Predation of the ribbed mussel geukensia demissa by the blue crab callinectes sapidus

Netherlands Journal of Sea Research 16:163-172 (1982)

PREDATION DEMISSA

OF T H E R I B B E D M U S S E L G E U K E N S I A BY T H E B L U E C R A B C A L L I N E C T E S SAPIDUS by R. S E E D

Duke University Marine Laboratory, Beaufort, North Carolina, U.S.A. * Department of Zoology, University College of North Wales, Bangor, Gwynedd, LL57 2Utl', Great Britain

CONTENTS I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . II. General Methods . . . . . . . . . . . . . . . . . . . . . . . . III. Experiments and R~sults . . . . . . . . . . . . . . . . . . . . . 1. The mussel population . . . . . . . . . . . . . . . . . . . . 2. Prey handling procedures . . . . . . . . . . . . . . . . . . . 3. Prey value . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Foraging strategy . . . . . . . . . . . . . . . . . . . . . . . IV. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . V. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . VI. References . . . . . . . . . . . . . . . . . . . . . . . . . . .

163 164 164 164 165 165 167 170

171 171

I. I N T R O D U C T I O N T h e w a y p r e d a t o r s select p r e y is central to our u n d e r s t a n d i n g of preda t o r - p r e y systems. O n e a p p r o a c h to this p r o b l e m has been to use the energy m a x i m i z a t i o n m o d e l which assumes t h a t p r e d a t o r s m a x i m i z e their net energy intake. T h e m o d e l requires t h a t p r e y items can be r a n k e d a c c o r d i n g to their e n e r g y value. M o s t tests of the m o d e l h a v e involved visual p r e d a t o r s (e.g. WERNER & HALL, 1974; CHARNOV, 1976). H o w e v e r , ELNER • HUGHES (1978) showed e x p e r i m e n t a l l y that Carcinus maenas, w h i c h locates a n d evaluates p r e y (Mytilus edulis) b y c h e m i c a l a n d tactile cues, a p p e a r s to c o n f o r m to predictions of O p t i m a l Diet T h e o r y based on the energy m a x i m i z a t i o n premise. Geukensia (Modiolus) demissa is a p r i n c i p a l c o m p o n e n t of the saltm a r s h m a c r o b e n t h o s along the Atlantic coast of N. A m e r i c a . T y p i c a l l y it occurs in the u p p e r intertidal zone living semi-infaunally a m o n g s t the roots of Spartina alterniflora Loisel b u t it c a n also be found a t t a c h e d to * Authors permanent address.

164

R. SI~ED

sea walls and wharf pillings (LENT, 1967 ; SEED, 1981), Callinectes sapidus Rathbun is also abundant in the saltmarsh ecosystem and whilst often regarded as a scavenger it is known to feed extensively on bivalves including Geukensia demissa (Dillwyn) (TAGATZ & HALL, 1971; SEED, 1980). This paper examines the foraging behaviour of Callinectes sapidus in laboratory aquaria to determine whether this crab, like Carcinus maenas, adopts an energy maximizing strategy when feeding on mussels. The size-fi'equency characteristics and local distribution patterns of Geukensia at Beaufort are briefly considered in the light of these experiments. II. GENERAL METHODS R a n d o m samples of Geukensia demissa were collected (July and August, 1979 and 80) from upper intertidal saltmarsh muds on Bird Shoal and from the sea wall adjacent to Duke Marine Laboratory (average tidal range 1 m). Marsh samples consisted of 0.25 m z quadrats dug to about 1 din, sea wall samples of 15 x 45 cm strips through the oyster zone. All mussels were removed and their shell lengths measured. Biomass (total damp weight) and dry tissue weight were recorded for subsamples selected to include several individuals from each size class represented in the population. Although no census was made of the local Callinectes population 5 to 12 cm crabs were especially abundant. These crabs tbllow the flooding tide to forage intertidally and are easily collected using dip nets and baited lines. Several larger crabs (13 to 18 cm) were obtained by trawling in the deeper Sounds. Maximum carapace width (between the prominent spines) and height of the major cheliped were noted for each crab. During all feeding experiments crabs were kept individually in plastic aquaria supplied with running seawater (28 to 30 ° C). Only male crabs were used to avoid potential bias caused by sexual differences in behaviour and cheliped morphology. Crabs were starved for 24 h to standardize hunger levels. Only undamaged, healthy mussels were used as prey. III. EXPERIMENTS AND RESULTS 1.

THE

MUSSEL

POPULATION

In the saltmarsh Geukensia demissa is highly clumped and densities are therefore variable. Densities of 35"/n 4 occurred in the most favourable regions but the overall marsh average was only 3 . 3 ' m 2.

165

P R E D A T I O N OF M U S S E L BY B L U E CRAB

The sea wall supported much higher densities (about 1300" m ~ ) . Here, however, oysters provided an extensive matrix which substantially increased the surface available for attachment. Most larger wellestablished mussels occurred in the upper intertidal zone. Both populations are dominated numerically by small mussels (Fig. 1), but the paucity of larger mussels on the sea wall contrasts with their comparative abundance in the marsh. Although less abundant larger mussels none the less account for the major part of the population biomass. a

%

%

cm

Fig. 1. Length (cm, 0) and biomass (g, histograms) distributions of Geukensia demissa. a. Saltmarsh population (n = 200). b. Sea wall population (n 276). 2.

PREY

HANDLING

PROCEDURES

Mussels are manipulated by the large outer maxiltipeds and the anterior walking legs as well as by the powerful chelipeds. Small mussels are easily crushed. Attacks on somewhat larger mussels are centred on the weaker umbones. The mussel is repeatedly manipulated until a weak spot is encountered and the umbones smashed (Plate Ia and b). When forced to feed on larger prey a slower method of attack is adopted. Here the posterior edges of the valves are gradually chipped until the chelipeds can be inserted and the adductor muscle severed. The valves are then grasped and torn apart (Plate Id and e). 3.

PREY

VALUE

Crabs were fed a wide range of mussels to determine the relationship between mussel size and prey value. Individual mussels were lowered into the aquaria and the following events timed: breaking time (Tb) , the time from first contact with the prey to the first bite of exposed flesh;

166

R. SEED

eating time (Te) , the end of T b to the completion of the meal; and handling time ( T h), the sum of Tb and Te. Prey value is defined as dry flesh weight (mg) divided by T h (min). Typical handling curves for 3 representative crabs (Fig. 2a) illustrate that T h varies as the cube of prey length reflecting the volume of flesh ingested. Variations in T h amongst similar sized mussels exist both within and between crabs. Within-crab variation is mainly due to variability in shell strength but differences in crab hunger levels may also be implicated. Between-crab b m(

minutes

it 2O

A/

20" -20

,/ J

• m i n -1

11"7 c m

O

10~

-lo

~o

-o

o

30-

/ o 20-

8'Ocm

10-

0 ,

it o

f

20

1

10

0

2

3

4

5

40-

30-

,/

30-

20-

10.

0

20-

5-2cm

10-

L;

0 cm

Fig. 2. a. Mussel handling times Th (min) plotted against shell length L (cm); curves fitted by the power function T h = aLa'15; results of 3 individual crabs of 11.7 cm (A) a 1.59, n = 30), 8.0 cm (C)) (a 0.33, n = 26) and 5.2 cm (O) (a 1.20, n - 20). Shaded bars indicate approximate minimum size for which edge-chipping is required, b. Consumption of mussels of different length under conditions of a constant prey availability of 5 mussels in each size class (histograms); also indicated are profitability curves (mg" min -1) calculated from power function (above) and the following equation describing the relationship between dry flesh weight W (mg) and shell length L ( c m ) inGeukensia:ln W - - 2 . 4 7 1 n L + 1.99 (n = 50).

PREDATION OF MUSSEL BY BLUE CRAB

167

variation is largely a function of crab size though certain crabs were evidently more experienced at opening mussels. Cheliped height is isometrically related to crab size (Fig. 3). Prey value curves decreased monotonically between the smallest and largest mussels (Fig. 2b). The relationship between T b and crab-mussel size ratio (Fig. 4) shows that mussels are opened more rapidly as this ratio increases. At ratios > 4.5 mussels are easily crushed (within 0.5 minutes). At intermediate ratios (3.5 to 4.5) Tb averages 2 to 3 minutes (umbone crushing) whilst at lower ratios T u increases steeply as edge-chipping increasingly becomes the predominant method of attack. clow cm 3-

O JO

0 0

0

0/0

yo0

0

o

o° o °

I

5

I

I

10

15

c o r o p o c e cm

Fig. 3. Relationship between claw height H (cm) and carapace width W in male intertidal ( O ) and trawled ( 0 ) Callinectes sapidus; line fitted by the power function: H = 0.15 W 1"°2 (n = 51). 4. F O R A G I N G

STRATEGY

Feeding behaviour was studied with both unlimited and restricted diets, the latter by presenting crabs with equal numbers of mussels of different size. The numbers of mussels consumed were monitored daily for 4 d without replacing eaten prey. Initially, smaller mussels were selected and only when these had been consumed did crabs proceed to attack progressively larger prey (Fig. 5).

168

R SEED minutes (7)

35-

25"

15-

5.

(17)

It',) o-

,

,

L

,

~

,

(:) ~

.o,, ,:, ,

~

,., ,

,., ;

,:, ,

2

crob/mussel

rotio

Fig. 4. Mean times (min) ± 1 SE required by Callinectes sapidus to open mussels of different relative sizes (crab to mussel ratios); observations (n = 138) based on 8 crabs (5.2 to 11.7 cm).

Similar experiments assessed the effects of unlimited prey. H e r e , however, crabs were allowed to feed for restricted periods (2 to 3 h). T h e numbers of mussels eaten were then counted and replaced by ones of numbers

day 1

15

~°'~I

I

day 3

day 4

unopened

c

!llL 1

day 2

3

5

1

3

5

1

3

5

7, 1

3

5

t m 1

3

Cffl 5

Fig. 5. Numbers of mussels of different length size (cm) consumed under conditions of limited prey availability (stippled columns indicate number of mussels remaining unopened on day 5). a. 11.7 cm crab (15 mussels offered in each 0.5 cm length class), b. 10.0 cm crab (15 mussels), c. 8.1 cm crab (10 mussels), d. 7.4 cm crab (10 mussels).

a

Handling techniques used by Callinectes sapidus to oprn Geukmsia demirsa. a. and Umbone crushing. c. Shells opened by umbone crushing. d. and e. Edge-chipping. Shells opened by edge-chipping; note ragged posterior valve margins.

11. f’.

169

PREDATION OF MUSSEL BY BLUE CRAB

similar size to maintain constant prey availability. These experiments were repeated until a consistent feeding pattern emerged. Diet curves with unlimited prey show that large mussels were seldom eaten even though these could be opened by all but the smallest crabs (Fig. 2b). A recurring feature amongst larger crabs ( > 8 . 5 cm) was the apparent reluctance to feed on the smallest, most profitable mussels. Since this may simply reflect low encounter rates with small prey 2 size classes of mussels (2 to 2.5 and 3.5 to 4 cm) representing more and less profitable prey respectively, were fed in different proportions to 4 crabs. These were monitored continuously for 1 h noting acceptance rejection sequences. Mussels were replaced as eaten to maintain constant prey availability. Although larger mussels were more frequently encountered they were rarely eaten (Fig. 6a). Small mussels were always eaten whenever encountered even when grossly outnumbered by larger prey. These experiments were repeated using mixtures of 1 to 1.5 and 2 to 2.5 cm mussels. Both size classes were easily opened and were rarely rejected (Fig. 6b). These results confirm that any reluctance to eat small, profitable mussels simply reflects low encounter rates with these prey items.

a

b

numbers 20 150-

3-5 - 4 - 0

150"

cm

10

100-

1-0-1-5cm

1002O

r_ 5

50-

SO-

0

5 50-

5

2-0 - 2-5

cm

5

5

502-0-2"5

cm

Fig, 6. Diets of crabs presented with different numbers of smaller and larger mussels (5 to 5, 5 to 10 or 5 to 20); indicated are the n u m b e r of mussels encountered (open columns) and the n u m b e r of mussels actually eaten (closed columns); 4 crabs (8.5 to 11.7 cm) used with each ratio, a. Mussels of 2.0 to 2.5 cm against mussels of 3.5 to 4.0 cm. b. Mussels of 2.0 to 2.5 cm against mussels of 1.0 to 1.5 cm.

170

R. SEED IV. DISCUSSION

GRAY (1957) showed that gill area to body weight ratios in Callinectes sapidus exceeded that of all other crabs in the Beaufort area. This undoubtedly contributes to the blue crab's particularly pugnacious nature. In the present investigation certain crabs routinely ate well over 50 mussels daily. Moreover, the complexity of the edge-chipping method and its consistency in all crabs studied suggests that this is a specific mussel opening technique. Large mussels were attacked but opened only with difficulty and prey value declined steeply at larger prey size. Small mussels are clearly most vulnerable as these are available to most crabs. Once beyond a certain size threshold, however, mussels are substantially protected from further predation by their large size (and low profitability). The biomodality of the marsh population is interesting in this context since the increased abundance of 3 to 4 cm mussels (Fig. 1) broadly coincides with the point at which larger intertidal crabs adopt the slower, edgechipping method. Furthermore, these mussels were generally avoided in laboratory experiments (Fig. 6a). Deficiencies in size classes close to those preferred by predators have been reported in other mussel populations (SEED & BROWN, 1975; POLLOCK, 1979). Size-limited predation is thought to be important in permitting close coexistence of predator and prey (PAINE, 1976). On the sea wall excessive predation fi~om crabs and gastropods probably results in high mortality so that mussels rarely survive beyond the critical threshold. Crowding, however, is known to depress growth rates in Geukensia demissa (ST~VEN & KUENZLER, 1979) and densities on the sea wall are substantially higher than in the marsh. Established Geukensia populations are confined mainly to the upper intertidal which constitutes a spatial refuge where predation pressure is relaxed. Heavy predation by blue crabs and perhaps more especially by mud crabs (SEEr), 1980) virtually excludes Geukensia from the lower shore. In the saltmarsh the umbones of larger mussels are protected deep in the sediment. Whether Callinectes can excavate these mussels is uncertain though Cancerpagurus does obtain much of its food by digging deeply into sand (SHELTON,KINNEAR & LIVINGSTONE,1979). The monotonically decreasing prey value curves for Callinectes contrast with the peaked curves for Carcinus m a e n a s /ELNER • HUGHES, 1978). This probably reflects differences in cheliped morphology. The chelipeds of Callinectes sapidus are elongate and sharply pointed so that even small mussels are gleaned efficiently. Cheliped biomechanics in this and other decapods are described by BROWN, CASSUTO ~2 Loos (1979). Blue crabs appear to actively select their prey. Small mussels are readily accepted, larger mussels repeatedly rejected. However, since

PREDATION OF MUSSEL BY BLUE CRAB

171

T h increases a n d p r e y value decreases with increasing mussel size, preference for smaller mussels simultaneously m a x i m i z e s net e n e r g y intake a n d minimizes h a n d l i n g time. T h e a p p a r e n t preference for all mussels w h i c h were easily crushed suggests t h a t time m i n i m i z a t i o n m a y be the basis for size selection. T i m e a v a i l a b l e for feeding on mussels at high tide is limited and crabs t h e m s e l v e s are m e a n w h i l e v u l n e r a b l e to p r e d a tion f r o m Shore birds. I n this situation m i n i m i z i n g h a n d l i n g time m a y be even m o r e i m p o r t a n t t h a n m a x i m i z i n g e n e r g y intake. E x p e r i m e n t s show t h a t Callinectes c a n c o n s u m e large n u m b e r s of Geukensia. W h e t h e r such l a b o r a t o r y studies reflect the field situation remains untested. H o w e v e r , p r e d a t o r s can influence the structure of benthic i n f a u n a in soft sediments (VmNsTF~IN, 1977) a n d field experiments are n o w required to assess the i m p a c t of Callinectes on n a t u r a l mussel populations. V. S U M M A R Y

Callinectes sapidus fed extensively on Geukensia demissa in l a b o r a t o r y a q u a r i a . Several p r e d a t i o n techniques used b y Callinectes to o p e n its p r e y are reported. P r e y v a l u e decreases m o n o t o n i c a l l y with increasing mussel size. C r a b s c o n s u m e d mussels o v e r a wide size r a n g e b u t were generally r e l u c t a n t to feed on larger mussels whilst smaller, m o r e profitably p r e y was available. T h e relative i m p o r t a n c e o f ' e n e r g y m a x i m i z a tion' a n d ' t i m e m i n i m i z a t i o n ' could not be distinguished. T h e distribution a n d p o p u l a t i o n structure of Geukensia at Beaufort, N. C a r o l i n a are briefly considered in terms of the foraging strategy of Callinectes.

VI. R E F E R E N C E S BRowN, S. C., S. R. CASSUTO& R. W. LOOS, 1979. Biomechanics ofchelipeds in some decapod crustaceans.~nl Zool. 188:143 159. CHARNOV,E. L., 1976. Optimal foraging: attack strategy ofa m a n t i d . Am. Nat. 110: 141-151. ELNER, R. W. & R. N. HUOHES, 1978. Energy maximization in the diet of the shore crab, Carcinus maenas.~. Anim. Ecol. 47:103 116. GRAY, I. E., 1957. A comparative study of the gill area ofcrabs.4iol. Bull. mat. biol. Lab., Woods Hole 112: 3442. LENT, C. M., 1967. Effect of habitat on growth indices in the ribbed mussel, Modiolus ( Arcuatula)demissus.--4P~hesapeake Sci. 8: 221-227. PA1NE~ R. T., 1976. Size-limited predation: an observational and experinaental approach with the Mytilus-Pisaster interaction. ~Ecology 57: 858473. POLLOCK,D. E., 1979. Predator-prey relationships between the rock lobster jasus lalandii and the mussel Aulocomya ater at Robben Island on the Cape West coast of Africa. Mar. Biol. 52:347 356.

172

R. SEED

SEED, R., 1980. Predator-prey relationships between the mudcrab Panopeus herbstii, the blue crab Callinectes sapidus and the Atlantic ribbed mussel Geukensia ( ~- Modiolus) demissa.--Estuar, coast, mar. Sci. U" 445--458. , 1981. A note on the relationship between shell shape and life habits in Geukensia demissa and Brachidontes exustus (Mollusca: Bivalvia).--J. moll. Stud. 46-" 293 299. SEED, R. • R. A. BROWN,1975. The influence of reproductive cycle, growth and mortality on population structure in Modiolus modiolus (L.), Cerastoderma edule (L.) and Mytilus edulis L. (Mollusca: Bivalvia). In: H. BARNES. Ninth European Marine Biological Symposium. Aberdeen Univ. Press: 257--274. SHELTON, R. G. J., J. A. M. KINNEARt~ZK. LIVINGSTONE,1979. A preliminary account of the feeding habits of the edible crab Cancer pagurus L. off N.W. Scotland. ICES C.M. K 35: 1 4 . Sa'IVEN, A. E. & E. J. KUENZL~R, 1979. The responses of two saltmarsh molluscs, Littorina irrorata and Geukensia demissa, to field manipulations of density and Spartina litter.~Ecol. Monogr. 49: 151-171. TAGATZ,M. E. 8z A. B. HALL,1971. Annotated bibliography on the fishing industry and biology of the blue crab, Callinectes s a p i d u s . ~ O A A Tech. Rept., NMFS SSRF 640: 1-94. VmNSTEIN, R. W., 1977. The importance of predation by crabs and fishes on benthic infauna in Chesapeake Bay.~Ecology 58:1199--1217. WERNER, E. E. & D.J. HALL, 1974. Optimal foraging and the size selection of prey b x the bluegill sunfish (Lepomis macrochirus).~Ecology 55:1042 1052.