BULLETIN OF MARINE SCIENCE, 26(3): 403-409, 1976

PREDATION ON LITTORINA IRRORATA (MOLLUSCA:GASTROPODA) BY CALLINECTES SAPlDUS (CRUSTACEA: PORTUNIDAE)

Paul V. Hamilton

ABSTRACT Callinectes sapidlls swim 10 Ihe surface in the intertidal zone during high tide, and remove Littorina irrorata adhering to plant stems near to and above the water line. Snails are carried to the bottom, cracked open, and eaten. Laboratory observations indicate specialized roles for each of the morphologically different chelipeds during shell opening. Concentration of predation on snails of a particular relative size is suggested by analysis of opercula in cardiac stomachs, and may be partly related to maximizing the amount of food obtained per unit time. The movement of L. irrorata up plant stems on an advancing tide probably serves as a defense against predation by C. sapidlls, Melongena corona, and possibly other predators.

The marsh periwinkle, Littorina irrorata and Neritina virginea were common items in (Say, 1822), is probably the most abundant the largely molluscan diet of C. sapidus in gastropod occupying the low energy inter- Louisiana. Tagatz (1968) states that Nas- tidal zones of the northeastern Gulf of sarius obsoletus is occasionally found in the Mexico. Sample densities on barrier beaches guts of blue crabs from the St. Johns River. may range from less than 100 snails per m~ Tagatz and Hall (1971) list several refer- at mean sea level, to almost 600 snails per ences to blue crab predation on commer- m2 at mean high water level, thus indicating cially important bivalves. a large potential food source for predators. This paper documents and describes the This snail feeds on the substrate during low frequent pred~tion on L. irrorata by C. tide and ascends stems of the upper inter- sapidus, and considers the function of the tidal plants, Spartina alterniflora (the dom- vertically oriented tidal movements of L. inant vegetation), Salicornia perrenis, and irrorata. ] uncus roemerianus during high tide. They usually remain about 15 cm above the water GENERAL OBSERVATIONS lihe (plant height permitting) during high Periodic daytime observations of blue tide, and often secrete a mucous holdfast crab activity were made along the barrier and seal the shell aperture with the oper- beach intertidal zone of Goose Creek Bay, culum, thus minimizing desiccation (Bing- a portion of the St. Marks National Wildlife ham, 1972). Pettitt (1975) reviews the Refuge, on the northeastern Gulf Coast of predators (including crustaceans) of other Florida. Figure 1 shows a stylized cross species of Littorina. However, Cherr's section of the upper intertidal zone in this (1974) report of many small L. irrorata in area. A detailed ecological treatment is the guts of Fundulus simi/is is the only provided by Kurz and Wagner (1957). reference to predation on this species I Predation on L. irrorata seemed to be the found. major activity of many blue crabs invading The blue crab, Callinectes sapidus Rath- the upper intertidal zone at high tide from bun, also inhabits this area, and while often May to October. For instance, all 34 crabs considered only a scavenger, it is also known encountered along approximately 600 m of as a predator of mollusks. Darnell (1958) shoreline, during a 2-hr period one after- found that the gastropods M elampus coffeus noon, were preying on L. irrorata. Many

403 404 BULLETIN OF MARINE SCmNCE. VOL. 26. NO.3, 1976

Juncul 25 N=Sl ond Sollcarnl. Sp.rlln. 20

15

10

Figure 1. Stylized cross section of the upper inter- tidal zone in the area studied. Arrows indicate 5 area within which the accumulation of tidal debris causes shorter vegetation, and where blue crab o predation was most frequently observed. 20 30 40 50 60

CARAPACE LENGTH Imml more crabs were undoubtedly overlooked. Several crabs were observed for more than Figure 2. Size-frequency histogram for 81 blue 1 hr continuously capturing and eating snails. crabs collected in the upper intertidal zone. Mean carapace length was 43.7 mm. Shaded area indi- Predation was most frequently observed cates crabs which had opercula of Littorina irrorata near the high tide line, where the water is in their cardiac stomachs and unshaded area indi- shallowest and the density of snails is the cates crabs which lacked opercula. highest. All 34 crabs mentioned above were within about 5 m from the mean high water line. Predation was only occasionally ob- thermore, not all ascents to the surface result served near the seaward edge of the Spar tina in the capture or even displacement of a zone, where water depth is usually 80 to snail from the grass. If no snails are encoun- 100 cm at high tide. tered, the crab either returns to the bottom, Blue crabs usually ascend to the air-water walks to an adjacent stem and ascends again, interface solely by swimming, but are some- or just swims on the surface to an adjacent times aided by grasping a plant stem with stem and resumes searching. It is not known the walking legs. Once at or near the sur- if crabs can detect the location of individual face, crabs hold onto a stem with the walking snails from the bottom, but if so, visual legs and remove a snail from the stem, perception would seem to be the probable usually with both chelipeds. This sometimes mechanism. involves extending a cheliped as far as 7 em A size-frequency histogram for 81 crabs above the water line. However, periodic collected by dip net amidst the vegetation killbacks of Spartina caused by the accumu- in the upper intertidal zone is shown in lation of tidal debris (Kurz and Wagner, Figure 2. Forty-seven crabs were males, 26 1957) result in shorter stems near the high were immature females, and 8 were mature tide line. Consequently many L. irrorata females (all sex determinations based only are unable to move above the water line at on abdomen shape). Six of the eight mature high tide, making them more accessible to females were parasitized by rhizocephalans, blue crabs. and hence may not have originally been Successful prey capture usually consists females. Crabs subsequently found to have of holding the snail in the vicinity of the opercula of L. irrorata in their cardiac mouth and descending to the bottom. How- stomachs formed a representative sub- ever, a blue crab frequently knocks snails sample of those collected. Possession of off plant stems or loses its hold on an indi- opercula was not related to whether the vidual before returning to the bottom. Fur- major cheliped (crusher) was on the right HAMILTON: PREDATION ON LlTTORINA BY CALLINECTES 405

100 1.0 " .. MEAN ESTIMATED 80 OPERCULUM .. SHELL WEIGHT LENGTH NUMBER Imgl Imml 6 ., OF .1 11 OPERCULA .2

40

.0 +--A ::, 35 45 55 65 CARAPACE LENGTH 20 Imm)

Figure 4. Relationship between carapace length and the mean operculum weight in the cardiac 0 stomachs for the 24 crabs which possessed more 0 40 60 80 than one operculum. Estimated shell lengths were CRAB NUMBER obtained as described in the text.

Figure 3. Distribution of 470 opercula recovered from 81 blue crabs, ordered sequentially from the Figure 4 shows the relationship between crab with the most opercula to the crabs with no opercula (A). A similar sequentially ordered ran- carapace length and mean operculum weight dom distribution (B) and a uniform distribution for the 24 crabs having more than one oper- (C) are included for comparison. culum in their cardiac stomachs. Weights were measured to the nearest 0.05 mg with a Mettler H51 balance. The estimates of or left. Eleven of the 81 crabs possessed shell lengths (right scale) in Figure 4 were only one functional cheliped. Five were obtained from a highly significant (P < .005) missing the minor cheliped (cutter) and linear regression line (y ~ .158x - 1.38, where had 38 opercula (18, 13, 3, 3, 1) in their y = operculum weight in mg and x = shell stomachs, while six wen, mIssing the crusher length in mm) based on pairs of shell length and none had opercula. and operculum weight measurements from Figure 3 shows the distribution of the 470 50 snails of various sizes collected at Goose opercula of L. irrorata recovered from these Creek Bay. These data show a significant 81 crabs, ordered sequentially from the crab (P < .005) relationship between crab size with the most opercula to the crabs with no and mean operculum weight (and hence opercula. The marked difference between snail size). the observed distribution (A), and both a sequentially ordered, random distribution of SHELL OPENING 470 opercula among 81 crabs (B), and a Field observations of shell opening by uniform distribution of 5.8 opercula per C. sapid us were hampered by the minimum crab (C), suggests some crabs are heavily approach distance (about 2 m) before caus- involved in predation on L. irrorata, while ing an escape response, and by plant stems others are not involved at all. Crabs with- obscuring the view. However, in those crabs out opercula in their cardiac stomachs typi- clearly seen, the chelipeds manipulated the cally had large amounts of molluscan shell snail shell in the vicinity of the oral append- pieces and parts of small crustaceans. Five ages. The presence of freshly crushed shells of the six crabs having the greatest number on the substrate after most crabs moved of opercula were in the 40.0- to 44.9-mm away indicated the snails were usually eaten size-class interval, and hence were average immediately. Seven clear observations gave sized crabs (Fig. 2). a mean time from capture of individual L. 406 BULLETIN OF MARINE SCIENCE, VOL. 26, NO.3, 1976

600 commonly aperture up and apex towards the crab. The major cheliped (crusher) is then moved so that the shell is positioned in the crotch of the claw where the largest molar tooth is located. The minor cheliped (cutter) .00 MEAN assists in keeping the shell in place by grasp- ing the portion of the shell furthest from the TIME crab. (sec I Most crabs attempt to crush the shell 200 across the body whorl, with the large molar tooth inserted inside the shell aperture. The large tooth often chips away much of the aperture before the shell is broken open

o completely. However, some crabs repeatedly 2.25 2.75 J.25 J.7.5 ..•.25 4,75 and successfully crush the apexes of shells CRAB!sNAIL SIZE RATIO presented to them, suggesting individual dif- Figure 5. Mean times required by blue crabs to ferences in this complex behavior. The crush snail shells of various relative sizes. Bars crushing technique used did not appear indicate one standard deviation. An observation related to whether the crusher was on the was terminated after 600 s if a crab was unable to right or left. Once the shell is broken open, crush a shell. the soft parts and adhering shell fragments are pulled behind the third maxillipeds, irrorata to resumption of locomotion of 22.7 where other oral appendages rapidly sort s (range, 10-32 s). However, I could not tissue and shell. Shell fragments are dis- determine if resumption of locomotion coin- carded, and the soft parts and attached cided with completion of feeding in each operculum are ingested. case. To determine the relationship between Aquarium observations of 10 blue crabs snail size and crushing speed, 84 L. irrorata more clearly elucidated the details of shell ranging from 9.2 to 20.8 mm in shell length opening. Crabs were held individually in were individually presented to six blue crabs 4 I closed-system marine aquaria at about ranging from 41.6 to 64.2 mm in carapace 20cC. Eight crabs had a right crusher and length, over a 2-week period. Crabs were a left cutter, and two had the opposite con- maintained individually as previously de- figuration. A photograph showing the mor- scribed. The time elapsed between arrival phological differences between the chelipeds of the shell at the oral area after being picked is included in Williams (1974, Fig. 16A). up by each crab, and the first removal of Over 100 observations of shell opening by snail tissue, was recorded for each presenta- C. sapidus indicate this behavior is highly tion. However, an observation was termi- stereotyped. A snail is typically manipulated nated if a crab was unable to crush a shell in the vicinity of the blue crab's mouth with after 600 s. No more than four snails were both chelipeds, the third maxillipeds and given to anyone crab in each 24-hr period, usually one or both of the second periopods. a level far below the satiation point for this The chelipeds overlap from one-third to size C. sapidus. A crab carapace length to one-half the length of the dactylus, with the snail shell length ratio was calculated for major cheliped held closest to the body. each presentation as a measure of relative This manipulation of the shell ceases period- size difference. ically with the shell ending up in one of two Figure 5 shows that a snail can be crushed positions. Usually the shell is held aperture above a crab-snail size ratio of 2.75, and a up and apex away from the crab, and less snail can be crushed more quickly as the HAMILTON: PREDATION ON LlTTORINA BY CALLlNECTES 407

in the field. These data suggest predation A 10 in nature generally involves crabs of cara- pace length three to five times greater than NUMBER the average shell length of their prey, and OF CRABS most often between 4.25 and 4.50 times greater. One possible reason for this concentration of predation in a particular relative size range is illustrated in Figure 6B. A snail B .30 shell length was calculated for the center .25 value in each size ratio interval in Figure DRY .20 6A, using the average carapace length of the WEIGHT 24 crabs (47.7 mm). Estimated dry body [gms] .15 weights corresponding to these shell lengths .10 were obtained from a highly significant (P <

.05 .005) linear regression line (y = .0033x - 3.75 '.25 '.75 .023, where y = dry body weight in grams CRAB/SNAIL SIZE RATIO and x = shell length in mm) based on 29 pairs of shell length (range 8.0 to 14.0 mm) Figure 6. A) Frequency histogram for the ratio and dry body weight measurements, using of crab carapace length to estimated mean shell snails collected at Goose Creek Bay within length for the 24 crabs whose mean operculum weights were shown in Figure 4. B) Maximum 2 weeks after the crabs were collected. These estimated amount of dry body weight obtainable snails were killed in ethanol, removed from in a 600 s period by an average sized crab feeding their shells and placed in an oven at l30°C on different sized snails. for approximately 60 min. The maximum amount of dry body weight obtainable in 600 s (excluding searching time) by an size ratio increases. Approximately 20 s are average sized crab was then calculated for required to crush even relatively small snails ~ach size r~tio interval, based on the average (size ratio greater than 4.50), reflecting the tImes reqUIred to crush shells of different time required to position the shell and relative sizes observed in Figure 5 (time for crusher cheliped. The large standard devia- the 4.75 to 5.00 interval was estimated at tions for the average times in the interme- 20 s). Figure 6B clearly indicates that blue diate size ratios (2.75 to 4.00) probably crabs can obtain the maximum dry weight reflect individual differences in crushing per unit time by feeding on snails in the ability or motivation. Relatively large snails 4.25 to 4.50 size ratio interval. This is the (2.25 to 2.50 size ratio) were discarded size ratio where cardiac stomach analyses soon after being picked up, while crabs indicate crabs actually feed most often in continued working on slightly smaller snails nature (Fig. 6A). (2.50 to 2.75) right up to the 600-s time limit. OTHER PREDATORS Figure 6A shows a frequency histogram for the ratio of crab carapace length to Predation on L. irrorata by the gastropod estimated mean shell length for the 24 crabs Melongena corona is very common in the whose ingested mean operculum weights study area during high tide. M. corona were shown in Figure 4. The estimated capture L. irrorata which fall into the water mean shell lengths were derived from mea- or those attached to short submerged plant sured mean operculum weights as previously stems. described, and are ultimately based upon A single specimen of the spiny boxfish, cardiac stomach contents of crabs captured Chilomycterus schoepji (26 em total length) 408 BULLETIN OF MARINE SCIENCE, VOL. 26, NO.3, 1976 was collected amidst the vegetation in the snails on which they feed in nature (based upper intertidal zone during this study, and on cardiac stomach contents in Figure 6A), was subsequently found to have five L. coupled with limited field observations indi- irrorata, one Pagurus longicarpus and some cating an average feeding time of approxi- L. irrorata shell particles in the stomach. mately 23 s, reveals close agreement between laboratory and natural behavior. Maximiz- DISCUSSION ing the amount of food obtained per unit Blue crabs involved in predation on L. time (Fig. 6B) is probably at least partly irrorata are either immature females or small responsible for the concentration of preda- (mostly male) adults (Fig. 2). Because of tion in the 4.25 to 4.50 size ratio interval their small size, the average sized L. irrorata (Fig. 6A). However, this concentration preyed upon is less than 15 rom in shell could also be contributed to by random length (Fig. 4). Such snails represent the selection of the snails within the size range smallest approximately 70% of the popula- each crab is capable of opening. tion, and most are not yet sexually active. The vertically oriented tidal movements Different use of the crusher and cutter of L. irrorata probably serve to minimize chelipeds in feeding has also been reported predation by C. sapidus, M. corona, and for the Nephropidae (Herrick, 1909), Calap- other predators. Although poorly adapted pidae (Shoup, 1968), Xanthidae (Rossi and for continued locomotion on a submerged Parisi, 1973), Ocypodidae (Hughes, 1966) sand-mud substrate, during high tide it would and other members of the Portunidae (Ebling seem most advantageous for these snails to et al., 1964; Seed, 1969), and probably exists attach to the base of plant stems and remain in other reptantian decapods. This phylo- close to their food source, were it not for genetically widespread occurrence of crusher the risk of predation. Submergence per se and cutter chelipeds among reptantians appears unimportant since L. irrorata can may be related to their widespread habit of withstand continued submergence in the predation on mollusks. However, it is the laboratory for as long as 14 days, while additional swimming ability of the blue crab remaining in the normal unretracted position. which enables it to utilize a food resource However, movement about 10 em above less accessible to completely benthic preda- the substrate on plant stems would suffice tors. Abbott's (1967) report of a blue crab to avoid predation by the non-climbing M. climbing 35 to 40 cm above the water line corona. Remaining 15 cm above the water on a plant stem, for no apparent reason, is line in tall vegetation (Bingham, 1972) may probably a rare occurrence, and such behav- serve to reduce the likelihood of predation ior was never observed by me. Herrnkind by C. sapidus, which was never observed (1968), however, observed blue crabs leav- reaching more than about 7 cm above the ing the water completely and moving up to water line. This behavior may also serve to 1 m onshore to capture fiddler crabs. reduce occasional predation by fish, and to The specialized use of the crusher cheliped minimize the likelihood of displacement by in shell opening, and analysis of the cardiac wave action and the resultant exposure to stomachs from 11 crabs lacking either a benthic predators such as M. corona. Two crusher or cutter cheliped, suggests that a other gastropods found near the study area, crusher cheliped is required for feeding on Melampus bidentatus and Cerithidea scalari- L. irrorata. In aquaria, the shortest average formis, also move above the water line on crushing times (less than 40 s) occurred plant stems at high tide, but the possible role when the crab to snail size ratio was greater of predation in their behavior has not been than 4.0 (Fig. 5). The observation that determined. Some significant benefit must crab carapace lengths are generally at least obviously accrue from moving above the 4.0 times greater than the shell lengths of water line as all three species expose them- HAMILTON: PREDATION ON LlTTORINA BY CALLINECTES 409

selves to potentially stressful environmental Ebling, F. J., J. A. Kitching, L. Muntz, and C. conditions (desiccation, insolation) in doing M. Taylor. 1964. The ecology of Lough Ine, XIII. Experimental observations on the so. destruction of My til us edulis and Nucella With essentially no shell sculpture, the lapillus by crabs. J. Anim. Ecol. 33: 73-82. relatively low shell spire of L. irrorata is Herrick, F. H. 1909. Natural history of the the only other morphological character of American lobster. Bull. Bur. Fish. 29: 149- potential value against crustacean predators 408. Herrnkind, W. F. 1968. Adaptive visuaIly-directed (Vermeij, 1975). This typicallittorinid spire orientation in Uca pugilator. Am. Zool. 8: has little value as a morphological defense 585-598. against C. sapidus since blue crabs usually Hughes, D. A. 1966. Behavioural and ecological begin crushing at the aperture. Hence L. investigations of the crab Ocypode ceratoph- irrorata illustrates that the behavior of gas- thalmus (Crustacea: Ocypodidae). J. Zool. London 150: 129-143. tropods must also be considered when eval- Kurz, H., and K. Wagner. 1957. Tidal marshes uating evolutionary adaptations against pre- of the Gulf and Atlantic coasts of northern dators. Florida and Charleston, South Carolina. Fla. St. Univ. Stud. 24: 1-168. ACKNOWLEDGMENTS Pettitt, C. W. 1975. A review of the predators of Littorina, especially those of L. saxatilis (Olivi) I thank Mr. Red Gidden and the St. Marks (Gastropoda: Prosobranchia). J. Conch. Lon- National Wildlife Refuge for cooperation and per- don 28: 343-357. mission to study there; Dr. William Herrnkind, Rossi, A. C., and V. Parisi. 1973. Experimental Dr. Lawrence Abele, Mr. R. Terumi Nishimoto, studies of predation by the crab Eriphia ver- and Mr. Joseph Halusky for many useful sugges- rucosa on both snail and hermit crab occupants tions; and Mrs. Elizabeth Hamilton for assistance of conspecific gastropod sheIls. Boll. Zool. 40: and preparation of illustrations. This study was 117-135. supported by the Psychobiology Research Center Seed, R. 1969. The ecology of Mytilus edulis L. of Florida State University through Grant PHS (Lamellibranchiata), on exposed rocky shores, MH 11218, and by NSF Grant BMS74-22276 to II. Growth and mortality. Oecologia 3: 317- Dr. William Herrnkind. 350. Shoup, J. B. 1968. Shell opening by crabs of the LITERATURE CITED Genus Calappa. Science 160: 887-888. Abbott, W. 1967. Unusual climbing behavior Tagatz, M. E. 1968. Biology of the blue crab, by Callinectes sapidus Rathbun (Decapoda, Callinectes sapidus Rathbun, in the St. Johns Brachyura). Crustaceana 13: 128. River, Florida. Fish. Bull. U.S. 67: 17-33. Bingham, F. O. 1972. The influence of environ- ---, and A. B. Hall. 1971. Annotated bibli- mental stimuli on the direction of movement ography on the fishing industry and biology of the supralittoral gastropod Littorina irro- of the blue crab, Callinectes sapid us. NOAA rata. Bull Mar. Sci. 22: 309-335. Tech. Rept., NMFS SSRF 640: 1-94. Vermeij, G. J. 1975. Marine faunal dominance Cherr, G. 1974. Species composition and diel variations in the icthyofaunal community of and molluscan shell form. Evolution 28: 656- an intertidal grassbed in the northeastern Gulf 664. of Mexico. Masters Thesis, Florida State WilIiams, A. B. 1974. The swimming crabs of University, 141 pp. the Genus Callinectes (Decapod a : Portunidae). Darnell, R. M. 1958. Food habits of fishes and Fish. Bull. U.S. 72: 685-798. larger invertebrates of Lake Pontchartrain, Louisiana, an estuarine community. Publ. ADDRESS: Department of Biological Science, Flor- Univ. Texas Inst. Mar. Sci. 5: 353-416. ida State University, Tallahassee, Florida 32306.