COMPARATIVE MORPHOLOGY OF THE ...

Proceedings of the Fourth International Crustacean Congress, 1998

COMPARATIVE MORPHOLOGY OF THE BALANIDAE (CIRRIPEDIA): A PRIMER TO A PHYLOGENETIC ANALYSIS BY FABIO BETIINI PITOMBO Departamento de Biologia Animal, Instituto de Biologia, Universidade Federal Rural do Rio de Janeiro, Km 47 da Antiga Rio Sao Paulo, 23890-000 Seropedica, RJ, Brazil and Museu Nacional, Universidade Federal do Rio de Janeiro, 20940-040 Rio de Janeiro, RJ, Brazil

ABSTRACT Since Leach's (1817) original description, the concept of the family Balanidae has undergone many modifications, nowadays comprising about 90 recent species distributed in three subfamilies and twelve genera. Most of the recent suggestions were directed toward an attempt to render the classification of the family more natural. However, there is still a lack of comparative anatomical studies dealing with the whole family, although some subfamilies and genera have been studied in more detail (e.g., the Balanus amphitrite complex; Megabalaninae, Concavinae, and Fistulabalanus). The monophyly of the Balanidae and their subgroups also needs to be ascertained. The· present study provides a comparative analysis of various morphological structures from the opercular plates, parieties, mouth, and appendages in order to establish primary homologies (sensu Pinna, 1992) between the character states found among the balanids and three functional outgroups (Chirona, Semibalanus, and Membranobalanus). Twenty-three species representing each of the currently accepted taxa of Balanidae were compared. This analysis demonstrated that there are many underestimated characters, such as appendages, and others that need more accurate evaluation because of their extensive interspecific variation (e.g., scuta! and tergal sculpturing) among the Balanidae. Some morphological patterns are described and homologies are proposed.

INTRODUCTION

Following the monograph by Darwin (1854), studies of cirripedes were directed toward an attempt at rendering the classification of the family more natural. Since Leach's (1817) original description, the concept of the family Balanidae has undergone many modifications, being reduced to approximately 90 recent species, distributed in 3 subfamilies and 9 genera (Hoek, 1907, 1913; Pilsbry, 1916; Newman, 1979, 1982; Newman et al., 1969; Newman & Ross, 1976; Henry & McLaughlin, 1975, 1984; Zullo, 1984, 1992). Although these authors suggested some affinities among different groups of Balanidae, little is known regarding phylogenetic relationships within balanid groups; in addition, the monophyly of balanid genera and subgroups remains to be established. © Koninklijke Brill NV, Leiden, 1999

Crustaceans and the Biodiversity Crisis

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FABIO BETTINI PITOMBO

Taxonomic studies of the Balanidae often lack comparative descriptions of the structures utilized, primarily because of the limited work on some groups (e.g., Henry & McLaughlin, 1975 on the Balanus amphitrite Darwin, 1854 complex; Henry & McLaughlin, 1986 on Megabalanus; and Zullo, 1992 on the Concavinae). Apart from the works of Bourguet (1977) on shell structure of Verrucomorpha and Balanomorpha, Barnes & Klepal (1971) on the penis structure of Cirripedia, and H!Z)eg et al. (1994) on the mouth appendages of Thoracica, few comparative anatomical studies have dealt with the morphological diversity of the group. This has led to misunderstandings and to inadequate use of some morphological characters, which may vary considerably, or else be present in-groups other than those analysed. In order to better understand the morphological variation within the family, a comparative analysis of some structures is presented. In this study, I will emphasize morphological features that may be characterized as primary homologies (sensu Pinna, 1992) among the species studied.

METHODS

Balanidae and three functional out-groups were compared (table I). The species were dissected, and their opercular plates, parietes, mouth, and cirral appendages described. The hard parts were cleaned, the opercular valves fixed on microscopic slides, and the parietal plates disassembled and properly stored (Newman & Ross, 1971). Soft parts were dissected using a stereomicroscope and mounted on slides with Hoyer's solution. Drawings were made using a drawing tube on a Zeiss Axioscop compound microscope. The classification and nomenclature of the setae were adapted from Henry (1974), Henry & McLaughlin (1975), and H!Z)eg et al. (1994 ).

RESULTS AND DISCUSSION PARIETES

Longitudinal tubes, septa, and secondary laminae The parieties may be solid as in Chirona amaryllis (Darwin, 1854) (fig. lB) and Membranobalanus declivis (Darwin, 1854) or porose. When porose the parietes are formed by outer and inner laminae, which are separated by longitudinal septa, forming longitudinal pores or tubes between them (fig. 1A, C, D-F). The septa vary in the degree of development, structure, and ornamentation among the groups studied. Septa may originate on the inner surface of the external lamina, reaching or not reaching the internal lamina, called primary and secondary septa,

COMPARATIVE MORPHOLOGY BALANIDAE

TABLE I List of the species studied, with the present taxonomic position of each ARCHAEOBALANIDAE Newman & Ross, 1976 Archaeobalaninae Newman & Ross, 1976 Chirona amaryllis (Darwin, 1854)* Membranobalanus declivis (Darwin, 1854)* Semibalaninae Newman & Ross, 1976 Semibalanus balanoides (Linnaeus, 1767)* BALANIDAE Leach, 1817 (sensu Newman & Ross, 1976) Ba1aninae Leach, 1817 Balanus Da Costa, 1778 Group of Balanus balanus** Balanus balanus (Linnaeus, 1758) Balanus crenatus Bruguiere, 1789 Balanus glandula Darwin, 1854 Group of Balanus nubilus** Balanus nubilus Darwin, 1854*** Balanus rostratus Hoek, 1883 Group of Balanus amphitrite** Balanus amphitrite Darwin, 1854 Balanus eburneus Gould, 1841 Balanus improvisus Darwin, 1854 Balanus reticulatus Utimoni, 1967 Balanus subalbidus Henry, 1974 Group of Balanus trigonus** Balanus laevis Bruguiere, 1789 Balanus spongicola Brown, 1837 Balanus trigonus Darwin, 1854 Group of Balanus perforatus** Balanus perforatus Bruguiere, 1789 Fistulobalanus Zullo, 1984 Fistulobalanus citerosum (Henry, 1974) Fistulobalanus albicostatus (Pi1sbry, 1916) Tetrabalanus Cornwall, 1941 Tetrabalanus polygenus Cornwall, 1941 Concavinae Zullo, 1992 Menesiniella Newman, 1982 Menesiniella aquila (Pi1sbry, 1916) Paraconcavus Zullo, 1992 Paraconcavus pacificus (Pilsbry, 1916) Paraconcavus mexicanus (Henry, 1941) Megaba1aninae Newman, 1979 Megabalanus Hoek, 1913 Megabalanus tintinnabulum (Linnaeus, 1767) Megabalanus rosa (Pi1sbry, 1916) Austromegabalanus Newman, 1979 Austromegabalanus psittacus (Molina, 1788) * Out-groups. ** Groups of Newman & Ross, 1976. *** One specimen, without the parietes.

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Fig. 1. Basal end of parietal plates, showing the wall structure. A, Semibalanus balanoides (Linnaeus, 1746); B, Chirona amaryllis (Darwin, 1854); C, Balanus ebumeus Gould, 1841; D, G, Fistulobalanus citerosum (Henry, 1974); E, H, Fistulobalanus albicostatus (Pilsbry, 1916); F, Austromegabalanus psittacus (Molina, 1788). bt, basal teeth; de, denticles; il, inner lamina; ps, primary septa; pt, primary tubes; rs, ramifying septa near the outer lamina; si, secondary inner lamina; ss, secondary septa; st, subsidiary tubes; ol, outer lamina.

respectively (fig. 1). Septa may also originate on the inner surface of the inner lamina as observed in Balanus balanus (Linnaeus, 1758) and B. rostratus Hoek, 1883. This is a diagnostic character for the Balanus balanus series of Pilsbry (1916: 138). The basal end of longitudinal septa may be denticulate (fig. lB-F) or smooth (fig. lA). When present, denticles together with the longitudinal septa


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are interlocked with the calcareous base, providing the attachment of the parietes to the base. Features of the tubiferous wall with an intricate dovetailing of the wall and the basis, distinguish the Balanidae from all the other Balanomorpha (cf. Newman & Ross, 1976). The presence of denticulate basal teeth on the base of the solid wall of Chirona amaryllis (fig. lB), as well as the observations made by Bourguet (1977) of interlaminate figures in the wall, similar to the other Balanidae, suggest affinities of this taxon with the Balanidae. A secondary row of longitudinal tubes (subsidiary tubes) is present in Fistulobalanus (fig. lD, E, G, H). These tubes are formed by two distinct processes: the ramification of the septa close to the outer lamina (fig. lD, E, G, H), and by anastomosis or linkage of the primary and secondary septa by an inner or secondary lamina (fig. lD, G). Fistulobalanus albicostatus (Pilsbry, 1916) has only the ramificating septa close to the outer wall (fig. IE, H) and F. citerosum (Henry, 1974) has both types (fig. lD, G). The secondary lamina is morphologically similar to the inner lamina of the parietes, and was called by Henry (1974) an "outer wall of primary tubes". Here I propose to call this lamina a secondary inner lamina due to the observed morphological similarity with the inner lamina and to the relationship with the secondary septa. Zullo (1984) considered the subsidiary tubes as one of the diagnostic features of Fistulobalanus. Both processes of subsidiary tube formation are found in Fistulobalanus amaraquaticus (Yamaguchi, 1980), F. dentivarians (Henry, 1974), F. klemmi Zullo, 1984, F. suturaltus (Henry, 1974), F. citerosum (Henry, 1974), and F. dentivarians (Henry, 1974), whereas Fistulobalanus pallidus (Darwin, 1854) and F. albicostatus do not have a the secondary inner lamina (Zullo, 1984; Henry, 1974; Utinomi, 1967; Yamaguchi, 1980). Utinomi (1967) described the wall structure of two taxa of Fistulobalanus that present only the ramifying septa, F. pallidus and F. albicostatus. In the two subspecies of F. albicostatus, F. a. albicostatus (Pilsbry, 1916) and F. a. formosanus (Hiro, 1938), Utinomi (1967: 213) observed that in the latter "the parietal pores shown at the base of the wall is much more complex than in the preceding albicostatus from Japan, the secondary pores formed close to the basal edge of the wall being intercalated deeply within the primary pores". In F. pallidus, he observed an "unusual multiparous structure of the wall" (Utinomi, 1967: 208209, text-fig. 3) distinct from that observed in F. albicostatus. These differences suggest a complexity of this structure. The two processes of formation of the subsidiary tubes have been considered a single character, and an accurate characterization of these structures must be done in order to understand the relationships of the genera.

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Sutural edges The sutural edges of the radii are either smooth as observed in Semibalanus balanoides (Linnaeus, 1767) and Membranobalanus declivis, or have transverse septa. The transverse septa exhibit a variable pattern among the species studied. The septa may be simple as in Chirona amaryllis, Balanus glandula Darwin, 1854, and B. crenatus Bruguiere, 1789 (fig. 2A), or with denticles with different degrees of complexity. In B. balanus and B. rostratus the denticles are present on the lower margin but also with smaller and irregular denticles on the upper side. In the observed species of the Balanus amphitrite group, B. trigonus group, B. perforatus group, Fistulobalanus, Tetrabalanus, and the Concavinae, the denticles are present only on the lower margin of the septa (fig. 2B). In Austromegabalanus psittacus (Molina, 1788) the denticles on the upper margin of the septa are irregularly disposed, and may be observed on the basal portion of the radii (fig. 2C). In addition, in A. psittacus, Balanus perforatus Bruguiere, 1789 and Menesiniella aquila (Pilsbry, 1916) the septa may ramify close to inner laminae. In species of Megabalanus, the developed denticles are regularly disposed on the upper and lower margins of the septa (fig. 2D). An increasing complexity of the sutural edge structure is observed within the Balanidae, from the smooth edge to edges with simple or ramifying septa, while also the septa present denticles with different patterns of complexity. Features of the sutural edges are used as diagnostic characters for some groups among the Balanidae. Newman (1979) used the septa denticles of the sutural edges of the radii to distinguish Megabalanus, with denticles regularly disposed on the upper and lower sides of the septa, from Austromegabalanus and Notomegabalanus, which have irregular denticles on the lower side only. Specimens of A. psittacus observed in the present investigation present upper and lower denticles in some parts of the sutural edge (fig. 2C), differing from observations made by Pilsbry (1916: 75) for A. psittacus " ... branching laminae, which deeply denticulate on their lower sides only". This feature was considered by Newman (1979) as a diagnostic one for Austromegabalanus and Notomegabalanus, and the above observations show the need of a revision of this character within the Megabalaninae. Alae, radii, and sheath The alae are an internal projection of the parieties, being contiguous to the sheath. In most of the species examined, the alae fit under the inner surface of the radii touching the adjacent sheath, which impedes the alae to slide over the adjacent paries (fig. 3B, D). In the studied species of Megabalaninae, Balanus


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-0-.5-m_m __ A,B,C,D Fig. 2. Sutural edge of the radii. A, Balanus crenatus Bruguiere, 1789 (lateral); B, Balanus amphitrite Darwin, 1854 (rostrum); C, Austromegabalanus psittacus (Molina, 1788) (lateral); D, Megabalanus rosa (Pilsbry, 1916) (carinolateral). il, inner lamina.

peiforatus, Paraconcavus pacificus (Pilsbry, 1916) and P mexicanus (Henry, 1941), and Menesiniella aquila, the sheath margin has a small projection covering the alar edge, forming a slot to its attachment (fig. 3A, C). These species

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b'

ol Fig. 3. Carinolateral plates, showing details of the sheath border and the longitudinal ridge of the inner surface of the radii. A, C, Austromegabalanus psittacus (Molina, 1788); B, D, Fistulobalanus albicostatus (Pilsbry, 1916). C, D, transversal plane (a'-b') of carinolateral plate; a, ala; as, articular surface for the adjacent ala; lr, longitudinal ridge; ol, outer laminae; psm, projected sheath margin; s, sheath; sm, sheath margin.


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also have a longitudinal ridge on the inner laminae of the radii, holding the ala and not allowing it to attain the sheath border (fig. 3C). Both structures, the sheath projection and the longitudinal ridge, are not described in literature and the observed morphological similarity suggests these structures to be a primary homology. Zullo (1992) observed many similarities among the Megabalaninae and Concavinae, and a close relationship between the B. peiforatus group and the Megabalaninae. The monophyly of a group formed by: Megabalaninae, Concavinae, and B. peiforatus is suggested, based on the characters described above. ARTICULAR PLATES

Scutum The articular ridge and furrow form the articulation with the tergum (figs. 4, 5). The articular margin presents two forms: (1) a folding of the external growth ridges alone (Balanus balanus, B. glandula, and B. rostratus) (fig. 4A); (2) a folding of the external growth ridges together with the extended basal margin of the articular ridge and the lower portion of the furrow, observed in all other species to differing degrees (fig. 4C, E, F). Among the species that present the extended basal margin Semibalanus balanoides, Membranobalanus declivis, Balanus nubilus Darwin, 1854, B. spongicola Brown, 1837 and B. trigonus (fig. 4C, D) present a reduced extension of the basal margin compared to the remaining species (figs. 4E, F, SA-D). The articular ridge and the open furrow is more developed when an extended basal margin is present. The articular furrow has three states of development among the taxa observed: (1) The furrow is narrow with its margins almost touching in Chirona amaryllis, Balanus balanus, and B. rostratus (fig. 4A). (2) The furrow is narrowly open with parallel borders, in B. spongicola and B. trigonus Darwin, 1854 (fig. 4C, D). (3) The furrow is open, widening at its lower portion, as observed in the others species (figs. 4E, F, SA-D). In Austromegabalanus psittacus, a particular articular ridge is found: the ridge is projected toward the inner face, contiguous with the adductor muscle scar, and reaching the inner margin of the lateral depressor muscle scar (fig. SA). The inner surface of the scutum has structures related to the attachment of different muscles and the tergal articulation. Two of these structures, the adductor muscle ridge and the articular ridge, may have different features. They may be continuous as observed in A. psittacus (fig. SA) or not. When not continuous, they may be confluent or separated by a narrow (fig. 5B, C) or a wide groove (fig. 50). Henry & McLaughlin (1975) observed confluent adductor and articular

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-=2 -m-m- C,D,F,G ::----A,B 5 mm

Fig. 4. External views of scuta and their articular margins. A, B, Balanus rostratus Hoek, 1883; C, D, Balanus trigonus Darwin, 1854; E, F, Fistulobalanus albicostatus (Pilsbry, 1916). A, C, E, tergal segment; B, D, F, frontal view; af, articular furrow; ar, articular ridge; bm, basal margin.


c

161

"2-m-m-A 1 mm B,C """"J_m_m--D

Fig. 5. Internal views of scuta and their articular margins. A, Austromegabalanus psittacus (Molina, 1788); B, Paraconcavus pacificus (Pilsbry, 1916); C, Megabalanus rosa (Pilsbry, 1916); D, Fistulobalanus albicostatus (Pilsbry, 1916). af, furrow; as, adductor depressor scar; adr, adductor muscle ridge; ar, articular ridge; lr, lateral depressor ridge; lp, lateral depressor pit; oc, occludent margin.

ridges only on Balanus eburneus Gould, 1841 and B. peruvianus Pilsbry, 1909. In B. eburneus, both ridges are clearly independent and distinct from those observed on Austromegabalanus psittacus.


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"2-m-m--A

c

1 mm B,C ,_I-m-m--D

Fig. 5. Internal views of scuta and their articular margins. A, Austromegabalanus psittacus (Molina, 1788); B, Paraconcavus pacificus (Pilsbry, 1916); C, Megabalanus rosa (Pilsbry, 1916); D, Fistulobalanus albicostatus (Pilsbry, 1916). af, furrow; as, adductor depressor scar; adr, adductor muscle ridge; ar, articular ridge; lr, lateral depressor ridge; lp, lateral depressor pit; oc, occludent margin.

ridges only on Balanus eburneus Gould, 1841 and B. peruvianus Pilsbry, 1909. In B. eburneus, both ridges are clearly independent and distinct from those observed on Austromegabalanus psittacus.

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The lateral depressor ridge may be present (fig. SA-C) or absent (fig. SD). When present, its shape and structure are variable. An isolated ridge bordering the inner margin of the lateral depressor muscle pit was found among the species of Concavinae studied (fig. SB) and in Balanus peiforatus. Two other forms of lateral ridges are observed, associated with the adductor and/or articular ridge. In Megabalanus rosa Pilsbry, 1916 (fig. SC), Balanus nubilus, and B. rostratus, there is a ridge bordering the inner margin of the lateral muscle contiguous with the adductor ridge. Austromegabalanus psittacus (fig. SA) presents an articular ridge that extends up to inner margin of the lateral muscle scar. This ridge is distinct from the isolated ridge of the Concavinae, but it can also be considered as a lateral muscle ridge. Zullo (1992) used the lateral depressor ridge as a diagnostic character for the subfamily Concavinae and defined it as the ridge bordering the inner margin of the lateral depressor muscle pit. None of the Concavinae species studied by Zullo (1992) had a ridge confluent with the adductor ridge. Zullo described only Tamiosoma (now Menesiniella according to Whittlesey (1998)) as having nearly confluent lateral and adductor ridges, but Menesiniella aquila presents an isolated ridge with distinct crests running parallel to the adductor ridge. Apparently, the lateral depressor ridge of the species of Concavinae is homologous, and its relationship to the other two forms of lateral ridge still needs to be ascertained. Tergum On the outer face along the carinal margin of the tergum, the growth ridges present two basic forms. In the first, the ridges are bent upward, keeping more or less the distance between them, producing an expansion of the carina] margin, as observed only in Membranobalanus declivis (fig. 6C). In the second form, the growth ridges are abruptly narrowed and upturned along the carina! margin, as observed in all others species studied (fig. 6A, B). Within this second form, the upturned growth ridges can be straight (fig. 6B) or develop a protuberance on the upper margin (fig. 6A). Henry & McLaughlin (197S) observed the protuberance on the carinal side in some species of the Balanus amphitrite group, some of which are now placed in Fistulobalanus. According to my observations and those of Henry & McLaughlin (197S), the protuberance of the carinal margin of the tergum is restricted to some species of the B. amphitrite group, including Fistulobalanus. The spur is formed by an abrupt alteration of the direction of the growth ridges on the outer face, producing a longitudinal elongation of the basal margin, the spur (fig. 6). The spur is delimited laterally by two imaginary longitudinal lines, placed where the growth ridges change their direction, the spur margins

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A

c 2mm

B,C

Fig. 6. Tergum outer face. A, Balanus ebumeus Gould, 184 1; B, Paraconcavus pacificus (Pilsbry, 1916); C, Membranobalanus declivis (Darwin, 1854). ecm, expanded carina! margin; em, carina! margin; pr, protuberance; scm, scuta! margin; fm, furrow margin; sm, spur margin.

(fig. 6A, B, C). The spur margins separate from the furrow margins in more highly evolved forms (fig. 6B). On the spur margins, a narrow groove is found on both sides (fig. 6A), or on one side only, or is absent (fig. 6C). In the Megabalaninae, Concavinae, Balanus perforatus, and Chirona amaryllis, the spur margins are infolded, almost closing the spur opening (fig. 6B), and the spur margins are separated from the furrow margin (fig. 6B). The spurs are highly modified among the different groups of Balanidae. Zullo (1992: 2) used the spur to characterize the subfamily Concavinae "well developed spur furrow .. . that is partially closed over in all species, and the spur has

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nearly parallel sides". Henry & McLaughlin (1975: 21) differentiated the spur fasciole from the spur furrow, as a two-state character among the species of their Balanus amphitrite complex. Both processes are "extended to apex in line with spur" and the chief difference among the two forms is the depth of depression, the spur fasciole being "nearly level, slightly depression", whereas the spur furrow has a "moderate to deep groove ... with sides sometimes infolded". Henry & McLaughlin (1975) observed the infolded spur only in Paraconcavus pacificus and P. mexicanus, species which were assigned to the Balanus amphitrite complex at that time and are at present in the Concavinae (cf. Zullo, 1992). The distinction between these two states is sometimes confusing and according to Newman (1996), there often is an ontogenetic continuum between the two. I propose a three state character for the spur structure: (1) The spur is formed only by the alteration of the growth ridges direction (fig. 6C); (2) the spur presents a longitudinal groove on at least one margin (fig. 6A), comprising the spur fasciole and part of the spur furrow of Henry & McLaughlin (1975); and (3) formed by an infolded furrow (fig. 6B). In the first two states (1 and 2) the spur margins are coincident with the furrow margin. In the infolded spur (state 3) the furrow margins are closing-in, being separated from the spur margin. APPENDAGES

Second maxilla The anterior margin of the distal lobe is covered by long smooth setae in all species studied. In most of the observed species, the extremity is simple and tapers to a slender point. A group of species have a characteristic enlargement, with three similar but distinct forms: (1) the F. albicostatus type setae (fig. 7 A-E) are found only in Fistulobalanus albicostatus; (2) the F. citerosum type setae (fig. 7G-M) only in F. citerosum; and (3) the Balanus amphitrite type setae (fig. 7N-Q), observed in six of the species studied (B. amphitrite, B. eburneus, B. improvisus, B. reticulatus Utinomi, 1967, B. subalbidus Henry, 1974, and Tetrabalanus polygenus Cornwall, 1941). The three forms of setae present a sub-terminal enlargement narrowing toward the tip. Both the B. amphitrite and F. citerosum setal types present bigger enlargements, differing in the shape of the terminal portion. Basal to this enlargement a folding process is observed (fig. 7 A-C, E, N-Q). The B. amphitrite seta has an asymmetric terminal part dislodged from the central axis (fig. 7N-Q), while the F. albicostatus seta has a more symmetric tip (fig. 7 A-E). The F. citerosum seta is more slender and may be a row of delicate (± 3 p,m) projections on the sub-terminal enlargement (fig. 7G-I). When present, the differentiated setae are gradually modified to a

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D

F

f

J_

K

0.015 mm

f-

J_

Fig. 7. Second maxilla, setae found on distal lobe anterior margin. A-F, Fistulobalanus albicostatus (Pilsbry, 1916); G-M, Fistulobalanus citerosum (Henry, 1974); N-Q, Balanus amphitrite Darwin, 1854. f, folding process; p, delicate (3 J-Lm) projections.

long, smooth seta (fig. 7F) from the distal lobe towards the proximal lobes anterior face. The proximal lobe is covered by foliate setae. Proximal on the distal lobe, the foliate setae mingle with the long smooth setae. The modified terminal tip observed on the anterior face of the second maxilla's distal lobe [=maxilla distal article of H!Zleg et al. (1994)] may be a morphological variation of the "smooth acuminate (simple) setae (2c)" of H!Zleg et al. (1994), as they are located at the same position on the second maxilla. Henry & McLaughlin (1975: 25) apparently observed these setae, stating that "some have setae with modified tips (bent) on the upper lobe". However, these authors furnished no other observations on this structure. Balanus amphitrite type setae are present only in

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the currently accepted species of the B. amphitrite group, with the exception of Tetrabalanus polygenus. The other two setae occur in the two Fistulobalanus species studied, which were previously assigned to the B. amphitrite complex (Pilsbry, 1916; Henry & McLaughlin, 1975; Newman & Ross, 1976). Zullo (1984), based on fossil evidence, states that "Fistulobalanus is an old balanid stock [and] may be related to the B. amphitrite complex, but only distantly"; the above evidence supports his observations. However, the morphological similarity and the taxonomic affinity of the species that possess modified setae, suggest that Fistulobalanus, the B. amphitrite group, and T. polygenus, form a monophyletic group. Cirrus III The inner (medial) face of the endopod of cirrus III has different sets of setae. Of these, the common pectinate seta with small pinnules separated by approximately 1 p,m on the upper half (fig. 8E) is found in representatives of almost all genera and groups analysed including the three out-groups, but not in the Balanus rostratus and B. balanus group. The other pectinate seta differs from the first one by the lengthening of the pinnules; it has pinnules longer than 7 p,m and spaced up to 20 p,m from each other. It is present in the three species of the B. balanus group, in B. rostratus, B. laevis, B. trigonus, Fistulobalanus albicostatus, and Austromegabalanus psittacus. In Balanus glandula, few pinnules are present (I to 10), each elongated towards the tip (fig. 8I), and setae with fewer pinnules are observed more frequently on the anterior side of the segments protuberance (fig. 8J). Balanus rostratus was formerly assigned by Pilsbry (1916) to the B. balanus series. Newman & Ross (1976) placed B. rostratus in the B. nubilus group. The presence of the above described pectinate setae with elongated pinnules among B. rostratus and the B. balanus group may indicate a close relationship of these species, but further investigations are necessary. The serrate or pinnate setae are covered on its distal third by 5 p,m-long pinnules separated by 5 p,m gaps (fig. 8F, K) in all representatives of the Balanus amphitrite group, B. spongicola, Fistulobalanus albicostatus, Menesiniella aquila, Paraconcavus pacificus and Tetrabalanus polygenus. This seta is similar to the type 3 seta "serrate setae with peg shaped denticles" of H!lleg et al. (1994). In Megabalanus rosa and M. tintinnabulum (Linnaeus, 1767), Paraconcavus pacificus, P. mexicanus, and Austromegabalanus psittacus, the setae are covered on the upper half with short, sheath-like spines with broad basis (fig. 8G). On the protuberance, the sheath-like spines may have their numbers reduced along the setal shaft, producing an almost smooth seta (fig. 8H). This seta resembles the foliate setae of H!lleg et al. (1994 ), and is apparently unique to Megabalaninae

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F

----A-F

0.025 mm -0.-02-5-mm G- K

J

H

1\ 1\ 1\ (\

/1

11

{\

a

g

Fig. 8. Setae found on inner endopodal face of cirrus III. A-F, Fistulobalanus albicostatus (Pilsbry, 1916); G, H, Megabalanus tintinnabulum (Linnaeus, 1767); l-K, Balanus glandula Darwin, 1854. A-D, denticulate setae; E, I, pectinate setae; G, H, foliate setae; F, K, serrate setae; A-E, G, I, medially on segments; F, H, J, on anterior margin protuberance; K, on posterior margin.

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and Paraconcavus, whereby its presence suggests affinity among both taxa. As Paraconcavus is now placed in the Concavinae, verification in other species of Megabalaninae and Concavinae is necessary to establish its homology. Fistulobalanus albicostatus has a group of bidenticulate setae with different grades of reduction in number of teeth (fig. 8A-D). In this species, the denticle with the enlarged basis is characteristic of the more developed setae, but setae with small and grouped teeth are also found (fig. 8C, D). F citerosum has bifurcate and multifurcate setae, which are morphologically distinct from the bidenticulate setae. The complex setae described by Henry (1974) occur in the species of the former Balanus pallidus group (now Fistulobalanus), and in Balanus inexpectatus Pilsbry, 1916 of the B. amphitrite complex (Henry & McLaughlin, 1975). Henry & McLaughlin (1975: 185) stated that B. inexpectatus has denticulate setae: "Denticulate setae with short apical ends and single or double row of 15-20 small teeth". The description, allied with the illustration of the setae (Henry & McLaughlin, 1975: 122, fig. 23d, e), indicates a distinct form of denticulate and bidenticulate setae, compared to F albicostatus illustrated herein. According to Henry (1974), Henry & McLaughlin (1975) and my observations, complex setae have distinct forms and vary among the species of Balanidae. The simple pectinate setae are the only type found among all species with complex setae (Henry, 1974; Henry & McLaughlin, 1975), but it was also observed in other species from different genera and groups. In addition, in F albicostatus the pectinate setae (fig. 8E) occur marginally to the denticulate seta. In F citerosum, the pectinate setae occur among the bifurcate and multifurcate setae. There seems to exist a morphological gradient among the pectinate and the others complex setae (bidenticulate, denticulate, bifurcate, and multifurcate). These observations indicate that although complex setae seem to be homologous structures, the character "complex setae" is variable and includes different states under the same name. The genus Fistulobalanus diagnosed only on the hard parts (Zullo, 1984) equals the B. pallidus group of Henry & McLaughlin (1975), diagnosed by the presence of the "complex setae" as well as a secondary row of parietal tubes and a vesicular sheath. Therefore, the status of the "complex setae" in the genus Fistulobalanus must be ascertained, and a redefinition of "complex setae", not including the pectinate setae, and with a proper characterization of this multistate character, is necessary. Darwin (1854: 2) stated in the introduction to his monograph, that the "softer parts" of the animal body in Balanomorpha did not furnish specific characters: "these parts are more alike in the different species, and I have found it impossible to give a diagnostic character thus derived". For this reason, Darwin did not use


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the "soft parts" extensively in his descriptions, and following his lead subsequent works on the Balanidae did not pay much attention to them. Henry (1974) and Henry & McLaughlin (1975) pioneered the methodical use of the "soft parts", furnishing a detailed description of the trophi and cirri for the Balanus amphitrite complex, and presenting numerous descriptive characters. HiZieg et al. (1994) presented a comparative analysis of the different forms of setation of the mouth appendages of six species of barnacles. The classification of HiZieg et al. (1994), although based on SEM in many aspects, can be compared with the observed setation of the mouthparts and in some cases the cirri.

CONCLUSIONS

In Fistulobalanus two processes of formation of the subsidiary tubes have been considered as a single character: (1) the ramification of the septa; (2) the secondary inner laminae linking the primary and secondary septa. A concise use of each state must be implemented in order to understand the relationships of the species of the genus. A close relationship between Balanus rostratus and the B. balanus group is observed. The scutum articular margin, shaped only by the folding of the external growth ridges in B. balanus, B. glandula, and B. rostratus, and the differentiated pectinate seta shown by B. rostratus and the species of the B. balanus group, suggest their affinity. The return of B. rostratus to the B. balanus group in accordance with the "Balanus balanus Series" of Pilsbry (1916), is proposed. In the Megabalaninae as well as in Balanus perforatus, Paraconcavus, and Menesiniella aquila, the sheath has a small projection on the edges of the alae, and a longitudinal ridge on the inner laminae of the radii, and they also present an infolded spur. The monophyly of the group formed by Megabalaninae, Concavinae, and B. peiforatus is suggested, based on the above-described characters. In the Megabalaninae and Paraconcavus the inner face of cirrus III presents a distinct seta covered with short, sheath-like spines, and this seta suggests affinity among both taxa. Chirona amaryllis must be considered to be within the Balanidae (hence an ingroup). It exhibits denticulate basal teeth along the basal margin, interlaminate figures in the wall similar to the others Balanidae, septa on the sutural edges of the radii, a sheath with a small projection on the alae edge, a longitudinal ridge on the inner laminae of the radii, and an infolded spur. These character states suggest that C. amaryllis may be closely related to the group formed by Megabalaninae, Balanus peiforatus, Paraconcavus, and Menesiniella aquila.

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The lateral depressor ridges of the species of Concavinae are morphologically similar, and a relationship to the other two forms of lateral ridge still needs to be ascertained. The morphological similarity and the taxonomic affinity of the species that present the modified setae on the second maxillae distal lobe, suggest that Fistulobalanus, the Balanus amphitrite group, and Tetrabalanus polygenus, form a monophyletic group. The variability observed on the setation of the inner endopodal face of cirrus III (complex setae, foliate setae, and pectinate setae) show the value of this and others structures of the cirri for systematic studies on the Balanidae. Although no phylogeny can be established as yet, only on the above-described characters some proposals of relationships arise already. Decisive conclusions must await the inclusion of these and other characters in a large matrix, analysed cladistically. Final decisions as to what character states are plesiomorphic and apomorphic must follow from such an analysis.

ACKNOWLEDGEMENTS

I wish to thank Dr. Paulo S. Young (Museu Nacional!UFRJ) for his incentive and assistance throughout the course of this study. Janet Reid (Smithsonian Institute) and Helio da Silva (lnstituto de Biologia/UFRRJ) for revision of the manuscript and helpful comments. This study was financially supported by Fundac;ao Universitaria Jose Bonifacio (FUJB) and Fundac;ao de Amparo a Pesquisado Estado do Rio de Janeiro (FAPERJ).

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HOEK, P. P. C., 1907. Cirripedia. Resultats VoyageS. Y. Belgica, 1897-1899. Rapp. Sci. Zoo!. 3-9. (Antwerp). - - , 1913. The Cirripedia of the Siboga-Expedition, B: Cirripedia sessi1ia. Siboga Exped. Mon., 31b: 129-275. LEACH, W. E., 1817. Distribution systematique de Ia classe des Cirripedes. Journ. Phys. Chim. Hist. nat., 85: 67-69. NEWMAN, W. A., 1979. On the biogeography of balanomorph barnacles of the southern ocean including new balanid taxa; a subfamily, two genera and three species. New Zealand DSIR Information Series, 137: 279-306. - - , 1982. A review of extant taxa of the "group of Balanus concavus" (Cirripedia, Thoracica) and a proposal for genus-group ranks. Crustaceana, 43 (1): 25-36. - - , 1996. Sous-classe des Cirripedes (Cirripedia Burmeister, 1834) super-ordres des Thoraciques et des Acrothoraciques (Thoracica Darwin, 1854- Acrothoracica Gruvel, 1905). In: J. FOREST (ed.), Traite de Zoologie Anatomie, Systematique, Biologie, 7 (2): 453-540. NEWMAN, W. A. & A. Ross, 1971. Antarctic Cirripedia. Monographic account based on specimens collected chiefly under the United States Research Program, 1962-1965. Antarct. Res. Ser., 14: 1-257. - - & - - , 1976. Revision of the Balanomorph barnacles; including a catalogue of the species. Mem. San Diego Soc. nat. Hist., 9: 1-108. NEWMAN, W. A., V. A. ZULLO & T. H. WITHERS, 1969. Cirripedia. In: R. C. MOORE (ed.), Treatise on invertebrate palaeontology, R. Arthropoda, 4 (1): R206-R295. (Geol. Soc. America, Univ. Kansas). PILSBRY, H. A., 1916. The sessile barnacles (Cirripedia) contained in the collections of the U.S. National Museum; including a monograph of the American species. Bull. U.S. natn. Mus., 93: 1-366. PINNA, M. C. C. DE, 1991. Concepts and tests of homology in the cladistics paradigm. Cladistics, 7: 367-394. UTINOMI, H., 1967. Comments on some new and already known cirripeds with emended taxa, with special reference to the parietal structure. Pubis Seto mar. bioi. Lab., 15 (3): 199-237. WHITTLESEY, K. E., 1998. The paleobiology, paleoecology, and statigraphic significance of Tamiosoma gregaria in the Pancho Rico formation, Salinas Valley, California: 1-218. (Thesis, Geological Science, University of Southern California). YAMAGUCHI, T., 1980. A new species belonging to the Balanus amphitrite Darwin group (Cirripedia, Balanomorpha) from Japan; an example of peripheral speciation. Journ. Palaeontol., 54 (5): 1084-1101. ZULLO, V. A., 1984. New genera and species of balanoid barnacles from the Oligocene and Miocene of North Carolina. Journ. Palaeontol., 58 (5): 1312-1338. - - , 1992. Revision of the balanid barnacle genus Concavus Newman, 1982, with a description of a new subfamily, two new genera, and eight new species. Journ. Palaeontol., 66 (6): 1-46.

First received 22 July 1998. Final version accepted 13 January 1999.