THE GLAUCOTHOE STAGE OF DARDANUS VENOSUS (H. MILNE-EDWARDS) 1 (: )

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

ABSTRACT The post-zoeal stage of the Dardanus venosus was identified when a planktonic specimen captured in the Florida Straits was held alive in the laboratory for more than a month and moulted to the first crab stage. A description is given of the glaucothoe, based primarily on this specimen but supplemented with other material. Exceptionally large size, an elongate telson and peculiar hooks on the dactyls of the ambulatory legs distinguish this form from described glaucothoes of other genera. Lack of detailed information on other within the hampers comparison and evaluation of characters.

INTRODUCTION The glaucothoe stage in hermit crab development is completely different from the zoeal stages which precede it and also sufficiently different from the crab stages which follow that knowledge of zoeal and adult forms alone does not often permit identification of the glaucothoe. Since positive identification can be made only by holding the glaucothoe alive until a recognizable crab stage is produced, or by obtaining the glaucothoe from zoeas of known identity, this stage in hermit crab ontogeny is the most poorly known. The hermit crab family contains several hundred species in a dozen genera but few glaucothoes are known. The post-larva of Paguristes turgidus (Stimpson) was described by Hart (1937), that of P. oculatus (Fabricius) by Pike and Williamson (1960). Dechance and Forest (1958) treated in detail the glaucothoe of Clibanarius erythropus (Latreille). The glaucothoe of Diogenes pugilator (Raux) is known (MacDonald, Pike and Williamson, 1957), as is that of Calcinus ornatus (Raux) (Pike and Williamson, 1960). At this laboratory, rearing of larvae from females of known identity has produced, among others, glaucothoes of Calcinus tibicen (Herbst) (Provenzano, 1962a) and of the land hermit Coenobita clypeatus (Herbst) (Provenzano, 1962b), and has permitted some com- parisons of post-larval characters within genera. The genus Dardanus contains in excess of 40 species but no glaucothoes reared from the egg or even from late zoeal stages have been described. Glaucothoe rostrata Miers, 1881 has been attributed to

IContribution No. 443 from The Marine Laboratory, Institute of Marine Science, Univer- sity of Miami. This research was supported by grants RG-16298 and G-20355 from the National Science Foundation. J 2 Bulletin of Marine Science of the Gulf and Caribbean 1/3( I) (Risso) by Pike and Williamson (1960) and the tail fan of a glaucothoe attributed to Dardanus peetinatus (Ortmann) was illustrated by Dechance and Forest (1958). Barnard (1950) gave a couple of figures of what he believed to be the glaucothoe of Dardanus arrosor (Herbst). In view of the general scarcity of information relating to this stage in Dardanus, any information at all might be helpful in establishing reference points of morphology for the eventual identification of collected material and the determination of systematic relationships. The present paper describes the external morphology of the post-zoeal stage of the marine hermit crab, Dardanus venosus (H. Milne-Edwards).

DESCRIPTION Material.-Two specimens, CL 3.2 mm: Straits of Florida off Miami, 25° 42' N, 80° 09' W, to 25° 42' N, 80° 01' W, estimated depth 50 m; Isaacs-Kidd midwater trawl, fished for one hour. R/V GERDA,cruise 6210, sta. G-9, night of 25 May 1962. (One of the specimens died within hours after capture, but the other, upon which most of the description is based, lived 41 days in the laboratory at 27° + 1°C and died in the moult to first crab.) One specimen, CL 3.2 mm: Northern Caribbean Sea southeast of Jamaica, 17° '08' N, 75° 02' W, to 17° 05' N, 74° 52' W, estimated depth 200 m; Isaacs-Kidd midwater trawl. R/V GERDA,cruise 5907, "Carib" sta. 19, 0950-1150 hrs, 10 May 1959. One specimen, CL 3.0 mm: Straits of Florida off Miami, 25° 39' N, 79° 40' W; Isaacs-Kidd midwater trawl with 930 m of wire out, fouled and trawl retrieved. R/V GERDA,cruise 6222, sta. G-47, 1906 hrs. 21 August 1962. Measurements of specimen yielding erab.-Shield (anterior carapace) length, 1.9 mm; width, 1.8 mm. Carapace length, rostrum to posterior medial margin (CL), 3.2 mm. Total length, tip of rostrum to posterior margin of telson, about 10.3 mm. Telson length measured along dorsal midline (excluding marginal setae), 1.4 mm; maximum width, 1.0 mm. Third pereiopod, dorsal length of dactyl from tip to propodus, 2.1 mm; dorsal length of propodus, 2.3 mm. Identi[ieation.-The first crab stage obtained from the GERDAglaucothoe bore considerable similarity in pigmentation to Dardanus venosus. Al- though most of the taxonomic features of the adult were not yet developed, the small clusters of bluish spinules characteristic of D. venosus were present on several pereiopods. No similar features are present in the adults of Dardanus arrosor and an undescribed species, the only other members of the genus known to occur in the West Indies. The glaucothoe of one of these other two species has been studied in detail by the writer and it 19631 Provenzano: Glaucothoe of Dardanus Venosus 13 differs in a number of respects, notably in the form of the telson. In fact, the telsons of all the four species of Dardanus known to the writer differ in detail, despite gross similarity. Laboratory rearings from the eggs failed to yield good glaucothoes of Dardanus venosus but several specimens died in the moult from last zoea to post-larva and although the specimens were not in sufficiently good condition to permit description of the glaucothoe from them alone, a comparison of the tel sons of the GERDA specimens with that of one of the laboratory reared failed to reveal any significant differences.

Morphology.-The general appearance of the glaucothoe is suggested by the semi-diagrammatic Figure la, but most characters necessary for generic and specific identification must be treated in more detail. The dorsal shield or anterior carapace is about as wide as it is long. The rostrum projects well beyond the anterolateral corners of the carapace and appears bilobed in dorsal view because the most distal portion tilts slightly ventrad. The dorsal surface of the shield has extremely fine setae scattered over it. The posterior and lateral margins of the carapace are lined ventrally with a fringe of setae.

FIGURE 1. Dardanus venosus, glaucothoe stage: a.-dorsal view; b.-abdomen, lateral view. The scales in this and all following figures represent 1.0 mm. 14 Bulletin of Marine Science of the Gulf and Caribbean [13(1) Maximum corneal width is only slightly less than the total eyestalk length. There are no ocular scales present. The abdominal somites are not armed with spines, but somites II-V, those bearing pleopods, posterolaterally have very distinctive downward projecting extensions of the cuticle (Fig. 1b). The maximum width of the telson (Fig. 2) is more than half the telson length measured in the midline, i.e., from the posterior margin of abdominal somite VI to posterior telson margin. Telson L/W ratio, 1.47. The minimum telson width is slightly more than one third the length. At each posterolateral corner of the telson there is a very noticeable marginal protuberance. The convex telson margin between these corners is armed with 17 strong, finely plumose setae in the GERDA specimen which yielded the crab and in the laboratory-reared specimen, but 19 in thc other GERDA glaucothoe. The Carib specimen has 17 setae on the telson and that from haul G-47, smaller than the others, has only 16. The lateral margins of the telson each bear several pairs of setae and the dorsal surface bears two medial rows of setae, two rows submedially and a few setae near the lateral margins. The posterior margin of the sixth abdominal somite has two groups at three setae near the midline and a pair of long setae at each posterolateral corner. The protopod of the uropod has a very strong, curved spine poster- iorly. The symmetrical tail fan has endopodites about four-fifths the size of the exopodites. The exopodite of the uropod bears 14-15 corneous

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FIGURE 2. Dardanus venosus, glaucothoe stage: tail fan. 19631 Provenzano: Glaucothoe of Dardanus Venosus 15 granules on its posterolateral margin, and is lined with approximately 50 setae, those of the lateral margins rather fine and those of the posterior and

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FIGURE 3. Dardanus venosus, glaucothoe stage: a.-antenna; b.-second pere- iopod; c.-third pereiopod; d.-fourth pereiopod; e-j.-fifth pereiopod, two views; g.-first pereiopod. 16 Bulletin of Marine Science of the Gulf and Caribbean [ 13(1) medial margins longer and stouter. The endopodite bears seven or eight corneous granules, and its margins have approximately 35 setae, which are finer and shorter along the lateral and proximal medial margins and longer and stouter on the posterior edges. The chelae are equal and similar, about 2.5 times longer than high (Fig. 3g). The movable dactyl is slightly more than one third the total length of the manus. There are a few setae on the dorsal and ventral margins of the hand but these are much more numerous on the movable dactyl where they occur in clusters of three or four, both laterally and medially. The dactyl of the second pereiopod (Fig. 3b) is shorter than the pro- podus and armed with a number of long setae but most distinctively with a pair of large, ventral triangular processes. There is a very small additional spine between the more distal process and the corneous acute terminus. The pair of processes appears to have a very slight slant toward the terminus. The propodus of the third pereiopod (Fig. 3c) is relatively less slender than that of the second but the difference is barely noticeable. The dactyl of this leg also bears a pair of large ventral processes and a much smaller one distally but the axes of the paired processes are more nearly perpen- dicular to that of the dactyl. The fourth pereiopod (Fig. 3d) has about 18 bulbous corneous granules on the propodus. There is a long subterminal seta on the dactyl and at least eight or nine others. The propodus bears more than half a dozen prominent setae, the carpus three distally, a couple more on the dorsal margin, and the merus also bears a few setae. The fifth pereiopod (Figs. 3e, 3f) is chelate. The spoon shaped dactyls have small corneous teeth or serrations distally. There are about 9 corneous granules on the movable dactyl and about 16 on the propodus. There are about seven large, curved setae on the movable dactyl and about 20 on the propodus, most of which are large and curved. There are six or seven setae distally on the carpus, and one or two more proximally. The merus bears half a dozen setae. The antennal flagellum (Fig. 3a) consists of 29 segments distal to two sturdy peduncular segments and a third from which arises the very small, suboval antennal scale. The terminal segment of the flagellum bears, in addition to the usual two or three tiny setae, a longer terminal seta which is about the length of the terminal segment itself. The peduncle of the antennule (Fig. 4a) consists of three segments, the most proximal containing the statocyst. The middle segment bears two setae dorsally, one long and the other shorter, and about four short setae distally. The distal segment of the peduncle has only a couple of small setae. The external or dorsal flagellum consists of 12 segments, of which 1963] Provenzano: Glaucothoe ot Dardanus Venosus 17 the distalmost three are elongate and bear prominent setae. Segments 4-11 are short and broad and bear numbers of aesthetes. The 12th segment, most proximal, carries no armature. The four-segmented inner or ventral flagellum has several setae on each of its segments. The mandible (Fig. 4b) is a stalked cup with a three-segmented (?) palp having on its distal segment one proximal and 17 more distal, short, stout setae. The maxillule (Fig. 4c) consists of an unsegmented palp bearing a terminal seta and a smaller seta proximally. The basal endite has approxi- mately 35 strong setae distally with about eight finer, slightly curved setae more proximally. The coxal endite bears setae in four groups, about 19

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a f g FIGURE4. Dardanus venosus, glaucothoe stage: a.-antennule; b.-mandible; c.-maxillule; d.-maxilla; e.-first maxilliped;f.-second maxilliped;g.-third maxilliped. 18 Bulletin of Marine Science of the Gulf and Caribbean [13(1) fine setae, 10 coarse setae distally, and a group of four, another of five setae more proximally. The maxilla (Fig. 4d) has approximately 100 setae fringing the scaph- ognathite. The endopodite is a simple unarmed elongated lobe. The basal endite is bilobed with about 2'0 marginal setae on the distal lobe and about 13 on the proximal lobe there is a total of eight fine setae more proximally on the basal endite. The coxal endite also is bilobed but the distribution of setae is more complex. The narrow distal lobe has four coarse setae distally and eight finer ones proximally. The proximal lobe bears at least 20 setae marginally, about 32 in a submarginal row and another 15 more proximally. The first maxilliped (Fig. 4e) has a broad, blade-like exopodite with 17 plumose setae marginally and a small unarmed lobe distally. The endopodite is an elongated, unarmed lobe. The basal endite bears about 18 coarse setae on the medial margin and a dozen finer ones submarginally. The coxal endite bears about 24 coarse setae on its distal portion, but not in a row, and about half a dozen fine setae more proximally. The second maxilliped (Fig. 4f) consists of an exopodite bearing half a dozen setae submedially and a short flagellum distally. The flagellum carries about 14 plumose setae, the most proximal of which are very small in comparison with the distal ones. The four-segmented endopodite has approximately 10 stout setae on the terminal segment, about 14 on the distal half of the penultimate segment, only about four on the next segment and a single seta on the most proximal. The third maxilliped (Fig. 4g) is the largest of the three and, like the second maxilliped, is biramous. The flagellum of the exopodite bears about 15 plumose setae, which increase in size distad. The distal portion of the flagellum appears to be segmented. The endopodite is five segmented. The terminal segment has about 17 stout setae, at least four of which are serrated. The penultimate segment carries about 6 setae distally and approximately 24 around the middle of the segment, some of which also are serrated. The antepenultimate segment bears 2 setae distally. The next segment proximally carries about four large and four small setae. The most proximal segment bears, in addition to about 15 setae, a ridge of corneous tubercles on its medial surface. Pleopods (Fig. 5) are present on abdominal somites II-V. One series was removed from one specimen. The exopodite of each carries 12 large, plumose setae. The endopodite bears minute corneous hooks at the distal margin. (Apparently four on pleopod II, five on pleopods III and IV, and three on pleopod V.) There are, in addition, a few fine setae on the medial margin of each endopodite. (Apparently three on pleopod II, five on pleopod III, four each on pleopods IV and V.) C%r.-There are several red-orange chromatophores scattered along the antennular peduncle, and large ones on the medial central portion of the 19631 Provenzano: Glaucothoe of Dardanus Venosus 19

\11 IV V FIGURE 5. Dardanus venosus, glaucothoe stage: pleopods of second to fifth abdominal somites. The setules on the large setae are omitted for clarity. eyestaJks. The chelipeds of the first crab stage, visible through the exo- skeleton of the gJaucothoe, show purple areas in the center of which are setae and a spinule. The dactyl of each walking leg has a few red-orange chromatophores, but the central portion of the dactyl is purplish. The stiff setae or bristles are colorless. The propodus of the walking leg is orange at both ends near the joints and purplish in the middle portion. Some of the setae are colorless but the largest are maroon with light tips. The gut is speckled red and there are orange spots at the bases of the pleopods, at the antero-Iateral corners of the telson, five along the posterior border of the telson, and two more in front of that row. The posterior portion of the protopod of the uropod is orange and there is orange pigment on the posterior portion of the uropods themselves.

DISCUSSION Among the features which immediately set the glaucothoe of Dardanus venosus apart from those of other genera are the form of the tail fan, es- pecially the telson, the remarkable ventral teeth on the ambulatory dactyls and, of course, the size. There are numerous other distinctive characters as well. A detailed comparison and evaluation of larval and post-larval characters within the various groups of hermit crabs is planned for a later date, but a few remarks here on general similarities and differences may be worthwhile. As a result of the work of Hart (1937), MacDonald, Pike and Williamson (1957), Dechance and Forest (1958) and Pike and William- son (1960) and, more recently, of studies being conducted at this labora- 20 Bulletin of Marine Science of the Gulf and Caribbean [13(1 ) tory (Provenzano, 1962a, 1962b, and unpublished data) we have a general idea of the major features which characterize the glaucothoes and indeed, even the zoeal stages of a number of hermit crabs. Thus far, the taxonomic alignments suggested by study of adult forms have been con- firmed by studies on earlier stages. Background and the details of this problem may be found in the papers cited. Glaucothoes of the Paguridae seem to be characterized by having the right hand larger than the left, the tail fan asymmetrical and the endo- uropod reduced to a functionless rod, whereas glaucothoes of the Coen- obitidae and Diogenidae, so far as known, are symmetrical with respect to hands and tail fan (except the aberrant genus Diogenes which has the left hand larger than the right) and have the endo-uropod well developed and functional. There are other differences but these are the most obvious. Glaucothoes of Coenobita may be distinguished readily from those of the Diogenidae by the non-attenuated, almost clublike antennules, an ex- tremely long seta on the terminal segment of the antenna, a reduced or even vestigial exopodite on the third maxilliped, the wider than long sub- oval telson, and other less obvious features (Provenzano, 1962b). Among the Diogenidae, glaucothoes of various genera may be separated on similar differences. However, none of the non-pagurid glaucothoes yet described (except for a few attributed to Dardanus) even approach in size the glaucothoe of Dardanus venosus. None of the described, identified post- larvae of other genera have the elongated telson apparently characteristic of Dardanus. The ventral tooth-like processes of the ambulatory dactyls are not known for Paguristes, Calcinus, Clibanarius, and Diogenes, but have been indicated in crude illustrations of some unidentified glaucothoes from the Pacific (Lebour, 1934) and for Dardanus arrosor. I have seen them also in glaucothoes of two other species of Dardanus and in that of Petrochirus diogenes (L.) (manuscript in preparation). The tail fan of the glaucothoe attributed by Dechance and Forest (1958) on rather good grounds to Dardanus pectinatus (Ortmann) bears a very great resemblance to that of Dardanus venosus, certainly so much more than other known glaucothoes do that we must assume the identification of D. pectinatus to be correct. (The specimen of Dechance and Forest was taken with first and later crab stages of that species.) There are minor, specific differences between these forms, notably the number of corneous granules on the posterolateral margins of the uropods being larger in D. pectinatus. The posterolateral protuberances on the telson of D. venosus are not illustrated for D. pectinatus and are absent in two other species of Dardanus (Provenzano, unpublished data ) so this may be considered a specific character. There may be a few more pairs of median setae on the dorsal surface of the telson of D. pectinatus and there are two more long setae on the posterior margin. This latter is probably not significant, 19631 Provenzano: Glaucothoe of Dardanus Venosus 21 however, as one of the GERDA specimens had 19 setae and this feature has been shown to vary slightly for species of other genera. The spines on the posterior margin of the proto pod of the uropods of both species are not so pronounced in the described glaucothoe of any other genus. Glaucothoe rostrata Miers also bears more resemblance to the glau- cothoe of Dardanus venosus than to known glaucothoes of any other genus of hermit crab. As stated above, Pike and Williamson have suggested that Miers's form is Dardanus calidus (Risso). Since the generic identity seems to be certain and as only one species of Dardanus is known from the vicinity of Madeira, there is every reason to believe their suggestion is correct. Barnard (1950) found a large glaucothoe in field collections in which juvenile Dardanus arrosor were common and attributed it to that species. His description is too brief to be of much value and his figure of the whole specimen is too small to indicate more than a general Dardanus-like form, but his detailed figure of an ambulatory dactyl very clearly shows the peculiar tooth-like processes found in D. venosus. These processes also have been found in other species of Dardanus (Provenzano, unpublished) and may be characteristic of the genus. Their function is evident from observations on the feeding of D. venosus glau- cothoe in the laboratory. The normally swims with its anterior three pairs of pereiopods extended directly in front. Upon encountering prey, such as decapod larvae, the pereiopods come into play and draw in the object encountered. The hooks on the dactyls help hold the active prey while it is being consumed. The dactyls of the right side of the specimen were in good condition shortly after capture, but after more than a month they had been worn or chewed down to stubs. The dactyls of the left side were not affected. Unfortunately, while other postlarval characters of D. venosus show considerable differences from those of other diogenid genera, no other Dardanus glaucothoes have been described in sufficient detail to permit comparisons of possible specific characters and evaluation of the systematic significance of such features as appendage setation.

LITERATURE CITED

BARNARD, K. H. 1950. Descriptive catalogue of South African Decapod Crustacea. Ann. South Afr. Mus., 38: 1-837, figs. 1-154. DECHANCE, M. AND J. FOREST 1958. Les glaucothoes de Catapaguroides timidus (Raux) et de Clibanarius erythropus (Latreille). Remarques sur Ie stade post-larva ire des pagurides. Bull. Soc. Zool. France, 83(2-3): 274-293, figs. 1-30. HART, J. F. L. 1937. Larval and adult stages of British Columbia Anomura. Canada J. Res., D 15: 179-220, figs. 1-11, pI. 1. 22 Bulletin of Marine Science of the Gulf and Caribbean [13(1)

LEBOUR, M. V. 1934. Larval Crustacea (Decapoda and Stomatopoda) Expedition S. A. R. Prince Leopold of Belgium, Duke of Brabant, to the extreme East (1932). Bull. Mus. roy. Hist. nat. Belg., 10(8): 1-24, figs. 1-19. 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. Land., 128 (2): 209-257, figs. 1-11. MIERS, E. J. 1881. Account of the zoological collections made during the survey of H. M. S. "Alert" in the Straits of Magellan and on the coast of Patagonia. Crustacea. Proc. zool. Soc. Land., 1881: 61-79, pI. 7. PIKE, R. B. AND D. I. WILLIAMSON 1960. Larvae of decapod Crustacea of the families Diogenidae and Pag- uridae from the Bay of Naples. Pubbl. Staz. Zool. Napoli, 31 (3) : 493-552, figs. 1-12. PROVENZANO, A. J., JR. 1962a. The larval development of Galcinus tibicen (Herbst) (Crustacea, Anomura) in the laboratory. BioI. Bull., 123(1): 179-202, figs. 1-13. 1962b. The larval development of the land hermit, Goenohita clypeatlls Herbst) in the laboratory. Crustaceana, 4(1): 207-228, figs. 1-12.