THE LARVAL STAGES of HOMOLA BARBATA (FABRICIUS) (CRUSTACEA, DECAPODA, HOMOLIDAE) REARED in the Laboratoryl

Home , Homolidae

BIOLOGICAL RESULTS OF THE UNIVERSITY OF MIAMI DEEP-SEA EXPEDITIONS. 55. THE LARVAL STAGES OF HOMOLA BARBATA (FABRICIUS) (CRUSTACEA, DECAPODA, HOMOLIDAE) REARED IN THE LABORATORyl

A. L. RICE British Museum (Natural History), Cromwell Road, London, S.W. 7, England

AND ANTHONY J. PROVENZANO, JR. University of Miami, Rosenstiel School of Marine and Atmospheric Sciences

ABSTRACT Larvae yielded by a female collected off Yucatan were reared to the seventh, and final, zoeal stage at 20°C and 36.2%0 salinity. The larvae, the first complete series available of any species of the family, are described and illustrated. Comparison of the reared larvae with others attributed to the same species but captured in Mediterranean and South African waters confirmed the morphological differences which previously had led to sug- gestions of specific or subspecific separation of the parent populations. Examination of adult material failed to reveal positive evidence of specific status of the separated populations. The setation of the uropodal endopods in Homola appears in the third zoeal stage, earlier than for any other decapod known. Recent studies of larval forms tend to confirm the view that the Homolidae are related to the Raninidae and are close to the line of descent of the true crabs, and that the family is well separated from both the typical Anomura and the much more primitive Dromiidea.

INTRODUCTION Homola barbata has been recorded in the eastern and western North Atlantic, in the Mediterranean, and in the South Atlantic near South Africa. Throughout its range (Fig. 1), H. barbata is the only recognized repre- sentative of the genus, except off the east coast of North America where a closely related species, H. vigil Milne Edwards, also occurs. Zoeal larvae attributed to Homola barbata have been described from the Bay of Naples (Cano, 1893; Pike & Williamson, 1960) and from Mes- sina (Thiele, 1905). Although none of these larvae was hatched from a known adult or molted to a certainly identifiable stage, the fact that H. barbata is the only species of the genus recorded from this fairly well studied area makes an erroneous identification rather unlikely.

1 Contribution No. 1194 from the University of Miami, Rosenstiel School of Marine and Atmospheric Sciences. This work was supported by research grant GB-7075X and ship support grant GB-7082 from the National Science Foundation; by research grant GM-I1244 from the National Institute of General Medical Sciences, U.S. Department of Health, Education and Welfare; and by the National Geographic Society-University of Miami Deep-Sea Biology Program. This paper is one of a series resulting from the National Geographic Society-University of Miami Deep-Sea Biology Program. 1970] Rice & Provenzano: Larval Stages of Homola barbata 447

FIGURE 1. Distribution of Homola barbata (circles) and H. vigil (triangles). Data from the literature and from unpublished records in the British Museum (N atural History) and the Rosenstiel School of Marine and Atmospheric Sciences, University of Miami. In most cases each symbol corresponds to one record, but in some areas, such as the east coast of the United States and in the Caribbean, there are more records than are indicated here.

Five zoeal stages taken in the plankton off South Africa and described by Rice & von Levetzow (1967) are very similar to the Mediterranean larvae and probably belong to the same species. Megalopal stages and terminal zoeae taken in the plankton of the Straits of Florida off Miami in 1963 were linked, through molts in the laboratory, with a first crab stage which was also identified as H. barbata (Rice, 1964). However, those Florida larvae differed from the Mediterranean and South African zoeae in a number of details, which suggests that what is con- sidered to be H. barbata may include more than one subspecies, or even species, with distinct larvae. 448 Bulletin of Marine Science [20(2)

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N I.lJ c.: ~ 0 ~ 1970) Rice & Provenzano: Larval Stages of Homola barbata 449 TABLE 1 NUMBERS AND PERCENTAGES OF LARVAE OF Homola barbata IN SUCCESSIVE STAGES

Stage No. of specimens Percentage I 140 100.0 11 115 82.5 III 108 76.5 IV 100 70.0 y 76 55.0 VI 24 17.5 V11 1 0.7

Obviously, it would be desirable to rear the larvae from adults taken in various parts of the known range. This paper presents the results of one such rearing made at the Rosenstiel School of Marine and Atmospheric Sciences of the University of Miami. We are indebted to Barbara Stolen for the illustration of the female crab and to C. Edith Marks and R. A. Feigenbaum for assistance in the laboratory. MATERIAL AND METHODS On 23 May 1967, an ovigerous female was taken at station P-582 by the R/V JOHN ELLIOTT PILLSBURY at Arrowsmith Bank in the Yucatan Channel (21°10'N, 86°18'W). The depths sampled by the otter trawl during this tow varied from 250 to 20 fathoms (457 to 36 meters), so there is no way of knowing accurately the depth at which the female was collected. The specimen was maintained alive on board the ship and was returned to the laboratory. One hundred and forty of the larvae hatched on 6 June 1967 were reared individually in compartmented plastic trays at 20°C and 36.27<'0 salinity. Newly hatched nauplii of Artemia were provided as food for the larvae. Details of the rearing method and treatment of the resulting material were similar to those described earlier (Rice & Provenzano, 1964), except that exuviae and dead animals were preserved in ethylene glycol. The female from which larvae were obtained (Fig. 2) is deposited in the museum of the Rosenstiel School of Marine and Atmospheric Sciences, and its catalogue No. is UMML 32: 3824. Carapace length of larvae was measured from the tip of the rostrum to the middle of the posterior margin of the carapace.

RESULTS None of the animals reached the megalopa stage, and only one individual reached the terminal zoeal stage, after molting six times. The numbers and percentages surviving into each successive stage are given in Table 1, 450 Bulletin of Marine Science [20(2)

FIGURE 3. Homola barbata, first zoea. which shows that the main mortalities occurred after the third molt and particularly between the fifth and sixth stages. The duration of the larval stages was rather more variable than is usual in laboratory-reared larvae, but molts occurred fairly regularly with peaks at about 9.5, 17.5, 26.5, 37, and 48 days after hatching.

MORPHOLOGY In the following descriptions of the larval stages, the illustrations are largely self-explanatory, but are supplemented by a summary of the armature of selected features in Table 2. Otherwise, the descriptions are generally restricted to the major changes in the anatomy from stage to stage and variations within a single stage.

TABLE 2 ARMATURE OF SELECTED FEATURES OF SUCCESSIVE ZOEAL STAGES OF Homola barbata

Marginal Artic- Setation of Setation setae of Natatory setae ulated Uropods of Zoeal Ant. 2 processes -~- scaphog- stage scale Mxp. I Mxp.2 Mxp.3 of tel son Exopod Endopod nathite I 9 4 4 10 5 II 12 6 6 4-5 11-12 11-12 1II 18-19 7-9 8-9 7-8 16-18 11-13 4-6 20-21 IV 24 10-11 11-13 11-12 23-25 20-24 13-18 38-41 V 27-30 13-15 16-18 14-17 29-34 25-35 22-30 55-62 VI 31-33 16-18 20-22 18-21 36-41 40-42 34-37 80-86 VII 34 21-22 25-26 25-26 45 45-47 40-42 100-103 1970] Rice & Provenzano: Larval Stages of Homola barbata 451

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FIGURE 4. Homola barbata, first zoea: a, b, dorsal and lateral views of abdomen, respectively; c, antennule; d, antenna; e, basal endite of first maxilla; f, endopod and scaphognathite of second maxilla; g, h, first and second maxillipeds, respectively. Bar scale represents 0.3 mm for a and b; 0.2 mm for c, d, g, and h; and 0.1 mm for e and f.

Stage [.-SIZE: Carapace length (CL) 0.67-0.76 mm. (4 spec.)

DESCRIPTION (Figs. 3 and 4.): The most striking features of the larvae are the rows of teeth on the winglike extensions of the carapace which seem to be typical of early-stage homolids. The length of the rostmm 452 Bulletin of Marine Science [20(2)

1.0 mm

FIGURE 5. Homola barbata: a, b, second zoea; c, d, third zoea. varied considerably in the specimens examined and could be much shorter than that shown in the illustration; this variation was largely responsible for the range in carapace length. The only other major variation at this 1970] Rice & Provenzano: Larval Stages of Homola barbata 453

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t- - .------I I------i 0.1 mm 0.5mm (b,c,d,el (0) FIGURE 6. Homola barbata, second zoea: a, abdomen; b, antennule; c, antenna; d, third maxilliped; e, portion of a telson inside which that of the third zoea is visible. stage was that the third maxillipeds either were represented by unarmed, unsegmented buds or were entirely lacking.

Stage II.-SIZE: CL 1.19-1.25 mm. (2 spec.) DESCRIPTION (Figs. 5, a, b, and 6.): The eyes are now free, and the carapace carries a pair of supraorbital spines. Each dorsolateral series of teeth is now divided into one lateral group and one posterior group on a short projection. The telson has added a pair of posterior processes and a pair of median hairs on the dorsal surface. The fifth abdominal somite has a small posterolateral projection on each side, not present in the first stage (see Fig. 6, a). The antennal spine (Fig. 6, c) is now much shorter than in the first stage, being less than 1.5 times the length of the scale. The third maxillipeds (Fig. 6, d) are now functional. Apart from an increase in their armature, the other thoracic appendages are virtually unchanged from the previous stage.

Stage Ill.-SIZE: CL] .50-1.62 mm. (3 spec.) DESCRIPTION (Figs. 5, c, d, and 7.): The sixth abdominal somite is now cut off from the telson and carries a pair of long dorsolateral spines 454 Bulletin of Marine Science [20(2)

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FIGURE 7. Homola barbata, third zoea: a, abdomen; b, detail of posterolateral angle of fifth abdominal segment; c, d, variations in the posterolateral angles of the telson; e, antennule; f, antenna; g, maxillule. and well-developed uropods with setae both on the endopods and the exopods. The telson (Fig. 7, a) is now quite unlike that of the second zoea. Typically it has eight or nine pairs of processes articulated to the posterior margin and a pair of strong, fused spines outside these. The dorsal surface carries one main pair of spines and three smaller pairs. The posterolateral angles are more or less tridentate (Fig. 7, c, d), the anterior of the three points being the outermost of the original series of "dorsal" spines, which is on the anterolateral margin rather than on the dorsal surface (see discussion). The antennule (Fig. 7, e) is now divided into two segments. The antennal endopod is unarmed, and the spine is only slightly longer than the 1970] Rice & Provenzano: Larval Stages of Homola barbata 455

FIGURE 8. Homola barbata, fourth zoea. scale (Fig. 7, f). The rest of the appendages are basically unchanged, but the pereiopods are represented by a pair of unsegmented, unarmed buds. Stage IV.-SIZE: CL 1.83-2.08 mm. (3 spec.)

DESCRIPTION (Figs. 8 and 9.): The original dorsolateral series of carapace spines is now reduced to an anterior group of 9-14 spines and a posterior group of 6-13 spines. The posterolateral series is also considerably reduced, in most cases leaving a stout naked spine at the lower angle, as in the specimen illustrated. In some specimens examined, there were as few as 20 spines in this series, while in others there were as many as 33 spines extending almost to the tip of the major spine. The short dorso- posterior spines have in most cases disappeared in this stage, leaving unarmed, blunt processes on either side of the median process on the posterior margin of the carapace. Again, a few specimens retained spines in this position. 456 Bulletin of Marine Science [20(2)

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FIGURE 9. Homola barbata, fourth zoea: a, telson; a', posterolateral angles of an abnormal telson; b, antennule; c, antenna; d, endopod of second maxilla; e, f, g, first, second, and third maxillipeds, respectively. 1970] Rice & Provenzano: Larval Stages of Homola barbata 457 Both rami of the uropods are now articulated with the protopod. The typical telson (Fig. 9, a) now shows no sign of the fused spine on the posterior margin in the third stage (but see Discussion). In all the specimens examined, the anterior member of the original series of dorsal spines is now greatly enlarged and there is a small spine on the anterolateral margin close to the outer angle. The condition of the other spines of the original series varied considerably; in all cases they were very small, but while some specimens had three pairs still present, others had only one. As in the previous stages, occasional abnormalities of the telson were seen, such as the example shown in Figure 9, a'; here, the outer angles of a single telson are illustrated, the right side being quite typical of the stage, while the left is obviously deformed. Such abnormalities are not rare among reared larvae of hermit crabs (Provenzano, unpublished). The antennule (Fig. 9, b) now shows the beginnings of segmentation of the flagellum and the formation of the statocyst. The antennal spine is now slightly shorter than the scale (Fig. 9, c). The endopod of the maxilla (Fig. 9, d) carries a long lateral seta not seen in the earlier stages. The first pair of pereiopods is present as unarmed, unsegmented buds, and the gills of these and some of the more posterior legs, as yet un- developed, are also present.

Stage V.-SIZE: CL 2.59-2.90 mm. (3 spec.)

DESCRIPTION (Figs. 10, a, b, and 11.): The rows of carapace spines have now completely disappeared. In most cases the posterolateral border of the carapace is smooth, but in a few specimens examined, one or both sides carried a very small tooth. Abdominal somites 2-5 each carry a pair of bilobed pleopod buds de- creasing in size posteriorly. The anterior pair of large spines on the dorsal surface of the telson (Fig. 11, a) is even more prominent-the other dorsal spines being minute. The flagellum of the antennule (Fig. 11, b) is divided into four segments and carries about 15 aesthetascs. The inner flagellum is represented by a small bud. The antennal spine (Fig. 11, c) is now less than half the length of the scale, whereas the endopod has begun to lengthen once more and is armed with a single terminal seta; the endopod shows signs of segmentation in some specimens. In one specimen the mandibles carried very small palps, but there was some doubt as to whether this was a stage V or stage VI zoea; the normal condition seems to be without mandibular palps at stage V. The endopod of the maxilla now has two lateral setae. The endopod of the second maxilliped (Fig. 11, e) now consists of five segments; apparently a subdivision of the subterminal segment of the earlier stages has occurred. The endopod of the third maxilliped (Fig. 11, f) is divided into three segments. 458 Bulletin ot Marine Science [20(2)

I 1.0 mm

FIGURE 10. Homola barbata: a, b, fifth zoea; c, d, sixth zoea.

The pereiopods are all present as unsegmented rudiments, the first pair being definitely chelate. The gill formula appears to be as complete as in the later stages, except that there is no sign of epipodites on the first three legs.

Stage VI.-SIZE: CL 3.27-4.53 mm. (6 spec.)

DESCRIPTION (Figs. 10, c, d, and 12.): The carapace is basically as in the previous stage. The pleopods are better developed than in the fifth stage, but are still unsegmented bilobed buds which increase in length before the next molt. All the dorsal spines on the telson except the large anterior pair and the minute pair near the posterolateral angles have disappeared. 1970] Rice & Provenzano: Larval Stages of Homola barbata 459

a / / ,(--I-r-- .

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1·0mm (a,d,e,f)

O'Smm (b,c)

FIGURE 11. Homola barbata, fifth zoea: a, telson; b, antennule; c, antenna; d, e, f, first, second, and third maxillipeds, respectively.

The flagellum of the antennule (Fig. 12, b) now consists of six or seven segments and carries 20-25 aesthetascs in five or six main groups. The inner flagellum is larger than in the previous stage, but is still unsegmented. The antennal endopod (Fig. 12, c) is about twice as long as the scale and shows the beginnings of four septa. The mandibles now have a pronounced, but unsegmented, palp. The endopod of the maxillule now has three plumose setae on the lateral margin of the proximal segment. The pereiopods are all well developed, showing signs of segmentation and even having spines (see Fig. 12, g). The full larval gill formula of 13 gills and 6 epipodites is now developed. 460 Bulletin of Marine Science [20(2)

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g ~----~-'

c:/

FIGURE 12. Homola barbata, sixth zoea: a, telson; b, antennule; c, antenna; d, e, f, first, second, and third maxillipeds, respectively; g, cheliped. Bar scale represents 2.0 mm for a; 1.0 mm for d, e, f, and g; and 0.5 mm for band c.

Stage VIl.-SIZE: CL 4.9 mm. (1 spec.) DESCRIPTION (Fig. 13.): The carapace is again very similar to that of the previous stage and to that illustrated by Rice (1964). The rami of the pleopods are now articulated with the basal joint, and the exopods carry a few plumose setae and a series of spines around the margin (Fig. 13, i). The outer flagellum of the antennule (Fig. 13, a) now carries about 50 aesthetascs and the inner flagellum consists of three segments. The an- 1970] Rice & Provenzano: Larval Stages of Homola barbata 461

FrGURE 13. Homola barbata, seventh zoea: a, antennule; b, antenna; c, man- dible; d, endopod of maxillule; e, f, g, first, second, and third maxillipeds, respectively; h, second pereiopod; i, pleopod from third abdominal segment. Bar scale represents 2.0 mm for e, f, g, and h; 1.0 mm for a, b, c, and i; and 0.5 mm for d. tennal spine (Fig. 13, b) does not extend beyond the first joint of the endopod, which consists of about 15 segments and is more than twice the length of the scale. The mandibular palp (Fig. 13, c) is now divided into two segments and bears some terminal setae. The endopod of the maxillule (Fig. 13, d) now has four plumose setae on the lateral margin of the proximal segment. The segmentation of the legs is virtually complete, and the dactyls show the beginnings of the armature which they will carry in the megalopa stage (see Fig. 13, h). 462 Bulletin of Marine Science [20(2)

DISCUSSION The only larvae of Homola previously described from the western At- lantic are the terminal zoeae described by Rice (1964). The stage VII larva reared from the egg is very similar in general anatomy to these zoeae, though slightly smaller (eL 4.9 mm, compared with 5.2-5.8 mm), but shows a greater degree of development of some of the appendages. Thus the antennal endopod is relatively rather longer in the reared specimen and the mandibular palp is armed with more setae and is two segmented, whereas in the plankton-caught larvae the palp narrows in the middle, but has no definite septum. The endopod of the second maxilla in the reared specimen has four lateral setae and is divided into two segments, while the illustration of this appendage in the plankton-caught material (Rice, 1964, Fig. 2, e) shows only three lateral setae and no septum. We have examined this material again, and find some indication of a septum, although it is not distinct. In none of the specimens are there more than three lateral setae on the proximal segment of the endopod of the second maxilla, but in one specimen one of these appendages does have a fine seta on the distal segment of the endopod. The segmentation and armature of the endopods of the third maxilliped and the legs are also rather further advanced in the reared specimen. These differences suggest that the terminal reared larva may be an ex- traordinary stage as a result of delayed metamorphosis in unfavorable conditions. However, it is not simply an extra stage added onto the end of a complete normal series, since the stage VI zoea which gave rise to it was much smaller and less well developed than the plankton-caught terminal zoea. Rice & von Levetzow (1967) described a series of five zoeal stages, attributable to Homola, taken in the plankton off South Africa, of which the youngest was obviously a second zoea and the oldest a terminal zoea. The lengths of these larvae formed an exponential series with a mean "growth factor" of 1.56 between successive stages. Gurney (1942) had suggested that a growth factor of 1.5 was the maximum likely to be found between successive larval stages of a single species, and the apparently rather high figure in the South African specimens therefore prompted a survey of published data on decapod larvae to examine the magnitude of growth factors throughout the group. The results of this survey (Rice, 1968) indicated that although growth factors of 1.5-1.6 are unusual they are certainly not unprecedented and do not necessarily indicate the omis- sion of an instar. Since the morphological differences between the South African larvae were also consistent with their being successive stages, Rice & von Levetzow concluded that there were six zoeal stages in the development of that form. 1970] Rice & Provenzano: Larval Stages of Homola barbata 463

10.0

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II III IV V VI VII Zoeal stage

FIGURE 14. Carapace lengths of successive larval stages of Homola barbata plotted on a logarithmic scale. Data from reared specimens (crosses) and from plankton-caught material (circles), the latter from Rice & von Levetzow (1967).

The measurements obtained from the reared larvae do not form as good an exponential series as the plankton-caught specimens (see Fig. 14). Al- though the figures for the reared larvae are based on measurements of a greater number of specimens, it is impossible to make accurate measurements of molted exuviae, and the animals used were therefore individuals which had failed to molt into the next successive stage and were possibly not normal. The plankton-caught animals, On the other hand, were pre- sumably healthy and normal. Nevertheless, the dimensions of the reared larvae are fairly close to an exponential series with an average growth factor between stages of about ].37, that is, considerably less than that for the South African larvae. As noted above, the oldest reared zoe a was slightly smaller than the last zoea taken in the plankton in the Florida Current, and it may be that under more favorable conditions a slightly higher growth factor would have produced a larger last zoea after fewer molts. The second, third, fourth, and seventh reared zoeae correspond fairly closely in their general degree of development with the supposed second, third, fourth, and sixth stages from the South African plankton. The fifth stage from South Africa, On the other hand, is in several respects 464 Bulletin ot Marine Science [20(2) intermediate between the fifth and sixth reared stages; this suggests that unfavorable conditions occurred in the laboratory, and that the two stages would have been replaced by a single stage in the sea. A possibly significant feature, apparently unique to larvae of Homola, is the early appearance of setation on the uropodal endopod. Rice & von Levetzow (1967) found it in their South African larvae, and we have found it again in this study. Total Duration ot Development.-The specimen which molted into the seventh stage did so on the 67th day after hatching. Judging from the durations of the previous stages, it would probably have been at least a further two weeks before this zoea molted to the megalopa, making the total duration of the zoeal stages under these conditions over eleven weeks. One megalopa caught in the plankton of the Florida Current lived at 20CC for 27 days in the laboratory before molting, so that the total time taken to complete metamorphosis at this temperature is probably not less than 15 weeks. Variations among the Larvae and Adults Attributed to Homola barbata.- The suggestion that there might be more than one species or subspecies known as Homola barbata first was made by Rice (1964). When Rice & von Levetzow (1967) described the series of larvae of Homola from the South African plankton, they were able to compare their specimens only with a few zoeal stages previously described from other parts of the world and attributed to the genus. Since they had no stage I larva, the only early zoea directly comparable with their own was the stage II from Naples described by Pike & Williamson (1960). These larvae differed only in very minor points, except that, whereas the row of teeth dorsally on the carapace was complete in the South African specimens, it is interrupted in the Mediterranean form. For the later stages, however, in addition to the terminal zoea from the Florida Current described by Rice (1964), there were descriptions available (albeit rather inadequate) of zoeae attributed to Homola from the Mediterranean (by Cano, 1893, and Thiele, 1905) and from South Africa (by Boas, 1880). Rice & von Levetzow concluded that the described larvae fell into three distinct groups; one of these groups included their own South African larvae and those described from the Mediterranean, the Floridian larvae formed a second type, and Boas's South African larvae yet a third. Now that a complete zoeal series from the western Atlantic has been described, these groupings still seem valid. A number of the distinctions between the larvae, such as the armature of the maxillipeds, uropods, and telson and the timing of the disappearance of the carapacial rows of teeth, are probably related to the rate of development. Other differences, such 1970J Rice & Provenzano: Larval Stages of Homola barbata 465 as the tendency for the dorsal spines on the carapace and abdomen to be shorter and less acute in the western Atlantic larvae than in the others, are rather difficult to quantify. However, in addition to these, there are a number of easily observed qualitative distinctions which are summarized in Table 3. Where comparisons are possible, the first three larval stages are all very similar, but the later stages differ in several features that are certainly clear enough to suggest a specific distinction in a genus in which the adults of the described species are separated on seemingly quite trivial characters. One of us (ALR) has examined small numbers of postlarval specimens identified as Homola barbata from the eastern and western North Atlantic, the Mediterranean, off South Africa, and off Rio de Janeiro, but has been unable to find consistent differences between specimens from different lo- calities. Although the samples examined are far too small to allow mean- ingful conclusions, there is at least an indication that the species grows considerably larger and matures later on the eastern side of the Atlantic than on the western side. Thus, there is a preponderance of specimens over 20.0 mm in carapace length amongst those examined from the Medi- terranean, the East Atlantic, and South Africa, including two berried females 25.0 mm and 36.0 mm CL, respectively. On the other hand, the largest specimen from the western Atlantic known to us is a male with a carapace length of 26.2 mm taken in the Yucatan Channel (in the collec- tion of the Rosenstiel School of Marine and Atmospheric Sciences), while the largest ovigerous female is one with a carapace length of 22.0 mm from Martha's Vineyard, Massachusetts (USNM 7301). Ovigerous females with carapace lengths as low as 10.3 mm have been taken in the Carib- bean region, and, since the first crab stage may have a carapace length of 9.0 mm (Rice, 1964), these animals are obviously very young. The large males from all parts of the species range show the great development of the chelipeds that is common in Brachyura, but in addition to this sexual allometry there are other differences between the large and small representatives of both sexes. Thus, with increasing overall size, the eyes become smaller relative to the carapace length, and the branchial and cervical carapacial grooves become more pronounced. Consequently, the ovigerous females examined do differ, those from the western Atlantic ex- hibiting a number of juvenile characters as compared with the much larger individuals from the east (see Fig. 15), perhaps indicating that they rep- resent a somewhat neotenous form. The molt of puberty obviously occurs very early in the western Atlantic animals, but small females are so poorly represented in the collections which have been examined from the eastern Atlantic and the Mediterranean that it is not possible to say whether it occurs later in these areas. Regardless of whether further studies on the adults reveal additional 466 Bulletin of Marine Science [20(2)

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FIGURE 15. Homola barbata: a, carapace of female from which the larvae described in this paper were obtained (carapace length 12.0 mm); b, carapace of ovigerous female from off Cadaques, Spain (BMNH, 1954.11.4.181), carapace length 37.4 mm. The larger specimen has all over the carapace a fine tomentum, which is not shown in the illustration. differences between the populations in different areas, the problem as far as the larval stages are concerned certainly warrants further work. Assum- ing that rearings of larvae from females from widely separated parts of the reported range confirm the variations indicated so far, a second approach should be to rear the larvae under a variety of environmental conditions, to determine whether the differences are due simply to the direct effect of the environment on a single pool of genes, or are reflections of estab- lished genotypic differences. The long estimated larval life would allow gene flow between adult populations great distances apart. (In 15 weeks, larvae could travel at least 1,000 miles across the North Atlantic, if Schel- tema's [1966] estimate of a mean velocity of 0.4 knots for the Gulf Stream is correct.) Nevertheless, even if such interchange takes place within the North Atlantic, it is quite possible that the populations in the Mediterranean and off the South African coast are effectively isolated from one another and also from the North Atlantic population. In such circumstances, genetic divergence is not only possible but to be expected, and the con- servatism of such widely distributed species is, perhaps, more worthy of comment than is their variability. The Development of the Telson.-In the above discussion, the term "dorsal telson spine" has been used to include those on the anterolateral margins, but there is reason to believe that these do not belong to the same series as the other dorsal spines. The first description of the telson of an early larva of Homola was that of Gurney (1924). He illustrated 468 Bulletin of Marine Science [20(2) a telson with five pairs of long, plumose articulated processes, a pair of unarmed articulated spines, and small acute outer angles. Gurney interpreted the naked spines as being the true second processes, and the small spines outside these as being the true first processes. In fact, the telson of Gurney's specimen is very similar to that illustrated by Pike & William- son (1960), the unarmed outer spine not being articulated to the telson itself. These authors interpreted the outer spine as being the first telsonal process and suggested that either the second or third process was entirely lacking. Pike & Williamson also stated that "there are also dorsal spines on the telson corresponding in number to the posterior processes," ob~ viously including in this "dorsal spine" category the outermost very small spines which are on the anterolateral margins rather than on the dorsal surface. Amongst the series of larvae described by Rice & von Levetzow, the telson of the third stage seemed something of an anomaly, because of the appearance of a pair of strong unarmed spines on the posterior margin; there seemed to be no sign of these spines in either the previous or sub- sequent stages. This feature prompted Rice & von Levetzow to suggest that these stage III larvae might belong to a different species from the other stages described. However, a similar condition occurs in the reared larvae described here, in which the third zoeae also have a fused spine on the posterior telsonal margin. This spine apparently disappears at the next molt. Fortunately, one second zoea died shortly before it would have molted, and the struc- ture of the future telson is visible within the old one (Fig. 6, e). This shows that the fused spine in the third stage is developed from the second plumose process of the second zoea, the outer plumose process being reduced to a very small spine. If this process of reduction in the posterolateral parts of the telson continues at the next molt, it is possible that, far from disappearing, the fused spine of the third zoea "takes over" as the outer angle of the telson. These fused spines are developed from the posterior processes which had three pairs of similar processes between them in the first stage; that is, they are the true fourth telsonal processes which are often enlarged in the later stages of "anomuran" larvae and form the main forks of the typical brachyuran telson. The first three processes may therefore be represented by the three points outside these large fused spines in the third zoea, which are in tum developed from the small spine on the anterolateral margin, the posterolateral angle itself, and the outermost articulated process in the first two zoeal stages. This interpretation thus agrees with that of Gurney, despite his erroneous illustration, but not with that of Pike & Williamson. Relationships of the Homolidae.-Williamson (1965) summarized the larval characters of the Homolidae as far as they were known at that time 1970] Rice & Provenzano: Larval Stages of Homola barbata 469 and compared them with typical anomuran and brachyuran larvae. While the homolid larvae resemble the Anomura (as exemplified by the Pa- guridea and the Galatheidea) in most of the characters examined, a number of features, particularly the nature of the second telsonal process and the length of the antennal spine, clearly ally them to the Brachyura rather than to the Anomura or to the Dromiidea with which they were grouped for a long time. The larvae of the Homolidae are generally at an evolutionary level comparable to that of the Paguridea and the Galatheidea and are much more advanced than the larvae of the Dromiidea. The only feature which Williamson found to be at variance with this conclusion was the presence of exopods on the first three legs of the last zoea of Homola reported by Rice (1964). This would indicate a much more primitive condition than ih either the Brachyura or the typical Anomura, but a re-examination of the Homola material revealed that the structures had been misidentified and are in fact epipods (see Rice & von Levetzow, 1967). Williamson suggested that the anomuran features of the homolid larvae have arisen independently of the Anomura by parallel evolution. He further suggested that the same might be true of the Raninidae, whose larvae are predominantly brachyuran but show a number of affinities with the Homolidae and conveniently bridge the gap between the homolids and the Brachygnatha. Since Williamson presented these views, our knowledge of the larval development of both the Raninidae and the Homolidae has improved (see Knight, 1968, and Rice & von Levetzow, 1967). Although this more recent work necessitates some slight changes in the summaries of the larval characters of the families given by Williamson, his main arguments of affinity between the Homolidae, the Raninidae, and the Brachygnatha on the one hand, and their distinction from the Dromiidea, Paguridea, and Galatheidea are, if anything, somewhat strengthened. Apart from the possession of both typical anomuran and brachyuran characters, Williamson pointed out that the larvae of the Homolidae and of the Raninidae have dorsal telsonal spines which are not found in any other family. In this context, it is interesting to find that the long plumose seta on the lateral margin of the endopod of the second maxilla in Homola (replaced by several setae in the late zoeae) is also found in Raninoides benedicti Rathbun (see Knight, 1968, figs. 33 and 34), but does not appear to be present in any other described larvae. The absence of this seta in Lyreidus tridentatus de Haan, the only other raninid of which the complete development is known, indicates that it may not be common, even within this family. Homolid and raninid larvae also resemble one another in lacking the long plumose setae on the lateral margins of the endopods of the first two 470 Bulletin of Marine Science [20(2) maxilJipeds, which are developed in the late zoeal stages of the Dromiidea and all known Anomura. These setae are also absent from all the higher brachyurans so far described, except for some grapsids, where they are much shorter than in the Anomura and may not be strictly homologous. Thus, although knowledge of the larva] development of the Homo]idae is still very restricted, the phylogenetic evidence it provides strongly suggests that the family is close to the line of descent of the true crabs and is well separated from both the typical Anomura and the much more primitive Dromiidea. SUMMARY The zoeal stages of Homola barbata reared from a berried female taken in the Yucatan Channel are described. Seven zoea] stages were obtained in the laboratory, the last of these corresponding to the meta zoea previous]y described from the plankton. This is the first complete zoeal series known for an homolid reared in the laboratory. The larvae of Homola appear to be unique among decapods in having the uropodal endopod setae in the third zoea] stage. Larvae and adults of "Homola barbata" from various geographical areas were compared. Variations amongst the larvae are not reflected in similar variations amongst the adults examined, although there is an indication that a somewhat neotenous, though not necessarily taxonomically distinct, form exists in some areas. The views of Williamson (1965) on the relationships of the Homolidae, based on studies of larvae, have been confirmed by more recent work including that reported in the present paper. The Homolidae appear to be related to the Raninidae and are close to the line of descent of the true crabs, but the family Homolidae is well separated from the much more primitive Dromiidea and from typical Anomura.

SUMARIO

ESTADOS LARVALES DE Homola barbata (FABRICIUS) (CRUSTACEA, DECAPODA, HOMOLIDAE) OBTENIDOS EN LABORATORIO Se describen los estados de zoea de Homola barbata obtenidos de una hembra fresada cogida en el Canal de Yucatan. Siete estados de zoea fueron ]ogrados en el laboratorio, e] ultimo de estos corresponde a la metazoea procedente de] p]ancton que ha sido descrita con anterioridad. Esta es la primer serie completa conocida de zoeas correspondientes a un hom6lido criado en laboratorio. Las larvas de Homola parecen ser las unicas entre los decapodos que, en la tercer zoea, tienen setoso el endo- podito del ur6podo. Se compararon las larvas y los adu]tos de "Homola barbata" proce- dentes de varias areas geograficas. Las variaciones entre las larvas no se 1970] Rice & Provenzano: Larval Stages of Homola barbata 471 reflejan en variaciones similares entre los adultos examinados, aunque hay indicaci6n de que una forma algo neotenica, aunque no necesariamente distinta taxon6micamente hablando, existe en algunas areas. Los puntos de vista de Williamson (1965) en cuanto a las relaciones de los Homolidae, basad os en estudios de las larvas, han sido confirmados por trabajos mas recientes incluyendo el presente. Los Homolidae parecen estar relacionados con los Raninidae y estan pr6ximos a la linea de des- cendencia de los verdaderos cangrejos, pero la familia Homolidae esta bien separada de la mucho mas primitiva Dromiidea y de los Anomura t1picos. LITERATURE CITED BOAS, J. E. V. 1880. Studier over Decapodernes Slaegtskabsforhold. K. danske Vidensk. Selsk. Skr., Ser. 6, 1(2): 25-210. CANO, G. 1893. Svillupo dei Dromidei. Atti Acad. Sci. fis. mat., Napoli, 6(2): 1-23. GURNEY, R. 1924. Crustacea. Part IX. Decapod larvae. Nat. Hist. Rep. Br. Antarct. Terra Nova Exped. (Zoo1.), 8: 37-202. 1942. Larvae of decapod Crustacea. Ray Society, London, 306 pp. KNIGHT, M. D. 1968. The larval development of Raninoides benedicti Rathbun (Brachyura, Raninidae), with notes on the Pacific records of Raninoides laevis (LatreilIe). Crustaceana, Suppl. 2: 145-169. PIKE, R. B. AND D. 1. WILLIAMSON 1960. Larvae of decapod Crustacea of the families Dromiidae and Homo- lidae from the Bay of Naples. Pubbl. Staz. zool. Napoli, 31: 553- 563. RICE, A. L. 1964. The metamorphosis of a species of Homola (Crustacea, Decapoda: Dromiacea). Bull. mar. Sci. Gulf & Carib., 14: 221-238. 1968. Growth 'rules' and the larvae of decapod crustaceans. J. nat. Hist., 2: 525-530. RICE, A. L. AND K. G. VON LEVETZOW 1967. Larvae of Homola (Crustacea: Dromiacea) from South Africa. J. nat. Hist., 1: 435-453. RICE, A. L. AND A. J. PROVENZANO 1964. The larval stages of Pagurus marshi Benedict (Decapoda, Anomura) reared in the laboratory. Crustaceana, 7: 217-235. SCHEL TEMA, R. S. 1966. Evidence for trans-Atlantic transport of gastropod larvae belonging to the genus Cymatium. Deep-Sea Res., 13: 83-95. THIELE, J. 1905. Uber einige steiHiugige Krebse von Messina. Zool. Jb., Suppl. 8 (Festchr. F. Mobius): 443-474. WILLIAMSON, D. J. 1965. Some larval stages of three Australian crabs belonging to the families Homolidae and Raninidae, and observations on the affinities of these families (Crustacea: Decapoda). Aus!. J. mar. Freshwat. Res., 16: 369-398.