Development and Metamorphosis of the Feeding Apparatus of the Stone Crab, Menippe Mercenaria (Brachyura, Xanthidae)

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JOURNAL OF MORPHOLOGY 172:299-312 (1982)

Development and Metamorphosis of the Feeding Apparatus of the Stone Crab, Menippe mercenaria (Brachyura, Xanthidae)

JAN ROBERT FACTOR Smithsonian Institution, Ft. Pierce Bureau, Ft. Pierce, Florida

ABSTRACT Analysis of the feeding apparatus of the stone crab, Menippe mercenaria (Brachyura, Xanthidae), has demonstrated that substantial internal and external morphological alterations occur at metamorphosis and suggests that the mastication of food shifts from the mandibles to the gastric mill at that time. These changes correspond to the changes in environment and diet that take place at metamorphosis, when the previously planktotrophic larvae begin benthic life. A detailed account of the structure and development of the mandibles is presented. The mandibles of all zoeal stages are similar: The incisor process has a series of teeth and denticles and the prominent molar process appears to be well adapted for grinding food. Megalopal mandibles are transitional but have the form that is typical of all subsequent stages: The expanded incisor process is rounded and toothless and the molar process is less prominent and has lost its grinding denticles. The cardiac stomach of the zoeal stages has no gastric mill; the medial and lateral teeth of the mill first appear in the megalopa. A very simple procedure is described for preparing larval mandibles for scanning electron microscopy using the molted exoskeletons from larval rearing experiments.

Development, settlement, and metamorpho- The paucity of functional studies on larval sis of the larvae of many marine invertebrate appendages and internal development is in groups have received considerable attention in contrast to the considerable literature concern- recent years (Chia and Rice, '78). The crusta- ing the functional morphology of appendages ceans are no exception. Most of the work on the and organ systems in adult decapods. Such larval development of decapod crustaceans, studies include several in which the authors however, has been concerned with the descrip- examined both the mouthparts and the gut tion of external features both to facilitate iden- and related their structure to feeding or diet. tification of larvae collected from the plankton For example, Patwardhan ('35b) compared the and to answer taxonomic questions (Rice, '80). gastric mill and mandibles of a variety of Functional considerations of external features decapods; Caine (75) studied feeding in the are usually lacking, and the development of commensal crab, Pinnotheres maculatus; internal features of decapod larvae has been Barker and Gibson ('77, 78) examined the feed- almost completely ignored. Studies that con- ing mechanism and structure of the gut in the sider the development of the digestive system lobster, Homarus gammarus, and the portunid of larval decapods appear to be limited to the crab, Scylla serrata; Coombs and Allen (78) de- work of Thompson ('03), who included the gut scribed the feeding structures of the shrimp, in his description of metamorphosis in a hermit Hippolyte varians; and Kunze and Anderson crab; Williams ('07), who described the ossicles (79) compared the mouthparts and gastric mill of the foregut of the lobster, Homarus ameri- in several species of hermit crabs. canus; LeRoux C71a,b), who studied the larval The life history of the stone crab, Menippe and juvenile foregut in the shrimp, Palae- mercenaria, typically includes five zoeal monetes varians; Regnault ('72), who examined stages, a megalopa, and a series of juvenile the larval development of the stomach of the shrimp, Crangon septemspinosa; and Factor ('8la), who described the development and metamorphosis of the digestive system of J.R. Factor's present address: Cornell University. Genetics and Homarus americanus. Development. Bradfield Hall. Ithaca. NY 14883.

0362-2525/82/1723-0299S04.00 1982 ALAN R. LISS. INC. 300 J.R. FACTOR stages leading to the adult. The larval devel- Zoeal and megalopal mandibles were pre- opment of external structures in this species pared for scanning electron microscopy from has been reported by Hyman ('25) and Porter the molted exoskeletons (exuviae) collected ('60). The present study examines the principal during larval rearing using the following sim- masticatory structures of the feeding appara- ple procedure. tus—the mandibles and the gastric mill —and Exuviae were preserved and stored in 70% follows their development from the first larval ethanol. Deposition of debris on the specimen stage, through metamorphosis, to the adult. was minimized by removing all seawater be- Metamorphosis from the last zoeal stage to the fore adding alcohol, thereby preventing precip- megalopa is accompanied by a variety of exter- itation of salts. Cleaning exoskeletons by soni- nal changes, including the loss of the carapace cation, even for a few seconds, caused them to spines, a change in the general shape and break apart and was not feasible. proportions of the cephalothorax, and the Specimens were mounted on a round glass transfer of the swimming function from the coverslip with a diameter equal to or less than thoracic maxillipeds to the newly developed that of the stub for the microscope being used. abdominal pleopods. Metamorphosis also The exoskeleton was transferred to the cover- marks the transition of the planktotrophic slip in a drop of alcohol, fine needles or forceps larvae to the benthic environment. This were used to tease the mandibles apart from change in habitat and diet is accompanied by the rest of the exoskeleton, and the prepara- substantial internal and external morphologi- tion was simply allowed to air-dry. Special dry- cal alterations in the masticatory apparatus. ing procedures, such as critical-point-drying or The nature of these structural changes and freeze-drying, were not necessary; the thick their functional significance for the developing cuticle of the mandible prevented its collapse. stone crab are the subject of this investigation. (Some problem was encountered with thin- walled first-stage mandibles, however, which MATERIALS AND METHODS did tend to collapse. This was avoided by critical-point drying entire first-stage larvae and The adult stone crabs used in this study were dissecting them to reveal details of the mandi- trapped in the Indian River coastal lagoon near bles.) The coverslip was mounted on a stub with the Smithsonian Institution's laboratory in Ft. a conductive colloidal graphite adhesive (Elec- Pierce, Florida. Juvenile stone crabs were col- trodag 191, Acheson Colloids Co.). The cover- lected from the oyster bars in the Indian River slip was lowered carefully to minimize trapped and from the sabellariid worm reefs along the air bubbles, which can cause it to pop off the adjacent coast. stub in the vacuum of the microscope. Three or All larvae were hatched from a single four small drops of the colloid were added ovigerous female, which was subsequently around the periphery of the coverslip to in- deposited in the Indian River Coastal Zone crease the conductance of electrons to the stub. Museum (IRCZM 89:4703). Larvae were raised After the adhesive was thoroughly dried, spec- at 20-21 °C in compartmented plastic trays in imens were sputter-coated with about 400 A seawater of 35-36%0 salinity by techniques of gold/palladium in a Technics Hummer previously described by Gore (73). At least Coater and observed in a Novascan scanning three specimens in each stage were examined. electron microscope. Charging was reduced by Larval stone crabs were fixed for light insuring that the mandible had good contact microscopy in 3% glutaraldehyde in 0.1 M with the coverslip, by increasing the thickness sodium cacodylate buffer at pH 7.0, postfixed of the coating (double- or triple-coating), or by in 1% Os04 in buffer, and embedded in a mix- operating the microscope at a low accelerating ture of Epon 812-Araldite 506, according to a voltage (5 kV or lower). Coverslips with speci- procedure used for transmission electron mens were removed from the stubs and stored microscopy (Factor, '81b). Plastic sections 1 /on in small petri dishes or micropaleontological thick were stained with toluidine blue-azure II slides. If further examination was necessary, and observed with a compound microscope. they were remounted and recoated. Juvenile stone crabs were fixed in seawater Because air-drying will cause distortion of Bouin's fluid (Humason, '62) and embedded in most structures, this technique is not suitable Paraplast (60-61 °C melting point). Serial for preparing entire larvae or for examining ap- paraffin sections 10 ^m thick were stained with pendages other than mandibles. Entire larvae hematoxylin and eosin or Mallory's triple stain and dissected material were fixed in 70% etha- (Humason, '62). nol, dehydrated in an ethanol series, treated METAMORPHOSIS IN THE STONE CRAB 301 with acetone, and critical-point-dried with C02 Position and structure of zoeal mandibles to replace the acetone. Juvenile and adult man- The mandibles are the most massive and dibles were dissected from entire specimens, obvious of the feeding appendages in zoeal sonicated to remove debris, and air-dried. stone crabs (Figs. 1,2). Removal of the more posterior appendages makes it possible to view OBSERVATIONS the mandibles from a posterior aspect and to appreciate their relationship to the cephalothorax of the larva (Fig. 3). The feeding apparatus of the adult stone The line drawings in Figure 4 illustrate three crab consists of the external mouthparts and views of a generalized zoeal mandible. The the internal gastric mill. The mouthparts are medial portion of the mandible which comes paired appendages that are specially modified into contact with food is called the gnathal lobe to handle food. The three anterior pairs of (GL) and consists of a ventral incisor process mouthparts (mandibles, maxillules, and maxil- (IP) and a dorsal molar process (MP). The lae) are cephalic in origin, and the three poster- incisor process bears a series of teeth along its ior pairs (first, second, and third maxillipeds) ventral edge; there are three major ventral are thoracic appendages. teeth (VT), one at each corner and one in the The zoeal maxillipeds are primarily loco- middle, with lesser ventral denticles (VD) inter- motory appendages with exopodites well spersed between adjacent teeth. There is also a equipped for this purpose with natatory setae. row of posterior teeth (PT) along the posterior During the zoeal stages the mandibles appear edge of the incisor process. The medial surface to be the primary masticatory structures, of the incisor is concave and, when considered whereas the maxillules and maxillae function together with the molar process, gives the more as manipulative mouthparts. At meta- gnathal lobe a spoon-shaped appearance. The morphosis to the megalopa, the function of molar process protrudes from the dorsomedial locomotion is transferred from the maxillipeds portion of the mandible at the base of the to the newly developed abdominal pleopods incisor process; the truncate distal surface and to a lesser extent to the thoracic pereio- bears several molar denticles (MD) and the pos- pods. The postmetamorphic maxillipeds may terior side has a single large molar tooth (MT) guide food into the mouth and, together with directed distally. The lateral lobe (LL) of the the mandibles and other mouthparts, prepare mandible is a rounded, broadly sloping struc- food for ingestion. They are not, however, ture that provides support for the gnathal lobe important masticatory structures. and is the site of muscle attachment and the The digestive system of the stone crab is points of articulation between the mandible divided into foregut, midgut, and hindgut. The and the cephalothorax. foregut, comprising the esophagus and the cardiac and pyloric stomachs, is lined with a layer of cuticle. In the cardiac stomach of the adult, this internal cuticle is organized into a series of Abbreviations plates or ossicles, some of which are elaborated and calcified to form the elements of the inter- A, anterior nal masticatory mechanism called the gastric ALT. accessory lateral tooth of gastric mill D, dorsal mill. (Maynard and Dando, '74, and Meiss and DCS, dorsal wall of cardiac stomach Norman, '77a,b, provide detailed descriptions GF. gland filter of pyloric stomach of the gastric mill in two brachyuran crabs.) GL. gnathal lobe of mandible Although the gastric mill is complex and con- IP, incisor process of mandible sists of many ossicles, muscles, and nerves, L,lateral LL, lateral lobe of mandible there are three primary masticatory struc- LT. lateral tooth of gastric mJU tures—the medial tooth, formed by the urocar- M, medial diac and prepyloric ossicles, and the two lateral MAP, mandibular palp MD. molar denticles teeth, formed by the zygocardiac ossicles. MET, medial tooth of gastric mill In the sections that follow, an account is pro- MP, molar process of mandible vided of the structure of zoeal mandibles and MT, molar tooth the developmental changes by which they are P, posterior PT, posterior teeth of incisor process transformed into the mandibles of the adult, as V, ventral well as the corresponding changes in the major VD, ventral denticles of incisor process features of the gastric mill. VT, ventral teeth of incisor process 302 JR. FACTOR

Fig. 1. First zoeal stage of the stone crab. Lateral view appendages. Anterior is to the top. Scale bar. 100 fim. illustrating position of the prominent mandible (arrow). Scale bar, 100 pm. Fig. 3. Posterior view of a pair of fith-stage mandibles, illustrating posterior teeth and complementary molar pro- Fig. 2. Ventral view of the first zoeal stage, indicating cesses with interdigitating molar teeth (arrows). Ventral is position of the mandibles (asterisks) in relation to other to the top. Scale bar. 50 pm.

Zoeal development it protrudes from the posteroventral corner of The mandibles of the first zoeal stage (Fig. 5) the molar process on the left mandible, but is have all of the elements of the generalized zoeal somewhat offset on the right mandible and is mandible described above. There are three ven- located away from the truncate end of the tral teeth on the incisor process and usually molar process. two ventral denticles between adjacent teeth, Several changes occur in the mandibles as although the number of denticles may vary the stone crab passes through the zoeal stages from one individual to the next. The incisor (Figs. 6-10). In addition to a general increase in process generally has two or three posterior size, there is also an increase in the number of teeth on the right mandible but the left mandi- posterior teeth and ventral denticles (Table 1). ble may have only a single tooth or none in this Although there is some variation among indi- position. The molar process is as wide as the viduals, the right mandible of the third stage incisor process and has several molar denticles generally has two or three posterior teeth (Fig. on its distal surface. The position of the single 6), whereas the left mandible has two, and by molar tooth differs on right and left mandibles; the fifth stage there may be four or five poste- METAMORPHOSIS IN THE STONE CRAB 303

GL 1

-VT

MD © ©

Fig. 4. Line drawings of a generalized zoeal mandible, illustrating important structural features. Posterior (4a) and posteromedial (4b) views of the entire mandible and a medial view of the gnathal lobe 14c) are shown.

rior teeth on the right mandible and two or Asymmetry of zoeal mandibles three on the left (Figs. 9-10). The number of The right mandible differs significantly from denticles usually increases to six on the poste- the left mandible in all zoeal stages. The larger rior half of the ventral edge and three on the number of posterior teeth on the right incisor anterior half in the third stage, and finally to process has already been noted. The more six and four by the fifth stage. There were interesting differences, however, occur on the three ventral teeth on the incisor process in all molar process. Examination of right and left zoeal mandibles examined. Comparison of the molar processes shows that the truncate distal first-stage mandible in Figure 5 with the fifth- surfaces are complementary. The curved ridge stage mandible in Figure 8 demonstrates that that forms the posteroventral edge of the right the incisor process is gradually extended dur- molar fits into a depression on the left molar, ing the zoeal stages, creating an increasingly and the molar denticles interdigitate (Figs. concave medial surface. The form of the entire 9,10). The asymmetrical placement of the zoeal mandible, including both lateral and single molar tooth on each mandible also gnathal lobes, is illustrated in Figure 7. The allows interdigitation of the molar process mandibular palp first appears as a rudimen- (Fig. 3). During feeding, the mandibles pivot on tary palp bud in the fifth stage, located on the two points of articulation, causing a rocking anterior side of the mandible (Figs. 9,10). motion that brings the molar processes 304 JR. FACTOR

Figs. 5-10. Scanning electron micrographs ofzoeal man- Fig. 8. Fifth-stage zoea. Gnathal lobe of right mandible dibles of the stone crab. Scale bars. 20 pm. with concave medial surface and grinding molar process. Fig. 5. First-stage zoea. Gnathal lobe of right mandible with prominent molar process. Figs. 9,10. Fifth-stage zoea. Anterior views of left (Fig. Fig. 6. Third-stage zoea. Medial view of right gnathal 9) and right (Fig. 10) gnathal lobes illustrating asymmetry lobe. of the mandibles. Complementary surfaces of the molar processes are visible: ridge on right molar process (arrowhead in Fig. 7. Fourth-stage zoea. Posterior view of entire right Fig. 10) fits into depression in left molar process (arrowhead mandible, illustrating gnathal and lateral lobes as well as in Fig. 91; molar teeth and molar denticles interdigitate. molar and incisor processes. Asterisk notes position of mandibular palp bud. METAMORPHOSIS IN THE STONE CRAB 305

TABLE 1. Teeth and denticles of zoeal mandibles in Menippe mercenaria Ventral denticles Posterior teeth Ventral teeth (right & left) Stage Right Wt (right & left) Anterior Posterior First zoea 2-3 0-1 3 2 2 Third zoea 2-3 2 3 3 6 Fifth zoea 4-5 2-3 3 4 6

together; their complementary surfaces viewed end-on, the incisor process can be seen appear well adapted for grinding food. to have a sharp cutting edge (Fig. 15). Except for their increased size, adult mandi- •- bles appear to be identical to those of the Megalopal mandibles juvenile (Figs. 16, 17). The most drastic change during the develop- Asymmetry is greatly reduced in juvenile ment of the mandibles occurs at the molt from and adult mandibles. There is only a slight dif- the last zoeal stage to the megalopa (Figs. ference in shape between right and left mandi- 11,12). At this time the gnathal lobe becomes a bles and no obvious complementarity (com- relatively flattened structure that lies against pare Figs. 13 and 14). There is, however, some the ventral surface of the cephaJothorax and difference in the posterior corner of the mandi- covers the mouth. The two surfaces of the bles near the molar process. The left mandible gnathal lobe can be described as inner (or dor- has a slight inward lip in this position, which is sal, toward the mouth) and outer (or ventral, formed by the end of the molar process (Figs. away from the mouth). The inner surface of the 13,16) and appears to have developed from the gnathal lobe is concave. The incisor process is posterior tooth of the megalopal molar process expanded to form most of the gnathal lobe; the (Fig. 11). The right mandible has no such lip incisor process of the left mandible has a and the molar process is not located at the very rounded edge that no longer bears teeth or den- corner of the mandible (Figs. 12,14,17). ticles (Fig. 11), and the right incisor process is When the megalopal, juvenile, or adult man- similar but bears a single tooth-like projection dibles pivot during feeding, the rocking motion (Fig. 12). The molar process is less prominent brings together the sharp edges of the expand- and is a fraction of the width of the incisor pro- ed incisor processes. In addition, it appears cess-it is now a simple mound with two teeth that the lip at the posterior corner of the left and is located at the posterior side of the inner mandible overlaps the cutting edge of the right surface. The posterior tooth of the molar pro- mandible and serves to grasp food. The struc- cess forms the corner of the left mandible, but tures and action of the postmetamorphic man- the molar process of the right mandible is off- dibles seem effective in cutting and grasping set slightly from the corner. It is in the mega- food, but not grinding. lopal stage that the mandibular palp is first well developed (Fig. 11). It lies in the concavity Development of the gastric mill on the inner surface of the gnathal lobe and The cardiac stomach of the first zoeal stage is serves to push food toward the mouth. The palp has three segments, and the distal seg- a simple sac (Fig. 18a). Developmental trends throughout the zoeal stages include an increase ment is setose. in the size of the sac and the formation of several ridges and channels. As late as the fifth zoeal Juvenile and adult mandibles stage (Fig. 18b), the cardiac stomach remains The general form, proportions, and orienta- essentially similar to that of the first stage- tion of the juvenile mandibles (Figs. 13, 14) are there are no obvious elaborations of the wall of similar to those of the megalopal mandibles. the cardiac stomach during zoeal development. The trend of simplification of the molar pro- As with the mandibles, the most drastic cess, begun in the megalopa, continues; the change in the cardiac stomach occurs at the two teeth of the megalopal stage are lost and molt from the last zoeal stage to the megalopal the process is now a relatively flat, shelf-like stage. Elements of the gastric mill, particu- structure at the posterior side of the gnathal larly the medial and lateral teeth, are first pres- lobe. The single tooth-like projection on the ent in the megalopa (Fig. 18c). edge of the right incisor process in the mega- The juvenile stone crab has a well-developed lopal mandible is absent in the juvenile. When gastric mill that closely resembles that of the 306 JR. FACTOR METAMORPHOSIS IN THE STONE CRAB 307 adult (Figs. 18d, 19-23). The grinding surfaces has been presented and the various parts of the of the medial and lateral teeth are heavily cu- mandible have been assigned names. The de- ticularized (darkened areas, Fig. 18d) and pre- velopmental trend in the structure of the zoeal sumably calcified. The medial tooth protrudes mandibles is one of an increase in size, an in- from the dorsal wall of the cardiac stomach, crease in the number of teeth and denticles on and lateral teeth and accessory lateral teeth ex- the incisor process, and slight changes in tend toward the midline from the lateral walls shape and proportion, including increased con- (Figs. 19,20). During mastication, the medial cavity of the medial surface. Despite these tooth is moved ventrally and anteriorly at the changes, the mandibles of all five zoeal stages same time the lateral teeth are brought toward follow the same basic structural plan. The ven- the midline of the stomach. This action moves tral and posterior edges of the incisor process the sides of the medial tooth across the knobs bear teeth and the molar process is prominent, and comb-like projections on the lateral teeth about as wide as the incisor process, and has (Figs. 21-23). In this way food trapped among complementary surfaces that are well adapted the medial and lateral teeth is ground into for grinding. Although the megalopa! mandi- small particles in the gastric mill. The particles bles are transitional, they have already at- are then sorted on the basis of size, in both the tained the form and orientation that is typical cardiac stomach and the pyloric filter, and the of all subsequent stages. The expanded incisor smallest particles pass into the midgut gland process is rounded and toothless, and the for final digestion and absorption. molar process has lost its prominence as well The medial and lateral teeth of the adult gas- as its grinding denticles. The postmetamor- tric mill (Figs. 24,25), as well as the general phic mandibles appear to be better adapted for shape of the cardiac stomach, are similar to cutting and grasping than for grinding. those of the juvenile stone crab. Developmental changes in the cardiac stomach correspond to those in the mandibles. DISCUSSION The cardiac stomach of the zoeal stages has no A detailed account of the structure and gastric mill and is not capable of grinding food. development of the mandibles of the stone crab The medial and lateral teeth of the mill are first recognizable in the megalopa. This analysis of the feeding apparatus of the stone crab indicates that substantial morphological alterations occur at metamorphosis and Figs. 11-17. Postlarval mandibles of the stone crab. In suggests that the mastication of food shifts all views, anterior is to the top. from the mandibles to the gastric mill at that time. These changes correspond to the changes Fig. 11. Megalopa. Gnathal lobe of left mandible with in environment and diet that take place at well-developed mandibular palp, expanded incisor process, and molar process with two teeth (arrows). Inner (dorsal) metamorphosis, when the previously plankto- view. Scale bar, 50 pm. trophic larvae begin benthic life. Patwardhan C35b), in the final paper of his Fig. 12. Megalopa. Gnathal lobe of right mandible. Inner comparative series on the gastric mill in adult view. Incisor process has a single tooth-like projection and decapods, also briefly described the structure molar process has two teeth (arrowheads). Mandibular palp has been removed. Scale bar, 50 jim. of the mandibles. He concluded (p. 171), "The efficiency of the gastric mill is correlated with Fig. 13. Juvenile. Gnathal lobe of left mandible (From a the efficiency of the external masticatory stone crab of 15-mm carapace width). Inner view. White arrow indicates inward lip of posterior molar process (also apparatus, chiefly the mandibles, the mandi- visible in Fig. 16). Mandibular palp has been removed. Scale bles being simple in the forms in which the gas- bar. 100 /un. tric mill is complex and vice versa." Patward- han generalized that in the reptantious Fig. 14. Juvenile. Gnathal lobe of right mandible (from a stone crab of 15-mm carapace width. Inner view. Scale bar, Brachyura, Anomura, and Macrura, which 100 pm. have complex gastric mills (i.e., efficient internal mastication), the mandibles are relatively Fig. 15. Juvenile. Medial view of the sharp cutting edge simple and have greatly reduced molar pro- of the incisor process. Scale bar, 100 /nn. cesses without any masticatory function (i.e., Fig. 16. Adult. Left and right mandibles, in situ (from a inefficient external mastication). Conversely, stone crab of 70-rrun carapace width). Outer (ventral) view. in the natantious Caridea, Penaeidea, and Arrow indicates inward lip at posterior corner of left Stenopodidea, in which the gastric mill is gnathal lobe. Scale bar, 2.0 mm. absent or greatly reduced, the mandibles are Fig. 17. Adult. Gnathal lobe of right mandible. Inner relatively complex with well-developed molar view. Mandibular palp has been removed. Scale bar, 1.0 mm. processes. 308 J.R. FACTOR

JUVENILE

Fig. 18. Line drawings representing cross sections through the cardiac stomach of first-stage zoeal (18a), fifth-stage zoeal (18b). megalopal (18c), and juvenile (15-mm carapace width) (18d) stone crabs.

Because so few studies of internal development have been carried out, only Limited Figs. 19-25. Scanning electron micrographs illustrating structures of the juvenile and adult gastric mill. comparisons are possible between the trends in adult decapods noted by Patwardhan and the Fig. 19. Juvenile. Ventral view of a dissected foregut (from a stone crab of 15-mm carapace width) illustrating situation found in the larval stages. A compar- position and orientation of elements of the gastric mill. ison of the condition of the mandibles and gas- Esophagus and ventral wall of cardiac stomach have been tric mill in those decapods for which informa- removed. Anterior is to the left. Scale bar, 0.5 mm. tion about both larvae and adults is available is Fig. 20. Juvenile. Anterior view of gastric mill showing summarized in Table 2 and presented below. relationship of medial, lateral, and accessory lateral teeth. The condition of the mandibles and gastric Ventral is to the top. (Crack in left lateral tooth is an artifact mill in the adult stone crab is typical of Pat- of preparation.) Scale bar, 0.25 mm. wardhan's generalization about the Reptantia Fig. 21. Juvenile. Medial tooth of gastric mill. Arrows (simple mandibles, complex stomach). The sit- indicate denticles on each side of medial tooth. Ventral is to uation is reversed, however, in the zoeal stages the top. Scale bar. 100 ^m. METAMORPHOSIS IN THE STONE CRAB 309

Pig. 22. Juvenile. Details of denticles on sides of medial Fig. 24. Adult. Medial tooth of gastric mill. Scale bar, tooth (indicated by arrows in Fig. 21). Scale bar, 50 nm. 0.5 mm.

Fig. 25. Adult. Lateral tooth (left) of gastric mill. Fig. 23. Juvenile. Lateral tooth (left) of gastric mill, illus- Anterior is to the left. Scale bar, 1.0 mm. trating knobs and row of comb-like projections. Dorsal view with anterior to the left. Scale bar, 100 nm. 310 JR. FACTOR

TABLE 2. Comparison of masticatory apparatus in larval and postlarual decapods1 Larval Postlarval Mandibles Stomach Mandibles Stomach

Stone crab, Menippe mercenaria, complex simple simple complex (Brachyura; Xanthidae) Present study

Shrimp, Palaemonetes varians, complex simple complex simple (Natantia: Palaemonidae) Patwardhan C35a), LeRoux ('71a,b), Fincham (79)

Shrimp, Crangon septemspinosa, complex simple complex simple (Natantia: Crangonidae) Regnault ('72)

Hermit crab, Pagurus annulipes, complex simple simple complex (Anomura: Paguridae) Thompson ('03), Nyblade ('70)

Lobster, Homarus americanus, simple simple simple complex (Macrura: Nephropidae) Herrick ('11), Factor ('78, '81a)

Complex: Grinding molar process in mandibles: grinding gastric mill in stomach. Simple: Cutting/grasping mandibles (no grinding molar process): no grinding gastric mill.

(complex mandibles, simple stomach), which the gastric mill. The adult, as is typical of other display the condition reported for adult carideans, also lacks the gastric mill. Larval Natantia. mandibles in this species have both an incisor LeRoux (71a,b) showed that the caridean process bearing setae that may serve as filters shrimp Palaemonetes varians has a simple and a grinding molar process. The adult mandi- stomach that lacks a gastric mill in the larval ble loses the incisor process but retains a grind- and juvenile stages, and Patwardhan (*35a) ing molar process. Crangon septemspinosa, demonstrated the absence of the mill in the then, appears to have complex mandibles and adult. Information on the mandibles comes simple stomach in both larval and postlarval from Fincham (79), who described the larval stages, although the larval stomach is some- development of this species. From his draw- what more complex than that of Palaemonetes ings, the zoeal mandibles appear to have well- varians. developed molar and incisor processes. Unlike Thompson ('03) discussed the digestive sys- me galop al and juvenile stone crabs, however, tem, including the gastric mill, in his descrip- the first postlarval stage of Palaemonetes vari- tion of the metamorphosis of the anomuran ans clearly retains the well-developed molar hermit crab Eupagurus longicarpus (actually process. The adult mandible is similar to that Pagurus annulipes; Roberts 70). He asserts of the postlarva (Patwardhan, '35a). This that there is no dorsal tooth during the zoeal shrimp, then, has complex mandibles and sim- stages and that lateral teeth are "simple and ple stomach in both larval and postlarval project upward instead of horizontally." stages. The dramatic changes in the feeding Thompson continued (p. 162), "The stomach of apparatus that characterize metamorphosis in the glaucothoe [first postlarval stage, equiva- the stone crab do not occur in P. varians. lent to the megalopa] ... may be regarded as Regnault (72) studied the development of transitional in type, its more elongate form, the stomach and mandibles in another horizontal lateral teeth ..., and well developed caridean shrimp, Crangon septemspinosa. In lateral-valve ridges recalling the stomach of this species the foregut develops gradually the adult. There are indications of a dorsal through larval life and reaches its most com- tooth...." The sixth stage, or first juvenile plex form in the last larval stage, when it is stage, has a stomach "of adult type, but with lined by plates and setae and has a well-devel- the parts less specialized." oped region between the cardiac and pyloric From Thompson's description, the develop- portions. It does not appear, however, to have ment of the gastric mill of this hermit crab is the medial and lateral teeth characteristic of similar to that of the stone crab, except for the METAMORPHOSIS IN THE STONE CRAB 311 presence of lateral teeth during the zoeal Additional information on the internal devel- stages. Examination of Thompson's plates opment of decapods is needed before meaning- does not fully clarify this point but suggests ful generalizations can be made. Despite the that he might have mistaken the ridges of the limited information available, the comparison zoeal stomach for lateral teeth. In any event, it presented here may be useful in providing a seems reasonable to assume that even if lateral framework for future analysis. teeth are present in the zoeae, the gastric mill Details of larval development of decapod is not functional before the medial tooth first crustaceans are contained in the substantial appears in the glaucothoe. literature on this subject, which comprises The larval development of external features several hundreds of papers. Recent studies of Pagurus annulipes is described by Nyblade have demonstrated that this wealth of infor- (70). He clearly showed an abrupt change from mation, perhaps uniquely available for the the zoeal to the megalopal mandibles, although crustaceans among major invertebrate taxa, it is difficult to determine from his illustration can be analyzed to provide insight into matters whether the zoeal mandibles have a molar pro- of taxonomic and systematic importance. The cess. Roberts (70) showed the mandibles of a structure of appendages, including the mouth- closely related species to have well-developed parts, has proven to be of considerable impor- molar processes in the zoeal stages and mega- tance in such analyses (Rice, '80; Van Dover lopal mandibles that are similar to those of the et al., in press). In addition, phylogenetic impli- adult. Thompson ('03) also illustrated a similar cations have been reported for mandibular transition from the zoeal to the megalopal structure in adult crayfishes (Bouchard, 77) mandibles. On the basis of information col- and adults in several species of the genus lected from several sources, we can tentatively Daphnia (Edwards, '80). conclude that this hermit crab has complex Most papers on larval development include mandibles and simple stomach in the zoeal descriptions of the mandibles, as well as other stages, but that the converse is true of the appendages. The accompanying illustrations postmetamorphic stages (beginning with the are often (but by no means always) simple line megalopa or glaucothoe), just as in the stone drawings, which are adequate for illustrating crab. most of the appendages, but which give little A final comparison may be made with the or no indication of the complex, three-dimen- American lobster, Homarus americanus. The sional structure of the mandibles. Reasons for lobster has three larval stages; since there is no this include the difficulty of extracting infor- megalopa, the fourth stage can be considered mation on three-dimensional structure from the first postlarval or first juvenile stage. The mouthparts mounted on microscope slides and early larval stages of the lobster have no gas- viewed with a compound microscope, and the tric mill, and the full complement of medial, difficulty of preparing line drawings with a lateral, and accessory lateral teeth are first realistic sense of depth. Sometimes only a present in the fourth stage (Factor, '81a). single mandible is illustrated, despite their Development of the mandibles corresponds to tendency to be asymmetrical. Although scan- the development of the gastric mill; the com- ning electron microscopy is perfectly suited to paratively delicate teeth of the first-stage man- the task of accurately illustrating the mandi- dibles are transformed into the more massive, bles, almost none of the papers on larval devel- molar-like teeth of the fourth stage (Factor, opment include scanning electron micrographs 78). These teeth on the incisor process should (a notable exception is Greenwood and Fielder, not be confused, however, with a molar pro- 79). cess. There is no evidence of a grinding molar Studies of larval development generally in- process in either the larval or postlarval stages volve rearing specimens in the laboratory; of the lobster. The adult mandibles (Herrick, molted exoskeletons are routinely collected '11) are essentially similar to those of the and fixed in alcohol and provide the history of fourth stage. The larval lobster, then, is charac- each animal, stage by stage. It is hoped that terized by simple mandibles and simple the availability of the very simple preparative stomach, and the manner in which food is mas- procedure described in this paper will encour- ticated is not clear. Postlarval lobsters have age investigators to pay additional attention the simple mandibles and complex stomach to mandibular structure in future studies of typical of the Reptantia, and metamorphosis larval development in decapods. This would brings about the feeding apparatus necessary make available detailed, accurate descriptions to process the substantial food they encounter and illustrations of these important mouth- in the benthic environment. parts for a wide variety of decapod larvae and 312 JR. FACTOR

would enable future comparisons of larval Gore, R.H. (1973) Pachycheles monilifer (Dana, 1852): The development, whether for taxonomic or func- development in the laboratory of larvae from an Atlantic tional purposes, to include the mandibles. specimen with a discussion of some larval characters in the genus (Crustacea: Decapoda: Anomura). Biol. Bull. 744/132-150. Greenwood, J.G., and D.R. Fielder (1979) The zoeal stages ACKNOWLEDGMENTS and megalopa of PoHunus rubromarginatus (Lanchester) (Decapoda: Portunidae), reared in the laboratory. J, Thanks are extended to Dr. John M. Ander- Plankton Res. 7/191-205. son, Dr. Robert H. Gore, Dr. Mary E. Rice, Ms. Herrick, F.H. (1911) Natural history of the American lob- Liberta E. Scotto, and Ms. Cindy L. Van Dover ster. Bull. U.S. Bur. Fish. 29/149-408. Humason. G.L. (1962) Animal Tissue Techniques. San for reading the manuscript and offering valu- Francisco: W.H. Freeman and Company. able comments and suggestions. I am grateful Hyman, O.W. (1925) Studies on the larvae of crabs of the to Ms. Julianne Piraino for her able technical family Xanthidae. Proc. U.S. Natl. Mus. 67/1-22. assistance with the scanning electron micro- Kunze, J., and D.T. Anderson (1979) Functional morphology of the mouthparts and gastric mill in the hermit crabs scopy, and Ms. Liberta E. Scotto for her help in Clibanarius taeniatus (Milne Edwards), Ctibanarius collecting and identifying stone crabs. Support uirescens (Krauss), Paguristes squamosus McCulloch and was provided by a Smithsonian Postdoctoral Dardanus setifer (Milne Edwards) (Anomura: Paguridae). Fellowship during the completion of this Aust. J. Mar. Freshwater Res. JO/683-722. LeRoux. A,A. (1971a) Etude anatomiqueet fonctionnelledu study. Article No. 26, Studies on Decapod proventricule des larves et des juveniles du premier stade Crustacea from the Indian River Region of de Palaemonetes uarians (Leach) (Decapode, Natantia). 1. Florida. Donnees anatomiques. Bull. Soc. Zool. Fr. 96/127-140. LeRoux, A.A. (1971b) Etude anatomiqueet fonctionnelledu proventricule des larves et des juveniles du premier stade de Palaemonetes uarians (Leach) (Decapode. Natantia). 2. LITERATURE CITED Les phenomenes mecaniques de la digestion. Bull. Soc. Zool. Fr. 96/141-149. Barker, P.L., and R. Gibson (1977) Observations on the feed- Maynard, D.M., andM.R. Dando (1974) The structureof the ing mechanism, structure of the gut, and digestive physi- stomatogastric neuromuscular system in Callinectes ology of the European lobster Homarus gammarus (L.) sapidus, Homarus americanus and Panulirus argus (Decapoda: Nephropidae). J. Exp. Mar. Biol. Ecol. 26: (Decapoda Crustacea). Phil. Trans. R. Soc. Lond. 26873/ 297-324. 161-220. Barker. P.L., and R. Gibson (1978) Observations on the Meiss, D.E., and R.S. Norman (1977a) Comparative study of structure of the mouthparts, histology of the alimentary the stomatogastric system of several decapod Crustacea. tract, and digestive physiology of the mud crab Scytta ser- I. Skeleton. J. Morphol. 752/21-53. rata (Forskal) (Decapoda: Portunidae). J. Exp. Mar. Biol. Meiss, D.E., and R.S. Norman (1977b) Comparative study of Ecol. 32/177-196. the stomatogastric system of the decapod Crustacea. II. Bouchard, R.W. (19771 Morphology of the mandible in hol- Musculature. J. Morphol. 752/55-75. arctic crayfishes (Decapoda: Astacidae and Cambaridae): Nyblade, C.F. (1970) Larval development of Pagurus annu- Ecological and phylogenetic implications. In O.V. Lind- lipes (Stimpson, 1862) and Pagurus pollicaris Say, 1817 qvist led): Freshwater Crayfish. 3. Papers From The Third reared in the laboratory. Biol. Bull. 739/557-573. International Symposium On Freshwater Crayfish At Patwardhan, S.S. (1935a) On the structure and mechanism University Of Kuopio, Kuopio Finland, Aug. 5-8, 1976. of the gastric mill in Decapoda. V. The structure of the Kuopio: University of Kuopio, pp. 425-452. gastric mill in Natantous Macrura-Caridea. Proc. India Calne, E.A. (1975) Feeding of Pinnotheres maculalus Say Acad. Sci. 7.8.693-704. (Brachyura: Pinnotheridae). Forma Functio &395-404. Patwardhan, S.S. (1935b) On the structure and mechanism Chia, F.-S., and M.E. Rice (1978) Settlement and Metamor- of the gastric mill in Decapoda. VI. The structure of the phosis of Marine Invertebrate Larvae. New York: gastric mill in Natantous Macrura-Penaeideaand Steno- Elsevier. pidae; Conclusion. Proc. Indian Acad. Sci. 25/155-174. Coombs. E.F., and J.A. Allen (1978) The functional morphol- Porter, H. (i960) Zoeal stages of the stone crab, Menippe ogy of the feeding appendages and gut of Hippolyte van- mercenaria Say. Chesapeake Sci. 7/168-177. ans (Crustacea: Natantia). Zool. J. Linn. Soc. 64:261-282. Regnault, M. (1972) Developpement de I'estomac chez larves Edwards, C. (1980) The anatomy of Daphnia mandibles. de Crangon septemspinosa Say (Crustacea: Decapoda: Trans. Am. Microsc. Soc. 99.2-24. Crangonidae); son influence sur la mode de nutrition. Bull. Factor, JR. (1978) Morphology of the mouthparts of larval Mus. Hist. Nat. Paris 67/841-856. lobsters, Homarus americanus (Decapoda: Nephropidae), Rice, A.L. (1980) Crab zoeal morphology and its bearing on with special emphasis on their setae. Biol. Bull. 754/383- the classification of the Brachyura. Trans. Zool. Soc. 408. Lond. 35/271-424. Factor, JR. (1981a) Development and metamorphosis of the Roberts, M.H., Jr. (1970) Larval development of Pagurus digestive system of larval lobsters, Homarus americanus longicarpus Say reared in the laboratory. I. Description of (Decapoda: Nephropidae). J. Morphol. 769/225-242. larval instaj-s. Biol. Bull. 739/188-202. Factor, JR. (1981b) Unusually complex basement mem- Thompson, M.T. (1903) The metamorphoses of the hermit branes in the midgut of two decapod crustaceans, the crab. Proc. Boston Soc. Nat. Hist. 37/147-209. stone crab {Menlppe mercenaria) and the lobster Van Dover. C.L., JR. Factor, and R.H. Gore (1982, in press): {Homarus americanus). Anat. Rec. 200/253-258. Developmental patterns of larval scaphognathites: An Fincham, A. A. (1979) Larval development of British prawns aid to the classification of anomuran and brachuyran and shrimps (Crustacea: Decapoda: Natantia). 2. Palae- Crustacea. J. Crustacean Biol, 2 (1). monetes (Palaemonetes) uarians (Leach, 1814) and mor- Williams, L.W. (1907) The stomach of the lobster and the phological variation. Bull. Br. Mus. Nat. Hist. (Zool.) food of larval lobsters. Rep. R.I. Comm. Inl. Fish. 37: 55/127-200. 153-180.