Juvenile Ontogeny and Metamorphosis in the Most Primitive Living Sessile Barnacle, Neoverruca, from Abyssal Hydrothermal Springs

BULLETIN OF MARINE SCIENCE, 45(2): 467-477. 1989

JUVENILE ONTOGENY AND METAMORPHOSIS IN THE MOST PRIMITIVE LIVING SESSILE BARNACLE, NEOVERRUCA, FROM ABYSSAL HYDROTHERMAL SPRINGS

William A. Newman

ABSTRACT Neoverruca brachylepadoformis Newman recently described from abyssal hydrothermal springs at 3600 m in the Mariana Trough, has the basic organization of the most primitive sessile barnacles, the extinct Brachylepadomorpha (Jurassic-Miocene). However, a subtle asymmetry diagnostic of the Verrucomorpha (Cretaceous-Recent) is superimposed on this plan, and it is evident that Neoverruca also represents a very primitive verrucomorphan. A median latus, unpredicted in such a form, occurs on one side as part of the operculum, and the outermost whorl of basal imbricating plates is the oldest, rather than the youngest as in the primitive balanomorphans, Catophragmus s.1.and Chionelasmus and as inferred in Bra- chylepas. Neoverruca is further distinguished from higher sessile barnacles in passing through a number of well developed pedunculate stages before undergoing an abrupt metamorphosis into the sessile mode. Theses unpredicted ontogenetic events in the life history of an early sessile barnacle indicate that the transitory pedunculate stage of higher sessile barnacles, first noted in Semibalanus balanoides by Darwin, reflects the compression ofpedunculatejuvenile stages into a single stage, rather than simply a vestigial reminiscence of their pedunculate ancestry. From these observations it is evident that the transition from a pedunculate to a sessile way of life was evolutionarily more complicated than previously understood, and this has a significant bearing on our understanding of the paleoecology as well as the evolution of sessile barnacles.

Abyssal hydrothermal vents have yielded two remarkable endemic barnacles, Neolepas zevinae Newman (1979) from approximately 2600 m, at 13° and 21°N on the East Pacific Rise, and Neoverruca brachylepadoformis in Newman and Hessler, 1989 from approximately 3600 m in the Mariana Trough in the western Pacific. The closest ancestors of Neolepas and Neoverruca, first appearing in the fossil record in the Mesozoic, have long been extinct and therefore Neolepas and Neoverruca are considered relics of Mesozoic age (Newman 1979; 1985; Newman and Hessler, 1989). McLean (1981, 1985) independently reached the same conclusion concerning some hydrothermal vent gastropod mollusks. The capitular organization of Neolepas represents an early stage in the evolution of scalpellomorphan pedunculate barnacles; a stage intermediate between that of the simpler but extinct eolepadines and the more complexly armored pollicipedines (Buckeridge, 1979). The latter subfamily, represented today by Scillaelepas, Pollicipes and Capitulum, includes the inferred Mesozoic ancestor of all sessile barnacles (Brachylepadomorpha, Verrucomorpha and Balanomorpha; Newman, 1987, fig. 10E). Neoverruca is, in many ways, much more remarkable than Neolepas. It represents the most primitive living sessile barnacle, and if there were no verrucomorphans, it would be classified as a slightly aberrant brachylepadomorphan. Indeed, as the sole surviving member of that radiation, it is a "living fossil." On the other hand, in light of the verrucomorphans, it constitutes the "missing link" between them and the extinct Brachylepadomorpha. Furthermore, some wholly unanticipated facets of the juvenile ontogeny, to be described below, further distinguish Neoverruca from other living sessile barnacles. These facets not only

467 468 BULLETIN OF MARINE SCIENCE, VOL. 45, NO.2, 1989 require a reevaluation of our current understanding of metamorphosis in sessile barnacles, but our views concerning the evolution of sessility itself.

JUVENILE ONTOGENY AND METAMORPHOSIS Neoverruca apparently passes through six or more pedunculate juvenile stages, but only a few were found associated with adults during the present study; several earlier and intermediate pedunculate stages are obviously missing from the sequence presented here (Fig. I; see caption for symbols used to identify plates in the text). The pedunculate mode involves substantial growth as well as morphological development and, therefore, must persist for a number of days before the abrupt metamorphosis into the sessile mode occurs. The earliest pedunculate stages observed are bilaterally symmetrical and similar in appearance to those of pollicipedine scalpellomorphans, including well developed cirri by which they are apparently capable of feeding. Unfortunately, the youngest pedunculate juvenile stage known is not the first, but since it is bilaterally symmetrical (Fig. lA-B), younger ones must have been also. It has the usual five chitinous, primordial valves (S-T -C). However, as will be described, the median latus (L) is not the next plate to appear; rather, it appears heterochronously after several other calcareous plates, and then only on one side (Fig. 1D, F, H etc.). Thus there is no true Neolepas-stage (R-S-L-T-C, but see below) in Neoverruca, as there is in the pollicipedines and as was inferred in the early ontogeny of a brachylepadomorphan (Newman, 1987, fig. 9A). Further "irregularities" in the ordering of plates are observed in the early ontogeny of Neoverruca, but before proceeding it should be noted that all plates are designated "capitular," none "peduncular," for the reasons to be enumerated shortly. An explanation is necessary because the capitular plates of scalpellomorphans, beyond the original five (S-T -C), are inferred to have been acquired phy- logenetically by transfer from the peduncle (Newman, 1982; 1987:35), and that such transfers occur ontogenetically was demonstrated by the development of subrostra in a species of Scillaelepas (Newman, 1980; fig. 11E, 0). These observations could be relevant to the pedunculate stages of Neoverruca, but as it turns out they are not. The criteria applied in designating all plates of Neoverruca "capitular" stem simply from taking the ontogeny of the animal at face value (Fig. 1): 1)the division between the peduncle and capitulum in the pedunculate stages is well defined and the plates are wholly capitular in position, 2) the peduncle of all pedunculate stages remains naked, 3) the appearance ofL after 11indicates that the latter was capitular before the heterochrony developed, and 4) the appearance ofthe subsequent three whorls within the basic ring (Fig. 2), and then after the metamorphosis into the sessile mode, indicates that they are presently capitular, as they probably were before the positional anomaly was acquired. The naked peduncle is generally moderately short (Fig. lA-B and C-D), but when a cyprid larva settles in a deep crevice, the peduncle of the ensuing juvenile can be relatively long (Fig. IE-F). The capitular plates are deployed in two whorls (Fig. lA-B); the first, R-S-T-C, is normal, but the second is incomplete; sr-RL- "L," but no CL-sc. The first pair of latera to appear would appear to represent L. However, as shown below, it actually represents 11.The appearance of 11before L is heterochronous compared to pollicipedine, balanomorphan and presumably brachylepadomorphan ontogenies. In the next stage of two, CL appears on one side before it appears on the other (Fig. 10 vs. C and F vs. E), and this is the first sign of the developing asymmetry. L,

A-J

Figure 1. Ontogeny and metamorphosis in Neoverruca brachylepadoformis Newman: A-F, three pedunculate and G-L, four sessile ontogenetic stages. For ease of comparison both sides of an individual are illustrated as right sides. All individuals are from between crowded adults and therefore will bend over, or are bent over to the side that becomes the FS-Fr side. Notable features: I) the first stage illustrated is bilaterally symmetrical, 2) the second stage is becoming bilaterally asymmetrical in the number and arrangement of plates, 3) L appears after 1', 4) S and T become functionally FS-Fr, and MS-MT upon the acquisition of sessility, 5) transition from pedunculate to sessile (E-F to G-H) is highly metamorphic and, following acquisition of sessility, 6) RL and CL of the movable side join (albeit temporarily) before Rand C, 7) the subsequent three whorls of imbricating plates appear inside rather than outside the primary basal whorl, making the latter the outermost whorl, and 8) plates of the outcrmost whorl, especially I', sr and sc, become deciduous. From the cyprid to the first sessile stage apparently takes several days. (C, carina; c, imbricating plate carinad of L tier; CL, carinolatus; c1, imbricating plate in CL tier; FS, fixed scutum; Fr, fixed tergum; L, median latus; I, imbricating plate in L tier; MS, movable scutum; MT, movable tergum; R, rostrum; r, imbricating plate rostrad of L tier; RL, rostrolatus; rl, imbricating plate in RL tier; S, scutum; sc, subcarina; sr, subrostrum; T, tergum. Scale bars = I mm.) 470 BULLETIN OF MARINE SCIENCE, VOL. 45, NO.2, 1989

The precocious side, marked by the appearance of CL (Fig. 1D, F etc.), is further distinguished by the appearance of L between the median basal angles of Sand T. Therefore, the precocious side is destined to be the relatively "normal," movable side; namely, that supporting MS-L-MT. While L is a relatively important plate in juveniles, its development becomes retarded in older individuals, and it is vestigial or even lost in old individuals (Newman and Hessler, 1989). The loss of normality on the movable side involves the meeting of the lateral margins of Rand C, but the meeting is preceded by the transient meeting of RL and CL (Fig. IH, J). On the opposite side L fails to appear; the basal margins of Sand T are relatively wide and remain between Rand C where they eventually become immovably "fixed" (FS-FT). These deletions and readjustments are con- cerned more with the developing, fundamental, verrucomorphan apomorphies than with the impending metamorphosis from the pedunculate to the sessile mode per se. The complete second or basal whorl consists of 8 plates (sr-RL-P-CL-sc; Fig. 2), and with its completion the last pedunculate stage is ready to undergo an abrupt metamorphosis into the first sessile stage (Fig. IE-F to G-H; N.H., I I is often lost on movable side, as in Fig. 1H and J or as nearly so in Fig. IL). As the figures show, the metamorphosis involves contractile, muscle-like fibers; these apparently draw the peduncle into the basal portion of the capitulum concomitant with a marked increase in the diameter of the basal whorl, as has been described in Semibalanus balanoides (Walley, 1969). The membranous basis so formed becomes cemented to the substratum in the process, and a basal rudiment of the peduncle may be seen cemented beneath it (Fig. 11). A plan view of the basic organization of the last pedunculate or first sessile form (somewhat earlier than the stage depicted in Fig. IG-H) is diagrammed in Figure 2. The lateral margins of Rand C on the movable side are still separated in the early sessile stages (Fig. 1H, J, K), as is the case in adult brachylepadomorphans. Except for the omission of an L, this arrangement is somewhat com- parable to the capitulum of Capitulum or, if the substitutions are ignored, identical to that of Scillaelepas s.1.;indeed, the arrangement is intermediate between their two morphologies. In older juveniles and the adult of Neoverruca, Rand C will eventually join on one side. But the eventual union of Rand C is heralded by the joining ofRL and CL (Fig. IH, J), a transient reminiscence probably indicative of the more primitive condition in the urverrucomorphan. In Neoverruca, development of individual plates of the outermost (oldest) basal whorl lags with growth so that, as Rand C expand and join, RL and CL become proportionately smaller and eventually become separated again (Fig. IH, J vs. K, L). Following metamorphosis into the sessile mode, modifications to the wall involve the addition of accessory whorls of plates. In individuals that settle and develop in narrow confines, such as between closely spaced adults, most are added to the precocious MS-L-MT side. When confined, juveniles of most pedunculate barnacles can simply bend over on one side, by muscular action and/or growth, thus enabling their cirri to extend outward rather than against the adjacent substratum. Likewise, the early pedunculate juvenile stages of Neoverruca can lie over on one side when confined, and thereby extend their cirri outward. But the pedunculate mode changes to the sessile mode; for the cirri to remain directed outward when confined, the shell wall cannot remain symmetrical. In fact, the asymmetry that began in the pedunculate stage is oriented with the retarded or incipient "fixed" side toward the substratum. Thus, fixation of the right or left side apparently depends on which side of the pedunculate capitulum is initially closest to the substratum. NEWMAN: JUVENILE ONTOGENY AND METAMORPHOSIS IN NEOVERRUCA 471

MOVABLE SIDE jRL-11_CL, / /MS-L- MT" " ROSTRAL sr R C sc CARINAL END "'''FS-FT~/ END RL- 11-CL FIXED SIDE Figure 2. Plan view of the first and second whorls of capitular plates in Neoverruca brachy/epadofor- mis Newman, prior to or immediately following metamorphosis from the last pedunculate to the first sessile juvenile stage (Fig. IE-F, G-H). In the formation of the 8-plated primary or basal whorl, I"s come to occupy the position primitively occupied by L's, and sr and sc are substituted for Rand C respectively. (Fig. I for explan. of symbols.)

The continued development of asymmetry in sessile juveniles under confined conditions includes 1)changes in the proportions of the plates, and 2) suppression of growth on the fixed side concomitant with 3) the addition and growth of accessory plates on the movable side. The sessile juveniles illustrated here (Fig. IG-H, I-J, K, L) all came from between crowded adults and are, therefore, moderately bent over. In unconfined individuals, the sagittal plane of the sessile shell grows vertically rather than bent over, and the imbricating, accessory plates develop nearly equally on both sides. Nonetheless, although the ensuing adult looks like a brachylepadomorphan, the symmetrical appearance is superficial; the movable/fixed arrangement still de- velops, with L deleted on the fixed side and Rand C meeting on the movable side. The arrangement of plates in tiers is the same in Neoverruca and Brachylepas, and there can be little doubt that the RL-L-CL tiers represent a homologous series in these two genera. However, the order in which the whorls are added in Neo- verruca, and which therefore is also likely the order in Brachylepas, was entirely unexpected, since it is dramatically different than in pollicipedine scalpellomorphans, in the balanomorphans (Chionelasmus and Catophragmus, and as here- tofore inferred in brachylepadomorphans in general (Newman, 1987). Namely, they are added inside rather than outside the second whorl (Fig. 2)! Therefore, the L tier has 14 inner and uppermost rather than outer and lowermost (Fig. IL). It follows that the outermost whorls are the oldest rather than the youngest, and that the relatively small size of some of the individual plates, such as I', is the result of arrested growth rather than youth. It is also likely that this is the case in Brachylepas. However, in contrast to other sessile barnacles having basal whorls of plates, including brachylepadomorphs as presently known, in Neoverruca the outermost plates are deciduous. This explains the absence OflI in some individuals (Fig. IH, J), or its near separation from the wall (Fig. IL), and the absence of sr (Fig. 1K, L) and sc (Fig. IL). While ontogenetic reductions in size and/or changes in shape of plates are known, deciduous plates are unknown in pedunculate and 472 BULLETIN OF MARINE SCIENCE, VOL. 45, NO.2, 1989 in other sessile barnacles. The existence of imbricating basal whorls with marginal plates that are deciduous as well as retarded in growth makes it easier to understand how the complex wall of Neoverruca could be transformed into that of Verruca; indeed, the extinct eoverrucids (Newman and Hessler, 1989) represent one of the intermediate morphologies in the reduction process.

DISCUSSION Darwin (1854: 130) noted that during cyprid metamorphosis in Semibalanus balanoides, I the young barnacle "may be said to be pedunculated," and the condition was subsequently recognized in this species by Runnstrom (1925) and Stubbings (1975), and in Verruca stroemia by Runnstrom (1926; Fig. 3H-K, A- D respectively, herein). These pedunculate stages are similar to the extent that each has a capitulum, provided with a few unca1cified plates, supported by a globular peduncle attached by a little disc of cement, presumably around the point where the cyprid larva's first antennae initially attached to the substratum. Walley (1969) observed that there were longitudinal contractile elements in this globular region in S. balanoides, and she noted that they were involved in the process leading to the fully sessile juvenile, but she didn't recognize them or the region as "pedunculate." In contrast to the apparently lengthy pedunculate series in Neoverruca, assumption of sessility in S. balanoides, beginning with the cyprid metamorphosis and ending with the sessile juvenile, takes only 24 h to complete (Walley, 1969). Bernard and Lane (1962) described what superficially might appear to be some unreconcilable differences in cyprid metamorphosis between Balanus amphitrite and Semibalanus balanoides (Fig. 3M-Q, G-K respectively). In the former, a nearly amorphous blob, rather than a "pedunculated" stage with chitinous capitular plates, forms within the cyprid shell. When the cyprid shell, thoracic cuticle and compound eyes are cast, the plateless blob remains attached to the substratum by a stalk and a dab of cement. This stage then draws down and assumes the conical form of a juvenile sessile barnacle before it adds the first of the capitular plates, the chitinous opercular valves (S-T), all within 4 to 6 h after settling. These findings were pretty much ignored by Walley (1969),2 but had Darwin's (1854) "pedunculate" stage been recognized as such, the plateless, stalked stage in Balanus amphitrite might have been seen for what it apparently is; namely, the much reduced pedunculate stage of more primitive forms such as Semibalanus balanoides and Verruca (Fig. 3A-D).

I Semibalanu.s balanoides is still referred 10 as Ba/anus balanoides, as a matter of "persona) preference," by some authors (Walker et aI., 1987). However, the generic status of a species is not arbitrary, it is a matter of science. The morphological criteria used in establishing genera provide first-order approximations of the genetic distance between taxa above the species level. Thus, the species of Semibalanlls are morphologically more closely related to eaeh other than to speeies of Balanus, and this faet needs to be taken into consideration in comparative studies. Furthermore, genera may be assigned to different families, and familial differences are further data on genetic distance as well as the direction of evolution in the relationship. In the present case, Semibalanus belongs to the Archaeobalanidae rather than the Balanidae, because its members are deemed morphologically more primitive than those of Balanus. Indeed, if the ontogenetie observations of Bernard and Lane (1962) on a species of Balanus are as substantively correct as they appear at face value, they add significantly to the genetic distance and to the phylogenetic ordering of the genera, and hence the families, involved here (Table I and footnote 2). , The low eredibility that apparently has been attributed to the ontogenetic work of Bernard and Lane (1962) was probably aggravated by a number of anatomical irregularities or misinterpretations on their pan; namely, I) a professed different relationship between the eompound eyes and the rest of the body as compared to other erustaceans, 2) retention of degenerated eompound eyes in the larva (normally shed with the cyprid shell or carapace, as they illustrate, Fig. 3 M herein), 3) uneritically evaluated eircumstantial evidence for suggesting that the eyprid may be able to feed, 4) attribution of functions to "ciliated" somatic cells (unknown in euanhropods), 5) "decortication" of the larva (unprecedented at the time) and, perhaps, 6) uncertainty among others as to what species was actually being worked on (Balanus amphitrite nil/eus. = B. venustur; B. amphitrite amphitrite = B. amphitrite s.s.; or possibly another member of the complex, B. reticliialus; Henry and McLaughlin, 1975). NEWMAN: JUVENILE ONTOGENY AND METAMORPHOSIS IN NEOVERRUCA 473

Table I. Summary of anamorphic and metamorphic changes involved in the ontogenetic (horizonal) and phylogenetic (vertical) acquisition and perfection of sessility. The ontogenetic process is inferred to have changed from anamorphic [ ] in urbrachylepadomorphans to metamorphic ( ), as seen in Neoverruca. In higher forms, beginning with Verruca, pedunculate juvenile stages are all but eliminated, primordial valves are lost as in Semibalanus and, ultimately, the ontogenetic acquisition of plates is delayed until sessility is established, as in Balanus (Fig. 3). The result of the subsequent compression of the metamorphic sequence includes not only the deletion of the presumably more vulnerable pedunculate stages from the ontogenetic series, but an absolute reduction in the time required from the freshly settled cyprid to first sessile juvenile, from a matter of days to one of hours. (N umber of stages, except where specifically known, arbitrary; p-, pedunculate juvenile with capitulum supporting the fundamental five chitinous primordial valves and a naked peduncle; P-, calcification and completion of principal capitular armament; Pp, advent of peduncular armament; PP, fully armored pedunculate form; sp, retardation of peduncular growth relative to capitulum and assumption of quasi-sessility; 8-, peduncle and its vestigial armament overgrown by basal perimeter of capitulum; Ss, contact of basal margin of capitulum with substratum and burial of peduncular rudiments in membranous basis; SS, consummation ofsessility (cementation of basal capitular margin to the substratum; (P-/Ss), metamorphosis oflast pedunculate juvenile with well developed, calcified capitular plates and naked peduncle to sessile mode (Fig. I); (p-/Ss), metamorphosis of transient pedunculate stage with primordial valves, rudimentary calcified plates and naked peduncle to sessile mode (Fig. 3, A-F); (x-ISs), metamorphosis of transient pedunculate stage with chitinous valves and plates to sessile mode (Fig. 3, G-L); (y-/ss), metamorphosis of plate less pedunculate stage into plateless sessile mode followed by appearance of chitinous valves etc. (Fig. 3, M-Q)

Stages

4 6 9 Etc. Pollicipedine p- P- P- P- Pp PP pp pp pp pp U rbrachylepadomorphan p- p- P- [p- Pp sp S- Ss SS] SS Neoverruca p- p- P- [(P-/Ss)SS] SS SS SS SS Verruca (p-/Ss) SS SS SS SS SS SS SS SS Semibalanus (x-ISs) SS SS SS SS SS SS SS SS Balanus (y-/ss) SS SS SS SS SS SS SS SS

Prior to knowledge of the pedunculate stages in the ontogeny of Neoverruca, the pedunculate stage noted in Verruca, in Semibalanus, and in Balanus, probably would have been considered, at least in my mind, as simply a vestigial reminiscence of their pedunculate ancestry rather than anything of significance in the evolution ofsessility per se. It is now apparent that it represents a stage reminiscent of functional pedunculate stages in the ontogeny of early sessile barnacles. There can be no question of this; the pedunculate stage of Verruca represents the con- densed pedunculate stages of more primitive forms such as Neoverruca, which in tum must have been inherited from their brachylepadomorphan ancestor. It is also apparent, taking the work of Bernard and Lane (1962) at face value, that the relatively amorphous pedunculate stage of Balanus represents a reduction of the pedunculate stage seen in Semibalanus. If monophyly rather than polyphyly is admitted for the sessile barnacles (Newman, 1987), then there appears to be no compelling reason why these balanoid pedunculate stages cannot be traced back to the common ancestor of all sessile barnacles, the urbrachylepadomorphans, and to their pollicipedine ancestor (Table I), just as Anderson (1987) has traced the reduced musculature and complete loss of feeding structures in the cyprids of Semibalanus and Lernaeodiscus back to the somewhat reduced but vastly more generalized condition seen in the cyprid of one of the most primitive living thoracican barnacles, [bla. Future evolutionary scenarios will need to consider that the acquisition of sessility was more complicated than previously understood; namely, it did not 474 BULLETIN OF MARINE SCIENCE, VOL. 45, NO.2, 1989

Figure 3. Ontogeny and metamorphosis in: A-F, Verruca stroemia MUller, 1776 (modified after Runnstrom, 1926) viewed from movable side (right side; A, C and E) and fixed side (mirror image; B, D and F); G-L, Semibalanus balanoides (Linnaeus, 1767) (modified after Runnstrom 1925); and M-Q, Balanus amphitrite s.1. Darwin, 1854 (modified after Bernard and Lane, 1962) viewed from right side. (Fig. I for explan. of symbols.) A-F: A-B, cyprid undergoing metamorphosis into pedun- culatejuvenile stage; note the pronounced asymmetry of the five chitinous, primordial valves of the movable and fixed sides, and the globular peduncle adjacent to the attachment point. C-D, as A-B, but with cyprid shell cast, more fully developed primordial valves, especially of the carina onto the movable side, and a more discreet peduncular rudiment. E-F, shortly after metamorphosis into the sessile mode accomplished by withdrawal of the peduncular rudiment and expansion of the basal margin of the capitulum; note calcification beginning beneath the primordial valves, and the appearance of a calcified rostrum and its growth around the perimeter to meet the expanding calcareous portion of the carina. (The chitinous primordial valves have honeycomb appearance; their calcified portions and the rostrum are stippled.) G-L: G, freshly attached cyprid beginning metamorphosis; H, appearance of five chitinous (non-primordial) valves supported by a globular peduncle; I, appearance of chitinous rostrum and median latus (Runnstrom's conclusion that the rostrum consisted of the rostrolatera could not be confirmed by Walley, 1969); J, basal expansion beyond confines of cyprid shell, "attachment organ" visible beneath peduncular rudiment; K, metamorphosis into sessile mode involving rounding up and broadening of the peduncle to form a membranous basis; L, = K viewed from beneath from carinal end; rudiment of attachment organ visible buried in membranous basis. This typical metamorphosis generally takes 24 hours. (Chitinous precursors of the valves and plates are stippled.) M-Q: M, cyprid metamorphosis and casting of cyprid shell, exposing plateless pedunculate stage consisting of a more-or-Iess amorphous capitulum with a stalk and attachment disc; N, metamorphosis into sessile mode by withdrawal of the peduncle into basal region concomitant with expansion of the basal margin of capitulum; 0 and P, complction of metamorphosis to sessile mode with assumption of conical form and presumptive differentiation into operculum and wall; Q, juvenile sessile barnacle with differentiating chitinous opercular valves and undifferentiated wall plates. This simplified metamorphosis was reported to take 4-6 h. (The chitinous precursors of the valves are stippled.) simply involve the shortening and eventual elimination of the peduncle, with concomitant changes in capitular organization, as authors since and including Darwin (1854) have inferred (Newman et al., 1969; Newman 1982; 1987; An- derson 1980; 1983). The presence of pedunculate stages and the abrupt meta- NEWMAN:JUVENILEONTOGENYANDMETAMORPHOSISINNEOVERRUCA 475 morphosis from pedunculate to sessile modes in Neoverruca, are incompatible with such a view. This metamorphosis must have been superimposed on an originally anamor- phoric ontogeny, at which time the evolutionary path toward virtual elimination of pedunculate juvenile stages all together was apparently opened. Following the compression into the single transitory pedunculate stage seen in the higher forms, Verruca stroemia, Semibalanus balanoides, and Balanus amphitrite, simplifica- tions in structure (loss of primordial and delay in appearance of chitinous valves) and reduction in the time required between the freshly settled cyprid and the first sessile juvenile stage (days to a matter of hours) were made (Table 1). The evolutionary pressures that led to the virtually complete elimination of pedunculate stages in higher sessile barnacles were likely similar to those that favored the evolution of the sessile mode in the first place; namely, the dramatic increase in shell-crushing predators, such as true crabs, in the late Mesozoic (Vermeij, 1977) and their significance to barnacles (Newman, 1979; 1982; 1985; Foster, 1987). A sessile juvenile should be more difficult to grasp and remove from the substratum than a pedunculate juvenile, as is generally the case with the adults. Smaller predators would be required to tackle juveniles, and small crus- taceans such as carideans, and even tanaidaceans (Oliver and Slattery, 1985), are among the likely candidates. Interspecific competition for space between juveniles may also have been involved (Moyse and Hui, 1981) if, as seems likely, sessile juveniles had a competitive edge over pedunculate ones. Whatever the evolutionary pressures that drove the brachylepadomorphans and early verrucomorphans to extinction elsewhere in the world, they are apparently absent from the refugium formed by these abyssal hydrothermal springs. Indeed, abyssal hydrothermal springs have, in Neolepas as well as Neoverruca, provided us with glimpses of antiquity found no place else on earth. Addendum: A balanomorph barnacle, more primitive than Catophragmus and Chionelasmus just noted above, was recently recovered by ajoint Japanese-French expedition to an abyssal hydrothermal field at approximately 2000 m in the North Fiji Basin (Yamaguchi T. and W. A. Newman, in press). Thus, the most primitive living scalpellomorph, verrucomorph and balanomorph are all know from abyssal hydrothermal springs. Knowledge of the ontogeny of the new balanomorph and its closest living relative, Chione/asmus, in conjunction with the ontogeny just described, throws a new light on our understanding of the evolution of the balanomorph wall (Yamaguchi and Newman, in press).

EPILOGUE

When first asked to participate in the D. P. Abbott Memorial Symposium, a biogeographical scenario camc to mind that seemed appropriate because of his interests in such matters. However, something even more appropriate surfaced; namely, the ontogeny ofa newly discovered and extremely primitive living sessile barnacle, and it is a pleasure to have this opportunity to dedicate it to him. An acquaintance with Don, respectfully known out of earshot as DPA, began in 1951 when R. I. Smith gave the last V.c.-sponsored summer course in invertebrate zoology for undergraduates at Hopkins Marine Station. The friendship continued, through barnacles he had collected on Ifaluk and on the R/V TE VEGAexpeditions (1968 and 1971), and when he would come to Berkeley to visit R. I. Smith and Cadet Hand. We became colleagues during the preparation of a barnacle chapter, begun in 1967 and published in Intertidal Invertebrates of California (Morris, Abbott and Haderlie 1980). The TE VEGAbarnacles are particularly relevant to the present study because they included the two most primitive living sessile genera known at the time. The first were specimens of Catophragrnus darwini Broch (1921), discovered by Th. Mortensen on islands off the west coast of Panama in 1914 but not seen again until DPA got some from the west coast of Coast Rica on 13 May 1968. These 476 BULLETINOFMARINESCIENCE.VOL.45. NO.2, 1989 formed the basis for his sketches of August, 1969, of some external features published in Observing Marine Invertebrates (Abbott, 1987, 279). And one ofDPA's specimens was used for the first published photograph of the species, in a paper involving the distribution of primitive balanomorphs (Stanley and Newman, 1980, fig. 3A). The second very primitive form was Chionelasmus darwini Pilsbry (1907), first collected in Hawaii by the ALBATROSSin 1902. It was not seen again in Hawaii until DPA took specimens from south of Molokai at approximately 450 m, on 4 September 1971. DPA's specimens were used for the first photographs of this genus [Newman and Ross, 1976, frontispiece; Stanley and Newman, 1980, fig. 3A], and later in a study of the arrangement ofimbricating plates in primitive balanomorphs (Newman, 1987, fig. 4). DPA enriched our lives and science in many ways and I would like to thank his students, not only for convening this symposium and thereby making it possible for us to express our gratitude, but for making the occasion of the symposium a most enjoyable and memorable one. I would also like to thank two anonymous referees for helpful comments and constructive criticisms of the manuscript.

LITERATURE CITED

Anderson, D. T. 1980. Cirral activity and feeding in the verrucomorph barnacles Verruca recta Aurivillius and V. stroemia (O.F. Muller) (Cirripedia). J. Mar. BioI. Ass. U.K. 60: 348-366. ---. 1983. Catomerus polymerus and the evolution of the balanomorph form in barnacles (Cir- ripedia). Pages 7-20 in J. Lowry, ed. Papers from the Conference on the Biology and Evolution of Crustacea. The Australian Museum, Sydney Memoir 18. --. 1987. The larval musculature of the barnacle lbla quadrivalvis Cuvier (Cirripedia, Lepa- domorpha). Proceedings of the Royal Society of London B231: 313-338. Bernard, F. J. and C. E. Lane. 1962. Early settlement and metamorphosis of the barnacle Balanus amphitrite niveus. 1. Morph. 110(1): 19-30 + pIs. 1-5. Buckeridge, J. S. 1979. Aspects of Australian biogeography: Cirripedia: Thoracica. Proceedings of the International Symposium on Marine Biology and Evolution in the Southern Hemisphere. Auckland, New Zealand 2: 485-490, 1978. Darwin, C. R. 1854. A monograph on the sub-class Cirripedia, with figures of all species. The Balanidae and Cirripedia, pp. 1-684 + pIs. 1-30. Roy. Soc. London. Foster, B. A. 1987. Barnacle ecology and adaptation. Pages 113-133 in A.J. Southward, ed. Barnacle biology. Crust. Iss. 5. Balkema, Rotterdam. Henry, D. P. and P. A. McLaughlin. 1975. The barnacles of the Balanus amphitrite complex (Cir- ripedia, Thoracica). Zool. Verhandel. 141: 203-212. McLean, J. H. 1981. The Galapagos Rift limpet Neomphalus: relevance to understanding the evolution of a major Paleozoic-Mesozoic radiation. Malacologia 21 :291-336. --. 1985. Preliminary report on the limpets at hydrothermal vents. Pages 159-166 in M. L. Jones, ed. The hydrothermal vents of the eastern Pacific: an overview. Bull. BioI. Soc. Washington. No.6. Moyse, J. and E. Hui. 1981. Avoidance by Balanus balanoides cyprids of settlement on conspecific adults. J. Mar. BioI. Ass. U.K. 61:449-460. Newman, W. A. 1979. A new scalpellid (Cirripedia); a Mesozoic relic living near an abyssal hydrothermal spring. Trans. San Diego Soc. Nat. Hist. 19(11): 153-167. ---. 1980. A review of extant Scillaelepas (Cirripedia: Scalpellidae) including recognition of new species from the North Atlantic, Western Indian Ocean and New Zealand. Tethys 9(4): 379-398. --. 1982. Cirripedia. Pages 197-221 in L. Abele, ed. The biology of Crustacea 1. Academic Press, New York. ---. 1985. The abyssal hydrothermal vent invertebrate fauna: A glimpse of antiquity? Pages 231- 242 in M.L. Jones, ed. The hydrothermal vents of the eastern Pacific: an overview. Bull. BioI. Soc. Washington. NO.6. ---. 1987. Evolution of cirripedes and their major groups. Pages 3-42 in A.J. Southward, ed. Barnacle biology. Crust. Iss. 5. Balkema, Rotterdam. --- and R. R. Hessler. 1989. A new cirriped from an abyssal hydrothermal spring; the "missing link" between the Brachylepadomorpha and Verrucomorpha. Trans. San Diego Soc. Nat. Hist. 21(16): 259-273. --- and A. Ross. 1976. Revision of the balanomorph barnacles; including a catalogue of the species. San Diego Soc. Nat. Hist. Memoir 9: 1-108. --, V. A. Zullo and T. H. Withers. 1969. Cirripedia. Pages R206-295 in R. C. Moore, ed. Treatise on invertebrate paleontology. Part R, Arthropoda 4, VoU. University of Kansas, Law- rence, and the Geological Society of America, Boulder. Oliver, 1. S. and P. N. Slattery. 1985. Effects of crustacean predators on species composition and population structure of soft-bodied infauna from McMurdo Sound, Antarctica. Ophelia 24(3): 155-175. NEWMAN:JUVENILEONTOGENYANDMETAMORPHOSISINNEOVERRUCA 477

Runnstrom, S. 1925. Zur Biologic und Entwicklung von Balanus balanoides (Linne). Bergens Mu- seums Aarbok 1924-25. Naturvidenskapelig raekke. nr. 5: 1-46. --- 1926. Uber die Platten-entwicklung von Verruca stromia, a.F. MUlier. Bergens Museums Aarbok. Naturvidenskapelig raekke nr. 3: 1-19. Stanley, S. M. and W. A. Newman. 1980. Competitive exclusion in evolutionary time: the case of the acorn barnacles. Paleobiology 6(2): 173-183. Stubbings. H. G. 1975. Balanus balanoides. L.M.B.C. Memoirs (E. Naylor cd.). Liverpool University Press, Liverpool. 175 pp. Vermeij, G. J. 1977. The mesozoic marine revolution; evidence from snails, predators and grazers. Paleobiology 3: 245-258. Walker, G., J. A. Nott and A. B. Yule. 1987. Structure and function in balanomorph larvae. Pages 307-328 in A. J. Southward, cd. Barnacle biology. Crust. Iss. 56. Balkema, Rotterdam. Walley, L. J. 1969. Studies on the larval structure and metamorphosis of Balanus balanoides. Philosophical Trans. Royal Soc. London B. 256(807): 237-280. Yamaguchi, T. and W. A. Newman. In press. A new and primitive barnacle (Cirripedia; Balano- morpha) from the North Fiji Basin abyssal hydrothermal field, and its evolutionary implications. Pacific Sci.

DATEACCEPTED: September 20, 1988.

AnDRESS: Scripps Institution of Oceanography, A-002, University of California-San Diego, La Jolla, California 92037.