J. Mar. Biol. Ass. U.K. (1999),79,1039^1044 Printed in the United Kingdom

Larval development of a warm-water immigrant , Solidobalanus fallax (Cirripedia: ) reared in the laboratory

Olga M. Korn* and Aleksey S. El¢movO *Institute of Marine Biology FEB RAS, Vladivostok, 690041, Russia. E-mail: [email protected]. ODepartment of Invertebrate Zoology, Moscow State University, Moscow, 119899, Russia

In 1994 a warm-water barnacle Solidobalanus fallax was recorded for the ¢rst time in the UK (South- ward, 1995). The naupliar development of this immigrant is now described, from larvae reared in the laboratory. The planktotrophic nauplii of S. fallax reached the cyprid stage 8 d after hatching, at 258C. Larval development includes six naupliar and one cyprid stage, following the typical pattern of the thoracican Cirripedia. Naupliar stages have a broad rounded convex cephalic shield without dorsal and marginal spines. Nauplii have a trilobed labrum with the small teeth found in other warm-water species. The abdominal process becomes nearly equal to the dorsal thoracic spine in stage VI. The arrangement of abdominal spines and larval setation are in the usual balanoid pattern. The signi¢cant di¡erence of the S. fallax larvae from those of the related temperate-water archaeobalanid species Hesperibalanus hesperius supports the classi¢cation of these species into separate genera.

INTRODUCTION amphitrite (Clare et al., 1995). Newly hatched Solidobalanus fallax (Broch) (Archaeobalanidae) ranged nauplii I were concentrated with a beam of light and then from Angola through West Africa and Morocco to transferred to 1-l beakers containing ¢ltered seawater with added antibiotics. For this study, nauplii were cultured at Algeria, occurring at 7^220 m depth (Newman & Ross, 25 C on a mixed diet of Skeletonema costatum (approxi- 1976; Southward, 1995). In 1994 this species was recorded 8 mately 5 10 4 71 for the ¢rst time in Europe, in the English Channel o¡ cells ml ) and Thalassiosira weis£ogi (approximately 3 103 cells ml71). Larvae were preserved Plymouth, at 44^56 m depth on the valves of the queen  scallop, Aequipecten opercularis (Southward, 1995). The in 4% formalin. Drawings were made using a camera discovery was followed-up by studies of the ecology, lucida, and measurements were made with an ocular larval development and settlement of this immigrant micrometer. species. The following measurements were taken: total body The family Archaeobalanidae comprises three subfami- length, from the anterior margin of the shield to the tip lies: Archaeobalaninae, Semibalaninae and Elminiinae. of the dorsal thoracic spine; shield width (the greatest In the subfamily Archaeobalaninae the larval stages are width of the body behind the frontolateral horns); shield known for Hesperibalanus hesperius (Barnes & Barnes, 1959; length, from the anterior margin of the shield to the Korn & Ovsyannikova, 1981), spongites (Moyse, hind shield margin, excluding the posterior shield spines 1961), Chirona hameri (Crisp, 1962), and galeata in naupliar stages IV,V and VI; the length of the fronto- (Molenock & Gomez, 1972; Lang, 1979). Solidobalanus lateral horns and posterior shield spines in naupliar fallax is another member of this subfamily.The purpose of stages IV, V and VI. Measurements were also taken of this paper is to describe the larval development of cyprid length, from the anterior to the posterior cara- S. fallax under laboratory conditions and to use larval pace margins; and cyprid depth, the distance between morphology as additional information for comparative the dorsal and ventral margins of the carapace at the studies of the archaeobalanine group. deepest point. Alphabetical setal formulae follow the system of Newman (1965) and Lang (1979). MATERIALS AND METHODS Specimens of Solidobalanus fallax were obtained by RESULTS trawling in June^November 1995 from the Plymouth area Larval culture (inside the Eddystone, mostly between East and West Rutts). Adults obtained from the shells of Aequipecten Larval development of Solidobalanus fallax includes six opercularis, and from the carapace and limbs of the spider naupliar and one cyprid stage, following the typical crab, Maia squinado, also from shells of Buccinum inhabited pattern of development in the thoracican Cirripedia. by hermit crabs, were maintained in the laboratory as Development through six naupliar stages to the cyprid broodstock using techniques, previously developed for took 8 d at 258C(Table1).

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Table 1. Time taken at 258C for the appearance Larval morphology of the larval stages of Solidobalanus fallax. Mean sizes of the larval stages are given in Table 2. Body shape and setation of appendages are illustrated in Larval stage Day of appearance Figures 1^6. Setal formulae (after Newman, 1965) are given inTable 3. I 1 Nauplius larvae have a broad rounded convex cephalic II 1 III 2 shield with a pair of fairly long posterior spines at stages IV 3 IV^VI and without any other (dorsal or marginal) spines. V 4 The shield is only slightly longer than broad. Frontolateral VI 5 horns are of medium length, directed forward from stage Cyprid 8

Figure 2. Solidobalanus fallax. Labras (ventral view) of Figure 1. Solidobalanus fallax. Body outlines (ventral view) of naupliar stages I^VI (A^F) and thoraco-abdominal processes naupliar stages I^VI (A^F) and cyprid stage (G). (lateral view) of naupliar stages II^VI (G^K). Scale bar: 100 mm. Scale bar: 100 mm.

Table 2. Measurements (mm) of the cultured larvae of Solidobalanus fallax.

SWor CD Stage N TL (Mean SD) SL (Mean SD) SP (Mean SD) (Mean SD) FL (Mean SD) Æ Æ Æ Æ Æ I 4 253 3.7 127 6.1 58 5.2 II 10 428 Æ10.6 190 Æ6.1 99 Æ4.2 III 10 502 Æ8.6 250 Æ4.7 91 Æ5.0 IV 10 595 Æ21.0 346 14.5 91 7.3 321 Æ7.3 104 Æ10.9 V 10 727 Æ20.5 451 Æ10.9 127 Æ9.3 415 Æ11.1 122 Æ7.8 VI 10 885 Æ33.7 562 Æ15.6 156 Æ9.1 500 Æ13.2 125 Æ14.5 Cyprid 10 688 Æ21.4 Æ Æ 323 Æ10.5 Æ Æ Æ TL, total length; SL, shield length; SP, posterior shield spine length; SW, shield width or CD, cyprid depth; FL, frontolateral horns length; N, number; SD, standard deviation.

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Figure 4. Solidobalanus fallax. Antennae of naupliar stages I^IV (A^D). Scale bar: 100 mm.

Nauplius I (Figures 1A, 2A, 3A, 4A, 6A) Body shape is typical of stage I balanoid nauplii. The cephalic shield is pear-shaped, with well-developed fron- tolateral horns folded at angles to the long axis of the body. Thoraco-abdominal processes are short and poorly Figure 3. Solidobalanus fallax. Antennules of naupliar stages developed. Trilobed labrum is devoid of teeth and hairs. I^VI (A^F). Scale bar: 100 mm. All setae are simple.

Nauplius II (Figures 1B, 2B, G, 3B, 4B, 6B) II and de£ected ventrally from stage IV. The labrum is Body shape is rounded. The frontal shield margin is trilobed, and the median lobe projects well beyond the convex. Frontolateral horns are long, slender and lateral ones. From stage II, the median labral lobe bears de£ected forward. Labrum has slender hairs. Two small several (1^3 pairs) of small teeth. Thoraco-abdominal teeth appear on the medial labral lobe. The abdominal processes are fairly long. In stage VI the abdominal process process is about 3/4 of the dorsal thoracic spine. The nearly matches the dorsal thoracic spine. The arrangement dorsal thoracic spine is barbed. The abdominal process of spines on the abdominal process is in the usual balanoid bears one pair of series-1 spines and some barbs proxi- pattern. As usually in balanoid larvae, antennae have one mally and distally. Some setae are plumose. cuspidate and one plumodenticulate seta, mandibles have two cuspidate setae. The mandibular plumodenticulate Nauplius III (Figures 1C, 2C, H, 3C, 4C, 6C) setae are poorly developed. The number and type of setae The cephalic shield has increased in size. The frontal varied little within each stage. shield margin is straighter. Frontolateral horns are shorter The diagnostic features of each larval stage can be than in stage II. The antennule bears the ¢rst preaxial summarized as follows. setae.

Table 3. Setal formulae for the nauplii of Solidobalanus fallax.

Antennule Antenna Mandible

Naupliar stage Exopod Endopod Exopod Endopod

VI S:SP:PSPP:SP:PPS:S 4P:8P PPPSP:SPP:PD:PSCP:G P:5P SSSS:PSPS:sPCP:PCP:G V S:SP:PSPP:SP:SP:S 3P:7PS PPPSP:SPP:PD:PSCP:G P:4PS SSSS:PSPS:sPCP:PCP:G IV SP:PSPP:SP:P:S 3P:6P PPPSS:SPS:PD:PSCP:G P:3PS SSSS:PSP:sPCP:PCP:G III S:PSPP:SP:P:S 2P:5P PPP:SP:PD:PSCS:G P:3PS SSS:PSS:PCP:PCP:G II SSPS:SP:P:S SP:4PS PPS:SP:PD:PSC:G P:3Ps SSS:PS:PCS:PC:G I SSSS:SS:S:S S:4S SSSS:SS:SS:SS:G S:3S SSS:SS:SS:SS:G

Setal types: S, simple; P, plumose; C, cuspidate; D, plumodenticulate; G, gnathobase; s, short seta.

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Figure 6. Solidobalanus fallax. Mandibles of naupliar stages I^VI (A^F). Scale bar: 100 mm.

Figure 5. Solidobalanus fallax. Antennae of naupliar stages V^VI (A^B). Scale bar: 100 mm.

Nauplius IV (Figures 1D, 2D, I, 3D, 4D, 6D) The cephalic shield has a posterior border with a pair of spines de£ected dorsally. The frontal shield margin is slightly convex, with a hollow near the naupliar eye. Figure 7. Cephalic shield outlines of naupliar stage VI of Frontolatral horns are de£ected forward and ventrally. Solidobalanus fallax (A), Hesperibalanus hesperius (B) and Balanus The labrum with two pairs of teeth. The dorsal thoracic crenatus (C). Scale bar: 100 mm. spine is longer than the abdominal process, as in stage III. There are two series-1, three series-2 abdominal spines, and some barbs proximally. DISCUSSION Breeding season NaupliusV (Figures 1E, 2E, J, 3E, 5A, 6E) Morphologically similar to stage IV except in size. Little is known about the reproductive pattern of Frontolateral horns are directed more frontally. There are Solidobalanus fallax. In the English Channel, Southward two series-1, about ¢ve series-2, and two series-3 abdom- (1995) recorded brooding individuals in late May, indi- inal spines. cating a potential for recruitment in British waters. In the present survey, gravid specimens were collected from June NaupliusVI (Figures 1F, 2F, K, 3F, 5B, 6F) till November. Juveniles of S. fallax were found in Body shape similar to stage V. Posterior shield spines are October and November, estimated to be 1^2-months old longer. The dorsal thoracic spine matches the abdominal by comparison with the laboratory-settled individuals, process in some specimens. A pair of compound eyes indicating settlement in August^September. Since adults appears laterally to the naupliar eye. Larvae possess collected in November spawned naturally in the labora- six pairs of series-2 spines. Series-1, 2, and 3 spines tory, larval development and settlement may continue on the abdominal process are in the usual balanoid until December if sea temperature allows. pattern.

Cyprid (Figure 1G) Larval development Fusiform in dorsal view, rounded anteriorly and more In present study, duration of larval development of pointed posteriorly. Small dorsal hump is seen in lateral S. fallax is considerably shorter in comparison with boreo- view. Anterior part with numerous oil cells. arctic . Obviously, this is due to the higher

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temperature of culturing. In other batches of larvae In spite of the super¢cial similarity between S. fallax and cultured at 228C cyprids appeared within 20 days. Larvae B. crenatus adults, their larvae have clear di¡erences (Figure of the temperate-water Hesperibalanus hesperius reached the 7A & C). Balanus crenatus nauplii have a body shape typical cyprid stage within 18 d under laboratory conditions at 20^ for the family Balanidae. They are pearshaped and elon- 228C (Korn & Ovsyannikova,1981). gated (shield length is much more than width). Frontolateral The north Paci¢c H. hesperius, predominantly of cold- horns and posterior shield spines are fairly short water distribution, ranging from the Bering Sea to (Branscomb & Vedder, 1982; Ovsyannikova & Korn, 1984). Monterey Bay (California) is fairly closely related to In terms of larval morphology, the family Archaeobala- S. fallax. Earlier, S. fallax and H. hesperius were placed in nidae is a heterogeneous group (Egan & Anderson, 1985; the same genus, Solidobalanus (Newman & Ross, 1976). In Korn, 1995). Larvae of Semibalaninae di¡er greatly from 1980 S. hesperius was classi¢ed as Hesperibalanus (Newman other subfamilies and show a pearshaped body shape & Abbot, 1980). After re-examination of the type material, typical of the family Balanidae. Archaeobalaninae nauplii Zullo & Kite (1985) proposed a generic separation based share some features with Elminiinae larvae. For example, on operculum characters and left Hesperibalanus as a two- the naupliar body form of S. fallax is similar to that of species genus including H. hesperius. All other members of Elminius covertus (Egan & Anderson, 1985). At the same Hesperibalanus and Solidobalanus are placed in the genus time, nauplii of and Hexaminius popeiana Solidobalanus until re-examination of adult morphology have dorsal shield spines (Molenock & Gomez, 1972; (Southward, 1995). Egan & Anderson, 1985). Acasta spongites larvae have A comparison of larvae of these two species showed the numerous marginal spines (Moyse, 1961). Similar to following (Figure 7 A,B). Larvae of both species have a S. fallax, nauplii of E. covertus have small labral teeth smooth cephalic shield without dorsal and marginal (Egan & Anderson, 1985). The abdominal process exceeds spines, long posterior spines de£ected dorsally and fairly the dorsal thoracic spine in larvae of E. covertus and long frontolateral horns de£ected anteriorly. The arrange- Hexaminius popeiana (Egan & Anderson, 1985). ment of spines on the abdominal process and setation Further studies of the larval morphology of archaeoba- formulae are in the usual balanoid pattern. lanid species will provide additional data for systematic However, H. hesperius nauplii II^III are slender, elon- and phylogenetic implications of larval di¡erences. gated, with very long thoraco-abdominal processes; the cephalic shield is almost triangular. The cephalic shield of nauplii IV^VI is trapeziform, with a straight anterior A.E. would like to thank the Ray Lankester Fund and the margin and only slightly convex lateral edges. Frontolateral Marine Biological Association of the United Kingdom for the horns and posterior shield spines are very long, especially investigatorship. A.E. is very grateful to Professor M. Whit¢eld, in American waters (Barnes & Barnes, 1959). Professor A. Southward, Dr E. Southward, Dr A. Clare, Dr J. In contrast, S. fallax larvae have a broad rounded Green and Mrs L. Mavin for their hospitality and help during cephalic shield. The shield is only slightly longer than his working visit to the Plymouth Marine Laboratory. Thanks are due to Mr R.C. Swinfen and the crews of RV `Squilla' and broad. Frontolateral horns and posterior spines are shorter RV `Sepia' for help in sampling. than those in H. hesperius. The cephalic shield in S. fallax is more convex, so frontolateral horns in this species are de£ected ventrally, whereas the posterior shield spines are REFERENCES de£ected more dorsally in H. hesperius. The abdominal Barnes, H. & Barnes, M., 1959. The naupliar stages of Balanus process remains shorter than the dorsal thoracic spine until hesperius Pilsbry. CanadianJournal of Zoology, 37, 237^244. stage VI in H. hesperius and becomes nearly equal at stage Branscomb, E.S. & Vedder, K., 1982. A description of the VI in S. fallax. 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Larval development of antennal endopods of this species are replaced with Elminius covertus Foster and Hexaminius popeiana Foster small rudimentary s-setae. It should be noted that the (Cirripedia: Archaeobalanidae: Elminiinae) reared in the total number of antennal and mandibular setae in stages laboratory. Australian Journal of Marine and Freshwater Research, IV^VI is considerably larger in S. fallax (antenna VI of 36, 383^404. S. fallax bears 26, but H. hesperiusö20 setae). It has repeat- Korn, O.M., 1995. Naupliar evidence for cirripede edly been mentioned that increase of setal complexity of and phylogeny. In New frontiers in barnacle evolution (ed. F.R. barnacle larvae is apparently related to occurrence in Schram and J.T. HÖeg), pp. 87^121. Rotterdam: A.A. warm waters, where ¢ne-meshed ¢lters are required to Balkema. [ Issues, no.10.] ¢lter the predominant small £agellates in such waters (Lee Korn, O.M. & Ovsyannikova, I.I., 1981. 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Journal of the Marine Biological Association of the United Kingdom (1999)

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