Predator-prey relationships between the mud crab Panopeus herbstii, the blue crab, Callinectes sapidus and the Atlantic ribbed mussel Geukensia (=Modiolus) demissa

Estuarlne and Coastal Marine Sdence (t98o) xx, 445-458

Predator-Prey Relationships between the Mud Crab Panopeus herbstii, the Blue Crab, Callinectes sapidus and the Atlantic Ribbed Mussel Geukensia (=Modiolus) demissa

R. Seed Department of Zoology, University College of North Wales, Bangor, Gwynedd, Wales, U.K. Received 25 October x979 and in revisedform H February 198o

Keywords: crabs; mollusca; predation; population variations; North Carolina coast Laboratory studies have demonstrated that the mud crab Panopeus herbstH H. Milne Edwards and the blue crab Calllnectessapidus Rathbun can consume large numbers of the Atlantic ribbed mussel Geukensia (=Modiolus) demlssa (DiUwyn). Various predation techniques used by these crabs to open their prey are reported. Although crabs could consume mussels over a wide size range they showed a marked reluctance to feed on larger mussels whilst smaller, more easily predated prey was still available. Under regimes of unlimited prey availability both crabs showed a pronounced preference for specific size classes of mussels. In Panopeus at least, this preferred prey size increased with size of predator. The distribution and population structure of Geukens~a at two contrasted sites at Beaufort, North Carolina could largely be interpreted in terms of the predatory activities of these two locally abundant decapods. Introduction The decapod Crustacea include a number of voracious predators which have the ability to influence profoundly both the local distribution patterns and population characteristics of their prey (Kitching & Ebling, x967; Ropes, i968; Seed, 1969; Seed & Brown, I975; Reise, x977; Pollock, I979). Although bivalve molluscs often feature prominently in the diets of many of these predatory decapods, most previous studies of these predator-prey relationships have concentrated on species of commercial importance. Elner & Jamieson (x979) for example have shown that rock crabs, Cancer irroratus and lobsters, IIomarus amedcanus are potentially important predators of Placopccten magdlan?cus, a scallop which supports a lucrative fishery along the eastern seaboard of North America. Stone crabs, Menlppe mercenaria, mud crabs, Panopeus herbstii and blue crabs, Callinectes sapidus all feed extensively on clams and oysters (Menzel & Hopkins, x956; McDermott, x96o; Eldridge et al., x976; MeKenzie, I97o; Krantz & Chamberlin, x978; Whetstone & Eversole, x978) whilst the shore crab Cardnus maenas is often a serious pest on commercial mussel beds (Dare & Edwards, x976). Elner & Hughes (r978) demonstrated that Carcinus selects specific size classes of prey in order to maximize its net energy intake per unit of foraging time. Prey selection also reduces intraspecific competition by partitioning prey items amongst the predator population. Mechanical aspects of predation by Carclnus on the mussel Mytilus edulis are examined by Elner (x978). 445 obo2-3524/8o/xoo445+x6 $02.00/o

9 x98o Academic Press Inc. (London) Ltd.

446

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Geukensia ( = Modiolus) demissa is abundant intertidally along much of the Atlantic coast of North America (Abbott, x974). It is especially prolific in salt marsh muds where it lives semi-infaunally amongst the roots of the cordgrass, Spartina alterniflora. Kuenzler (x961b) has shown that in the salt marsh ecosystem Geukensia is an important biogeochemical agent. Observations by McDougall (x943) and Lent (x967a), however, show that ribbed mussels can also flourish in more exposed intertidal habitats such as bridge supports and wharf pilings. Apart from Kuenzler's (x96xa, b) work surprisingly little is known about the ecology of Geukensia. Various gastropods (Wells, I958a, b; Blake, x96o) and crabs are known to be potential predators of Geukensia but precisely to what extent these are responsible for natural mortality is largely conjectural. This paper examines the feeding behaviour of two locally abundant crabs, Panopeus herbstii and Callinectes sapidus on G. demissa in laboratory aquaria and attempts to explain the local distribution patterns and slze-frequency characteristics of two contrasted mussel populations at Beaufort, North Carolina in the light of these observations. The study area and general methods Two mussel populations were sampled between late June and mid August x979; one from the sea wall on the eastern side of Piver's Island adjacent to Duke University Marine Laboratory, and one largely for purposes of comparison, from the salt marshes on nearby Bird Shoal. Both sites are exceedingly sheltered and experience minimal wave action. Tides in this geographical locality vary from around o. 7 m on neaps to I. 3 m on springs with an average tidal range of approximately x.o m. In the local salt marshes Geukensia occupies a relatively narrow vertical band in the upper intertidal zone where it lies buried in dense clumps amongst the roots of Spartina with only the posterior margins of the shell exposed above the surface of the compacted sediment. On the sea walls and wharf pilings, Geukensla is found along with another mussel Brachidontes exustus amongst the dense clusters of Crassostrea virginica which form such a prominent feature of the local intertidal fauna. Most of this sea wall community is contained within a 45 cm wide zone, the uppermost fringes of which form a conspicuous 'oyster line' some 3 ~ cm below MHWS. Below this oyster]mussel zone the sea wall is covered by a thin carpet of the red alga Gelidium crinale. This 'bare zone' is about 2o--25 cm wide and extends down to the mud line. At the base of the sea wall, almost totally covered by anoxie mud, there were a few isolated mussels with large, heavy shells. Extending from the base of the sea wall down to low water mark, clumps of large oysters which had become detached from the high density population above, littered the mud surface. Very few oyster clumps extended beyond low water mark. Entire colonies of Gcukansla were either dug up from selected areas of marsh or scraped from the sea wall population and transported back to the laboratory where they were hand sorted. The length of each mussel was then measured to the nearest o.x mm using vernier calipers. Samples, each of about xSO mussels, were also collected from the two sites; these were selected so as to include several individuals in each of the size classes represented in these populations. Each mussel was cleansed of any fouling organisms and its shell length, height and width recorded (Figure x). These data were then fitted to the allometrie equation: y = Ax b wherey and x are pairs of size variables, and the constants .4 and b estimated by least squares regression. These regressions were then used to generate the data contained in Tables I and 2. Details of shell allometry in Geukensia will be more fully documented elsewhere.

Predator-prey relationships

447

Height

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Figure x. (a) Shell parameters in G. demissa (b) master cheliped of P. herbstii showing parameters measured (c) cheliped of C. sapidus. TABLE 1. Shell characteristics of Geukensia demissa Sea wall mussels* (n = 15o) Length Height (cm) (cm) 0"5 x'5 2"5 3"5 4"5 5"5 6"5 7"5 8"5

0"26 0"75 1"22 1.68 2"13 2"58 3"02 3"46

XVidth (crn) o-14 0"46 0"78 x.xx 1"45 1"79 2"x4 2"49 .

Length tieight x-92 2"oo 2"05 2.o8 2"11 2"13 2"15 2"17 . .

Salt marsh musselsb (n = 148)

Length ~Vidth

Height ~Vidth

Height (cm)

Width (cm)

Length IIeight

3"57 3"26 3"21 3"15 3"IO 3"07 3"04 3"o1 .

1-86 1.63 1"56 1"51 z'47 1"44 1"41 x.39

0.23 0"67 1.1o 1"52 1"95 2"37 2"79 3 "2I 3"62

o.i2 0"40 o"71 1"o4 1"39 1"74 2.xo 2"47 2"85

2"17 2"24 2"27 2"30 2"31 2"32 2"33 2"34 2"35

Length ~Vidth

Height Width

4"17 3"75 3"52 3"37 3"24 3"16 3"xo 3"04 2"98

I'92 1"68 1"55 1"46 X'4o 1"36 1"33 x'3o x'27

*Maximum shell length 7"46 cm. bMaximum shell length 8-6o cm. T,~tm 2. Shell characteristics of Geukemia and Brachidontes* at the Piver's Island site

Geukemla demissa (n = 43) Brachidontes exntstus (n -----44) Length Length Height Length Length Height Length Height Width (cm) Height ~,Vidth ~,Vidth Height i d tHeight h (cm) W (cm) Width Width (cm) (cm) 0"50 0"75 x.oo 1"25 1"5o z'75 2.00

0-26 0"39 o.5i o'63 0"75 0"87 0"99

o"14 o.22 0"30 0"38 0"46 0"54 0"62

z'92 x.92 x'96 1"98 2"oo 2"Ol 2"02

3"57 3"41 3"33 3"29 3"26 3"24 3"23

x.86 z.77 1"7o 1"66 x "63 1"6t x'6o

"Maximum shell length 2"15 cm.

0"33 0"48 0"63 0"77 0"92 z'o6 1"2o

o.18 0"30 0"42 0"54 0"67 0"80 o'94

z'52 x.56 1"59 x'62 x"63 x'65 1"67

2"78 2.5 ~ 2"38 2"31 2"24 2"19 2"I3

1"83 z.6o 1"5~ 1"43 1"37 x'33 I'28

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The extensive population of Panopeus at the Piver's Island site was examined by making standard xo rain searches (n = 6) in which all observable crabs [except for very small individuals < i . o cm carapace width (CW) ]were collected. In the laboratory these were identified, counted and sexed. Carapace width and the maximum height and gape (Figure x) of the major cbeliped were also recorded. The relationships between these parameters were briefly examined by means of the allometrie equation (see above). Although Callinectes is abundant in the Beaufort area no attempt was made to census the local population of this swimming crab. However, small to medium-sized crabs, particularly those between 6.o-8.o cm CW which were used in most of the feeding experiments, were especially abundant. These were easily collected by hand net from the sea wall when, at high tide, they could be observed feeding on mussels and oysters in the intertidal zone. Several larger crabs (up to 16.o cm CW) were obtained by trawling in the local Sounds. The extensive literature relating to the decapods of N. Carolina is summarized by Williams (I965). Feeding experiments were carried out in plastic aquaria filled to a depth of approximately 20 cm with running seawater at 274-2 ~ The dimensions of these aquaria were 45 cm • 35 cm (for experiments involving Callinectes) and 30 cm• cm (for those with Panopeus). Male crabs were used in all the experiments to avoid any potential bias that might arise through minor sexual differences in morphology or behaviour. Hunger levels were standardized by starving the crabs for 48 h before each experiment. Only undamaged, healthy mussels from the sea wall population were used as prey. Silt, faeces and shell fragments were siphoned out of the tanks daily. The critical upper threshold of prey size that a crab of any given carapace width could open was determined by presenting crabs of different size with small mussels. As these were consumed they were replaced by progressively larger mussels until 5 consecutive days elapsed without further loss. The possible adverse effects of captivity and/or lack of appetite were then controlled for by offering mussels below the critical size and showing that these were readily consumed. Whenever possible the techniques used by the crabs to open their prey were observed directly. However, shell remains were also collected after each successful attack in order to examine how they had been opened and to assist in interpreting and describing the actual technique employed. Feeding behaviour was studied under regimes of both unlimited and restricted prey availability, the latter by presenting crabs of three different size ranges with equal numbers of mussels in each of several length categories. These were scattered at random over the floor of the aquaria and the number of mussels in each size class which had been consumed was monitored daily for x4 days. None of the mussels which had been eaten were replaced. Similar experiments were set up for large and medium-sized Panopeus and for small Callinectes in order to assess the effects of diets with unlimited prey. Here, however, the experiments were monitored twice daily for 5 days and any mussels which had been consumed were replaced by ones of similar size so as to maintain constant prey availability. Some measure of potential feeding rates were obtained by offering crabs an unlimited supply of mussels within a specific 'preferred' size range. The rate at which these were consumed was monitored daily for 7 days. Results

The musselpopulation Table x compares the overall shell characteristics of the two Geukensia populations and shows that sea wall mussels were both taller and slightly wider than salt marsh mussels of comparable length. On the sea walls and pilings Geukensia coexists with another mussel.

Predator--prey relationships

449

Brachfdontes exustus. Although rarely exceeding z.o cm in length at the Piver's Island site

(the largest specimen in the samples was z.x 5 cm) this small mytilid is extremely common, more especially at lower tidal levels. Table ~ documents the shell characteristics of these two mussels and shows that at any given length Brachidontcs is both significantly taller and wider than Gettkensia. The size and shell proportions of the largest mussels collected at the sea wall site irrespective of species are shown in Table 3. Apart from the limited number of large, thick-shelled mussels present at the base of the sea wall it is clear that the largest mussels at this site occur principally in the upper intertidal zone. The sea waU and salt marsh populations differ markedly with respect to their overall size-frequency distributions. Figure 2(a) shows that both populations are dominated, at T ~ g n 3. Size and shell characteristics amongst samples of the largest occurring mussels collected at four tidal levels at the Piver's Island site

Level High oyster zone B Low oyster zone r Tlase of sea wall Oyster clumps on low shore mud 4

Length (cm)

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Length tleight

Length Width

Height Width

n

5"78(o-57) a 2"69(0"26) 4"z7 (o-60 2"09 (0"24) 6'68(0-79) 3"o6(o'35)

x.86(o-x8) x'38 (0"25) 2"27(o'23)

2.x5(o.i2 ) 3"o8(o"I7) 2"o4(o'x2) 3"x3 (o-zz) 2"z9(o'x4) 2"97(o'x9)

x'44(o'zo) x'54(o'xs) x'36(o'o9)

25 23 26

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=Values are means:t:t sin. (in parentheses). b"Upper and lower halves of the main sea wall oyster belt respectively. dAll mussels in this sample were Brachidontes. Other samples contained only

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450

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least numerically, by relatively small mussels <2.0 cm in length. However, the paucity of larger mussels in the sea wall population contrasts with the pronounced bimodal distribution of the salt marsh population where mussels 3-o-9.o cm in length account for over 60% of the population. The relationship between shell length and total biomass (damp weight of shell and tissue) in Geukensia is described by the following power function: Biomass = o.o8 length2";~; r ~ = o.99; (n = 65). Using this equation it is possible to examine how total biomass within these populations is distributed amongst mussels of different shell length. Plots of mussel biomass per unit length class [Figure 2(b)] are interesting for they demonstrate that whilst larger mussels may indeed be less abundant numerically, they account, nonetheless, for the vast bulk of the biomass in these populations. This is particularly evident in the salt marsh population where mussels <3.o cm in length make only a minor contribution (<2"o%) to the total biomass.

The Panopeus population P. herbstii is exceedingly abundant at the Piver's Island site where it accounts for over 8o% of the local population of mud crabs ( > I.O cm CW). Densities averaged 46.o4-7.8 crabs per standard io rain search (n = 6). This value, however, excludes the large numbers of very small mud crabs which inhabit the deep interstices of the oyster clumps and which could not therefore be rapidly extricated. The sex ratio (males : females) of the combined samples was i : o.7o (n = 276 ). Size-frequency distributions of male and female Panopeus are shown separately in Figure 3- Although there was little difference in the mean carapace widths of male (2.06• cm) and female (i.9o4-o.43 cm) crabs, the largest occurring individuals (i.e. those >3.0 cm CW) were all males. 30 I I I | Female n=l14

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Figure 3. Size-frequency distributions (carapace width) of male and female P. herbstii at the sea wall site. Panopeus is markedly heterochelous. The major cheliped, which may be the right or left claw (57 : 43% respectively) is considerably larger and has a pronounced peg on the dactylus (Figure I). Claw height is positively allometrie with respect to carapace width (for a sample of 45 male crabs and xxo female crabs b = v35; A ----0.29; r 2 ---- 0"96) so that the claw becomes proportionately larger with overall increase in body size. Male chelipeds were slightly larger than those of female crabs though t h e differences were statistically indistlnguishable. Since female crabs were not used in any of the feeding experiments, the

Predator--prey relationships

45 x

relationship between maximum hei~zht and gape of the major cheliped was estimated only for male crabs (n -----56). This relationship is one of negative allometry (b = 0.67; A = o.79; i

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Figure 5. Daily feeding rates of three size classes of P. herbstli with limited prey availability. (a) 3"7-4"0 em C W (b) 2"9-3"u cm CW (c) 2"2-2"4 em CW. Four crabs were used in each experiment and ten mussels in each size class were offered. Stippled areas indicate the number of mussels remaining unopened after 34 days.

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452

r 2 = 0.92 ) indicating that increase in maximum gape occurs rather more slowly than increase in height. This suggests that as the cheliped grows so it becomes a proportionately thicker and more robust structure. These results contrast markedly with those obtained for Callinectes, albeit for a rather small sample of crabs varying from 6.5-r5. 5 cm in carapace width (n = x x). Here claw height was negatively allometric with respect to carapace width (b = o.65; A = o.37; r ' ~ o.93 ) whereas the relationship between claw gape and claw height was virtually one of isometry (b = I.o5; A = x.3o; r 2 -~ o.95 ).

Feeding experiments T h e relationship between the critical length of mussel that could be opened and crab size is examined for Panopeus in Figure 4 from which it is clear that the maximum size of prey available for consumption is broadly proportional to the size of the predator. Large crabs (i.e. those over 3.0 cm CW) could open virtually all size ranges of mussels that were represented to any appreciable extent in the sea waU Geukemia population whereas smaller crabs were progressively more restricted as to the size of mussels which they could handle. Even relatively small crabs, however (c. 1"5 cm CW) could consume mussels between x.o-2.o cm in length. Feeding behaviour in Callinectes was examined in only three size ranges of crab. Large crabs (15.0-I6.o cm CW) crushed all size ranges of Geukensia except for the largest of the thick-shelled mussels (>8"0 cm) from the base of the sea wall. I~{edium-sized crabs Doy 5~1"

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Figure 6. Daily feeding rates of three size classes of C. sapidus with unlimited prey availability. (a) xs'o-x6-o cm CW (b) xo-o-tx.o cm CW (c) 6"o-7"o cm CW. Two crabs used in experiments (a) and (b) where five mussels in each size class were offered; three crabs used in experiment (c) where ten mussels in each size class were offered. Stippled areas indicate the number of mussels remaining unopened after x4 days.

Predator-prey relationships

453

(xo.o--xx.o cm CW) and small crabs (6.0-7.0 cm CW) consumed mussels up to 5"5 cm and 4-8 cm in shell length respectively. The results of experiments with restricted prey availability are illustrated in Figures 5 and 6. Early in these experiments (Day z) most crabs selected the smaller size classes of mussels and only when these had been completely depleted did they proceed to attack larger prey. This apparent avoidance of large mussels, however, was not due to lack of appetite since the chipped posterior margins of many of these shells was dear evidence of unsuccessful attaeks on these mussels. The results obtained for large Panopeus [Figure 5(a)] were rather different in that these crabs fed initially on medium-sized mussels before subsequently attacking first the smaller and then the larger size classes of Geukensia. Figure 7 summarizes the results of the experiments in which crabs were fed a diet with unlimited prey availability. Only large and medium-sized Panopcus and small Callhwetes were used in this particular series of experiments. Panopeus exhibited a pronounced preference for specific size classes of mussels. Whilst larger crabs [Figure 7(a)] fed on all size classes of prey offered, they showed a marked preference for mussels within the x.o-3.o cm range. Optimal prey for smaller crabs [Figure 7(b)] on the other hand, consisted principally of mussels < i . o cm in shell length. Callinectes, like Panopeus, again exhibited a marked reluctance to feed on larger items of prey when smaller mussels were in constant supply [Figure 7(c)]. Table 4 shows that both mud crabs and blue crabs are potentially capable of consuming large numbers of Geukemia. Each Callhwctes, for example, devoured an average of :[8"8-t-5"7 mussels (2.o-3.o cm) per day over a period of 7 days. Large Panopeus each ate x3.7+2. 9 somewhat smaller mussels (i.o-2.o era) per day whilst smaller mud crabs, approximately 2.o-2- 5 cm carapace width each consumed between five and six mussels daily. Even very small crabs were capable of devouring substantial numbers of small Geukensia. Several experiments of a very preliminary nature, using five Callinectes (6-o-7.o cm CW) and five Panol)eus (2.5-3.o cm CW) were set up to examine whether certain prey species might prove to be more attractive to these crabs. Each experiment was run for 24 h. (o) I

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454

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TABLE4. Feeding rates of crabs presented with specific size classes of Geukemia Duration of each experiment was 7days Number of mussels eaten predator- 1 day- x Predator and size (cm)

Calllnectes (6"5) Panopeus (3"5; 3"8) Panopeus (2"4; z'5) Panopeus (x'9) Panopeus (o"8-1"2)

Number of crabs Number of prey in experiment offered daily 2 2 2 2 4

6o* 40 40 4~ 3~

Size of prey (era)

2-3 x-2 x-2 t-2 o-5-x'o

Max

Mean (-4-s.D.)

28 x9 9 9 3

x8"83b (5"65) x3"7x (2"86) 5"x4 (2"9I) 5"86 (Z'4I) 2"oo (0"97)

*Only 40 offered on days x-2. ~This value increases to 22"6o (-4-4.95) if results for days x-2 are excluded from the calculation.

Braehidontes is both taller and wider than Geukemia of similar length (Table 2) and might therefore prove more difficult to crush. However, when presented with an equal number of these two mussels, neither Callinectes nor Panopeus showed any significant preference for either prey species; virtually equal numbers of the two mussels were consumed by both crabs. Blue crabs did, however, show a marked preference for mussels when offered a mixture of Geukensia and Crassostrea of similar size suggesting that oysters are perhaps more difficult to crush; over 9o% of the shells consumed were mussels. This propensity for mussels, however, was less evident when they were offered with somewhat smaller oysters. Even so, mussels were still consumed at approximately twice the rate of the oysters. Panopeus showed no apparent systematic preference for either oysters or mussels, consuming both bivalves at broadly similar rates.

Feeding behaviour Panopeus was a far more conservative predator than Callhtectes and was never actually observed consuming its prey. Collections of broken shell fragments, however, indicated that most of the mussels eaten by mud crabs had been opened in a remarkably consistent fashion [Plate i(a)]. These shells contrast markedly with those attacked by Callineetes. Close inspection of these predated shells suggests that Panopeus probably relies largely on the strength of its massive major cheliped, with its broad molar-like surface, to crush open its prey. The peg like structure on the daetylus of this large claw probably functions as an effective punch, enabling the claw to apply considerable force to a very restricted area of the mussel shell. Callinectes, by contrast, is a particularly pugnacious predator. Although not markedly heterochelous the elongate chelipeds of this crab are large and powerful with exceedingly sharp, strongly toothed cutting surfaces. When feeding on mussels the prey is manipulated not only by the chelipeds but also by the anterior walking legs and the large outer pair of maxillipeds. The fringes of hair on the inner edges of the walking legs are especially sensitive and once these contact a suitable item of food it is greedily scooped forwards towards the mouth. Small mussels, usually < i . o cm in length, were easily crushed outright. During this process the prey was held by one eheliped whilst force was applied to the shell by the other cheliped. Once the shell had been crushed, flesh was torn away by means of the claws and mandibles. Most attacks on slightly larger mussels (x.o-3.o cm) were centred on the weaker umbonal region of the shell. After each unsuccessful attempt to open the shell the position of the mussel was adjusted slightly until a weak spot was found and the umbones smashed. If the shell could not be opened after several crushing attempts it was usually abandoned for another mussel. Larger mussels could not generally be crushed and an alternative, somewhat slower, method of attack was adopted. Here the posterior edges of the shell were gradually

Predator-prey relationships

455

chipped away until the chelipeds could be forced between the valves and the adductor muscles severed. The valves were then grasped by the chelipeds and pulled open in order to expose the flesh. Shells attacked in this manner frequently had a rather ragged appearance but otherwise remained intact. Plate z(b) shows a selection of mussel shells that have been predated by Calllnectes and illustrates the varied nature of the shell fragments. Discussion Although feeding experiments have demonstrated that Callinectes and Panopeus are capable of consuming large numbers of Geukensia it is not certain to what extent such laboratory studies can be considered representative of the field situation. However, many of the small to medium-sized blue crabs which regularly follow the incoming tide were observed foraging amongst the intertidal oysters and mussels. P. herbstii is the largest occurring species of mud crab and although rarely exceeding 3"5 cm in carapace width (the largest individual in this study was 4"9 cm CW) this stout bodied crab has extremely powerful chelipeds with which to crush its prey. Mussels consumed by Panopeus were remarkably uniform in appearance [Plate z(a)] suggesting a relatively stereotyped method of attack. Callineetes, by contrast, exhibits several specific mussel opening techniques which vary according to the size and shell strength of the prey. Elner (z978) describes five distinct, Iargely size related, mussel opening techniques in Carcinus. He showed that crabs seek out and exploit weak spots in the umbones by a process of trial and error eventually smashing the mussel through a cumulative process whereby minute fractures in the shell sub-structure are gradually extended. Opening techniques similar to those described by Elner (I978) have also been observed by Harger (z97z) for Cancer antennaria and Paehygrapsus crassipes whilst Krantz & Chamberlin (z978) noted several specific patterns of shell destruction when Callineetes was fed a diet of cutchless oyster spat. Crabs generally locate their prey through chemical and tactile sense organs on the antennae and walking legs. In Callinectes the latter are particularly sensitive and any mussels coming into contact with them were immediately drawn forwards under the carapace to the mouth. Panopeus and Callinectes both fed on mussels over a relatively wide size range. The maximum size of prey that any given crab could open was broadly proportional to the size and strength of the predator. Both crabs, however, exhibited a marked reluctance to feed on larger size classes of prey whilst smaller, more easily predated mussels were available. This apparent preference for prey well below the critical size that they can consume, has been noted by previous workers (e.g. Lunz, z947; ~icDermott & Flower, z953 ; McDermott, z96o; Whetstone & Eversole, 1978). When presented with diets of unlimited prey availability crabs selected prey of a preferred size, the range of which, in Panopeus at least, increased with the size of the predator. Prey selection has recently been demonstrated in Carclnus lnaenas by Elner & Hughes (i978) and in Cancer irroratus and Ilomarus amerieanus by Elner & Jamieson (I979). Carcinus forages optimally, maximizing its energy intake by actively selecting its prey, Mytilus edulis. Elner & Hughes (z978) also showed that there was no upper limit to the size of mussels which could be predated since Carcinus could utilize an alternative method of attack which was effective for all larger size ranges of prey. This method, however, was rather slow and consequently prey value decreased rapidly at larger prey size. Nevertheless, suboptimal prey could be incorporated into the shore crabs' diet by increasing its relative abundance. Both Callinectes and Panopeus are capable of consuming large numbers of mussels. Relatively small blue crabs used in these experiments (Callinectes can grow to well over

456

R. Seed

20"0 cm CW) each ate an average of 18"84-5. 7 mussels (2.o-3.0 cm) every day (maximum 27.o day-Z) whilst Panopeus, approximately 2.o cm in carapace width attained mean daily predation rates of 5"94-2"4 mussels (1.o-2.o cm) per day. Even very small Panopeus (,.o 1.o cm CW) which are extremely abundant amongst the oyster clumps were each capable of consuming significant numbers of small mussels. McDermott (i96o) found that Panopeus ate one and two year old oysters at the rate of o.15-o'7o oysters per crab per day (crabs 2.2-3. 3 cm CW could kill oysters up to a mean size of 3.6 cm; one small Oeukensla 2.o cm long which was present in the aquarium was also smashed). Menzel & Hopkins (1956) reported that a single Callinectes could consume as many as 19 oyster spat per day. Krantz & Chamberlin (1978) noted that whilst lO-Z5 cm blue crabs could consume 4.o cm oysters, crabs 6"5-8"o cm could not feed on oysters larger than 2-5 cm. The smaller size classes of Goukensla are clearly most vulnerable since these are available to virtually all size ranges of crabs. However, once beyond a certain critical size range, probably around 3.o-4.o cm in this population, these mussels will experience increasing immunity from these predatory decapods and their life expectancy will be correspondingly enhanced. Size-limited predation has previously been documented in several other marine bivalves (e.g. Seed & Brown, 1975; Paine, 1976; Whetstone & Eversole, z978). The different size frequency distributions of Geukensia at the two sites are interesting in the light of these laboratory experiments. Both populations are dominated by small mussels (<2"o cm) but the scarcity of larger mussels at the sea wall site contrasts markedly with their relative abundance in the salt marsh. These differences in population structure are tentatively attributed largely to crab predation. At the Piver's Island site, crabs, particularly Panopeus, are exceedingly abundant and their foraging activities probably result in very heavy mussel mortality such that relatively few individuals survive to any appreciable size. Predatory gastropods are also present in the sea wall community and these too must undoubtedly contribute to Geukensia's demise at this site. However, a protective shell, together with the ability to air gape when exposed by the tide (Lent, 1967b) enable Geukensia to survive at somewhat higher tidal levels than many of its major predators. Thus, although a suboptimal habitat from the point of view of feeding and growth, the high intertidal zone provides a spatial refuge in which predation pressure is considerably relaxed. It is significant, therefore, that the largest occurring mussels on the sea walls and wharf pilings are those occupying the higher tidal levels (Table 3). The large mussels at the base of the sea wall are probably isolated survivors of earlier settlements which have escaped predation by virtue of their protective habitat. Alternatively these large mussels may have re-established themselves at this level after breaking away from the high density sea wall population above. Whatever their history these thick-shelled mussels are now probably too large to be eaten by most of their major predators. In the low shore, heavy predation effectively prevents any substantial mussel population from becoming established though a few small individuals do survive in the protected interstices of the clumps of large oysters which have become detached from the dense population above. Around low water mark most oysters are infested by Clione celata, a sponge which seriously weakens the shell. The combined effects of sponge infection and heavy crab predation result in the virtual exclusion of these bivalves from the sublittoral in this locality. Ebling et al. (I964) demonstrated experimentally that the absence of Mytilus from much of the shallow sublittoral in Lough Ine, S.W. Ireland, was due largely to crab predation. Newcombe (1935) showed that Mytilus edulis could fluorish subtidally in the Bay of Fundy when protected from predators. Potential mussel predators were less evident in the local salt marshes than at the sea wall site. Here small mussels occur near the marsh surface (often attached to the posterior shell

Predator-prey relationships

457

margins of larger conspecifics) where they would seem to have relatively little protection especially from crabs which could easily dig them out. Larger mussels, however (>3"0 cm) mostly occurred in dense tightly bound clusters within the compacted sediment and were therefore probably less accessible to predators. Furthermore, the almost vertical orientation of these mussels is such that the vulnerable umbones are offered the maximum degree of protection deep in the substratum. The abundance of small mussels in both populations is unlikely to be due to recent settlement since the main recruitment period of Geukensla in this area is reported to occur from late August until October CMcDougall, 1943). Kuenzler (1961a) explained the persistence of small mussels throughout the year in a Georgia salt marsh, where ripe adults occurred only during late summer, in terms of highly variable growth rates (see also Seed (I969) for Mytilus e&dis). Heavy mortality rates amongst small mussels may prevent all but a few individuals from any single year class from surviving beyond a certain critical size range. Itowever, those which do survive, enter a pool of larger mussels whose body size and firm anchorage then protects them from further serious predation. Certain sublittoral populations of 3lodiol,ts modiolus and Aulocomya ater have also been found to be deficient in size categories close to those preferred by certain predatory crabs (Seed & Brown, 1975; Pollock, 1979 respectively). Kuenzlcr (I961a) suggests that the bimodal distribution of weight classes in Geukensia is largely explicable in terms of the high mortality of small mussels that occurs especially during summer and autumn. It is uncertain to what extent these laboratory observations are representative of the field situation where alternative sources of food are available. AIorcover, in these laboratory experiments, isolated mussels were scattered over the floor of the aquaria whereas in natural populations they are firmly bound by byssus threads in dense clusters with many of the smaller, more vulnerable size classes protected in the interstices between larger individuals. Elner & Hughes (1978) have shown that predation rates of Carchms maenas on small Mytilus edulis were lower when mussels were presented in dumps than when they were dispersed over the floor of the aquarium. Krantz & Chamberlin (z978) also comment on the greater ease with which cultchless oyster spat, rather than spat that was attached, could be manipulated by Callinectes. McDermott (i96o) however, found that crowding in oyster spat actually increased its vulnerability to predation by Panopeus. Accepting that laboratory experiments are no substitute for direct field observations these results do indicate that Callhwctes and Panopeus arc capable of consuming large numbers of Geukensia and must therefore have at least the potential to profoundly influence both the local distribution patterns and population structure of this prey species. Aclmowledgements The author wishes to thank the Director of Duke University Marine Laboratory, Dr J. D. Costlow, for providing research facilities and Dr R. N. Hughes for commenting on the manuscript. References

Abbott, R. T. z974 American Seashells (2nd edition). D. van Norstrand Reinhold, 663 pp. Blake, J. "~V. z96o O.wgen consumption of bivalve prey and their attractiveness to the gastropod, Urosalphur einerea. Limnology and Oceanography 5~ 273-280. Dare, P. J. 6; Edwards, D. B. z976 Experiments on the survival, growth and yield of relald seed mussels (i~ytilus edulls L.) in the Menai Straits, North Wales. Journal du Conseil, Conseil Permanent lnternational pour L'Exploration de la .~Ier 37~ x6-28. Ebling, F. J., Kitching, J. A., Muntz, L. & Taylor, C. HL 1964. Experimental observations of the destruction of 2~I),tilus edulis and Nucella lapillus by crabs. Journal of Anhnal Ecology 33~ 73-82.

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Eldridge, P. J., Waltz, W., Graey, R. C. & IIunt, tl. H. 1976 Growth and mortality rates of hatchery seed clams ~Iercenaria mercenaria in protected trays in waters of S. Carolina. Proceedings of the National Shellfisheries Association 66, x3-zo. Elner, R. W. 1978 The mechanics of predation by the shore crab, Carcbtus maenas (L.) on the edible mussel, 3Iytilus e&dis L. Oecologia (BerlbO 36~ 333-344. Elner, R. W. & Hughes, R. N. I978 Energy maximization in the diet of the shore crab, Carclnus maenas. ffourt,al of Anin,al Ecology 47~ xo3-r x6. Elner, R. W. & Jamieson, G. S. 1979 Predation of sea scallops, Placopecten magellanlcus, by the rock crab, Cancer irroratus, and the American lobster Homarus amerieanus, ffournal of the Fisheries Research Board of Canada 36~ 53 x-543. Harger, J. R. r 97z Competitive co-existence: maintenance of interacting associations of the sea mussels 3lytilus edulis and ~lytilus californianus. Vellger 14~ 387-41o. Kitching, J. A. & Ebling, F. J. 1967 Ecological studies at Lough ,lne. Advances in Ecological Research 4~ x97-z9 x. Krantz, G. E. & Chamberlin, J. F. t978 Blue crab predation on cultchless oyster spat. Proceedings of the National Shellfisher&s Association 68~ 38-4z. Kuenzler, E. J. 1961a Structure and energy flow of a mussel population in a Georgia salt marsh. Limnology a~td Oceanography 6~ 191-2o 4. Kuenzler, E. J. 1961b Phosphorus budget of a mussel population. Limt~ology and Oceanography 6~ 4oo--4x 5. Len.t, C. M. 1967a Effect of habitat on growth indices in the ribbed mussel, z'~Iodiolus (Arcuatula) demissus. Chesapeake Science 8~ 2zI-zz 7. Lent, C. 1~I. 1967b Air-gaping by the ribbed mussel, 3lodiolus demissus (DillxxTn): effects and adaptive significance. Biological Bulletin of the marine blolog&alLaboratory, Wood's Hole 134~ 60--73. Lunz, G. R. 1947 Callbzectes versus Ostrea.ffournal of the Elisha 3litchell Scientific Society 63j 81. Menzel, R. W. & Hopkins, S. H. r956 Crabs as predators of oysters in Louisiana. Proceedings of the Natiotml Shellfisheries Association 46, 177-184. l~lcDermott, J. J. x96o The predation of oysters and barnacles by crabs of the Family Xanthidae. Proceedings of the Pennsylvania Academy of Science 34~ x99-211. McDermott, J. J. & Flower, F. B. r953 Preliminary studies of the common mud crabs on oyster beds of Delaware Bay. National Shellfisheries Association z952 Convention Addresses, pp. 47-5 o. bIcDougall, K. D. x943 Sessile marine invertebrates of Beaufort, North Carolina. Ecological 3Ionographs x3~ 32r-374. McKenzie, C. L. 197 ~ Causes of oyster spat mortality, conditions of oyster setting beds and recommendations for oyster bed management. Proceedings of the National Shellfisheries Association 60,

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Newcombe, C. L. I935 A study of the community relationships of the sea mussel, 3Iytilus edulls L. Ecology x6~ 234-243. Paine, R. T. 1976 Size limited predation: An observational and experimental approach with the llXytilus-Pisaster interaction. Ecology 57, 858-873. Pollock, D. E. 1979 Predator-prey relationships between the rock lobsterffasus lalandii and the mussel Aulocomya ater at Robben Island on the Cape ~,Vest coast of Africa. ~Iarbte Biology 5z~ 347-356. Reise, II. 1977 Predator exclusion experiments in an intertidal mudflat. Helgolh'nder rrissensehaftliche 2~leeresuntersuehungen 3o~ a63-z7r. Ropes, J. W. 1968 The feeding habits of the green crab, Carcbzus maenas (L.) Fishery Bulletin Fish and Wildlife Service. U.S. Department of the bzterior 67~ 183 -203. Seed, R. 1969 The ecology of 2~lytilus edalis L. (Lamellibranchiata) on exposed rocky shores. II. Growth and mortality. Oecologia (Berlin) 3~ 3z7-35o. Seed, R. & Brown, R. A. 1975 The influence of reproductive cycle, growth, and mortality on population structure in 3Iodiolus modiolus (L.) Cerastoderma edale (L.) and 3lytilus edulis L. (Mollusca: Bivalvia). Proceedings of the 9th European Marine Biolog&al Symposium z57-z74. ~,Vells, II. ~,V. 1958a Feeding habits of i[lurexfuls Ecology 39~ 556-558. V,'ells, H. W. 1958b Predation of pelecypods and gastropods by Fasciolaria hunteria (Perry). Bulletbz of 3Iarine Science of the Gulf and Caribbean 8, 15z-166. Whetstone, J. M. & Eversole, A. G. 1978 Predation on hard clams, 2~[ercenaria mercenaria by mud crabs, Panopeus herbstiL Proceedings of the National Shellfisheries Association 68~ 4z-48. Williams, A. B. 1965 Marine decapod crustaceans of the Carolinas. Fishery Bullethz Fish and Wildlife Service U.S. Department of the b~terior 65~ x-z98.