Prey selection and the impact of the starfish Marthasterias glacialis (L.) and other predators on the mussel Choromytilus Meridionalis (Krauss)

J. E.up. Mar. Biol. Ecol., 1984, Vol. 75, pp. 19-36 Elsevier

19

JEM 210

PREY SELECTION AND THE IMPACT OF THE STARFISH

MARTHASTERZAS

GLACZALZS (L.) AND OTHER PREDATORS ON THE

MUSSEL CHOROMYTZLUS

MERZDZONALZS

(Krauss)

A. J. PENNEY Seu Fisheries Research Instirute. Private Bag X2, Rogge Bay 8012. South Africa and

C. L. GRIFFITHS Zoology Department. University of Cape Town, Rondebosch 7700. South Africa Abstract: The diet of the starfish. Marthasferiasglacialis (L.), consists of a variety of mollusc species. as well as ascidians and barnacles. Starfish densities are maximal where mussels, Choromytilus meridionalis (Krauss), are abundant and in such areas mussels form the bulk of the diet. Laboratory feeding experiments indicate that Marthasrerias glacialis select mussels of particular sizes and that the length of prey taken is an increasing function of predator arm length. The time taken to consume each mussel is determined by the ratio of shell length to starfish size. The number of mussels consumed per day increases only slightly with starfish size, but because the prey taken increase in size, energy consumption is maintained at a relatively consistent I ‘Y.of predator body energy per day. Using prey selection and feeding rate data for different sized starfish, predictive three dimensional predation surfaces are developed for a natural starfish population feeding on either one or two cohort Choromytilus meridionalis populations. The models indicate that predatory effort should be concentrated on the smallest mussels when a single adult cohort is present, but on recruiting mussels just above the minimum prey size limit where two cohorts are present. Other major predators of mussels, the rock lobster, Jaw lalandii (Mime Edwards), and the whelk, Natica tecta Anton, appear to select similar size-ranges of prey to starfish, despite their differing body forms and feeding methods. Since the juveniles of all three predators can only take small mussels, predator recruitment may well depend upon the successful settlement of strong mussel cohorts. Evidence for such entrainment of predator cohorts to settlements of mussels is presented.

Many marine predators are known to be selective in the-size range of prey they consume. The size of prey taken is generally an increasing function of individual predator size and predators display both upper and lower prey size limits, beyond which their prey are protected in “refuges in size” (Paine, 1965, 1974, 1976; Dayton, 1971; Menge & Menge, 1974; Sutherland, 1974; Leviten, 1976; Vince eta/., 1976; Edwards & Huebner, 1977; Franz, 1977; Griffiths & Seiderer, 1980; Griffrths, 1981a). Within these ultimate size constraints predators may select prey in such a way as to maximize net energy gain (Hughes, 1980), particularly where prey handling time is large in relation to the time taken to locate prey (Elner & Hughes, 1978). Depending on the predation pressure, such prey-size preferences can profoundly affect prey population 0022-0981/84/$03.00

0

1984 Elsevier

Science

Publishers

B.V.

20

A.J.PENNEY AND CL. CRIFFITHS

structure, particularly by depleting prey that fall within the preferred size range. Car&us maenas, for example, has been shown to be a voracious omnivore that may influence

both the distribution and population dynamics of its prey (Ropes, 1969; Reise, 1977) to the extent of decimating commercial Mytilus, Mya, Gemma and Mercenariu beds (Ropes, 1969; Walne & Dean, 1972; Dare & Edwards, 1976). Predation by the crabs Cancer and Portunus can also control the distribution of Mytilus edulis (Ebling et ai.. 1964). Selective predation on prey populations may also produce bimodal prey sizodistributions, such as those caused by Cancer and Carcinus predation on Modiolab modiolus (Seed & Brown, 1975) Lunatia heros predation on Mya arenaria (Commitc~, 1982) and Jasus lalandii feeding on Aulacomya ater (GritIiths & Seiderer, 1980). The black mussel, Choromytilus meridionalis, forms extensive beds in the lower intertidal and subtidal zones along the South African west and southwest coasts (Grifliths, 1981b). C. meridionalis is preyed upon by a variety of predators, including fish, such as the musselcrackers Sparodon durbanensis and Cymatoceps nusutus, the keip gull Larus dominicanus, the oystercatcher Haematopus moquini, the rock lobster Jasus lalandii, the gastropods Natica tecta and Nucella cingulata and the star&h MarthasteriaJ glacialis (Griffiths, 1981b). The predatory effects of two of the resident invertebrate predators have been studied. Jasus lalandii is a major benthic predator on shallow sublittoral reefs (Field et al., 1977 ; Velimirov et al., 1977) where it preys mainly on the mussels Aulacomya ater and Choromytilus meridionalis (Heydorn, 1969; Newman & Pollock, 1974; Pollock, 1978, 1979). Its feeding rate and prey preferences have been discussed by GritXths & Seiderer (1980). Natica tecta occurs in high densities on intertidal Choromytilus meridionab beds in False Bay where it feeds entirely on mussels (GrifXths, 1981a). The sizes of C. meridionalis taken by both Jasus lalandit’(Griffiths & Seiderer, 1980) and Naticu tecta (Griffiths, 198 la) are an increasing function of predator size and both predators only take prey within restricted upper and lower size limits. Marthasterias glacialis has previously been reported to be a mollusc predator (Ebling et al., 1966) and Branch (1978) concluded from field survey data that Choromytilus meridionalis is the preferred prey of Marthasterias glacialis along the South African coastline. Griffiths (1981b) found that M. glacialis was an insignificant predator oi’ mussels in the intertidal zone but it appears to be an important predator on subtidal Choromytilus meridionalis beds. Predation rates and size selection of Marthasteriai gfaciaiis preying upon black mussels were investigated in order to assess their effect on mussel population structure relative to other major invertebrate predators.

METHODS

Natural predation by M. glacialis was studied on the mussel bed at Bailey’s Cottage on the west coast of FalseBay, SouthAfrica(34”06’47”S : 18”28’01”E), the same site used by Griffiths (198 la) in the assessment of predation by Natica tecta. Choromytilus meridionalis here form a dense, continuous covering over the rocky substratum from

abundant abundant common scarce absent absent absent

Fishoek Kalk Bay Buffels Bay Simonstown Dalebrook Seaforth Sunny Cove

density

Site

glaciulis

C. meridionalis abundance

Marrhasterias

(m - ‘)

12.60 unknown 8.60 0.90 0.40 0.02 0.01

density

M. glacialis

and prey selection

61 87 27 8

meridionab

Choromytilus

in relation

TABLE

meridionalis

6 18 29 10 8 22

3

41

1

18 16 20 28

Barnacles

4

SPP.

Burnupena

24 6 4 4

Lamarck

porceilana

Crepidula

Pyura

8 33

(Heller)

stolonifera

by M. glacialis

at sites in False Bay (adapted

of prey taken

abundance

I

22 3

6

(Gmelin)

sinensis

O.~wlefe

Per cent composition

to Choromytihs

8 11 8 6

Lamarck

longicosta

Patella

28 8 17 52

16

I1 6

14 13 12 17

7

5 7

Number of prey species

1978 and unpubl.

Other

from Branch,

240 180 100 90 100 240 360

Sample size

data).

22

A.J. PENNEY

AND CL.

GRIFFITHS

=: 1 m above L.W.S. to 5-6 m depth (Griffiths, 1981b). The reef has a relatively smail area of z 1.8 ha and is discrete, being bordered by an offshore sandy substratum. Starfish densities on this mussel bed and at other sites on the west coast of False Bal (see Table I) were determined by Branch (unpubl.) by means of skindiving surveys in which all starfish lying within 1 m of 50-m transect lines laid parallel to the shoreline were counted. Transects were repeated z 5 m apart until the seaward edge of the reer was reached. The selection of prey in the field was investigated by simultaneous measurement of starfish and of the prey item being handled at the time of collection. Starfish size -was measured as the length of the longest arm from its tip to the centre of the aboral disc. Five SCUBA surveys, z 1 wk apart, were conducted at Bailey’s Cottage during April-May 1981 and again during January 1982. All feeding starfish encountered during a random search of the entire reef were investigated, the possibility of duplicate measurements being prevented by removing the prey from each starfish after measurement. Experimental prey selection studies were conducted in a closed-circuit sea-water aquarium facility maintained at 15 “C and equipped with flow-through tanks ranging in volume from 12 to 66 I. Startish for use in experiments were collected during the initial SCUBA surveys at Bailey’s Cottage during April 1981 and allowed to acclimate to the experimental system, without food, for 1 wk prior to the feeding experiments Starfish were separated into l-cm size classes on the basis of arm length and placed in tanks of increasing volume so that the relative volume available to starfish of differen: sizes was appoximately equal. Starfish were provided with five C. meridionalis per I-cm size class from < l-9 cm shell length, randomly scattered on the tank floors. Tanks; were inspected at least twice daily, empty mussel shells removed, measured and replaced by fresh mussels of the same size class. The time taken for starfish to feed on individual mussels of different sizes during the experiments was measured as the time from initial transferral of a mussel to the oral region to the discarding of the empty shell. Experiments ran in this way for 29 days. RESULTS

PREDATOR

SIZE-FREQUENCY

DISTRIBUTIONS

A combined Marthasterias glacialis size-frequency distribution derived from measurements taken on field surveys conducted during this study and by Branch (unpublished) is shown in Fig. 1. Subtidal densities of M. glacialis in False Bay vary from 0.5 . m ’ to local maxima of 35 . m _ ’ (Branch, 1978). The average density of starfish occurring on the mussel beds surveyed was 5.65 + 8.39 (SD) * m- * and is used in all subsequent calculations in which the effect of natural starfish populations on mussel beds is assessed. The relationship between starfish arm length and wet mass is given by the equation

PREDATION

23

ON CHOROMYTILUS

0.33124 x L(cm)2.48657(r2 = 0.97467; n = 62). Wet mass values can be converted to dry mass or energy using the following relationships, given by Field et al. (1980): 1 g wet mass = 0.42 g dry mass; 1 g dry mass = 8.34 kJ. W(g)

=

I

2

3

4

5

6

8

7

STARFISH

ARM

9 LENGTH

IO

11

12

13

14

15

16

~,m)

Fig. 1. Combined size-frequency distribution of 841 Murthasterius glacialis measured at sites in False Bay with black mussel populations: mean density was 5.65 f 8.39. m ’ (derived from Branch, 1978 and unpubl. data).

FIELD

MARTHASTERIAS

GLACIALIS

PREY

SPECIES

SELECTION

The relative contributions of various prey species to the natural diet of M. glacialis are shown in Table I (modified after Branch, 1978, by inclusion of unpublished data). Choromytilus meridionalis abundance estimates and starfish density measurements have been included to show the relationships between black mussel abundance and both starfish density and the percentage of mussels in the diet of starfish. EXPERIMENTAL

MARTHASTERIAS

GLACIALIS

PREY

SIZE

SELECTION

The size distributions of Choromytilus meridionalis consumed by starfish of increasing size during aquarium prey size-selection experiments are shown in Fig. 2. In addition to a steady increase in the mean size of mussel consumed per starfish size class, Marthasterias glacialis appears to be restricted to taking prey within upper and lower prey size limits.

A.J. PENNEY AND C. L. GRIFFITHS

24

. r

!.

i’

T

i L

,-j 6

7

8

9 3lARFISH

IO

II ARM

12 LENGTH

13

14

15

16

4,

(CO,,

Fig. 2. Choromytilus meridionalis taken byMarthasteriasglacia1i.s ofincreasing arm length under rxperlmenui conditions of equal prey availability (n = 194): the actual mussels eaten (0) are shown together with thf. mean sizes selected (0) (+ SD), and the regression through the means (_r = 8.1748 t 2.5592.~; c.’ 0.9635).

EXPERIMENTAL

M. GLACIALIS

PREY CONSUMPTION

RATES

The time taken for starfiih to feed on individual mussels of different sizes increased exponentially from x 2 h to 10 h as mussel shell length increased relative to starfish size (Fig. 3). The overall mean handling time was 5.1 h per mussel over the size ranges used. Throughout the experiments it was noticed that starfish activity was increasingly inhibited by disturbance as starfish size increased, but that undisturbed starfish of all sizes showed similar activity levels. As a result, the number of “feeding days” recorded during experimental manipulation declined with increase in starfish size. To exclude this effect from consumption rate estimates, the numbers of mussels eaten during the prey selection experiments were expressed per feeding day. The number of mussels consumed per feeding day increased with starfish size from ~0.7 to 1.5 (Fig. 4). The energy content of the mussels consumed per starfish size class was calculated using the relationships for Choromytzk~ meridionalis given by Grifliths (1980): flesh dry mass (g) = 1.25 x 10 - 5 x shell length (mm)2.646 where 1 g flesh dry mass = 19.5 kJ. The rapid increase in energy consumed per starfish size class per day (Fig. 4) resulted from the slight increase in the number of mussels eaten, coupled with the increased size of mussels selected by larger startish. As a result, the overall energy consumption remained at z 1% of starfish energy value per day for all starfish size classes.

/’

//

10

20

MUSSEL

30

SHELL

40

LENGTH

1 . :

50

(O/o

of

4

60

starfIsh

70

arm

length1

Fig. 3. Time taken for Marfhasterias glacialis to consume Choromytilus meridionalis under experimental conditions (n = 36): mean consumption times per mussel size class and standard deviations are shown together with the exponential curve fitted to the means (4’ = 2.97533. e”~o’475x; r* = 0.9106).

I

iP’

:

n’

,

14.

‘I

?

14

t 0

,’ .

i /

,

~12

I

/I

,’

z -

. numberr __*’ .

_-

.

0

/ O/’

.,

12 0

l., 7

8

9

IO

STARFISH

11 ARM

I 2

13

LENGTH

14

15

16

17

ICrnl

Fin. 4. Number (0) and energy content (0) of Choromytilus meridionalis consumed per feeding day by Mkhasterias glacialis of increasing arm length under experimental conditions of equal and unlimited prey size class availability: curves fitted by eye.

.A.J. PENNEY

26

AND C.L. GRIFFITHS

DISCUSSION

PREY

SELECTION

BY MARTHASTERIAS

GLACIALIS

Although M. gIacialis were recorded from all sites during this study, including those where there were no mussels, starfish density appears to be correlated with availability of black mussels (Table I). The proportion of mussels eaten is also a function of availability and where abundant they form the bulk of the diet. Like Pisaster ochruceu.~ and P. giganteus (Landenburger, 1966, 1968), Marthasterias glacialis thus shows :I strong tendency to aggregate on black mussel beds. In addition to the species preference. there is a close relationship between size of prey selected and size of starfish. This ma!result from an active selection based on the balance between time taken to open the prey and the amount of energy obtained therefrom (cf. Elner & Hughes, 1978), or may be a passive consequence of the mechanics of predation behaviour (i.e. the ease wnh which prey of different sizes can be manipulated). MODELLINC

AND PREDICTION

OF PREDATION

ON CHOROMYTILUS

MERIDIO>VALI.\

BEDS

Previous authors have warned against extrapolating results from asteroid feeding n-1 captivity to the natural environment (Reese, 1966; Mauzey et al., 1968) because manipulation of starfish frequently inhibits their behavioural responses (Landenburger, 1966: Dayton, 1975). Landenburger (1968), however, found Pisaster ochraceus to be an insatiable feeder in captivity if left undisturbed and the proportion of Marthasteritrs glacialis active in experimental tanks during this study was found to be similar to that estimated during field surveys. We therefore feel justified in attempting to utilize our laboratory results to predict the annual predatory pressure exerted by M. gfacialis OP. mussel beds under natural conditions. The daily consumption rates (Fig. 4) and prey size selection data (Fig. 2) for starfish in each size class were first combined and scaled up to give the annual consumption patterns for starfish of different sizes (assuming an equal, non-limiting availability of mussel sizes). Seasonal fluctuations in feeding rate were not taken into account, since water temperatures in the study area remain between 15 and 20 “C throughout the year (Griffiths, 1977). The curves for each starfish size class were then combined and iteratively smoothed to produce a three-dimensional predictive predation surface of mussel numbers consumed by a population of one starfish per size class feeding on equally abundant mussel size classes (Fig. 5). Under natural conditions prey of dif%rent sizes are, of course, seldom equdly abundant. Indeed, in False Bay Choromytilus meridionalis recruitment generally occurs only once in 4-6 yr (GritXths, 1981b), so that the size structure of the population differs greatiy from year to year. Other workers have shown that when prey size distributions vary in this way, the size distribution of prey taken by starfish often proportionally reflects the relative abundance of the various prey size classes available (Landenburger, 1968 ; Doi, 1976). Assuming this to be true for Marthasterias glacialis, it is possible to

ON CHOROMYTILUS

PREDATION

27

incorporate the effects of changing prey size distribution into the predictive predation surface. This was accomplished as follows. First, the percentage of mussels available in each size class was calculated for two natural mussel populations (shown in Figs. 6A and 7A), an adult cohort Choromytilus meridionalis population present at the study site during 1974 and a two cohort mussel population present in 1975 (after Griffrths, 1980). The predicted numbers of mussels taken from each size class in Fig. 5 were then multiplied by these percentages of availability and converted to energy values. The

“>

5, /;;; “/

8 STARFISH

,I

\

,I 10

8 STARFI

,\ ,\ ,\ ,\ ,\

SH

ARM

12

10 ARM

12

14

LENGTH

16 k ml

14 LENGTH

(cm;

6

Fig. 5. A, three-dimensional surface showing the predicted numbers and size distribution of mussels taken annually by a Marthasterius glacialis population consisting of one individual per l-cm size class; at this stage the model assumes an equal and unlimited availability of prey of different sizes; B, the same data given in the form of a two-dimensional contour diagram.

A. J. PENNEY AND C. L. GRIFFITHS

28

resultant energy consumption fwes were scaled for each starfish size class such that when summed they equalled the experiment&y determined annual energy ccmsumptiurt for a single starfish of that size (from Fig. 4). The predicted surfaces of energy consumed from the two natural mussel populations were then multiplied by the number of starfish of each size in the natural population in Fig. 1 to give starfish population consumption figures and finally reconverted back to numbers of prey taken. The resultant predicted predation surfaces are shown in Figs. 6 and 7. The extent to which starfish would adapt their predation patterns to the prey available on these two occasions is clearly illustrated. When preying on the single mussel cohort shown in Fig. 6A, the majority of the prey would have been taken from the 40-60 mm

10

10

20

40 Stittt

8

I@

5lARFISH

12

ARW

14

LENGTH

50 LENGTH

60

70

‘6

1.

IO 5IAKFISH

12 ARhl

14 LtNGIh

16 ,ii>

90

,in.

I., 8

80

irnn’

I

8

I

10 iiAKFlSH

I,,

12 AKM

,

,

13

1’

,j

LtNLTH

Fig. 6. A, size-frequency distribution of a single adult cohort Choromytitus meridionalis population at the study site in 1974 (from GriBiths, 1980); BC, predicted predation surface and contour diagram of numbers of mussels consumed (I 00 m - z yr - *) by a Mu&u~etiu~ g&&&r population preying on A; D,E, predicted predation surface and contour diagam of energy consumed (100 m -‘. yr- ‘) by a M. gkci& population preying on A.

PREDATION

ON CHOROMYTILUS

29

size range (Fig. 6B,C), although most of the energy removed would have derived from larger 50-70 mm mussels taken by large starfish (Fig. 6D,E). When an additional cohort of juvenile mussels was present (Fig. 7A), the major energetic intake by the starfish would still have come from the adult cohort (Fig. 7D,E), but large numbers of recruiting mussels would also have been consumed (Fig. 7B,C). Histograms summarizing the predicted total number of mussels consumed per 100 m* per year from the two prey populations (Fig. 8A,B) clearly show how predation should be concentrated on recruiting cohorts when these are available. The extent to which this situation actually occurs under natural conditions can be seen by comparison with field data collected during similar one and two mussel cohort situations in 1981 and 1982. When

; Z 220.

A

-

a

z 15.

IO

20

30 SHELL

IO STAKFISH

8

IO STARFISH

12

ARM

12 ARM

14

,cr11

60

70

80

90

~nr~,s

Ic\

1in7

16

14

50 LENGTH

16

LENGTP

LENGTH

40

STARFISH

8

IO STARFISH

Fig. 7. A, size-frequency distribution of a two cohort Choromqtilus in 1975 (from Grifliths, 1980); B,C, predicted predation surface and consumed (100 m _ ‘. yr _ ‘) by a Mur~hasterias glacialis population surface and contour diagram of energy consumed (100 m- ‘. yron A.

ARM

12 ARM

12

14

I6

LENGTH

14 LENGTH

cn),

I6 ,irv

meridionalis population at the study site contour diagram ofnumbers of mussels preying on A; D,E, predicted predation ‘) by a M. glacialis population preying

A. J. PENNEY

30

AND C. L. GRIFFITHS

only adult mussels were available, starfish were forced to consume mussels > 40 mm. just within their upper prey size limit (Fig. 8C). Following the settlement of a second cohort, however, the starfish fed almost exclusively on individuals just above their lower prey size limit (Fig. 8D).

(

i

’

*

-I j ii

STAKr’\r

a,,:

/ rN<,lri

7,

,TAHF’St-

4v’M

Lti4b:n

Fig. 8. Predicted size-frequency distributions of mussels consumed (100 m ” yr r) by Manhaurenu.\ glacialis preying on: A, a single adult cohort Choromytilus meridionalis population (from Fig. 6B) and B. ii two cohort C. meridionalis population (from Fig. 7B), and comparison with the actual prey selected by field populations ofMarthasterinsglacialis; C, during 198 1, when a single mussel cohort was present and D, durrng 1982, when two cohorts of mussels were present; mean sizes selected ( + SD) are shown together with the experimentally observed upper and lower prey size limits (----) deduced by eye from Fig. ^7

A similar predictive predation surface may be derived for Nutica tecta from the prey selection histograms given by Griffrths (1981a). Equivalent data are also available for rock lobsters (Griffrths & Seiderer, 1980), although another species of mussel, Aulacomya ater, was used as experimental prey in that study. Since prey selection by rock lobsters seems to be largely a function of shell strength (Grifliths & Seiderer, 1980), the A. ater sizes were converted to those of Choromytilus meridtialis with equal shell failure loads (as given by Griffiths & Seiderer, 1980). To allow the resultant predictive predation surfaces to be scaled up to predict natural predation by these two predators. size-frequency histograms comparable to that for Marthastetius glacialis (Fig. 1) were taken from Pollock (1979) for an unexploited rock lobster population at Robben Island off the west coast of the Cape Peninsula (Fig. 9A) and from Griffrths (198 la) for 3 Nutica tectu population at our study site in False Bay (Fig. 9B). Histograms of the predictive total percentages of mussels that should be selected by the three natural predator populations under conditions of equal prey availability are shown in Fig. 10. Despite the marked differences in predator sizes and predation techniques, it is signifi-

PREDATION

31

ON CHOROMYTILUS

cant that our simulation suggests that all the predator populations would select the majority of their prey over similar size ranges (lo-60 mm for Murthasterias glacialis, lo-50 mm for Jusus Zalundiiand 20-35 mm for Nutica tectu) given equally available prey in each size class. Predicted predation surfaces constructed for the selected Jaw lalandii and Natica tecta populations preying on natural one and two cohort Chorornytilus meridionalis beds _______

/

I

3025-

CARAPACE

30.

LENGTH

(cm)

B

25.

SHELL

WIDTH

lmml

Fig. 9. Typified size-frequency distributions for two black mussel predators: A, an unexploited Jams lulundii population at Robben Island with a mean density of 0.81 me2 (from Pollock, 1979). B, a Nutica tecta population in False Bay with a mean density of 62. m- * (from Grifiths, 1981a).

32

A.J. PENNEY

AND C. L. GRtFFiTHS

indicate an even more pronounced concentration of predation on recruiting mussels than suggested for ~~~~~#~~j~ ~~~c~~~~~. The high proportion of small rock lobsters 6-8 cm carapace length (&. 9A) woufd result in heaviest predation on the smailer mussels (30-50 mm) of an ad& cohort (Fig. 1IA,B), while under conditions ofmussei recruitment, predatory effort would be concentrated almost exclusively on the smaller age class (Fig. 1 IGD). Due to their relatively smail size (Fig, 9B), Naricrr mm would be restricted to feeding on the smallest individuals (25-35 mm) from an adult mussci cohort (Fig. 12A,B). As these exceed the m~~murn prey size available to small X. razz,. gastropods belaw z 20 mm shell width would be unable to obtain mussel preq under

SHELL

ttNGri-1

; m !,Ij

Fig. IO. Predicted size seiecxion histt,grams for naturaf predator populations preying ~h~~~~n~ri~~~~ ~e~id~~n~~~~~ A, seIection by the ~~~~~u~~eriffsg!txhiis population shown by the Jesus lalundii population shown in Fig. 9A; C, selection by the ,%cica cecca Fig. 9B; the predicted total numbers of mussels removed per 100 m2 per year are 734918 respectively.

on cquaii~ avaiiobk in Fig. I : B. selccri~ popuktictn shown 11; 143 27% 200 376 ~xl

3.3

ON CHOROMYTILUS

PREDATION

these conditions. IV. tectu populations therefore rely heavily on recruiting mussels for the survival of juveniles (Fig. 12C,D). These predation patterns mean that Choromytilus meridionalis are most vulnerable to predation during their first year, and particularly over the size range 20-30 mm. The predicted annual energy requirements for the three predator populations considered,

0

8

ROCK LOBSTER

10 CARAPACE

12 LENGTH

14 (rm,

6 ROCK

8

10

LOBSTER CARAPACE

12 LENGTH

14 (cm)

Fig. 11. Predicted predation surfaces and contour diagrams of numbers of mussels consumed (100 m ‘. yr _ ‘) by a Jasus lalundii population preying on: A,B, the 1974 single cohort Choron?+~s meridionalis population shown in Fig. 6A; C,D, the 1975 two cohort C. meridionalis population shown in Fig. 7A.

Fig. 12. Predicted predation surfaces and contour diagrams of numbers of mussels consumed (100 m -‘.yrr) by a Natica tecfa population preying on: A,B, the 1974 single cohort ChoromJvilus meridionalis population shown in Fig. 6A; C,D, the 1975 two cohort C. meridionalis population shown in Fig. 7A.

34

A. J. PENNEY

AND C. L. CRIFFITHS

calculated as the total energy content of the mussels under their respective predicted predation surfaces, are 6028 kJ * m - ’ for Marthastetis ghxkalis, 5835 k3 * m ’ for Jams lalandii and 9010 W * m - * for Natica few. Standing stock estimates for Chovo~~~~~~ ~e~~~~~is given by GrifXths (1981b) vary between 19 125 kJ *rn ’ and 21675 kJ * m - ’ so each predator appears to have the potential to alter significantly the density and size-frequency structure of mussel beds. Indeed, the concentration nt’ predation by rock fobsters on small ~u~~u~yu ater has been shown to result in a bimodal prey distribution on rock lobster grounds (Pollock, 1979; Griffiths, unpublished data) and Jaw lalandii appears to be capable of totally eradicating recruiting settlements of mussels (Poliock, 1978). GrifBhs (198 la) has also found that Natica tectu is capabk of totally depleting intertidal recruiting C~~~~~~~~~ ~e~d~onu~~ cohorts and M~~t~~steriasgZuciulishas been found to be responsible for decimating a recruiting black mussel population on an artificial reef in False Bay (Fricke et al., 1982). Despite the ability of the predators studied to adapt their diet to the av~ability of’ prey size classes (within the confines of their respective upper and lower prey size limits) the availability of suitable prey appears to be an important factor controlling the success of predator recruitment. Griff~ths & Seiderer (1980) have suggested that rock lobster production may be severeIy curtailed by the scarcity of mussels of preferred sizes, and that food restrictions would be most severe for small rock lobsters that arc unable successfully to attack larger prey. Similar dependence has been been shown for naticids. Ansell (I 960) recorded the appearance of Lunatic alderi in an area following a very successful Yeplusst~a~~u settlement, while Broom (1982) observed that fluctuations in Nutica macuhsa are closely related to the changing abundance of young Anadura prey. Grifftths (1981a) found Natica tecta and Choromytilus meridimafis population densities and size-frequency d~st~butions to be interde~ndent and concluded that successful black mussel settlement is necessary to allow for Natica tectu recruitment and growth. Entrainment of asteroid recruits to recruiting prey cohorts has aiso been demonstrated. Superabund~t prey serve as focai points for Asterzas rubens outbreaks, with successful Myths recruitment conditions being necessary for successful Asrerias rubews recruitment (Sloan, 1980). Birkeland (1974) suggested that the first few meals of an asteroid following met~o~hosis are critical to its reagent potent&.! and Nauen (1978) has shown that newly metamorphosed A. &ens are capable of waiting for some months for a suitable feeding opportunity before commencing growth. The successful development of h4arthmterhw ghacialis settlements in our study area appears to rely on a similar entrainment to rrxruiting black mussel cohorts. For instance, the appearance of M. glaciaalison a;nartificial reefcloseiy followed the dense settlement of a Choromyrilus meridionaks cohort and predation by the starfish was concentrated almost exclusively on the mussels. Such entrainment of predator to prey cohorts, combined with the strong size selection preferences shown by mussel predators, appears, in fact, adequately to explain the marked interrelationship frequently observed between recruitment and growth of predator and prey populations on mussel beds.

PREDATION ON CHOROMYTILUS

35

ACKNOWLEDGEMENTS

Financial support for this study was received from the Department of Environmental Affairs and Fisheries. The authors also wish to thank Dr. G. M. Branch, University of Cape Town, for permission to cite his unpublished data on Marthasterias glacialis densities and size-frequency distributions and Miss C. Illert for production of the artwork. REFERENCES ANSELL,A. D., 1960. Observations on predation of Venus striatula (Da Costa) by Natica alderi (Forbes). Proc. Malacol. Sot. London, Vol. 34, pp. 151-164. BIRKELAND,C., 1974. Interactions between a sea pen and seven of its predators. Ecol. Monogr., Vol. 44. pp. 21 l-232. BRANCH,G.M., 1978. The response of South African patellid limpets to invertebrate predators. 2001. Afr., Vol. 13, pp. 221-232. BROOM, M.J., 1982. Size selection, consumption rates and growth of the gastropods Natica maculosa (Lamarck) and Thais carinijizra(Lamarck) preying on the bivalve Anadara granosa (L.). J. Exp. Mar. Biol. Ecol., Vol. 56, pp. 213-233. COMMITO,J. A.,1982. Effects of Lunatia heros predation on the population dynamics of Mya arenaria and , Macoma balthica in Maine, U.S.A. Mar. Biol., Vol. 69, pp. 187-193. DARE, P.J. & D. B. EDWARDS,1976. Experiments on the survival, growth and yield of relaid seed mussels (Mytilus edulis L.) in the Menai Straits, North Wales. J. Cons. Cons. Perm. Int. Explor. Mer, Vol. 37, pp. 16-28. DAYTON,P. K., 1971. Competition, disturbance and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecol. Monogr., Vol. 41, pp. 351-389. DAYTON,P.K., 1975. Experimental evaluation of ecological dominance in a rocky intertidal algal community. Ecol. Monogr., Vol. 45, pp. 137-160. Dor, T., 1976. Some aspects of feeding ecology of the sea stars, genus Astropecten. Publ. Amakusa Mar. Biol. Lab., Vol. 4, pp. l-19. EBLING, F.J., J.A. KITCHING, L. MUNTZ & C.M. TAYLOR, 1964. The ecology of Lough Ine. XIII. Experimental observations of the destruction ofMytilus edulis and Nucella lapillusby crabs. J. Anim. Ecol., Vol. 33, pp. 73-82. EBLING,F. J., A. D. DAWKINS,J. A. KITCHING,L. MUNTZ & V. M. PRAY, 1966. The ecology of Lough Inc. XVI. Predation and diurnal migration in the Paracentrotus community. J. Anim. Ecol., Vol. 35, pp. 559-566. EDWARDS,D. C. & J. D. HUEBNER,1977. Feeding and growth rates of Polinices duplicatus preying on Mya arenaria at Barnstable Harbour, Massachusetts. Ecology., Vol. 58, pp. 1218-1236. ELNER,R. W. & R.N. HUGHES, 1978. Energy maximization in the diet of the shore crab, Carcinus maenas. J. Anim. Ecol., Vol. 47, pp. 103-116. FIELD, J.G., N. G. JARMAN,G. S. DIECKMANN,C. L. GRIFFITHS, B. VELIMIROV& P. ZOUTENDYK,1977. Sun, waves, seaweed and lobsters: the dynamics of a west coast kelp-bed. S. Afr. J. Sci.. Vol. 73, pp. 7-10. FIELD, J. G., C. L. GRIFFITHS, R. J. GRIFFITHS, N. JARMAN,P. ZOUTENDYK,B. VELIMIROV& A. BOWES, 1980. Variation in structure and biomass of kelp communities along the south-west Cape coast. Trans. R. Sot. S. Afr., Vol. 44, pp. 145-203. FRANZ, D. R., 1977. Size and age-specific predation by Lunatia heros (Say, 1822) on the surf clam Spisula solidissima (Dillwyn, 1817) off western Long Island, New York. Veliger, Vol. 20, pp. 144-150. FRICKE,A.H., K. KOOP & G. CLIFF, 1982. Colonization and viability of an artificial steel reef in False Bay, South Africa. Trans. R. Sot. S. Afr., Vol. 44, pp. 499-512. GRIFFITHS, C. L. & L. J. SEIDERER, 1980. Rock lobsters and mussels - limitations and preferences in a predator-prey interaction. J. Exp. Mar. Biol. Ecol., Vol. 44, pp. 95-109. GRIFFITHS, R. J., 1977. Reproductive cycles in littoral populations of Choromytilus meridionalis (Kr.) and

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