Pacific Science (1990), vol. 44, no. 4: 384-400 © 1990 by University of Press. AIl rights reserved

Morphology of the Feeding Apparatus Of Cancer novaezelandiae in Relation to Diet and Predatory Behavior!

PAUL D. CRESWELL 2 AND ISLAY D. MARSDEN 2

ABSTRACT: Morphology of the mouthparts, gastric mill, and chelae of the cancer , Cancer novaezelandiae Jacquinot, 1853, was inves­ tigated in relation to dietary composition and predatory behavior. Mouthparts and gastric mill were typical of those ofother large, predatory brachyurans, with similar structure for male and female, small (60-70 mm) and large (120-130 mm carapace width) . The third maxilliped had large crista dentata, and the inner margin of the mandible was rounded, with a sharp, cutting edge. The large, robust chelae were homeochelous with respect to structure and dental pattern. A large diastema was present and both chela exhibited high mechanical advan­ tage (0.36 and 0.37 for left and right chela, respectively). Relative growth of the propodus was positively allometric, which remained constant throughout crab growth. Morphological features ofthe feeding apparatus suggested adaptations for macerating coarse, particulate material. This was supported by foregut analysis showing a predominance of sessile and slow-moving macroinvertebrates in the diet. Bivalve and gastropod molluscs followed by dominated the diet; fish, sponges, coelenterates, and plant matter occurred less frequently. Little variation in dietary composition was evident with crab sex, size, or season. Cancer novaezelandiae adopted fivedistinct techniques to open bivalve shells and three techniques to open gastropod shells. These include direct, umbone and posterior crushing, umbone splitting, posterior chipping, and aperture breakage and spire removal. The success of these techniques was dependent upon crab size and prey size and shape. Large crabs were able to use direct crushing over a wider size range of prey than smaller crabs. The structural and behavioral adaptations permit C. novaezelandiae to specialize on mollusc prey and may explain its migrations into areas dominated by molluscan species.

BRACHYURAN CRABS EXHIBIT WIDE dietary sion, or mating, rather than diet. The func­ tendencies , feeding on sediment, algae, and tional relationships of the feeding apparatus mobile and sedentary prey. The chelae are the are therefore best explained by examination main manipulatory structures in crabs that of not only the chelae, but also the structure feed predominantly on molluscs, but these of the mouthparts and gastric mill. The mor­ differ greatly in morphology within the por­ phology of such structures is regarded as tunid , xanthid, and cancrid crabs (Brown et similar in carnivorous crabs, although clearly al. 1979). Differences in cheliped form , struc­ the ofprey consumed can vary consider­ ture, and robustness, however, may reflect ably from to bivalve molluscs habitat adaptations, display behavior, aggres- (Warner 1977). This study investigates the morphology of the feeding apparatus and feeding behavior of Cancer novaezelandiae, relating it to the 1 This stud y was financed by University of Canterbury natural diet ofcrabs collected from its habitat. Research grant 574995. Manu script accepted 29 January 1990. Cancer novaezelandiae is a species endemic to 2 Department of Zoology , University of Canterbury, New Zealand commonly found in harbors, Private Bag, Christchurch I, New Zealand. , and open rocky coastlines (Bennett 384 Morphology of Cancer Feeding Apparatus-CRESWELL AND MARSDEN 385

1964, McLay 1988). Its depth range is between Where possible, individual food items were oand 60 m, where it can be found buried in identified to species level. However, for the fine sediment, under rocks , stones, and among analysis ofresults, they were grouped into one (Bennett 1964). Juveniles are found of 10 taxonomic categories. These were bi­ in shallow rocky areas living among seaweeds. valve and gastropod, cephalopod, amphipod Because there was no detailed information on and isopod, crab, shrimp, fish, sponge, co­ the feeding apparatus of C. novaezelandiae, elenterate, and plant. Amorphous material we examined the chelae, mouthparts, and gas­ was grouped as unidentified matter. tric mill ofa wide size range ofcrabs. The aim Frequency ofoccurrence ofeach food cate­ was to examine structure of the feeding ap­ gory was recorded for each crab on a presence paratus, including growth of the chelae , in or absence basis. The relative contribution of relation to dietary composition. We also each food category to the overall abundance examined the ability of C. novaezelandiae in and volume within the stomach was assessed the laboratory to open selected species of bi­ using a points method (see Elner 1981). A valve and gastropod prey found in the habitat. high correlation was found between the two methods of diet estimation (male, r = 0.89; female, r = 0.99; n = 10). Frequency of oc­ currence was therefore subsequently used to compare statistically the effects of crab size, MATERIALS AND METHODS sex, and season on crab diet. Data were ex­ pressed in percentage terms based on total Natural Diet number offood items found in those stomachs Cancer novaezelandiae was collected bi­ containing food . Empty stomachs were not monthly between June 1985 and April 1987 included in the analysis. from shallow subtidal sites within Lyttelton Crabs were divided into three size groups: Harbour (430 38' S, 1720 44' E). Traps were small (40.0-60.0 mm), medium (61.0-100.0 set at Diamond Harbour wharf 1-2 hr after mm), and large (101.0-160.0 mm carapace sunset to coincide with time of maximum width) . Seasonal variation in diet was ex­ feeding activity. Traps I m2 (I O-mmwire mesh) amined for spring (Sept. -Nov.), summer baited with fish enclosed in nylon (O.l-mm (Dec. -Feb.), autumn (Mar.-May), and mesh) bags were lowered to depths ofbetween winter (June-Aug.) using 1986 data only. 1.0 and 4.5 m and left for a period of 15 min. Results were compared using chi square Crabs were also collected by 10-min trawls at goodness-of-fit tests on frequency of occur­ a depth between 3.0 and 6.0 m using 1.5-m rence data using 5% level of significance. beam trawl (IO-mm mesh net and 2-mm mesh cod-end) from a channel between Quail Island Structure ofthe Feeding Apparatus and Diamond Harbour. Trawls were taken between 0900 and 1200 hours. The mouthparts (third maxilliped and All crabs were killed immediately by pierc­ mandibles), gastric mill, and chela were re­ ing the dorsocardiac region and placed into moved from five male and female specimens 10% formalin. In the laboratory, sex and of two size classes (60.0-70.0 mm and 120.0­ carapace width of each crab were recorded. 130.0 mm carapace width). These were drawn The gastric mill (proventriculus) was ex­ under a stereomicroscope using a camera tracted and its contents examined under a lucida. The relationship between mouthpart binocular microscope. size and crab size was investigated using Diet was assessed for abundance and length/width ratio of basi-ischium and en­ volume using both the percentage occurrence dopod of the third maxilliped. and the points methods. These methods have The mechanical advantage (MA) of the been used previously to describe stomach con­ chelipeds is defined as the ratio of distance tents of brachyurans (Paul 198I, Williams from the pivot to the tip of the dactylus (L2), 1981, Choy 1986, Wear and Haddon 1987). and the distance between pivot and point of 386 PACIFIC SCIENCE, Volume 44, October 1990

previous studies of brachyuran growth patterns (Huxley 1932, Hartnoll 1974, 1978, Davidson , and Marsden 1987). Regression lines were CHH fitted using least squares regression (model I) F2 \ procedure following the natural logarithmic transformations. Student t tests were used to compare the slope and y intercepts of regres­ CHL sion lines for left and right chela and between male and female crabs. Differences were ac­ FIGURE I. Dimensions used in measurements of the cepted or rejected using a 5% level of signi­ chela. CHH, pro podus height; CHL, propodus length; ficance. All slopes were tested against a value L,IL2 , mechanical advantage. Dotted arrowsindicate the directions through which forces FI and F2 act. of 1.0 using t tests. A slope ofb < 1 indicated negative allometry, while a slope of b > I in­ dicated positive allometry. Where the slope of insertion of the dactylus of the closer muscle the line did not differ significantly from I, apodeme (Ll) (Figure 1) (see Warner and there was isometry, and both structures grew Jones 1976, Brown et al. 1979). The force at the same rate . produced by this system increases with an increasing Ll jL2 ratio, and thus MA is re­ Predatory Behavior on Molluscs garded as a good indication of the stress applied by the chela. Behavior experiments were undertaken Correlations of the left and right MA and using four crabs from each of three size crab size were obtained. Comparisons of groups: large (105.0-115.0 mm), medium mean MA between left and right chela and sex (80.0-90.0 mm), and small (55.0-65.0 mm were made with Student t tests using a 5% carapace width). Crabs were maintained indi­ level of significance. vidually in seawater (salinity 36%0) in large glass aquaria (36 x 20 x 38 em) at 16-1 8° C under fluorescent lights on a 12 lightjl2 dark Morphometries ofthe Chela hour regime. Only male crabs were used in all Crabs collected during the sampling pro­ experiments to reduce variability caused by gram for dietary composition were used to possible sexual differences in morphology and examine the morphometries and relative predatory behavior. Crabs with lost or re­ growth of the chela. Individuals with missing generated chelipeds or walking legs were not or regenerated appendages were excluded . In used. the laboratory, the following measurements Four prey species were presented indivi­ were made to the nearest 0.1 mm using ver­ dually to crabs. Prey used were blue , nier calipers: carapace width (CW), measured Mytilus edulis aoteanus Powell, collected at the widest part; chela propodus height from the upper midtidal zone ofNorth Brigh­ (CHH), from tip of the large dorsal spine to ton beach , Christchurch (43° 29' S, 172° 43' base of the chela; and chela propodus length E); cockle, Austrovenus stut ehburyi Wood, (CHL), from base to tip of the propodus along collected from the low of the ventral margin (Figure I). Carapace width Avon-Heathcote , Christchurch (43° was used as the reference dimension. 33' S, 172° 44' E); spotted whelk, Cominella Relative growth of the chela was examined maeulosa Martyn, and catseye, Turbo sm arag­ mathematically using the allometric growth dus Gmelin, both collected from midtidal equation levels of Lab Rocks and Wairepo Flats, Kai­ koura (42° 25' S, 173° 42' E). Collections were Y=aXb made regularly and only undamaged indi­ where Yand X are morphological dimensions viduals in good condition were used as prey and a and b are growth constants. items. Bivalve length was measured along the This method has been used extensively in longest axis ofthe shell; gastropod height was Morphology of Cancer FeedingApparatus-CRESWELL AND M ARSDEN 387

T ABLE I diately. Approximately 60 trials were per­ LI ST OF ORGANISMS ANDT HEIR ID ENTIFYING FEATURES formed for each prey species and each size REM OVED FROM FOREGUTS OF 186 MALE AND FEMALE group ofcrab. Each crab was used in no more CRABS FROM L YTTELTON HARBOUR BETWEEN J UNE 1985 than 15 trials , with a maximum ofthree trials AND A PRIL 1987. per day. All trials were performed under natural da ylight conditions because initial FOOD TYPES TYPES OFFRAGMENTS experiments revealed no differences in feeding Mollusc behavior between day and night . At the begin­ Bivalve/ Gastrop od Shell fragment s, tissue, ning ofall experiments crabs were starved for Myt ilus edulis aoteanus gill filaments, perio­ 24 hr to standardize hunger level. Austrovenus stutchburyi stracum chips Venerupis largillieriti Paphies australis Cominella maculosa RESULTS Cephalopod Chromatophore-covered . Octopus maorum flesh Natural Diet Crustacea Amph ipod / Isopod Exoskeleton fragments, From a total of547 crabs collected between lsocladus armatus including appendages (i.e., limbs, thoraci c June 1985 and April 1987, only 186 (34%) plates, antennae, spines, contained ingested material in the foregut. eyestalks) They consisted of 120 (64.2%) males and 66 Crab / Shrimp Fragmented exoskeleton, (35.8%) females ranging in size from 40.0 mm Cancer novaezelandiae including carapace and to 135.0 mm carapace width. Nectocarcinus antarcticus leg fragments: gills, Callianasa filholi eyestalks, gastric mill Fourteen species were identified from Halicarcinus whitei ossicles, mouthparts stomach remains (Table I). Phyla represented Hemigrapsus edwardsii (including maxil­ included (bivalves, gastropods, and Upogebia hirtifrons lipeds, maxillae, and cephalopods), Crustacea (amphipods, iso­ mandibles) pods, crabs, and shrimps), Porifera (sponges), Teleost Coelenterata (sea anemones and hydroids), Pleuronectidae Muscle and fibers, scales, Chordata (fish), and Algae (Phaeophyceae, skeletal fragments, jaw, teeth, fin rays Chlorophyceae, and Rhodophyceae). Diet was composed of two main categories: Mol­ Porifera Spicules, spores lusca and Crustacea (Figure 2). Molluscs Coelenterata composed one-third of all food items found, Hydroids Mass of tentacles, stalk with bivalves and gastropods constituting the Sea anemone Anthopleura aureoradiata major dietary components. Crustacea were the second most important food category, Plant Green algae Small pieces of frond , composing one-fifth ofthe diet. Fish , sponges, Brown algae groupings of cells coelenterates, and algae were infrequently Red algae encountered. Dietary composition of male and female crabs consisted of the same food types in relatively similar proportions (X2 = measured from spire tip to posterior tip ofthe 8.447, df = 8, NS). siphonal canal. With respect to crab size, no significant Crabs were presented with an individual differences in dietary composition were ob­ prey item of a particular species, chosen at served between the three size groups of crabs random from a wide size range. The beha­ between 40 and 160mm carapace width (X2 = vioral responses ofeach attack sequence were 25.9, df = 18, NS). All crabs contained recorded. The cheliped used to open prey (left molluscs as the principal prey type; however, or right) was also noted. Once prey had been crabs of40-60 mm carapace width consumed opened, consumed, or rejected , another prey considerably a greater proportion of am­ item of a different size was presented imme- phipods and isopods. Crab, fish, and algal 388 PACIFIC SCIENCE, Volume 44, October 1990

50 MALE 45

>- 40 (,) c: ~ 35 CO ~ u. 30 CI) g' 25 -c: ....8 20 CI) a. 15

10

5 o UN BG CP CR SH AI FI PO co AL Food Category

50 FEMALE 45

40 >­o c: 35 CI) :J ....g 30 u. g, 25 co -a; 20 ....(,) ~ 15

10

5 o UN BG CP CR SH AI FI PO CO AL Food Category

FIGURE 2. Percentage frequency of occurrence ofdietary composition for male (n = 120)and female (n = 66) crabs collected between June 1985 and April 1987. Key: UN , unidentified material; BG, bivalves and gastropods; CP, cephalopods; CR, crabs; SH, shrimps ; AI, amphipods and isopods; FI , fish; PO, porifera; CO, coelenterates; AL, algae. Morphology of Cancer Feeding Apparatus-CRESWELL AND MARSDEN 389 remains were found only in stomachs oflarger tylopodite, articulate freely and are sparsely crabs. covered with setae. The basal segment of the No clear seasonal pattern in dietary com­ exopodite distal to the coxopodite interlocks position was evident during 1986 (X2 = 32.06, with the basi-ischiopodal and meropodal sec­ df = 24, NS). Molluscs, followed by crus­ tions of the endopod when in a resting posi­ taceans, dominated all seasons. tion . The flexible terminal segment of the exopodite is held posterior to the endopodal Stru cture ofthe Feeding Apparatus meropodite, which is covered extensively with long setae. THIRD MAXILLIP ED AND MANDIBLES. Apart The mandible is heavily chitinized; the main from the size differences, there were no ob­ portion is elongate and divided into two parts, vious differences in shape between the same an inner part, which acts as a jaw, and an mouthparts from large (120.0-130.0 mm) and outer apophysis for the attachment of the small (60.0-70.0 mm carapace width) crabs. mandibular muscles. The inner region of the Also, no differences in basi-ischium and en­ mandible is rounded, lacking teeth, with a dopod length/width ratios of the third maxil­ sharp margin to the incisor process. The man­ liped between large and small crabs were dibular palp arises dorsally from the apophy­ observed (2.45 and 4.12 for basi-ischium and sis ofeach mandible, with the palpal segment endopod, respectively). uniformly covered with setae around the The structure of the third maxilliped is periphery. shown in Figure 3. The basi- and ischium of GASTRIC MILL. The cardiac-stomach is a the third maxilliped endopod are flattened large, spherical, dorsoventrally flattened sac. dorsoventrally and fused to form a platelike Parts of the membranous wall are thick and structure. The medial margin of the basi­ calcified, forming three major ossicles. The ischium is fringed by a dense row of short single urocardiac ossicle on the dorsal wall setae and bears numerous blunt, rounded bears a single tooth; on the lateral wall, a pair teeth, the crista dentata. The distal portion of of zygocardiac ossicles also bear single teeth. the meropodite is also flattened and articu­ The lateral teeth consist of denticular pro­ lates distally with the carpopodite. The three cesses and 15-20 small transverse ridges distal segments, particularly the terminal dac- (Figure 4). In addition, smaller supportive ossicles (mesocardiac, pterocardiac, exocar­ diac, and pre-pectineal ossicles) are present. A row of dense setae was present within the gastric mill lying immediately behind the urocardiac ossicle. DACTVLOPODITE Although the size of the cardiac-stomach increased with crab size, the structure of the gastric mill remained relatively unchanged. However, the number of transverse ridges of the lateral tooth appeared to increase with crab size. In addition, no structural differ­ ences between the sexes were observed.

CHELAE. Male and female chelae showed monomorphism or homeochely, with the left and right chelipeds being similar in size and structure. No differences were observed with 10mm respect to chelal dental pattern between males

FIGURE 3. Third maxilliped of C. novaezelandiae. and females and different-sized crabs (Figure Removed from 91-mm carapace width male crab. Left 5). The occlusive surfaces of the chela bear side, oral view. 4-5 discrete , blunt, molariform teeth on both 390 PACIFIC SCIENCE, Volume 44, October 1990

MESOCARDIAC OSSICLE UROCARDIAC OSSICLE PTEROCARDIAC OSSICLE

PRE·PECTINEAL OSSICLE - ---,If ZYGOCARDIAC OSSICLE

EXOCARDIAC OSSICLE

LATERAL TOOTH

DORSAL TOOTH

20mm

F IGURE 4. Gastric mill of C. novaezelandiae. Ventral view of dorsal surface of the cardiac-stomach. Lateral walls spread out.

II 0 10mm O ...... 0 0 ••0 -.»

••• __0 0-0 0 0 0 O O "oO" oo c- o C\:) . " ". ~

~ 10mm

F IGURE 5. Lateral view of right chela of male (I 22 mm carapace width) (left) with occlusive surfaces of the dactyl (right, top) and propodus (bottom). the dactylus and propodus. Adjacent to the (n = 20) for females, which were not signifi­ molar teeth lies a sharp distal tooth on both cantly different (t = 1.5, df = 115, NS; t = fingers. When the chela is closed, these distal 0.506, df = 41, NS). No differences were tips come into contact; however , no contact is found with respect to mean MA for left and made between the molar teeth of the dactylus right chelae of males and females (t = 0.296, and propodus. Hence during claw closure df = 82, NS; t = 0.1723, df = 74, NS). The there is a relatively large gap. relationship of MA and crab size is shown in The left and right chela, respectively, have Figure 6. Correlation analy ses suggest that a mean mechanical advantage of 0.38 ± 0.03 MA remain s constant throughout crab (n = 61) and 0.38 ± 0.03 (n = 56) for males growth (r 2 = 0.74, n = 79; r 2 = 0.71, n = 77 and 0.37 ± 0.02 (n = 23) and 0.37 ± 0.03 for left and right chela, respectively). Morphology of Cancer Feeding Apparatus-CRESWELL AND MARSDEN 391

0.5

11) o Cl ttl 0.4 C -ttl •• > "0 « 0.3 (ij • (J C .cttl 0.2 (J 11) ::E • LMA 0.1 o RMA

O +--r--.----.--,-----..---,,.--r---r--r--.----.--,-----..---,,.--r--,--,..--r-...... -----,----r---r-.------, 30 5040 60 70 80 90 100 110 120 130 140 150 Carapace Width (mm)

FIGURE 6. Relation ship between mechanical advantage and carapace width of left (n = 79) and right (n = 77) chelae. Sexes combined.

TABLE 2

LINEAR CONSTANTS OFTHE REGRESSION EQUATIONS FOR RELATIVE GROWTH OFTHE CHELAE INMALEAND FEMALE CRABS

DIMENSION a b SEM r2 n A .S.

Male Left propodus height -2.0019 1.132 0.0117 0.98 166 11.3 +VE Left propodus length - 1.0987 1.083 0.0085 0.99 165 9.86 +VE Right propodus height - 2.0623 1.147 0.0094 0.99 160 15.6 + VE Right propodus lengt h - 1.0780 1.079 0.0077 0.99 159 10.3 +VE Female Left propodus height - 2.0043 1.125 0.0338 0.93 79 3.70 +VE Left propodus length - 1.0217 1.052 0.0259 0.96 78 2.01 + VE Right propodus height - 1.9429 1.1128 0.0277 0.96 76 4.07 + VE Right propodus length - 1.0751 1.0662 0.0261 0.96 77 2.54 +VE

N OTE: Y = aX", where X = carapace width; Y = chela dimension; a = y intercept; b = slope; SEM = standard error of the mean; r2 = correlation coefficient; n = sample size; I = slope tested against I; A.S. = allometric status.

Morphometries a/the Chela and female crabs was not significantly different (Table 4).Growth of the chelae Allometric growth equations of propodus dimensions was significantly positively allo­ height and length are shown in Table 2. No metric . Propodus height increased at a faster differences in propodus growth rate were rate than propodus length, ultimately confer­ found between male and female crabs of simi­ ring a robust, thick-bodied shape. Although lar size (Table 3). Relative growth of the left chela growth appeared to remain constant and right propodus height and length for male with increasing crab size, there was a slight 392 PACIFIC SCIENCE, Volume 44, October 1990

TABL E 3 subsequently located by rapid lateral exten­ COMPARISONOF LINEAR CONSTANTSOF REGRESSION sion s of both chelipeds. After contact, large EQUAnONSOF DIMENSIONS OF THE PROPODUS BETWEEN pre y items (> 35 mm, cockles > 30 MALEAND FEMALECRABS mm, whelks> 25 mm, catseyes > 20 mm) were immediately swept under the body and DIMENSION df held by the first three pairs ofwalking legs for Left propodus height between 5 and 10 min. During that time no y intercept 0.015 NS attempt was made to open prey. Slope 0.212 NS Individual small prey were grasped im­ Left propodu s length mediately and crushed by the chela, or pushed y intercept 0.660 NS Slope 1.150 NS into the mouth and readily devoured. Right propodu s height Medium and larger prey, however, were ex­ y intercept 0.950 NS ten sively manipulated before opening by Slope 1.160 NS chelipeds, first and second pairs of walking Right propodus length legs, and third maxillipeds. The chelipeds y intercept 0.029 NS Slope 0.476 NS rotated prey, exposing all regions of the shell to the chelipeds, mouthparts, and walking legs. This behavior may allow the crab to TABLE 4 " recognize" prey species and size and, there­ fore , to assess the feasibil ity of opening pre y. COMPARISONOFLINEAR CONSTANTS OF REGRESSION EQUATIONS OF THE PROPODUS INMALEANDFEMALECRABS TECHNIQUES EMP LOYED TO OPEN PREY . Once pre y had been accepted by the crab, attempts DI MENSION df to open the shell followed immediately. Dif­ Male ferent techniques were employed to success­ Left vs right propodus height fully open bivalves and gastropods. y intercept 0.922 NS M ytilus edulis aoteanus and Austrovenus Slope 0.950 NS stutchburyi : Five distinct techniques were Left vs right prop odu s length y intercept 0.410 NS employed to open mu ssels; four were em­ Slope 1.759 NS ployed to open cockles. These were as follows: Female ( I) Direct crushing (DC) Left vs right propodu s height Direct crushing was usually the first tech­ y intercept 0.327 NS Slope 0.280 NS nique attempted by C. novaezelandiae to open Left vs right propodus length mussels and cockles regardless of shell size. y intercept 0.478 NS However, this technique was onl y successful Slope 0.546 NS on small and medium-size prey ( < 45 mm and 30 mm shell length for mussels and cockles, resp ectivel y). Prey was manipulated so that indication ofan increase in allometry for male the left, right, or both chela enclosed the shell, crabs greater than I 10.0 mm carapace width. with the plane of the hinge line oriented ran­ domly to the lateral crushing action of the Predatory Behavior on Molluscs chela. Often the umbone tip or posterior edge of the shell was held between the third maxil­ PREY DETECTION . La rge, medium and small lipeds to provide increased leverage to the C. novaezelandiae readily accepted all prey crushing chela. items presented. Approximately 5- I20 sec after the introduction of indi vidual pre y into (2) Umbone crushing (UC) the tank, an increase in antennular flickering Umbone crushing was used to attack bi­ rate was observed, suggesting that an olfactory valves of all sizes, but was only successful on response had occurred. The crab then moved those of small and medium size (20-60 and quickly in the direction ofthe prey which was 15-40 mm shell length for mussels and Morphology of Cancer Feeding Apparatus-CRESWELL AND MARSDEN 393 cockles, respectively). The shell was mani­ gaps and the shell valves were pried apart in pulated so that the crushing chela applied much the same way as umbone splitting. pressure directly to the umbone region, with Cominella maculosa and Turbo smaragdus: the hinge line perpendicular to the lateral Three distinct techniques were employed to crushing angle of the chela . Usually the non­ open gastropods: crushing chela gripped the shell to steady the mussel and provided leverage for the crushing (1) Direct crushing (DC) chela. Direct crushing was the first method em­ ployed to open whelks of all sizes; however, (3) Umbone splitting (US) it was only successful on small gastropods Splitting the umbone (also known as (< 20 and 25 mm shell height for whelks and "wedging" [Wear and Haddon 1987])resulted catseyes, respectively). The crab grasped the in the separation of mussel and cockle valves shell using the chela and/or the third maxil­ down the hinge line. This technique was em­ lipeds while the other chela was used to crush ployed only after direct and umbone crushing the whelk directly acro ss the body whorl. had failed. Umbone splitting was successful in opening large mussels up to 75 mm and (2) Aperture breakage (AB) cockles up to 50 mm shell length. The shell This was both the most common technique was manipulated so that the propodus and and the most successful method used by C. dactylus of the crushing chela lay directly in novaezelandiae to open gastropods that could plane with the hinge line at the umbone end. not be directly crushed. Two variations of this Force was then applied, causing the tips ofthe method were evident. In the first method, the chela to be inserted between the shell valves. dactyl of one chela gripped the columella Once a gap had been created, the propodus tightly. The shell was then twisted, fragment­ and dactylus could be inserted before severing ing the lip piece by piece, which resulted in a of the shell adductor muscle. peeling effect ofthe aperture lip. In the second method, the dactyls of both chelae were in­ (4) Posterior crushing (PC) serted into the aperture, so that the outer lip Crushing ofthe posterior region ofthe shell was grasped firmly by both chelae . They were was the most infrequent attack method used then twisted in a synchronized fashion so by the crab and was applied only to mussels. that the force generated from one chela was During attempts to utilize this attack method, directed against the other, causing the lip the shell tended to slip away from the chela. to fracture. After the aperture lip had been The crushing chela enclosed the posterior peeled back to maximum operculum retrac­ region of the shell, with the hinge line perpen­ tion , the columella was attacked and the flesh dicular to the leteral crushing action of the was removed. chela. Only medium-size mussels (20-30 mm shell length) were opened by this technique. (3) Spire removal (SR) Crabs occasionally grasped the columella (5) Posterior chipping (PCH) of the shell with one chela while the other Chipping away the posterior shell edge was severed the shell spire. Spire removal was only used after all other methods had failed. In employed on whelks. This technique was comparison with other methods, chipping was rarely successful because the chela tended to time consuming and was employed only on slip over the apical shell whorls. Medium and medium and large shells (29-75 and 15-35 large whelks (25-45 mm shell height ) were mm shell length for mussels and cockles, re­ successfully opened by this technique. spectively). The shell was manipulated to During attempts to open prey species, after allow the tips of both propodus and dactylus considerable effort had been applied by one to chip away small fragments of the posterior cheliped, crabs were regularly observed trans­ shell edge. Eventually, continued chipping led ferring the prey to the opposing cheliped. In to creation of gaps between shell valves. The all three size groups of crabs, neither the tip of one finger was then inserted into the right nor left chela was favored during the 394 P ACIFIC SCIENCE, Volume 44, Octo ber 1990

TABLE 5 PERCENTAGE FREQUENCY OFTECHNIQUES EMPLOYED TO OPENPREYVERSUS PREY SIZE(mm) FOR EACH OF THE FOUR PREYSPECIES TESTED

PREY OPENING SPECIES TECHNIQUE PREYSIZE(mm)

Mytilus edu/is aoteanus 5-15 20-30 35-45 50-60 65- 75

Large DC 100.0 50.0 12.5 0.0 0.0 crabs UC 0.0 36.7 56.3 7.7 0.0 US 0.0 0.0 31.5 84.6 100.0 PC 0.0 14.3 0.0 0.0 0.0 PCH 0.0 0.0 0.0 7.7 0.0 Medium DC 100.0 26.7 0.0 0.0 0.0 crabs UC 0.0 53.3 18.7 0.0 0.0 US 0.0 13.3 75.0 100.0 0.0 PC 0.0 0.0 0.0 0.0 0.0 PCH 0.0 6.7 6.3 0.0 100.0 Small DC 100.0 0.0 0.0 0.0 crabs UC 0.0 50.0 0.0 0.0 US 0.0 50.0 87.5 87.5 PC 0.0 0.0 0.0 0.0 PCH 0.0 0.0 12.5 12.5

Austro venus stut chbury i 10-20 21-30 31-40 41-50

Large DC 100.0 70.5 0.0 0.0 crabs UC 0.0 16.0 18.2 0.0 US 0.0 0.0 73.7 100.0 PCH 0.0 13.6 9.1 0.0 Medium DC 50.0 13.9 0.0 0.0 crabs UC 50.0 36.1 0.0 0.0 US 0.0 36.1 100.0 100.0 PCH 0.0 13.8 0.0 0.0 Small DC 14.3 0.0 0.0 0.0 crabs UC 28.6 9.5 0.0 0.0 US 42.9 80.9 100.0 100.0 PCH 7.1 4.8 0.0 0.0

Cominella maculosa 5-15 16-25 26-35 36-45

Large DC 100.0 100.0 0.0 0.0 crabs AB 0.0 0.0 100.0 40.0 SR 0.0 0.0 0.0 40.0 Medium DC 100.0 36.3 0.0 0.0 crabs AB 0.0 63.6 100.0 100.0 SR 0.0 0.0 0.0 0.0 Small DC 9.1 0.0 0.0 crabs AB 90.0 91.6 100.0 SR 0.0 8.3 0.0 Morphology of Cancer Feeding Apparatus-CRESWELL AND MARSDEN 395

TABLE 5 (continued)

PREY OPENING SPECIES TECHNIQUE PREY SIZE (mm)

Turbo smaragdus 5-10 11-15 16-20 21-25 26-30

Large DC 0.0 100.0 50.0 50.0 0.0 crabs AB 0.0 0.0 50.0 50.0 100.0 Medium DC 0.0 66.1 10.0 0.0 0.0 crabs AB 0.0 33.0 90.0 100.0 100.0 Small DC 100.0 25.0 0.0 crabs AB 0.0 75.0 100.0

NOTE: Approximately 60 observations were performed for each crab size when crabs were presented with prey species. Key: DC, direct crushing; UC , umbone crushing; US, umbone splitting; PC, posterior crushing; PCH, posterior chipping; AB, aperture breakage; SR, spire removal.

TABLE 6 attempt sequence to open prey (x 2 = 0.272, GOODNESS-OF-FIT STATISTICS OFTECHNIQUES EMPLOYED 0.0204, and 0.1053; df = 1; NS; n = 40, 60, TOOPEN PREY AND CRAB SIZE and 38 for small, medium, and large crabs, respectively). PREY SPECIES df r

Mytilus edulis aoteanus 5.49 6 0.482 NS INFLUENCE OF CRAB AND PREY SIZE ON OPEN­ Austrovenus stut chburyi 62.18 6 0.001 *** ING TECHNIQUES. The relative frequency of Cominella maculosa 15.48 4 0.004 ** opening techniques used by small, medium, Turbo smaragdus 1.98 2 0.372 NS and large crabs to successfully open a size

NOTE: Crab size classes grouped. range ofall four prey species is shown in Table •••, P < 0.01; •••, P < 0.001. 5. Goodness-of-fit tests showing the influence of prey size and crab size on opening tech­ TABLE 7 niques are shown in Tables 6 and 7. The techniques employed to open cockles GOODNESS-OF-FIT STATISTICS OFTECHNIQUES EMPLOYED TO OPEN PREY AND PREY SIZE FOR LARGE and whelks were dependent upon crab size. (105-115 mm CARAPACE WIDTH), MEDIUM (80-90 mm), Large crabs were able to successfully employ AND SMALL (55-65 mm) CRABS direct crushing over a wider size range of prey than smaller crabs. However, all crabs, CRAB regardless of size, used similar methods to 2 PREY SPECIES SIZE X df po open mussels and catseyes. Mytilus edulis Large 66.00 12 0.001 *** When individuals of all four prey species aoteanus Medium 85.36 12 0.001 *** were presented to large and medium crabs, Small 73.67 9 0.001 *** opening techniques were influenced by prey Austrovenus Large 61.92 9 0.001*** size. For small crabs, prey size was important stutchburyi Medium 30.80 9 0.001*** when attacking mussels and catseyes. As prey Small 11.37 9 0.498 NS size increased, different techniques were pro ­ Cominella maculosa Large 31.31 6 0.001 *** gressively employed depending on the success Medium 23.02 3 0.001 *** of a previous particular method. However, Small 2.91 4 0.276 NS when small crabs were presented with cockles Turbo smaragdus Large 11.92 4 0.010** and whelks, prey size was unimportant. In­ Medium 8.69 3 0.033* stead, small crabs employed one technique Small 8.00 2 0.018* (usually umbone splitting in cockles and aper­ NOTE: tural breakage in whelks) regardless of prey ••, P < 0.05; ••, P < 0.01; •••, P < 0.001. size. 396 PACIFIC SCIENCE, Volume 44, October 1990

DISCUSSION species that is also a predator of bivalve and gastropod molluscs. It possesses large third The morphology of the feeding apparatus maxillipeds bearing a well-developed crista of male and female C. novaezelandiae is de­ dentata and large, rounded mandibles. These signed to handle a diverse array offood types. mouthparts enable the gripping and tearing of This is supported by foregut analysis showing large food fragments. In contrast, L. varie­ a predominance of sessile and slow-moving gatus feeds predominantly on algal material, benthic macroinvertebrates and in the labora­ using its chelipeds to pluck and scrape algae tory a wide repertoire of opening techniques off rocks and stones. The third maxillipeds are that successfully open molluscs of differing reduced in size, with a reduced crista dentata size and geometric shape. composed of 3-4 blunt teeth . The mandibles The structure of the mouthparts of C. show a distinct angular process that may act novaezelandiae is typical of that of a number to cut plant material. The mandibles of E. of cancrid and portunid crabs. The third tuberosa are similar to those of O. truncatus, maxillipeds and mandibles are large and are but the third maxillipeds are more reduced the principal means offood maceration before and lack crista dentata (Schembri 1982). ingestion. The presence of a strongly devel­ These mouthparts are well suited to feed on oped crista dentata on the third maxillipeds, small soft-bodied and detritus that together with the development of large, characterize the diet of E. tuberosa. incisor-edged mandibles, appears to be a com­ The morphology of the gastric mill of C. mon feature among predatory brachyurans novaezelandiae reflects a carnivorous diet. The associated with a large, particulate macro­ strongly developed urocardiac and zygocar­ phagous diet. They are present in diac ossicles and lack of pointed teeth are maenas L. (Borradaile 1922), Ovalipes guadul­ similar to features found also in Callinectes pensis Saussure (Caine 1974), and Scylla sapidus Rathbun, where the foregut is well serrata Forskal (Williams 1978). In C. equipped to handle a variety of coarse hard novaezelandiae the crista dentata is adapted and soft material (Warner 1977). In C. novae­ both to crush small fragments of shell and to zelandiae setation within the gastric mill was function as a clamp facilitating the tearing of restricted to small brushes directly posterior flesh away from shell fragments. The incisor­ to the urocardiac ossicle. This is consistent edged mandibles are also designed to crush with the findings of Scharfer (1970), who sug­ and tear shell and flesh before shunting food gested that the degree of setation increased as to the foregut. All surfaces ofthe mouthparts diet moved from coarse particular matter were particularly setose, and along the medial toward more finer aqueous material. margins large, stout bristles were present. The size and structure of the chelipeds, to­ Setation may serve to hold or bind food to gether with their mechanical properties, deter­ the surfaces ofthe mouthparts during feeding mine the type and size of prey that can be (Warner 1977), and setae have a chemosen­ successfully exploited. C. novaezelandiae is sory function in assisting the "tasting" and homeochelous and therefore is typical of sorting of food fragments before digestion. other cancrid crabs; the two chelipeds are Few previous studies have investigated the morphologically similar in size and shape. relationship between functional morphology Although growth of the chela in male and of the feeding apparatus and diet of brachy­ female crabs was similar, for male crabs urans. However, differences in third maxil­ greater than 110.0 mm carapace width, a liped and mandible morphology in Ozius small increase in chela growth was apparent. truncatus Milne Edwards, Leptograpsus Such increased relative growth of chela for variegatus Fabricus, and Ebalia tuberosa large crabs (well above the size ofpuberty) has Pennant have been attributed to their differ­ not been reported previously for other bra­ ing activities during feeding (Schembri 1982, chyuran species (Hartnoll 1982). However, Skilleter and Anderson 1986). Cancer novae­ because this increase was not found in female zelandiae is most similar to o. truncatus, a crabs it is assumed that it is not associated Morphology of Cancer Feeding Apparatus-CRESWELL AND MARSDEN 397 with feeding, but rather with courtship and species, with bivalve and gastropod molluscs, mating behaviors. followed by amphipods, isopods, and bra­ The predominance of heterochely in mol­ chyurans dominating the diet. Studies by luscivorous brachyurans is attributed to poly­ Feder and Paul (1980) showed that Alaskan functionism (Brown et al. 1979, Du Preez , Cancer magister Dana, 1984): with each cheliped performing different fed primarily on small bivalves (48% of roles during . For example, the left stomachs), with crustaceans occurring in 30% chela of portunids is for holding and cutting of stomachs. Similarly , Northern while the right chela is used to crush prey. C. magister fed primarily on (56.1%) However, in homeochelous crabs such as C. and amphipods/isopods (23.6%) (Gotshall novaezelandiae, the chelae are large and 1977). Other prey items included hydroids, robust, and when closed they exhibit a per­ polychaetes, cephalopods, echinoderms, and manent diastema. Such morphological fea­ fish found as minor dietary components. tures enable the delivery ofa strong compres­ Differences in dietary composition with sive force along the entire length of the crab sex have been demonstrated in some por­ cheliped, and tubular and spherical objects (a tunid crabs (Ropes 1968, Elner 1980). Cho y characteristic of molluscs) can be held within (1986) showed that for male Liocarcinus the diastema. Although the chelae of C. puber L. molluscs formed a greater proportion novaezelandiae lack specific adaptations for ofthe diet than in female crabs and concluded cutting prey, polyfunctionism is exhibited by that this difference reflected cheliped strength, both chela, with no particular handedness with male crabs possessing larger, stronger being obvious. chelae than females . Because no morpho­ It has been suggested that mechanical ad­ logical differences were found in the feeding vantage reflects chelae function (Vermeij apparatus of male and female C. novaezelan­ 1976, Warner and Jones 1976). Brachyuran diae, it is not surprising that diet of male and species that exhibit heterochely possess dif­ female crabs was similar. Stevens et al. (1982) ferent chelal mechanical properties respective also found a lack ofvariation in diet with sex to their crushing, cutting, and holding roles. ofcrab for C. magister. Homeochelous brachyurans, on the other Differences in dietary composition with hand, show similar mechanical properties for crab size have been reported previously both chelae. Previous studies have found that (Gotshall 1977, Feder and Paul 1980, Stevens the cheliped mechanical advantage ofcancrid et al. 1982). Estuarine C. magister underwent crabs ranges between 0.31 and 0.40 (Vermeij distinct ontogenetic changes in food prefer­ 1976). For L., the mean value ences with age (Stevens et al. 1982), a feature of 0.32 ± 0.0 I is capable of exerting a mean also reported by Gotshall (1977) for the same maximum force of 496 kN· m- 2 that can species. This switching is believed to be a be maintained over a long period of time direct result of changed mechanical advan­ (Warner and Jones 1976). The large, robust tages of the chela with body size. It has been chelae of C. novaezelandiae are morpho­ postulated that ontogenetic change may de­ logically similar to those of C. pagurus. crease competition for food between age However, because the New Zealand species classes that occupy the same territory (Pyke et has a higher mechanical advantage (0.37 and al. 1977). In the present study no change in 0.38 for left and right chelae, respectively) , it diet was found for C. novaezelandiae between is probably capable ofexerting a greater com­ 40.0 and 135 mm carapace width. The diet of pressive force. This adaptation is important three size classes of postmetamorphic benthic for predation on sedentary prey such as crabs consisted ofthe same food types in rela­ molluscs, which require considerable strength tively similar proportions. for crushing rather than great speed for Laboratory experiments demonstrated that catching. C. novaezelandiae readily accepted and con­ The dietary composition of C. novaeze­ sumed a variety ofmollusc species. After prey landiae was similar to that of other cane rid capture, shells were usually manipulated ex- 398 PACIFIC SCIENCE, Volume 44, October 1990 tensively, with physical contact being the most may reflect stereotyped crab behavior pat­ likely mechanism used to recognize prey terns and prey size, rather than cheliped species and assess the feasibility of success­ morphology. fully opening the shell. Few studies have demonstrated the influ­ Once accepted, a large repertoire of open­ ence of prey shell morphology on opening ing techniques was demonstrated by C. novae­ techniques. Gastropods were more resistant zelandiae to open bivalve and gastropod shells to predation by C. novaezelandiae than bi­ in the laboratory. The success ofthe methods valves. The conical shape of gastropods re­ used appeared dependent upon prey size and stricts the regions available for shell attack species and crab size. Similar techniques for and penetration to only two planes . In con­ opening bivalves and gastropods have been trast, bivalves exhibit three planes for crush­ reported for a number of brachyurans, par­ ing, providing more scope for developing ticularly portunids feeding on similar prey different opening techniques. Similar findings species. Ovalipes catharus White, when pre­ were shown for C. pagurus, L. puber, and O. sented with individual M. edulis aoteanus, was truncatus when presented with bivalve and shown to exhibit five opening techniques gastropod prey species (ap Rheinallt and and generally utilized a characteristic attack Hughes 1985, Lawton and Hughes 1985, sequence (Davidson 1986). Moreover, tech- : Chilton and Bull 1986). niques employed were dependent on prey size, Cancer novaezelandiae, from its dietary com­ with small mussels being crushed directly position, feeding apparatus morphology, and while larger mussels were opened by splitting predatory behavior, seems specialized for op­ of the umbone and chipping of the posterior portunistic feeding on molluscs . Together, edge. Similar results were also observed by the mouthparts, chelae, and gastric mill func­ Wear (1984) for O. catharus. Carcinus maenas tion effectively to crush and ingest molluscan used five distinct methods to attack mussels prey items. This allows C. novaezelandiae to and three methods to attack dogwhelks, inhabit areas such as rocky shores, estuaries, Nucella lapillus L. (Cunningham and Hughes and harbors, which are characteristically 1984). The five methods used by O. catharus dominated by molluscs (Knight 1971 , Knox and C. maenas are also those observed for C. 1983). It may also explain the observed daily novaezelandiae when presented with identical intertidal migrations of this crab into rock y prey species of a similar size. habitats (T. Chadderton, pers. comm.) where Crab size was also an important factor in it is likely to find a wide size range of many determining the success of a particular open­ different prey species. ing technique for both bivalves and gastro­ pods. Larger C. novaezelandiae were capable of exerting stronger forces and could crush ACKNOWLEDGMENTS larger prey than small crabs. Large crabs used more time-consuming techniques (i.e., pos­ We thank Colin McLay for his interest in terior chipping) only to attack larger, more this project and help in identifying stomach robust prey. contents and Allen Rodrigo, who assisted The similarity in opening techniques ob­ with statistical packages. We would like to served between portunids and C. novaeze­ thank the Zoology Department for providing landiae in the present study is an interesting facilities and technical assistance. feature with respect to hetero- and homeo­ chely morphology and function. Similar methods were used by portunids and C. LITERATURE CITED novaezelandiae to open bivalves and gastro­ pods, suggesting that opening techniques for AP RHEINALLT, T. , and R. N. HUGHES. 1985. molluscs are general features among large, Handling methods used by the velvet swim­ predatory crabs. Such opening techniques ming crab Liocarcinus puber when feeding Morphology of Cancer Feeding Apparatus-CRESWELL AND MARSDEN 399

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capod crustacea: Cyclograpsus punctatus, WARNER, G. F. 1977. The biology of crabs. Diogenes brevirostris, and Upogebia afri­ Elek Science, London. 202 p. cana. Zoologia Afr. 5: 309-326. WARNER, G. F. , and A. R. JONES. 1976. Lever­ SCHEMBRI, P. J. 1982.The functional morpho­ age and muscle type in crab chelae. J. Zool. logy ofthe feeding and grooming apparatus 180:57-68. ofEbalia tuberosa (Crustacea: Leucosidae). WEAR, R . G. 1984. Paddle crabs are probable J. Nat. Hist. 16:467-480. predators. Catch 11 : 11 -13. SKILLETER, G. A. and D. T. ANDERSON. 1986. WEAR, R . G., and M. HADDON. 1987. Natural Functional morphology of the chelipeds, diet of the crab Ovalipes catharus around mouthparts and gastric mill of Ozius trun­ central and northern New Zealand. Mar. catus and Leptograpsus variegatus. Aust. J. Ecol. Prog. Ser. 35:39-49. Mar. Freshwater Res. 37:67- 80. WILLIAMS, M . J. 1978. Opening of bivalve STEVENS, B. G., D. A. ARMSTRONG, and R. shells by the mud crab Scylla serrata. Aust. CUSIMANO. 1982. Feeding habits of the J. Mar. Freshwater Res. 29:699-702. Dungeness crab Cancer magister as deter­ ---. 1981. Methods for analysis ofnatural mined by the index of relative importance. diet in Portunid crabs. J. Exp. Mar. BioI. Mar. BioI. 72: 135-145. Ecol. 52: 103-113. VERMEIl, G. J. 1976. Patterns in crab claw size: the geography of crushing. Syst. Zool. 26: 138-151.