The Larval Development of Calcinus tibicen (Herbst) (Crustacea, Anomura) in the Laboratory

The Larval Development of Calcinus tibicen (Herbst) (Crustacea, Anomura) in the LaboratoryAuthor(s): Anthony J. Provenzano, Jr.Source: Biological Bulletin, Vol. 123, No. 1 (Aug., 1962), pp. 179-202Published by: Marine Biological LaboratoryStable URL: http://www.jstor.org/stable/1539514 .

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THE LARVAL DEVELOPMENT OF CALCINUS TIBICEN (HERBST) (CRUSTACEA, ANOMURA) IN THE LABORATORY1

ANTHONY J. PROVENZANO, JR. Institute of Marine Science, University of Miami, Miami 49, Florida

Since the first studies on hermit crab development in the early 19th century, workers have had to rely on reconstructions of developmental sequences from planktonic material. In some instances it has been possible to maintain larvae taken from the plankton through one moult in the laboratory and thus to tie together series of larvae believed to represent single species. This was the method used by Thompson (1904) in his classic work on Pagurus development, and by more recent workers as well (MacDonald, Pike and Williamson, 1957; Pike and Williamson, 1960; Dechance, 1961). The reconstruction method may be used profitably only in waters with restricted faunas. Planktonic larvae from any but the most intensively studied areas can seldom be identified with certainty. In tropical waters which are generally less well studied and in which there are usually several times the number of species and genera found in temperate seas, the reconstruction technique is much less useful.

Although the tropical Western Atlantic contains the second richest pagurid fauna in the world (Wass, unpubl.; Provenzano, 1959, 1961a, 1961b) there is not a single species of the family Diogenidae in the West Indies for which the larval development is known. Excepting two species of Paguristes which have abbreviated development (Hart, 1937; Pike and Williamson, 1960) no hermit crabs of that family have previously been reared in the laboratory from the first zoea to the post-larval stage.

Fortunately, in recent years advances have been made in the development of techniques for rearing several decapod groups in the laboratory. Broad (1957a, 1957b) and Dobkin (in press) have been able to rear caridean shrimps. Costlow and Bookhout (1959, 1960a, 1960b, 1961a, 1961b), Knudsen (1958, 1959a, 1959b), Hart (1960) and Chamberlain (1961) have been successful with a variety of brachyuran crabs. Forss and Coffin (1960) pointed out the applicability of a method for rearing several decapod groups and Coffin (1960) was able to rear a species of the hermit crab family Paguridae. At this laboratory a terrestrial hermit crab of the family Coenobitidae has been successfully reared to metamorphosis (Provenzano, in press).

Until very recently there have been no descriptions of larvae of the tropical hermit crab genus Calcinus. According to Pike and Williamson (1960), the glaucothoe stage described and figured by Bouvier (1922) and attributed by him to Clibanarius may be the postlarva of Calcinus ornatus (Roux) of the Mediterranean. Bourdil- lon-Casanova (1960) described and figured a zoea taken from the plankton, which she believed to be the first stage of Calcinus ornatus. Pike and Williamson (1960)

1 Contribution no. 395 from the Marine Laboratory, University of Miami, Florida. This work was supported by National Institutes of Health grant no. RG-7166(A) and National Science Foundation grant no. G-16298, and the present paper constitutes a scientific report to those agencies.

179



ANTHONY J. PROVENZANO, JR.

were able to obtain the first zoea of C. ornatus from a laboratory hatching and by holding identical larvae from the plankton through one moult in the laboratory they were able to obtain the second stage. Similarly they obtained and described five zoeal stages and one glaucothoe stage for that species.

In the Western Atlantic only two species of Calcinus are known to occur (Pro- venzano, 1960). Lewis (1960) gave a very brief description and a figure for the first zoea of Calcinus tibicen (Herbst) but neither is sufficiently detailed for use in identification. No other reports on larvae of this genus are known. The present paper describes the larval development of Calcinus tibicen in the laboratory.

MATERIALS AND METHODS

Ovigerous females of Calcinus tibicen were collected at Bear Cut, Biscayne Bay, Florida. In the laboratory they were kept in large fingerbowls containing filtered sea water until hatching occurred. In the first experiment, conducted from 7 June 1960 to 3 August 1960, approximately 40 larvae were removed by means of a wide- bore pipette to plastic compartmented trays, five larvae to each compartment of about 50 cc. capacity. Every second day larvae were transferred to corresponding compartments in fresh trays containing filtered sea water and freshly hatched Artemia nauplii as food. Temperature of the standing sea water during this period gradually increased from 26.5? C. to 30.30 C. with diurnal fluctuations of about 1? C. Salinity samples taken at each change of water were titrated and values ranged from 31.1 ppt to 35.0 ppt. The second experiment ran from 17 April 1961 to 7 June 1961. Approximately 150 larvae were placed singly in individual compartments containing filtered sea water and freshly hatched Artemia. A number was assigned to each compartment and every second day larvae were transferred to correspondingly numbered compartments in freshly prepared trays. By daily examination of the trays for exuviae and for dead animals, and by preserving exuviae of each larva in an ap- propriately numbered vial it was possible to follow the complete history of each specimen. Temperatures ranged from 26.0? C. to 29.0? C. during the experiment. Salinity was semi-controlled by storage of filtered sea water in five-gallon carboys. Three lots of water were used during the development of these larvae, according to the following schedules: from 17 April to 12 May, salinity of 35.52 ppt during stages I-V; from 12 May to 22 May, salinity of 37.41 ppt during stages V, VI, some VII, and glaucothoe; and from 22 May to termination of the experiment, salinity was 37.07 ppt and affected stages VII, VIII, and some glaucothoes. No attempt was made to control illumination other than to prevent direct sunlight from falling onto the transparent boxes.

Larvae and exuviae were preserved in 5-7% sea water-formalin buffered with

hexamethylene tetramine or were rinsed in fresh water and stored in 70% ethyl alco- hol. After staining in Mallory's acid fuchsin red, specimens and exuviae were dis- sected in 85% lactic acid and appendages were mounted in Hoyer's medium. Draw-

ings of whole larvae were made from live, immobilized animals or from freshly killed

specimens. A stereoscopic dissecting microscope with magnifications up to 36 x was used for dissections and for making camera lucida drawings of whole animals. En-

largements of appendages and other parts were drawn using a camera lucida with a monocular microscope at 90 x and details were checked at 450 x.

180



LARVAL DEVELOPMENT OF CALCINUS

The descriptive portion of the text was based chiefly on specimens under the microscope at the time of description. Usually appendages of at least two or three, sometimes five or six, different animals were examined during preparation of the descriptions. Notes made on additional material were incorporated later.

Setae were drawn as they appeared with respect to number, position, and length but setules when present were illustrated semi-diagrammatically. In most illustrations of appendages the setules are shown as somewhat shorter and much less numerous than in the specimens.

Duration refers to the time range between moults for animals which successfully passed through a given stage. This "normal" duration was often exceeded by larvae which died without moulting to the subsequent stage and such data are not included in the values for duration.

Measurements were made with the aid of an ocular micrometer. Total length (TL) was measured from the tip of the rostrum to the posterior border of the telson, exclusive of all telson processes. Length of carapace (CL) was measured from the tip of the rostrum to the most posterior lateral margin of the carapace including the lateral spines. The numbering of telson processes follows the system of Pike and Williamson (1960) not MacDonald, Pike and Williamson (1957).

The females from which larvae were obtained are on deposit in the Marine Museum of the Institute of Marine Science, University of Miami.

This work was initiated during a pilot study supported by the National Institutes of Health, U. S. Public Health Service, and was completed with support of the National Science Foundation. I am indebted to both those agencies. I would like to thank Sheldon Dobkin and Dr. Gilbert L. Voss for criticisms of the manuscript.

RESULTS

The number of zoeal stages through which Calcinus tibicen may pass in the laboratory before moulting to the glaucothoe stage is variable. The glaucothoe was obtained after six, seven or eight zoeal instars. The principal features of each stage are as follows:

First Zoea. Figs. 1, I; 2, I. Size. TL 1.9 mm.; CL 1.3 mm. Duration. From five to eight days.

The carapace has a prominent carinate rostrum and there is a large corneous submarginal spine postero-laterally on each side of the carapace. The eyes are immobile. The fifth abdominal somite has a prominent very slightly curved medio- dorsal spine and a smaller lateral spine on each side of the same somite. There is a dorso-lateral pair of fine hairs on somites two, three and four which are not noticed on later stages. The sixth somite is fused to the telson (Fig. 3, I) which is broader than long, notched medially, and armed with seven processes on each side. The first or outermost process is apparently fused to the telson, but a line of demarcation

may be seen. The second process is a fine hair bearing setules. Processes three to seven are strong plumose spines articulated with the telson. There is a red pigment

181




!IV 1.0 mm ! IV

VI

FIGURE 1. Calcinus tibicen. Zoeal stages I-VI, dorsal view.

spot at about the mid-point of the antennule and diffuse orange-red pigment over the thorax, but under the carapace. In some specimens there is a diffuse bluish pigment on the telson.

The antennule (Fig. 4, I) terminates in at least one aesthete and four other

processes. There is a very prominent subterminal plumose seta. The antennal endopodite is fused to the basipodite and bears two long terminal

plumose setae and one subterminal seta less than one-half as long as the others (Fig. 5, I). A short, toothed spine is present on the ventral surface of the basipodite. The antennal scale is about three times longer than wide, slightly longer than the

endopodite, is concave on the lateral margin and bears a terminal tooth. Sub- terminally there is a short hair followed by nine, rarely eight, longer plumose setae.

The mandibles are dissimilar, simple toothed processes. The three-segmented endopodite of the maxillule (Fig. 6, I) has three terminal

setae with another distally on the second segment. The proximal endite of the basi-

podite has six setae of which four are branched, two simple. The distal endite terminates in two large spines and two non-plumose setae.

182




1.0 mm

FIGURE 2. Calcinus tibicen. Zoeal stages I-VI, lateral view.

The maxilla (Fig. 7, I) bears six or seven setae on the proximal lobe of the coxal endite, four on the distal lobe. There are four setae on both proximal and distal lobes on the basal endite. The bilobed unsegmented endopodite bears four setae, the scaphognathite five plumose setae.

The first maxilliped (Fig. 8, I) has a prominent curved seta upon a papilla

183




0.5mm r r~~~~~~~-

FIGURE 3. Clcins tbicen. The teson, zoea I-V FIGURE 3. Calcinus tibicen. The telson, zoea I-VI.

proximally on the medial margin of the basipodite, with about nine additional setae along the medial margin. The exopodite is composed of two indistinct segments and terminates in four long plumose setae. The endopodite is five-segmented, the terminal segment bearing four plumose setae apically with a fifth proximally. The

184




Iv

6 /

antennule, zoea I through glaucothoe.

185

I

FIGURE 4. Calcinus tibicen. The




11

E E In dj

v I VW

FIGURE 5. Calcinus tibicen. The antenna, zoea I through glaucothoe.

antepenultimate segment bears a single distal hair medially. The other segments bear a pair of setae medially. There is a row of very fine setules along the lateral margin of the endopodite.

The second maxilliped (Fig. 9, I) has only three setae on the medial margin of

186




I 11

0.5 mm 4

V

FIGURE 6. Calcinus tibicen. The maxillule, zoea I through glaucothoe.

the basipodite. The exopodite has four long plumose terminal setae. The endopodite is only four-segmented, the terminal segment having four apical setae and one seta subdistally. The other segments each have a pair of distal setae medially.

The third maxilliped (Fig. 10, I) is a uniramous rudiment.

Second Zoea. Figs. 1, II; 2, II. Size. TL 2.5-2.6 mm.; CL 1.5 mm. Duration. From three to five days.

Mobile eyes serve to distinguish the second zoea from the first. The dorsal spine of the fifth abdominal somite is still very prominent, much larger than the laterals. The sixth somite is still fused to the telson which bears an extra pair of processes medially (Fig. 3, II). The outermost process on each side of the telson is clearly not fused to the telson. In addition to the same red-orange coloration as noted for the previous stage, there is diffuse blue on the anterior carapace ventrally and a blue cast to the carapace dorsally, especially in the cardiac region.

The antennule (Fig. 4, II) has five or six terminal processes, at least one of which is an aesthete. There is a large plumose seta subterminally and a pair of small fine setae at about the same distance but on the opposite side.

The antenna (Fig. 5, II) is essentially unchanged in form and setation. There

187




I 11

E

'

FIGURE 7. Calcinus tibicen. The maxilla, zoea I through glaucothoe.

is a small tooth laterally on the basal portion in addition to the spine at the base of the endopodite.

The mandible is unchanged to any notable degree. The segmented endopodite of the maxillule (Fig. 6, II) is unchanged and the

coxal endite still has four feathered setae and three simple setae but the basal endite now has four large teeth and two setae.

The maxilla (Fig. 7, II) has seven setae upon the proximal lobe of the coxal endite and four setae on the distal lobe. Apparently there are five on the proximal lobe of the basal endite and four on the distal lobe. The endopodite has two proximal and three distal setae. The scaphognathite has six or seven short plumose setae. The first maxilliped (Fig. 8, II) has six plumose natatory setae on the exopodite. The endopodite still has five setae on the terminal segment and there are two distally

188




E E

I) 0

iV

? V I

FIGURE 8. Calcinus tibicen. The first maxilliped, zoea I through glaucothoe.

189

I?




0.5mm - .. ..

G

FIGURE 9. Calcinus tibicen. The second maxilliped, zoea I through glaucothoe.

190




t it II1

0.5 mm I

VI G

FIGURE 10. Calcinus tibicen. The third maxilliped, zoea I through glaucothoe.

on the medial side of the penultimate segment. The antepenultimate segment bears one seta medially and one laterally. The two proximal segments each bear one seta laterally and two medially. There are eight or nine setae along the medial margin of the basipodite in addition to the proximal hooked process.

The second maxilliped (Fig. 9, II) has six natatory setae on the exopodite. The four-segmented endopodite bears five setae on the terminal segment and on each of the two next proximal segments there are three setae, one of them laterally, two

medially. The most proximal segment has only two setae medially. There are three setae on the medial margin of the basipodite.

191




The third maxilliped (Fig. 10, II) is a jointed uniramous appendage with five plumose terminal setae.

Third Zoea. Figs. 1, III; 2, III. Size. TL 3.0 mm.; CL 1.7-1.8 mm. Duration. About five days, from approximately the 12th day after hatching to the

17th day. Aside from increase in size there is no major change in form of the cephalothorax.

The fifth abdominal somite still bears a prominent medio-dorsal spine and a pair of lateral spines. The sixth abdominal somite is no longer fused with the telson and bears a postero-medio-dorsal spine as well as unjointed uropods (Fig. 3, III). The exopodite of the uropod bears usually eight, sometimes seven, plumose setae and has two inconspicuous hairs situated medio-ventrally while the endopodite of the uropod is a simple unarmed bud. The telson is armed laterally with an unfused hairless tooth. The second process as in earlier stages is an inconspicuously plumose hair and medially to this third process is a feathered articulated spine. The fourth process has become a large unarmed fused spine. Processes five to nine are articulated plumose setae. The total count of telson processes is 9 + 9.

The antennule (Fig. 4, III) is segmented. The terminal segment bears two large and three fine processes while the basal peduncle bears three large plumose setae and two or three very small setules.

The antennal scale (Fig. 5, III) bears about 12 medial plumose setae. The articulated endopodite has a single terminal seta. The armed spine and the hooked tooth at the base of the endopodite and scale are still present.

The mandible has a few more very small teeth on the cutting edge. The maxillule (Fig. 6, III) is essentially unchanged. The maxilla (Fig. 7, III) appears unchanged except for the scaphognathite which

may have up to 11 plumose setae. The first maxilliped (Fig. 8, III) has six natatory setae on the exopodite. The

five-segmented endopodite has four terminal setae and one proximal seta on the ultimate segment. The penultimate segment bears a pair of setae medially. The antepenultimate segment bears one medial and one lateral, while the next two proximal segments each bear one seta laterally and one large and one small medially. There are three groups of about three setae on the medial margin of the basipodite and two setae near the proximal hooked process.

The second maxilliped (Fig. 9, III) also has six natatory setae on the exopodite. The four-segmented endopodite has on the distal segment four terminal setae and one proximal seta. The penultimate segment bears two setae medially, one laterally as does the antepenultimate segment, but the first segment bears only two medial setae. There are three or four setae on the medial margin of the basipodite.

The third maxilliped (Fig. 10, III) bears five or six natatory setae.

Fourth Zoea. Figs. 1, IV; 2, IV. Size. TL 3.8-4.2 mm.; CL 2.0-2.4 mm. Duration. Usually four or five days, rarely six.

The spines of the fifth abdominal somite have become relatively smaller, especially the lateral. The telson armature (Fig. 3, IV) may be similar to that of the preced-

192




ing stage but in six of seven specimens taken at random and examined, a very small medial articulated spine was also present. The most readily noted characteristic of this stage is the changed armature of the now articulated uropods. The exopodite of the uropod has a strong curved outer spine with nine or ten plumose setae along the inner margin of the uropod. The endopodite bears four or five plumose setae. The exopodite has two medio-ventrally placed very inconspicuous hairs; the endopodite has one.

The antennule (Fig. 4, IV) has its terminal segment ending in two large and four small sensory processes. At the distal end of the proximal segment there are four small setules and four large plumose setae.

The antenna (Fig. 5, IV) is basically unchanged but now there are 13-15 setae in addition to the terminal tooth on the antennal scale. The endopodite still terminates in a single seta.

The mandible shows no essential change. The maxillule (Fig. 6, IV) has on the coxal endite three or four curved plumose

setae and a similar number of simple setae. The basal endite has usually five but occasionally six strong teeth plus two setae. The endopodite is unchanged.

The maxilla (Fig. 7, IV) has from 9-12 plumose setae on the scaphognathite. The endopodite bears four large setae and one smaller. The proximal lobe of the coxal endite bears seven to eight setae; the distal lobe, four. The proximal lobe of the basal endite bears four; the distal lobe also four.

The first maxilliped (Fig. 8, IV) still bears a prominent curved seta at the proximal medial corner of the basipodite and distally there are two, three and two setae along that margin. The exopodite bears six natatory setae. The five-segmented endopodite has five setae on the terminal segment, a pair distally on the penultimate segment, and one laterally, one medially on the antepenultimate segment. There are two medial and one lateral setae distally on the next segment and again on the most proximal segment.

The second maxilliped (Fig. 9, IV) also bears six natatory setae on the exopodite. On the four-segmented endopodite there are five setae terminally, two medially and one laterally on both the penultimate and antepenultimate segments and only two medial setae on the proximal segment.

The third maxilliped (Fig. 10, IV) is a jointed uniramous appendage with sometimes four, more usually five or six natatory setae.

Fifth Zoea. Figs. 1, V; 2, V. Size. TL 4.3-4.9 mm.; CL 2.3-2.7 mm. Duration. Usually five days, occasionally four or six.

This stage differs little in gross appearance from the preceding stage, but the length of the telson is now about equal to the width and there is an articulated medial telson spine in most specimens, making the armature formula 9 + 1 + 9 (Fig. 3, V). The exopodite of the uropod retains the curved outer spine and now bears 10-11 plumose setae while the endopodite bears from six to seven. The exopodite bears four inconspicuous setae ventrally.

The antennule (Fig. 4, V) has about four terminal sensory aesthetes. There are usually three, rarely four large plumose setae distally on the basal segment and

193




another large seta with three or four very fine processes subdistally. A simple lobe arises from the same distal area of the basal segment or peduncle.

The antenna (Fig. 5, V) is basically unchanged, the scale bearing 14-16 plumose setae. The endopodite reaches two-thirds the length of the scale and terminates with one or two processes.

The mandible is essentially unchanged, having added a few fine teeth. The maxillule (Fig. 6, V) has four curved plumose setae on the proximal endite

and four simple setae. On the distal endite there are five to seven strong teeth and two setae. The endopodite is unchanged.

The maxilla (Fig. 7, V) bears 13-19 plumose setae on the scaphognathite. The endopodite bears three plus three setae. The distal lobe of the basal endite bears four setae, the proximal lobe five; the distal lobe of the coxal endite bears four, the proximal lobe 9-11 setae.

TABLE I

Characters of a "terminal" zoea VI and a "non-terminal" zoea VI

Larva no. 49 Larva no. 117

Leg buds very well developed very small Pleopod buds present not present Telson armature 9 + 1 + 9 10 + 10 Telson L/W ratio 2.4/1.8 2.2/1.7 Uropod setae

exopodite 13-14 12 endopodite 9 7

The first maxilliped (Fig. 8, V) has groups of about two, three, three and two setae on the medial margin in addition to the curved proximal process and a single seta near it. The exopodite bears six natatory setae, of which four are situated on a partially distinct distal segment. The terminal segment of the endopodite bears five setae. The penultimate segment bears two medial setae distally. The antepenultimate segment bears one seta medially and another laterally. The two proximal segments each bear two medial setae and one lateral seta.

The second maxilliped (Fig. 9, V) has three setae on the medial margin of the basipodite. The exopodite bears six or seven natatory setae. The endopodite is similar to that of the preceding stage.

The third maxilliped (Fig. 10, V) is uniramous and bears seven or eight natatory setae. There may be the beginning of an endopodal lobe.

Sixth Zoea. Figs. 1, VI; 2, VI. Size. TL 4.8-5.6 mm.; CL 2.6-3.3 mm. Duration. Usually four or five, rarely six days.

Larvae in the sixth zoeal stage may produce a glaucothoe directly or may moult into a seventh zoeal stage. The degree of apparent difference between stage VI and stage V or between two stage VI larvae is related to the future fate of the larva. For example, some characters of two stage VI larvae which died without moulting are shown in Table I.

Larva no. 49, had it survived, probably would have produced a glaucothoe, judg- ing from results with other larvae. Larva no. 117 would have produced another zoeal stage, the form of which was distinguishable beneath the cuticle. In the

194




present study three classes of stage VI larvae were observed but were not always distinguished before termination of the experiment. Some moulted directly from stage VI to the glaucothoe; some moulted from VI to VII and then to glaucothoe; some moulted from VI to VII to VIII and then to glaucothoe. The following description of stage VI is based primarily on a series (no. 65) in which the glaucothoe was produced directly from this stage.

The telson (Fig. 3, VI) is distinctly longer than wide. The antennule (Fig. 4, VI) bears three large and several smaller terminal

aesthetes. There are three subterminal pairs of processes. The lobe at the joint of the terminal and basal segments extends nearly to the end of the terminal segment. There are three small setae and four large plumose setae at the distal end of the basal segment, with another large one (or two in some specimens) more proximally.

TABLE II

Characters of several stages in a series producing the glaucothoe after six zoeal stages. (Larva no. 65)

Stage III IV V VI

Telson L/W 1.4/2.0 1.8/2.0 2.1/2.0 2.4/2.0 Telson armature 9 +9 9+9 9+1 +9 9+1 + 9 Uropod setae

exopodite 8 10 12 14 endopodite 0 5 7 9

The antennal scale (Fig. 5, VI) bears 16 or 17 plumose setae while the endopodite which is now two-segmented exceeds the scale in length and terminates in a single hair (but occasionally in three, of which two are small and inconspicuous).

The mandible is not changed notably. The bud of a mandibular palp could not be distinguished in available material.

The maxillule (Fig. 6, VI) is unchanged with respect to the endopodite but the basal endite has five apparently articulated and two non-articulated teeth and two simple setae. The coxal endite bears four larger curved plumose setae and five smaller simple setae.

The maxilla (Fig. 7, VI) upon the proximal lobe of the coxal endite bears 13 setae, on the distal lobe four. The proximal lobe of the basal endite bears eight, the distal lobe four or five setae. The endopodite bears five setae and the scaphognathite has about 19-20 plumose setae.

The first maxilliped (Fig. 8, VI) still bears the curved proximal process on the basipodite with additional setae along the medial margin. The exopodite bears six natatory setae. The five-segmented endopodite has the same arrangement of setae as in the preceding stage.

The second maxilliped (Fig. 9, VI) bears three setae on the medial margin of the basipodite and the exopodite bears seven natatory setae. The armature of the four-segmented endopodite is similar to that of the preceding stage.

The third maxilliped (Fig. 10, VI) may be uniramous in a long developmental sequence. When the sixth zoea is the penultimate zoea in a series the basipodite may be slightly swollen. When it is the last zoea, the third maxilliped may be biramous, the endopodite being represented by a long lobe arising from the proximal

195




FIGURE 11. Calcinus tibicen. The glaucothoe, lateral view (above) and dorsal view (below).

portion of the basipodite and bearing two or three setae. The exopodite in a terminal stage VI usually bears eight natatory setae.

Zoeal stages VII and VIII.

These stages, both or the first of which were sometimes passed through prior to attainment of the glaucothoe, are the result of non-uniform rates of internal growth coupled with a more or less regular moulting cycle. There were no essential addi- tions or changes from preceding stages except that where the preceding stages were somewhat retarded as regards degree of setation, these later stages appeared to make

G

FIGURE 12. Calcinus tibicen. The telson and uropods of the glaucothoe (G) and the first crab (C).

196




mdl

0.5mm II I - 1

FIGURE 13. Calcinus tibicen. Glaucothoe. P1, Ps, P4, P5, first, third, fourth and fifth pereipods; mdl, mandible; p12, p13, p4,, pl,, the pleopods of the second, third, fourth and fifth abdominal somites.

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up for it. Thus in one stage VIII specimen while the telson ratio of 2.6/1.4 indicated a slightly more elongate telson than in the final zoea of a series in which only six zoeal stages were found, the same animal had a telson armature count of 11 + 11 processes and the uropods bore 14-15 setae on the exopodites, 9-10 setae on the endopodites as in terminal stage VI. The antennal scale of a stage VIII may also resemble that of a terminal stage VI, having 16 plumose setae. In a series with eight zoeal stages the earlier stages at least as far back as stage III were somewhat less advanced than the corresponding stage of a shorter series. Table II summarizes changes of a few characters within one series.

Glaucothoe. Figs. 11, 12G, 13. Size. TL 3.5-3.9 mm.; CL 1.4-1.6 mm. Duration. This stage was attained 32-40 days after hatching for larvae which

passed through only six zoeal stages, and after 39-42 days for larvae which passed through eight zoeal stages. Most specimens of the 1961 series died within 48 hours after attaining this stage. One glaucothoe lived for six days until killed accidentally. In the 1960 series one specimen attained the glaucothoe on the 37th day after hatching but lost one leg during transfer operations on the 47th day. Nevertheless the animal survived, regenerated the leg, and on the 57th day after hatching moulted to the first crab stage. In C. tibicen the carapace has lost the postero-lateral spines and is now divided

into sections. The rostrum is blunt but well developed. The pereiopods are free and functional, the chelipeds being subequal and the other legs symmetrical. The abdomen is not quite twice the length of the cephalothorax. The abdomen bears biramous pleopods on somites two to five, but only the exopodite of each carries setae.

The telson (Fig 12, G) is subrectangular, not indented as in the crab (Fig. 12, C), and may bear from 9-15 plumose setae terminally with two pairs laterally. Glaucothoes attained after zoea VI had 11 setae, one attained after VIII had 15 setae along the posterior margin. There may be a few pairs of smaller setae medio- dorsally on the telson as well. The uropods are changed somewhat from the preceding zoeal stage and now bear corneous nodules along the posterior margin in addition to plumose setae. The exopodite may bear from 20-23 plumose setae plus a few

very fine simple hairs. The endopodite may bear from 13 to 15 plumose setae as well as a few simple hairs.

The eyes, together with the eyestalks, are about two times longer than wide and are widest at the eyes.There are no ocular scales apparent. (Note: In the first crab stage the eyestalk is wider than the eye and there is a simple, acute scale at the base of each.)

The antennule (Fig. 4, G) is now distinctly biramous with three segments com-

posing the internal or ventral ramus. The terminal segment may have up to nine small setae, the others two or three. The external or dorsal flagellum which arises from the same peduncular segment is composed of five articles. The most proximal is unarmed, the terminal segment bears a few fine setae. The intervening segments each bear a number of aesthetes.

The antenna (Fig. 5, G) reaches to the tips of the cheliped and has a scale at the base very different from the zoeal scale. In the endopodite there are two peduncular segments followed by about 10 flagellary segments, each of which bears a few short setae.

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The mandible (Fig. 13, mdl) has a cuplike grinding surface and a three-segmented palp, the distal end of which bears 12-13 short setae.

The maxillule (Fig. 6, G) has lost the segmentation of the endopodite which now appears as a simple palp bearing a few setae. The basal endite bears a greatly increased number of stout spines and setae, about 17-21, distally and a pair proximally. The coxal endite also bears a greatly increased number of setae.

The maxilla (Fig. 7, G) bears a double row of setae on the proximal lobe of the coxal endite, about seven on the distal lobe. There is a large number of setae on the lobes of the basal endite but the endopodite no longer bears any setae. The scaphognathite is very well developed and has approximately 65 short plumose setae.

The first maxilliped (Fig. 8, G) is radically changed. The exopodite is short and broad, bearing seven plumose setae along the exterior margin. The endopodite is unsegmented and is devoid of setae. The basipodite appears bilobed and bears about 18 setae on the distal lobe and about six on the proximal lobe.

The second maxilliped (Fig. 9, G) is least changed of all the mouthparts. The exopodite is clearly unsegmented distally.

The third maxilliped (Fig. 10, G) is biramous and bears about six to eight plumose setae terminally on the exopodite. The ultimate and penultimate segments of the endopodite are heavily armed with setae, some of which bear setules. The antepenultimate segment has a row of distal setae while the proximal segment bears only three or four simple setae. The ischium has a row of fine tubercles or teeth along the medial margin.

The chelipeds are about equal in size, each with a few setae. The second and third pereiopods (Fig. 13) have the dactyli about half the length of the propodi. There are a few setae on the dactyl and four horny spines ventrally in addition to the corneous terminus. There are setae and a couple of short spines distally on the propodus. The fourth pereiopod is non-chelate and the propodus has a double row of about 15 corneous granules on the latero-ventral surface. The fifth pereiopod bears granules on both dactyl and propodus and very long setae are present on these segments.

The pleopods are biramous, the inner ramus being unarmed. The pleopod of the fifth somite is shorter than the preceding ones. The number of setae is eight on the pleopod of the second somite, nine on the others.

DISCUSSION

The first stage larva attributed by Bourdillon-Casanova (1960) to Calcinus ornatus (Roux) bears very close resemblance to that described by Pike and William- son (1960) from a laboratory hatching. There are minor differences in that the antennal scale has 11 plumose setae and the short seta of the antennal endopod is half as long as the others according to Bourdillon-Casanova, whereas Pike and Williamson reported nine plumose setae on the scale and the short seta as one fourth as long as the others. If these are in fact objective differences they may well be within range of variability for a single species as indicated in the present paper, but evaluation of such characters is hampered by the general lack of detailed descriptions of hermit crab larvae. The antennule of C. ornatus was not figured by Pike and Williamson, but Bourdillon-Casanova showed it terminating with three aesthetes and three setae in addition to a large plumose subterminal seta. In C. tibicen I was

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able to distinguish with certainty only one aesthete and four other processes which may have been aesthetes.

The combination of prominent postero-lateral carapace spines and the presence on the fifth abdominal somite of a single medio-dorsal spine and a pair of lateral spines is common to both species and may be unique to the genus, but Pike and Williamson also attributed an unidentified larva lacking the fifth abdominal medio- dorsal spine to Calcinus. In the first zoea of C. ornatus the medio-dorsal spine of the fifth abdominal somite is shorter than the pair of lateral spines, whereas in C. tibicen it is distinctly longer. The very small lateral spines or teeth on the second, third and fourth abdominal somites of C. ornatus were not distinguished in C. tibicen.

A character of questionable status is the endopodite of the maxillule which according to Pike and Williamson is two-segmented in C. ornatus and which in other Diogenidae never has more than two segments. In C. tibicen this endopodite appeared to have three segments in the specimens for which dissection of the appendage was successful. Hart (1937) reported three segments for the maxillulary endopodite of Paguristes turgidus and Orlamunder (1942) showed three segments for Birgus latro. Coenobita clypeatus also has been shown to have a three-segmented endopodite (Provenzano, in press). Both these latter species are members of the family Coenobitidae, presumably derived from the same line as the Diogenidae to which Calcinus belongs.

Comparison of later zoeal development of C. tibicen with that of other species of Calcinus is restricted to the work of Pike and Williamson. Those authors obtained their first stage larvae from a laboratory hatching and the subsequent stages from the plankton. They did not illustrate completely each stage including appendages but did describe certain essential features of each stage. Size of first stage larvae is similar for the two species, but the fifth and sixth zoeae of C. tibicen are slightly larger than the fifth zoea of C. ornatus. Other characters mentioned by those authors for later zoeal stages do not differ significantly from those of C. tibicen, with the exception that the postero-medio-dorsal spine on the sixth abdominal somite of C. tibicen is not certainly indicated in the illustrations of the later stages of C. ornatus. In both species the telson becomes more elongate during zoeal development.

The glaucothoes of the two species are very similar in gross appearance and this similarity may extend to details. Appendages are not illustrated or described in detail by Pike and Williamson but Bouvier (1922) for Glaucothoe grimaldi gave enlarged figures of the first, second, and fourth pereiopods, the antennule and antenna and the tail fan in addition to a figure of the whole animal. Between that form and the glaucothoe of C. tibicen there are a few minor differences which if later confirmed may prove to be significant at the specific level. Such differences include number of spines on the ventral margin of the ambulatory dactyl and relative lengths of some antennal segments, as well as certain setation. In all important respects, however, Glaucothoe grimaldi resembles the two glaucothoes certainly known for Calcinus and in fact, as Pike and Williamson have already indicated, Bouvier's form may belong to C. ornatus. Pike and Williamson stated that the glaucothoe of C. ornatus has the pleopods (each?) armed on the outer ramus with nine plumose setae, where in C. tibicen there are only eight on the pleopod of the second abdominal somite, nine on the others.

Insofar as the description and illustration of C. ornatus and Glaucothoe grimaldi

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indicate, the similarities between glaucothoes of several species may be much more significant than any differences. Until now glaucothoes of two species within one genus of Diogenidae have not been compared in detail. Rather the few descriptions available were for species of hermit crabs in different genera, and differences between most of these seemed to be quite distinctive. Whether those differences were generic in significance or merely specific could not be ascertained, especially since in Paguristes, the only diogenid genus for which larvae of more than one species were known, there seem to be notable differences between the larvae. Recently it was shown that zoeae and glaucothoes of two species of Coenobita are more similar to each other than to those of other genera of hermit crabs (Provenzano, in press). The present study also confirms that two species of a genus of diogenid hermits even as larvae bear more resemblance to each other than to members of other genera, a long accepted hypothesis for which there has been little direct evidence.

SUMMARY AND CONCLUSIONS

1. Larvae of Calcinus tibicen (Herbst) were reared in the laboratory from hatching to the post-larva on a diet of Artemia nauplii. Temperatures ranged from 26? to 30? C. Salinity in one experiment fluctuated between 31 ppt and 35 ppt and in the second experiment salinity was maintained between 35.5 ppt and 37.1 ppt. Under these conditions the zoeal phase of development was completed in 32 to 42 days. The number of zoeal stages in the laboratory development of this species is variable, the glaucothoe being attained after six, seven or eight zoeal stages.

2. Six zoeal stages and the glaucothoe have been described and illustrated. The only two species of Calcinus for which zoeae are certainly known share the apparently unique features of a pair of prominent submarginal postero-lateral spines on the carapace and a medio-dorsal and pair of lateral spines on the fifth abdominal somite. The species apparently differ in that C. tibicen has the postero-medio-dorsal spine of the fifth abdominal somite longer than the laterals, a postero-medio-dorsal spine is present on the sixth abdominal somite of zoea III and older larvae, the maxillulary endopodite is three-segmented, and there are no minute lateral spines on abdominal somites two to four.

3. Adequate comparisons of the zoeal appendages and glaucothoe characters of C. tibicen with those of other species are not possible until more detailed descriptions are available, but the information which has been published indicates close similarity of larval characters of species within a genus.

LITERATURE CITED

BOURDILLON-CASANOVA, L., 1960. Le meroplancton du Golfe de Marseille: Les larves de Crustaces Decacpodes. Rec. Trav. Sta. Mar. Endoume, Fasc. 30, Bull., 18: 1-286.

BOUVIER, E. L., 1922. Observations complementaires sur les crustaces decapodes (abstraction faite des carides) provenant des campagnes de S.A.S. le Prince de Monaco. Result. Camp. Sci. Monaco, Fasc., 62: 1-106.

BROAD, A. C., 1957a. Larval development of Palaemonetes pugio Holthuis. Biol. Bull., 112: 144-161.

BROAD, A. C., 1957b. Larval development of the crustacean Thor floridanus Kingsley. J. Elisha Mitchell Sci. Soc., 73: 317-328.

CIIAMBERLAIN, N. A., 1961. Studies on the larval development of Neopanope texana sayi (Smith) and other crabs of the family Xanthidae (Brachyura). Chesapeake Bay Inst. Johns Hopkins Univ., Tech. Rept. 22, pp. 1-37, Pls. 1-16.

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202 ANTHONY J. PROVENZANO, JR.

COFFIN, H. G., 1960. The ovulation, embryology, and developmental stages of the hermit crab Pagurus samuelis (Stimpson). Publ. Walla Walla College Dept. Biol. Sci. and Biol. Sta., No. 22, pp. 1-5.

COSTLOW, J. D., JR., AND C. G. BOOKHOUT, 1959. The larval development of Callinectes sapidus Rathbun reared in the laboratory. Biol. Bull., 116: 373-396.

COSTLOW, J. D., JR., AND C. G. BOOKHOUT, 1960a. The complete larval development of Sesarma cinereum (Bosc) reared in the laboratory. Biol. Bull., 118: 203-214.

COSTLOW, J. D., JR., AND C. G. BOOKHOUT, 1960b. A method for developing Brachyuran eggs in vitro. Limnol. Oceanogr., 5: 212-215.

COSTLOW, J. D., JR., AND C. G. BOOKHOUT, 1961a. The larval development of Eurypanopeus depressus (Smith) under laboratory conditions. Crustaceana, 2: 6-15.

COSTLOW, J. D., JR., AND C. G. BOOKHOUT, 1961b. The larval stages of Panopeus herbstii Milne- Edwards reared in the laboratory. J. Elisha Mitchell Sci. Soc., 77: 33-42.

DECHANCE, M., 1961. Sur la morphologie externe des larves de pagurides, I. Catapaguroides timidus (Roux). Crustaceana, 2: 53-67.

DOBKIN, S., in press. Larval development of Palaemonetes paludosus (Gibbes) (Decapoda, Palaemonidae) reared in the laboratory. Crustaceana.

FoRsS, C. A., AND H. G. COFFIN, 1960. The use of the brine shrimp nauplii, Artemia salina, as food for the laboratory culture of decapods. Publ. Walla Walla College Dept. Biol. Sci. and Biol. Sta., No. 26, pp. 1-15.

HART, J. F. L., 1937. Larval and adult stages of British Columbia Anomura. Canad. J. Res., D., 15: 179-220.

HART, J. F. L., 1960. The larval development of British Columbia Brachyura. II. Majidae, sub- family Oregoniinae. Canad. J. Zool., 38: 539-546.

KNUDSEN, J. W., 1958. Life cycle studies of the Brachyura of western North America, I. General cultural methods and the life cycle of Lophopanopeus leuconmanus leucomanus (Lockington). Bull. So. Calif. Acad. Sci., 57: 51-59.

KNUDSEN, J. W., 1959a. Life cycle studies of the Brachyura of western North America, II. The life cycle of Lophopanopeus bellus diegensis Rathbun. Bull. So. Calif. Acad. Sci., 58: 57-64.

KNUDSEN, J. W., 1959b. Life cycle studies of the Brachyura of western North America, III. The life cycle of Paraxanthias taylori (Stimpson). Bull. So. Calif. Acad. Sci., 58: 138-145.

LEWIS, J. B., 1960. The fauna of rocky shores of Barbados, West Indies. Canad. J. Zool., 38: 291-435.

MACDONALD, J. D., R. B. PIKE AND D. I. WILLIAMSON, 1957. Larvae of the British species of

Diogenes, Pagurus, Anapagurus and Lithodes (Crustacea, Decapoda). Proc. Zool. Soc. Lond., 128: 209-257.

ORLAMUNDER, J., 1942. Zur Entwicklung und Formbildung des Birgus latro L. mit besonderer Berucksichtigung des X-Organs. Zeitschr. wiss. Zool., 155: 280-316.

PIKE, R. B., AND D. I. WILLIAMSON, 1960. Larvae of decapod Crustacea of the families

Diogenidae and Paguridae from the Bay of Naples. Pubbl. Staz. Zool. Napoli, 31: 493-552.

PROVENZANO, A. J., JR., 1959. The shallow-water hermit crabs of Florida. Bull. Mar. Sci. Gulf and Carib., 9: 349-420.

PROVENZANO, A. J., JR., 1960. Notes on Bermuda hermit crabs (Crustacea; Anomura). Bull. Mar. Sci. Gulf and Carib., 10: 117-124.

PROVENZANO, A. J., JR., 1961a. Note on Paguristes cadenati, a hermit crab new to Florida. Quart. J. Fla. Acad. Sci., 23: 325-327.

PROVENZANO, A. J., JR., 1961b. Pagurid crabs (Crustacea; Anomura) from St. John, Virgin Islands, with descriptions of three new species. Crustaceana, 3: 151-166.

PROVENZANO, A. J., JR., in press. The larval development of the tropical land hermit Coenobita clypeatus (Herbst) in the laboratory. Crustaceana.

THOMPSON, M. T., 1904. The metamorphoses of the hermit crab. Proc. Bostont Soc. Nat. Hlist., 31: 147-209.

WASS, M. L., Unpubl. Pagurid crabs of the western North Atlantic south of Cape Hatteras. Doctoral Dissertation, University of Florida, Gainesville, 281 pp., 5 pls. June, 1959.



Documents

The Larval Development of Calcinus tibicen (Herbst) (Crustacea, Anomura) in the Laboratory