator, but by shifts in diet to successively less-preferred prey with concomitant successive changes in rates of growth and survivorship. Such patterns will, in turn, influence the character and structure of the whole community (see Hughes, 1980; Underwood et al., 1983). For example, size of predatory whelks is often related to the rate of feeding (i.e. a developmental response as discussed by Murdoch, 1971; see examples in Menge, 1974; Edwards & Huebner, 1977; Bayne & Scullard, 1978; Berry, 1982; Broom, 1982). Thus, the previous feeding history of a population of predators may well determine the prevailing pattern of growth and asymptotic size. This, in turn, through relationships of sizes of predators to predatory behaviour may influence the survival of subsequent recruitments of prey species

GROWTHOFWHELKSONDIFFERENTPREY

15

and, therefore, influence the structure of the intertidal community for long periods. For example, a substantial proportion of a new spatfall of Tesseroporu might survive and reproduce in an area of shore previously dominated by Galeolaria (where whelks are likely to be small and relatively sparse). In an area previously dominated by oysters, where the whelks are large and more numerous, the barnacles would suffer greater mortality. Factors such as rates of growth and mortality of predators on different types of prey, and the effects of diet and learning on the behaviour of predators (see Morgan, 1972; Pratt, 1976) might perhaps be incorporated into models of predator-prey interactions. Classical population models, in which the abundance of recruits in each generation is considered to be a function (often a simple function) of the abundance of the parental generation (e.g. Cushing & Harris, 1973; May et al., 1979; Pimm, 1982) are clearly not applicable to rocky intertidal communities in southeastern Australia (see also Underwood & Denley, in press; Underwood et al., 1983). The present paper does not offer any alternative model, but demonstrates the importance of the link between rates of growth and mortality of a major predator, and the availability of different species of prey. This demonstrates an addition to the complexities necessary before the system could be satisfactorily modelled. Spatial variations in rates of growth and mortality of species in intertidal communities increase the complexity of interactions among species over and above the inherent complexity caused by variations in the intensity and timing of recruitment of these species.

ACKNOWLEDGEMENTS

This study was supported by Commonwealth Postgraduate Research Awards to M.J.M. and P.G.F., funds from the University of Sydney Research Grant, and from the Australian Research Grants Committee (to A.J.U.). We are grateful to Professor D. T. Anderson, Dr. P. A. Underwood, Ms. M. Wynne-Jones, Mr. P. Jernakoff and our colleagues, past and present, in the Ross Street Marine Laboratories for discussion, advice and help in the field-work and preparation of the paper; for the latter we also thank two anonymous referees.

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