J. Mar. Biol. Ass. U.K. 2000), 80, 995^1005 Printed in the United Kingdom

All three species of Ptychodactiaria belong to order Actiniaria : )

Valerie A. Cappola and Daphne G. Fautin* Department of Ecology and Evolutionary Biology, and Natural History Museum and Biodiversity Research Center, University of Kansas, Lawrence, Kansas 66045, USA. *Corresponding author, e-mail: [email protected]

Ptychodactiaria, currently recognized as an order equivalent to Actiniaria sea anemones sensu stricto) and `true' or hard corals) of cnidarian class Anthozoa, contains three monotypic genera, Dactylanthus, Ptychodactis,andPreactis, in two families, Ptychodactiidae and Preactiidae. Features that had been considered distinctive to the order among hexacorallian anthozoans were that gametes mature in protrusions fromthe mesenteries, as in octocorallian anthozoans, and that gametes do not mature embedded in mesogloea. However, we found that ptychodactiarian gametes develop in the mesenteries, surrounded by mesogloea, as in other sea anemones. We conclude that the three species constitute a clade, the most distinctive feature of which is medially fused mesenteries at the proximal end of the body. This clade merits subordinal status within order Actiniaria. We rede¢ne Ptychodactiaria and its component taxa, moving Dactylanthus fromfamily Ptychodactiidae to family Preactiidae.

INTRODUCTION members of tribe of suborder Nynantheae; another tribe of Nynantheae, Athenaria, is characterized Ptychodactiaria, currently recognized as an order by lack of both base and basilar muscles). England in equivalent to the Actiniaria sea anemones sensu stricto) England & Robson, 1984) asserted that Preactis has and Scleractinia `true' or hard corals) of cnidarian class basilar muscles, and therefore removed the absence of Anthozoa, contains three monotypic genera in two basilar muscles as a character of Ptychodactiaria, but we families: Dactylanthus and Ptychodactis comprise family did not ¢nd basilar muscles in P. millardae. The de¢nite Ptychodactiidae, and Preactis belongs to family Preactiidae. base and lack of basilar muscles do characterize this At present, the order is de¢ned by only one apomorphy, group as well as some groups of actiniarians. `Gonads not enclosed in the mesogloea' England in `Filaments without ciliated tracts' is the third attri- England & Robson, 1984, p. 315). Our histological data bute of Ptychodactiaria listed by Carlgren 1949). do not support this unusual position of the gonads: ex- Members of Protantheae also lack them, and, indeed, amination of all three species showed the gametes are ptychodactiarians had been placed among protanthean surrounded by mesogloea, as in other anthozoans. actiniarians by Appello« f 1893) and Carlgren 1911). Although our data support the three species constituting However, the mesenterial ¢laments of Preactis have a clade, the clade does not merit ordinal status. ciliated tracts England & Robson, 1984; personal The systematic arrangement of sea anemones sensu lato observation). Thus, neither the presence nor the absence orders Actiniaria, , and Ptychodac- of mesenterial ¢laments distinguishes ptychodactiarians tiaria) currently used is that of Carlgren 1949). In his fromactiniarians. 1949 catalogue, Carlgren raised to ordinal level the The fourth character listed by Carlgren 1949), which actiniarian family Ptychodactiidae, then consisting only he Carlgren, 1911) had de¢ned in his redescription of of Ptychodactis patula and Dactylanthus antarcticus.In1984, Dactylanthus antarcticus, is `Distal end of the ¢laments of England in England & Robson) rede¢ned the order the imperfect mesenteries drawn out into two lobes giving Ptychodactiaria to accommodate the new and this part of the ¢lament the appearance of a bisected species Preactis millardae, which has characteristics inter- funnel'. This character, which is not found in any mediate between those of actiniarians and the other actiniarian, was omitted in England's rede¢nition of the ptychodactiarians, leaving the arrangement of gonads as order England & Robson, 1984). It is insu¤ciently the only character distinguishing Ptychodactiaria. Attri- signi¢cant to de¢ne an entire order, we have found this butesöand how interpretation of themhas changed feature to be a stage in mesentery development. through timeöof the three species that constitute order The ¢fth and sixth characters relate to the position and Ptychodactiaria are presented inTables 1 & 2. morphology of the gonads. Where we use the term Carlgren 1949) de¢ned the order with six characters. `gonad', it is for consistency with writings that we cite. The ¢rst two page 10) were `de¢nite base but without However, zoantharian cnidarians lack discrete gonads basilar muscles'. A de¢nite base with no basilar muscles is Fautin, 1999), and what is meant by `gonad' is actually characteristic of actiniarian suborders Protantheae and the gametogenic tissue of the mesenteries. Carlgren Endocoelantheae, as well as tribe Boloceroidaria of 1949) wrote of Ptychodactiaria `Gonads below the suborder Nynantheae basilar muscles are found only in ¢laments, not enclosed in the mesogloea but stalked,

Journal of the Marine Biological Association of the United Kingdom 2000) 996 V.A. Cappola and D.G. Fautin Ptychodactiarians are actiniarians but layered on either sideit of vesicles' Not embedded in mesogloea Covered with `tentaculate Spirocysts, basitrichs, atrichs Preactis millardae original description England in England & Robson, 1984 lamella but attached to itstalks by columns column Eggs not embedded in mesogloeal Dactylanthus antarcticus redescription Carlgren,1911 egg placement] [Female illustrated; no comment about Studded with simple vesiclesNo comment Outgrowths `Auswuchse') in 24 Spirocysts in outgrowths, rare in Cystiactis antarcticus original description Clubb,1908 f, 1893 « spermcapsules as in other actiniarians circumferentially in tentacles No comment No comment Present No comment Ptychodactis patula original description Appelo Notable features of the Ptychodactiaria according to the original descriptions and a redescription. on incomplete mesenteries 9. Fusion of mesenteries No comment No comment Proximal Proximal 1.2. Mouth3. Actinopharynx4. Siphonoglyphs5. Cycles of mesenteries6. No. of complete mesenteries7. Fertility of mesenteries8. Ciliated tracts on 24 ¢laments Half-funnel structures Rudimentary distal 5, irregularly arrayed Absent Absent No Always comment open 2 Short, strongly plicated All No comment 24 2 No comment Not long, extensible 2 Wide Absent Well developed All 12 or 24 2 Greatly expanded Present 2, hexamerously arrayed 24 All 2 10.11. Mesenterial retractor muscles12. Gametogenic tissue Poorly Gonad developed structure Proximal to ¢laments Eggs not enclosed in mesogloea, Weak but well marked No comment Weak Proximal to ¢laments Weak, 2 per mesentery Same level as ¢laments 13.14. Longitudinal column muscles15. Sphincter muscle Present16. Basilar muscles17. Parietobasilar muscles Column morphology18.19. Tentacle array, number Cnidae Absent No distinct ones Furrowed No longitudinally comment and Marginal, 5 rows Weak Small Rare on oral disc, same as those 24 No comment Di¡use, endodermal Weak Absent or weak Faint Absent 24 distalmost column outgrowths) None on oral disc Absent Absent Present, very weak Absent Table 1.

Journal of the Marine Biological Association of the United Kingdom 2000) Ptychodactiarians are actiniarians V.A. Cappola and D.G. Fautin 997 f ), and by e atrichs, heterotrichs ^ ^ ^ ^ ^ Spirocysts, e e )by Dunn 1983 d e , 1949 e c f ,1940 b as stated by Carlgren 1911) spirocysts in tentacles and column protuberances f ^^ ^^ 12, 24 in larger specimens ^^ ^^ 2 Not entirely below ¢laments Not apparent ^^ ^^ ^^ Digitiform, 24 Atrichs everywhere, , 1934 a e d c d g d d e d e d in tentacles depicted secondary mesenteries d d Present Absent Atrichs everywhere, spirocysts ^^^ 2 2 12 Notasprominentasusually Weak Proximal to ¢laments on Absent Vesicle-like outgrowths Short, 24 Weak, di¡use 7)as altered by Carlgren 1911 ^ d Short ^ ^ ^ columns 5 f « c d b d spirocysts in tentacles described ^^^^^ Not as reduced as Appelo ^^ ^^ ^^ Slightly coalesced ^^ ^^ ^^ Absent ^^ ^^ Atrichs everywhere, Dactylanthus antarcticus Ptychodactis patula Dactylanthus antarcticus . g a a 4)and d d ^ a a a d columns 2 f reported them a a « a a a lamella by stems and column ^^^ ^^^^^^ ^^^^^^ ^^^^^^ ^^^^^^ ^^^ Present , and in Dayton et al. 1997 f Ptychodactis patula Characters of on incomplete mesenteries 3. Siphonoglyphs 4. Cycles of mesenteries5. No. of complete mesenteries Always 12, usually 24 9. Irregularly Fusion arranged of mesenteries Proximal half not fused 2. Actinopharynx Degenerate 6. Fertility of mesenteries 7. Ciliated tracts on ¢laments 8. Half-funnel structures distal 1. Mouth Wide 10. Mesenterial retractor muscles Weak 16. Parietobasilar muscles17. Column morphology18. Tentacle array, number Appello Smooth Numerous Table 2. 11. Gametogenic tissue12. Gonad structure 13. Longitudinal column muscles 14. Sphincter muscle 15. Basilar Eggs muscles attached to mesogloeal 19. Cnidae Absent Spirocysts rare in tentacles England in England & Robson 1984

Journal of the Marine Biological Association of the United Kingdom 2000) 998 V.A. Cappola and D.G. Fautin Ptychodactiarians are actiniarians recalling the arrangement of the gonads in the Alcyo- examined from Darwin Canal, Chile 458260S748050W) naria'. In Ptychodactis, gametogenic tissue is proximal to USNM 96507 and 96508), and one specimen of Preactis `below') the ¢laments on all mesenteries. However, in millardae collected in Oudekraal, Coast of Good Hope, Dactylanthus, only the secondary mesenteries have this South Africa California Academy of Sciences [CAS] arrangement; gametogenic tissue and ¢laments of the 34038). primary mesenteries are arrayed as they are in actiniar- The characters previously used to de¢ne Ptychodac- ians. In Preactis, gametogenic tissue and ¢laments may tiaria Tables 1 & 2) were reassessed Table 3) in all three occur at the same level of a mesentery Figure 1), as in ptychodactiarian species. typical sea anemones. Carlgren's characterization of the gonads as not being enclosed in mesogloea and being RESULTS stalked is both a misrepresentation of the literature and factually in error, as we show below. Immature females of Ptychodactis patula and Dactylanthus antarcticus have oocytes on either side of a thin lamella of mesenterial mesogloea, each oocyte surrounded by MATERIALS AND METHODS mesogloea Figures 5A & 6, respectively). In the The general morphology and cnidae in museum speci- specimens studied, ova of P. patula measured 45^65 mm mens of Ptychodactis patula Figure 2), Dactylanthus antarcticus in diameter, and ova of D. antarcticus measured 25^40 mm Figure 3), and Preactis millardae Figure 4) were studied. in diameter. In a mature male P. patula Figure 5B), the Cnidae were measured in squash preparations at Â1000. spermcapsules occupy the centre of the mesogloeal Histological sections 8 mmthick prepared frommesen- lamella. The sperm capsules of the specimen of Preactis teries, column^oral disc region, and column^base region millardae studied are enclosed in mesogloea Figure 7). were stained with Heidenhain's azan Presnell & The gametes of D. antarcticus and P. millardae lie between Schreibman, 1997). the two bands of longitudinal retractor muscles of the Two complete specimens of Ptychodactis patula and one mesenteries; those of Ptychodactis patula lie between the wedge of an were examined. One complete single retractor muscle band and the edge of the mesen- specimen bearing Swedish Museum of Natural History tery. [SMNH] catalogue number 20214) and that from which The gametogenic tissue of P. patula is proximal to the wedge was taken a syntype: SMNH 4887) were the mesenterial ¢laments on all mesenteries, as it is on the collected in TrondheimFjord, Norway. The other secondary mesenteries of D. antarcticus. However, on the complete specimen came from the mouth of Kotzebue primary mesenteries of D. antarcticus, there is a middle Sound, Alaska US National Museumof Natural History region in which both ¢laments, which extend distally, and [USNM] 55624). Four specimens of D. antarcticus were gametogenic tissue, which extends proximally, occur. Ciliated tracts are absent in both species. Filaments occur along the free edge of all mesenteries of Preactis millardae, with ciliated tracts only at the level of the actinopharynx; gametogenic tissue extends about 80% the length of the mesentery, from just proximal to the mesenterial ¢laments distally to just proximal to the actinopharynx. Distal to the gametogenic tissue, the two bands of retractor muscles lie side by side, thereby forming a single band, unlike in ¢gure 6 of England & Robson 1984) Figure 1 in this paper), which shows themremaining separate to the distal end of the animal. The mesenteries of Ptychodactis patula are regularly arrayed, contrary to what Appello« f 1893) reported. They are also regularly arrayed in the other two species. The members of each pair and couple of mesenteries are fused medially, which produces separated pockets of coelenteric space at the proximal end of the animal. In P. patula the mesenteries are fused only at their extreme proximal ends, whereas fusion occurs along a quarter their length in D. antarcticus and a third their length in Preactis millardae. Individuals of the latter two species are highly extensible in length, so the extent of the fusion may di¡er in life and in preservation. The structures described by Carlgren 1911) were interpreted by us as bisected funnels on the incomplete mesenteries of D. antarcticus to be the distalmost portion of the mesenteriesöthat part attached to the underside of the oral disc. Such structures are also Figure 1. Diagrammatic longitudinal section of Preactis present in Ptychodactis patula but are absent in Preactis millardae ¢gure 6 in England & Robson, 1984). Z, zone of millardae, in which all the mesenteries are complete in fusion. the specimen examined.

Journal of the Marine Biological Association of the United Kingdom 2000) Ptychodactiarians are actiniarians V.A. Cappola and D.G. Fautin 999 O Same level as ¢laments ,proximalto¢laments 8 2 , some at same level as ¢laments; 8 , indicates an inference. O 100 24 distalmost tentaculate vesicles) Distalmost tentaculate vesicles  Ptychodactis patula Dactylanthus antarcticus Preactis millardae Features of the Ptychodactiaria from re-examination of all three species. 1. Mouth2. Actinopharynx3. Siphonoglyphs4. Cycles of mesenteries5. No. of complete mesenteries6. Fertility of mesenteries7. Ciliated tracts on ¢laments8. Half-funnel structures distal on9. incomplete Fusion of mesenteries mesenteries Developmental stage 24 Very short, 4 strongly *or folded 5), regularly Absent arrayed Absent All Capable of opening wide Developmental stage Proximal end Short, strongly 2, regularly folded arrayed Developmental stage Capable of opening wide 12 Short, or strongly 24 2 folded Absent 2, regularly arrayed Capable of opening wide All Proximal quarter of body Proximal third of body 24 Present 2 All Table 3. 19. Cnidae*, indicates a feature that has been reported but that did not occur in the specimens we examined; Spirocysts, atrichs Spirocysts, atrichs Spirocysts, basitrichs, atrichs 10. Mesenterial retractor muscles11. Gametogenic tissue Single, weak Proximal to ¢laments Double, weak 1 Double, weak 12. Gonad structure13. Longitudinal column muscles14. Sphincter muscle15. Basilar muscles16. Parietobasilar muscles17. Column morphology18. Tentacle array, number Absent Enclosed in mesogloea Absent Absent Furrowed Absent Marginal, longitudinally and circumferentially 24 columns of tentaculate vesicles Covered with tentaculate vesicles Enclosed in mesogloea Absent Di¡use Enclosed Absent endodermal in or mesogloea absent Absent Absent Absent Absent Absent

Journal of the Marine Biological Association of the United Kingdom 2000) 1000 V.A. Cappola and D.G. Fautin Ptychodactiarians are actiniarians 5) m). m Female 6) m). Dactylanthus m Live specimen of 3) CAS 34038). In preservation, the animal Preactis millardae CAS 34038) diameter of the indicated sperm capsule is about 40 Live specimen of 4) Preactis millardae Male m); B) male USNM 55624) width of the indicated sperm capsule is about 40 m 7) m). m : A) expanded SMNH 20214) diameter about 40 mm); B) contracted USNM 55624). Gametogenic region of mesenteries showing that mesoglea stained blue) surrounds developing gametes, both male and female. 7) ^ 5 Ptychodactis patula USNM 96057) diameter of the indicated egg is about 25 Preserved specimens of : A) female SMNH 20214) diameter of the indicated egg is about 55 7. 2) ^ photographed by L. Peck, British Antarctic Survey. Specimens we studied were as long as 50 mm. Ptychodactis patula antarcticus is 100 mm long. Photograph by T.M. Gosliner. Figures 2 Dactylanthus antarcticus

Journal of the Marine Biological Association of the United Kingdom 2000) Ptychodactiarians are actiniarians V.A. Cappola and D.G. Fautin 1001

Table 4. Cnidae of the three species of Ptychodactiaria. Number following species name is number of specimens in which capsules were measured. Capsule measurements are range of lengthÂwidth in mm; number of capsules measured follows in parentheses. Measurements for the oral disc of Ptychodactis patula are absent because one specimen was gaping so wide its oral disc was obliterated, and no cnidae were found in the other; measurements for the column of Preactis millardae are absent because it is so densely covered with tentaculate vesicles that contamination was unavoidable. Atrichs of all species varied in appearance; ¢gure 10 A.c., B.b., and B.e in England & Robson 1984)illustrate some variants.

Ptychodactis patula Nˆ2) Dactylanthus antarcticus Nˆ4) Preactis millardae Nˆ1)

Tentacles Spirocysts 11.6^18.9Â2.5^3.2 21) 15.3^26.6Â2.3^3.3 54) 16.2^21.8Â2.9^4.0 13) Basitrichs ^^13.3^22.7Â2.8^3.5 17) Atrichs 13.7^24.9Â3.0^4.9 30) 18.4^31.0Â2.7^5.0 78) 17.0^33.1Â3.0^4.0 19) Tentaculate Vesicles None in this species Spirocysts ^ 14.9^25.0Â2.0^3.4 45) 16.3^21.5Â2.9^3.4 10) Basitrichs ^^15.8^18.7Â2.3^3.3 11) Atrichs ^ 16.3^33.5Â2.7^4.3 69) 19.4^30.5Â2.8^4.2 21) Oral Disc Spirocysts ^^15.7Â3.0 1) Atrichs ^ 13.7^24.6Â2.0^4.4 63) 15.3^19.0Â2.1^3.1 18) Actinopharynx Basitrichs ^^17.9Â2.3 1) Atrichs 11.7^19.1Â2.0^4.1 15) 14.8^27.5Â2.7^4.7 70) 14.8^25.9Â2.6^4.3 20) Mesenterial Filaments Atrichs 15.1^25.0Â2.3^4.1 14) 12.5^24.4Â2.5^4.3 14.1^25.7Â2.0^3.3 19) one was 4.9 mmwide) 64) Column Measured in 3 specimens Atrichs 14.9^20.6Â2.5^4.6 21) 16.3^23.7Â2.7^4.4 29) ^

The actinopharynx of all species is proportionally shorter & Robson as B.c. termed a heterotrich) rather than that than is typical of sea anemones, and is highly plicate. The illustrated as A.b. termed a basitrich). siphonoglyphs of D. antarcticus and P. millardae are prolonged aborally, as has been reported e.g. Clubb, 1908; England & Robson, 1984, respectively). The ¢ne DISCUSSION transverse ridges on the siphonoglyph of D. antarcticus Gametogenic tissue were ¢rst noted by Carlgren 1911). As has been reported for example by Appello« f, 1893), Ptychodactis patula lacks The single apomorphy ostensibly distinguishing siphonoglyphs. It has a unique crinkled sheet of tissue Ptychodactiaria fromother anthozoans of subclass where some but not all, in our experience) of the , and uniting its three genera, is the structure complete mesenteries attach to the aboral end of the of the gametogenic tissue England & Robson, 1984). In siphonoglyph. This structure was described by Appello« f other anthozoans, gametes arise in the endoderm but move 1893, p. 5) as resembling `eines Grunkohlblattes'öa leaf into the mesogloea, which surrounds them as they mature of kale. To us, each resembles a fully extended folding Hyman, 1940; Fautin, 1999). Gametes in members of fan. order Ptychodactiaria are supposedly not surrounded by Wecould not ¢nd ectodermal longitudinal muscles in the mesogloea, presumably maturing in the endodermal column of any of the three species, despite reports of it in tissue fromwhich they arise. We found ptychodactiarians P.patula according to Appello« f, 1893) and D. antarcticus not to di¡er fromother anthozoans in this regard; their according to Clubb, 1908; Carlgren, 1911). Such muscula- maturing gametes are enclosed in the mesogloea of the ture is clear in sections examined from Gonactinia prolifera, mesenteries. This misconstruction of the nature of the a protanthean actiniarian, and Corallimorphus sp., a coralli- gametogenic tissue of these species seems due to the thin- morpharian. Examining both whole and histolo- ness of the mesenterial mesogloea, perhaps the maturity gical sections, we were unable to ¢nd basilar muscles in of the specimens studied, but mainly misinterpretation any species including Preactis millardae, the only ptychodac- and overgeneralization of the literature. tiarian species in which they had been reported England In describing the ¢rst ptychodactiarian known to science, & Robson, 1984). Nor did we ¢nd parietobasilar muscles, Ptychodactis patula, Appello« f 1893, p.14) distinguished the which have been reported for Ptychodactis; patula by gametogenic tissue in a passage translated from German Appello« f, 1893) and D. antarcticus by Clubb, 1908; as follows: `In the latter [other actiniarians]öas far as we Carlgren, 1911). knowöthe eggs displace the mesogloea so that they are Size and distribution of cnidae are given in Table 4. entirely embedded in it. Only the youngest eggs are an Cnidae resemble those illustrated in ¢gure IV of Carlgren exception to this, in that they are accompanied [or 1940) and ¢gure 10 of England & Robson 1984), except attached] by a short and wide stalk [or stem] of meso- that every basitrich of Preactis millardae we found had a gleal lamella. In Ptychodactis by contrast, the very thin visible tubule so it resembled that illustrated by England [mesogleal] lamella ms) [reference to a ¢gure] continues

Journal of the Marine Biological Association of the United Kingdom 2000) 1002 V.A. Cappola and D.G. Fautin Ptychodactiarians are actiniarians unbroken through the entire ovary and the eggs o) is true of other sea anemones and of the mature male [reference to a ¢gure] are arrayed on both sides of it, all specimens of P. patula we examined Figure 5B). connected by longer or shorter stalks to the lamella. The Carlgren 1949) seems to have interpreted Appello« fas stalks are branches of the mesoglea and form a ¢brous meaning the gametes lie outside the mesentery, attached capsule around the egg'. to it by a stalk, as is true in members of anthozoan Appello« f 1893) noted the capsule is so thin in some subclass Alcyonaria see ¢gure 177A in Hyman, 1940; places that it is indistinguishable fromthe egg membrane. ¢gure 1A in Benayahu, 1991). Thus, Carlgren's 1949) He di¡erentiated between what he considered unusual de¢ning character of order Ptychodactiaria appears to female gonads and normal, actiniarian-like male gonads, have been a misinterpretation of Appello« f 1893), the which are completely enclosed in mesogloea and lack word `stiel' being considered to refer to a pedicle, as in the stems. He illustrated plate II, ¢gure 5) an enlarged view Alcyonaria, rather than perhaps to a trophonema, as in of a developing oocyte with a `stiel'öa stalk or stem. The some sea anemones. Moreover, the distinction Appello« f direction the stalk extends is unclear in the enlarged had made between the sexes was lost. Finally, gametes view; in a low-power view plate II, ¢gure 1), connections were regarded not as maturing in the mesogloea, where, of eggs to both mesogloea and mesentery edge are even in the Alcyonaria, their development occurs. Stalked apparent. If it extended between egg and mesogloeal gonads, di¡erences between the sexes in mode of gamete layer of the mesentery, the stalk is a strand of mesogloea maturation, and development outside the mesogloea that surrounds the egg, so the egg is clearly enclosed in would be unique among hexacorallian anthozoans. mesogloea. If it extended between egg and edge of the mesentery, the stalk resembles a trophonema Nyholm, 1943; Dunn, 1975), a tube through which nutritive mate- Musculature rial passes fromthe gastrovascular cavity to the devel- Among the features Appello« f 1893) considered demon- oping egg in some anthozoans Larkman & Carter, 1982; strated Ptychodactis is related to the protanthean actiniar- Fautin, 1999). ians were ectodermal nervous system and longitudinal Dactylanthus antarcticus was described in actiniarian musculature of the column. England in England & family as Cystiactis antarctica by Clubb 1908), Robson, 1984) placed Preactis in its own family, who illustrated ova on both sides of a thin lamella of Preactiidae, based partly on the presence of basilar mesogloea but did not comment on the structure of the muscles and the lack of ectodermal longitudinal muscles. gametogenic tissue. In redescribing the species and trans- Perhaps the intersection of the ectodermwith the rather ferring it to the new genus Dactylanthus, Carlgren 1911) ¢brous mesogloea of these animals was misinterpreted as compared the gonads to those of P. patula. He concluded longitudinal musculature. The column of all specimens of that in both species, the gonads are proximal to the ¢la- Ptychodactis patula we examined had circumferential wrin- ments and the eggs are not embedded in the main part of kles: we infer the bunched tissue gave the impression of the mesogloea but are attached with mesogloeal stalks to longitudinal muscles, because this is where Appello« f the mesogloeal lamella. Carlgren 1949, p.10), in creating 1893) stated the musculature was particularly prominent. order Ptychodactiaria, asserted the gonads are `not The longitudinal ectodermal musculature of the tentacu- enclosed in the mesogloea but stalked, recalling the late vesicles tentacle-like protrusions fromthe column) arrangement of the gonads in the Alcyonaria', and did of Preactis millardae `continues for ...a short distance on to not distinguish between the sexes. In rede¢ning the order, the column' England & Robson, 1984, p. 317); such England in England & Robson, 1984, p. 315) asserted muscles could have been misinterpreted in D. antarcticus only `Gonads not enclosed in the mesogloea'. Carlgren as being associated with the column. may have meant that the gametes do not lie in the centre Our ¢nding that basilar muscles are absent con¢rms of the mesentery, in the mesogloeal lamella, but the impli- Carlgren's 1949, page 10) statement that ptychodactiar- cation is that they are not surrounded by mesogloea. ians have a `de¢nite base but without basilar muscles,' but England in England & Robson, 1984, p. 325) clearly that is not unusual among hexacorallians. Perhaps the considered there to be no mesogloea around the gametes, ridges we observed along the base of some mesenteries stating, in regard to the taxonomic position of ptychodac- were misconstrued as basilar muscles. There was no tiarians,`As the gonads are not enclosed in the mesogloea evidence of musculature in these ridges, which might be of the mesenteries, the Actiniaria are precluded'. the result of bunching of tissue in contraction. Thus, as ptychodactiarians were described and re- Reports of parietobasilar muscles in Ptychodactis patula described, accounts of the gametogenic tissue Tables 1 & 2, and D. antarcticus were equivocal. Appello« f 1893) stated character 12) became less precise. Although he recognized they occur in the former species but Carlgren 1949) that each oocyte is surrounded by mesogloea, Appello« f reported themabsent. In the latter species, Clubb 1908) 1893) considered that di¡erent fromthe situation in described themas smalland Carlgren 1911) as faint. We actiniarians with which he was presumably familiaröan did not ¢nd them. actiniarian oocyte is clearly embedded in mesogloea if the mesogloeal lamella is thick, but in sea anemones without a thick mesogloeal lamella, developing gametes Mesenteries lie lateral to the lamella, with mesogloea stretched Among the features of the mesenteries Appello« f 1893) around themsee e.g. Wedi & Dunn, 1983). Moreover, considered allied Ptychodactis with protanthean actiniarians gametes of the female ptychodactiarians we examined were the lack of ciliated tracts and stomata. Carlgren's appeared to be immature, and it is possible that they 1949, p.10) feature `¢laments without ciliated tracts' move into the centre of the mesentery as they mature, as applies to the species he was including in order

Journal of the Marine Biological Association of the United Kingdom 2000) Ptychodactiarians are actiniarians V.A. Cappola and D.G. Fautin 1003

Ptychodactiaria P. patula and D. antarcticus), but not to Cnidae Preactis millardae. Oral stomata are present in P. millardae; Sizes of cnidae we found in Ptychodactis patula agree if stomata are taxonomically important in sea anemones, with data given by Carlgren 1921, 1940). Our data on it is at the species level. D. antarcticus are identical to those of Carlgren 1940) and A feature by which Carlgren 1949, p.10) de¢ned agree very closely with those reported by Dunn 1983) Ptychodactiaria is `distal end of the ¢laments of the and England & Robson 1984), although England & imperfect mesenteries drawn out into two lobes giving Robson also reported heterotrichs and possibly holotrichs. this part of the ¢lament the appearance of a bisected The holotrichs might have been developing atrichs funnel'. He Carlgren, 1911) analogized these structures England & Robson, 1984). Based on the variability we with the ciliated tract in the mesenterial ¢laments of observed in the appearance of atrichs in all three species other actiniarians. We interpret this structure, which we Table 4), we infer the `heterotrichs' were also atrichs. It is observed in Ptychodactis patula and D. antarcticus specimens likely there is more than one type of atrich, but we could of Preactis millardae we examined lack incomplete mesen- not sort themeasily: the tubule of somewas neatly teries), as a stage in mesentery development. England's wound in contrast to that of others, and a few capsules description of mesentery development in P. millardae see had a tubule that was neat only at one end; and the width England & Robson, 1984) is consistent with this inter- of some short capsules was greater than that of some long pretation. capsules. Data on Preactis millardae agree with published The proximal fusion of mesenteries, which is the most ¢gures except for minor di¡erences; for example, we distinctive feature of these animals, may be associated found some atrichs in the ¢laments smaller than any with behaviour. Preactis millardae and D. antarcticus are reported by England & Robson 1984), and they did not elongate, £exible animals that undergo peristalsis, crawl ¢nd spirocysts on the oral disc we found one). along the substratumwith the column, and prey on octo- We found in Ptychodactis patula, as noted by Carlgren coral colonies England & Robson, 1984; Dayton et al., 1921, p.11),`Spirocysts in the column and in the oral disc 1997, respectively). Their formand behaviour caused extremely rare, also in the tentacles not common. Nema- Dayton Dayton et al., 1997) and L. Peck British tocysts not especially numerous ...' Indeed, nematocysts Antarctic Survey; personal communication to D.G.F.) in specimen USNM 55624 were nearly absent. initially to mistake individuals of D. antarcticus for holothurians. We agree with England & Robson 1984) and Dayton et al. 1997) that the distinctively short and Distribution extensible actinopharynx allows the animals to engulf octo- Ptychodactis patula is arctic^boreal Carlgren, 1939) and coral prey, which may be large relative to the anemone; the possibly panarctic Dayton et al., 1997). It has been large amount of tissue necessary for such £exibility forms reported fromlatitudes of 63 ^70³N: in Norway, it has pockets and folds in contraction. Although Ptychodactis been collected at depths of 188^350 mAppello « f, 1893; patula is not elongate, the ¢rst specimens of it reported Carlgren, 1939); north of Iceland it was collected at 80 m were associated with octocorals Appello« f, 1893). Appello« f Carlgren, 1921); and it has been collected in Kotzebue 1893) remarked that P. patula gaped so much even when Sound, Alaska, at unspeci¢ed depth Carlgren, 1934). alive that the mesenterial ¢laments were exposed, and, in Dactylanthus antarcticus has a south circumpolar distribu- extreme cases, the body assumed the form of a disc, tion. Dredged specimens have been reported from exposing the entire gastrovascular cavity Figure 2A). around Antarctica at latitudes of 64^788Sanddepthsof However, the mouth of some specimens we studied 37^610 m, and from the southern tip of South America Figure 2B) was closed and the gastrovascular cavity was 54822^230S64842^520W) at 106^110 mDunn, 1983). not exposed, just as in other actiniarians. Live specimens were observed by SCUBA divers in the The South African actiniarian Korsaranthus natalensis Chilean fjords of Canal Darwin 45823.50S7480.800)and Carlgren, 1938) also crawls along the substratumand Estrecho Collingwood 518520S73843.60W) at 25^40 m preys on octocorals, and has an unusually short, deeply Dayton et al., 1997). folded actinopharynx and a simple cnidome Riemann- Preactis millardae is known only fromthe Western Zu« rneck & Gri¤ths, 1999). Thus these morphological Cape of South Africa 34^378S): divers have found it at features appear to be related to behaviour, as Riemann- 10^20 mat Oudekraal on the Cape Peninsula and at Zu« rneck & Gri¤ths 1999) speculated, rather than to Roman Rock in False Bay; stranded specimens have been phylogenyöK. natalensis is a member of the largest sea collected fromMaclear's Beach near Cape Point and near anemone family, . Cape Point and near Hermanus England & Robson, 1984). Tentacles The protrusions on the column of members of family Systematics Preactiidae have been termed outgrowths `Auswuchse' The three species Ptychodactis patula, Dactylanthus in D. antarcticus by Carlgren, 1911) and `tentaculate antarcticus,andPreactis millardae do not constitute an vesicles' in Preactis millardae by England & Robson, order; their common characters do not di¡erentiate them 1984). Their histological structure and complement of fromactiniarians. The three species do, however, forma cnidae are identical to those of tentacles, but since clade supported by proximally fused mesenteries, all tentacles are de¢ned as arising fromthe oral disc e.g. mesenteries being gametogenic, lack of basilar and parie- Stephenson, 1928), we adopt the termtentaculate vesicles tobasilar muscles, and weak retractor muscles. Only the for them. ¢rst of these four characters is unique to this clade.

Journal of the Marine Biological Association of the United Kingdom 2000) 1004 V.A. Cappola and D.G. Fautin Ptychodactiarians are actiniarians

Based on 18S rDNA sequences and neighbour-joining distinct siphonoglyphs that are prolonged aborally. analyses, Berntson et al. 1999) found that D. antarcticus, Cnidome: spirocysts, atrichs, and basitrichs. the only ptychodactiarian they considered, lies within Actiniaria. We found the same thing in a parsimony Genus Dactylanthus Carlgren, 1911 analysis of sequence data from28S rDNA obtained in Column with 24 longitudinal rows of tentaculate vesicles; our laboratory by T.R. White. The nearest relative of 24 marginal tentacles on oral disc. Sphincter muscle very D. antarcticus in the analysis by Berntson et al. 1999) weak, di¡use. All mesenteries or only primary ones was Haloclava sp., an athenarian anemone suborder complete. Cnidome: spirocysts and atrichs. Nynantheae). In our analysis, the nearest relatives of D. antarcticus were some species of family Actiniidae Genus Preactis England in England & Robson), 1984 suborder Nynantheae); our analysis did not include any Column covered with tentaculate vesicles that are not athenarian species, but did include members of six clearly arrayed in rows or columns; no tentacles on oral thenarian families and some species of order Scleractinia. disc. Sphincter muscle absent. All mesenteries complete. In referring to Carlgren's 1911) family-level taxon, Cnidome: spirocysts, atrichs, and basitrichs. Stephenson 1921, p. 508), stated `the Ptychodactidae must be kept apart fromthe ordinary Actinians ...in a group of their own and of higher rank than a family'. We This research was supported by US National Science Foundation grant DEB 9521819 in the programme Partnerships consider this assessment still accurate, and therefore for Enhancing Expertise in PEET). We thank restore Stephenson's 1921) taxon Ptychodacteae, which Adorian Ardelean for technical assistance, Gu« nter Fo« rsterra for he considered one of three tribes of Actiniaria, the others assisting with translations, Tracy R. White for data, two being Protantheae and Nynantheae. Those taxa are now anonymous referees for improving the manuscript, and Terry considered to be suborders, and a third has been recog- Gosliner and Lloyd Peck for photographs. Specimens were nized, the Endocoelantheae Carlgren, 1949).We consider kindly loaned by the California Academy of Sciences, Swedish Ptychodacteae a fourth suborder of Actiniaria. Museumof Natural History, and US National Museumof Natural History. We recognize both described families, Ptychodactiidae and Preactiidae, but move Dactylanthus fromthe formerto the latter. We rede¢ne all taxa of this clade below. REFERENCES Appello« f, A., 1893. Ptychodactis patula n.g. & sp. der Suborder Ptychodacteae Stephenson, 1921 Repra« sentant einer neuen Hexactinien-Familie. Bergens Diagnosis. Actiniaria with a de¢nite base, lacking basilar Museum Aarbog, 4,3^22. and parietobasilar muscles. Mesenteries of each pair and Benayahu, Y., 1991. Reproduction and developmental pathways couple fused medially at animal's proximal end. One or of Red Sea Xeniidae Octocorallia, Alcyonacea). Hydrobiologia, two weak retractor muscles per mesentery. All or almost 216/217,125^13 0. all mesenteries fertile. Filaments with or without ciliated Berntson, E.A., France, S.C. & Mullineaux, L.S., 1999. tracts. Actinopharynx short, highly folded. Sphincter Phylogenetic relationships within the class Anthozoa phylum muscle weak or absent. Cnidome: spirocysts, atrichs, and Cnidaria) based on nuclear 18S rDNA sequences. Molecular basitrichs. Phylogenetics and Evolution, 13,417^433. Carlgren, O., 1911. Ûber Dactylanthus Cystiactis) antarcticus Clubb) zugleich ein Beitrag zur Phylogenie der Actiniarien. Family Ptychodactiidae Appello« f, 18 9 3 Wissenschaftliche Ergebnisse der Schwedischen Su« dpolar-Expedition Diagnosis. Column short, smooth or wrinkled in con- 1901^1903, 6,Zool.II,1^31. tracted specimens) without outgrowths. Tentacles simple, Carlgren, O., 1921. Actiniaria I. Danish Ingolf-Expedition, 5, numerous, not retractile. Gametes develop proximal to 1^241. ¢laments on all mesenteries. As many as ¢ve cycles of Carlgren, O., 1934. Some Actinaria from Bering Sea and arctic mesenteries; those of ¢rst and second cycles complete. waters. Journal of the Washington Academy of Sciences, 24, One weak retractor muscle per mesentery. Sphincter 348^353. muscle absent. Actinopharynx little di¡erentiated from Carlgren, O., 1938. South African Actiniaria and Zoantharia. the oral disc; siphonoglyphs absent. Cnidome: spirocysts Kungliga Svenska Vetenskapsakademiens Handlingar, series 3, 173), 1 148. and atrichs. ^ Carlgren, O., 1939. Actiniaria and Zoantharia of the Scottish National Antarctic Expedition, 1902^1904. Transactions of the Genus Ptychodactis Appello« f, 18 93 Royal Society of Edinburgh, 49,791^800. As for family; with about 100^122 tentacles that are long- Carlgren, O., 1940. A contribution to the knowledge of the itudinally ridged, at least in preserved specimens. structure and distribution of the cnidae in the Anthozoa. Kungliga Fysiogra¢ska Sa« llskapets Handlingar, n.f., 513), 1^62. Family Preactiidae England in England & Robson), 1984 Carlgren, O., 1949. A survey of the Ptychodactiaria, Diagnosis. Column elongate with vesicular outgrowths Corallimorpharia and Actiniaria. Kungliga Svenska tentaculate vesicles) that are histologically identical to Vetenskapsakademiens Handlingar, series 4, 1,1^121. tentacles. Tentacles absent on oral disc or only at margin. Clubb, J.A., 1908. Coelentera. IV.öActiniae. National Antarctic Gametes and ¢laments at same level on at least primary Expedition 1901^1904, Natural History, Zoology, IV,1^12. Dayton, P.K., England, K.W. & Robson, E.A., 1997. An unusual mesenteries; on higher-order mesenteries, gametes may , Dactylanthus antarcticus Clubb, 1908) order be proximal to ¢laments. Twelve pairs two cycles) of Ptychodactiaria), on gorgonians in Chilean fjords. Proceedings mesenteries, one or both cycles complete. Two weak of the 6th International Conference on Coelenterate Biology ed. J.C. retractor muscles per mesentery. Sphincter muscle weak den Hartog), pp.135^142. Leiden: Nationaal Natuurhistorisch or absent. Actinopharynx well developed with two Museum.

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Dunn, D.F., 1975. Reproduction of the externally brooding sea Presnell, J.K. & Schreibman, M.P., 1997. Humanson's animal tissue anemone Epiactis prolifera Verrill, 1869. Biological Bulletin. techniques. Baltimore: The Johns Hopkins University Press. Marine Biological Laboratory,Woods Hole, 148,199^218. Riemann-Zu« rneck, K. & Gri¤ths, C.L., 1999. Korsaranthus Dunn, D.F., 1983. Some Antarctic and sub-Antarctic sea natalensis Carlgren, 1938) nov. comb. Cnidaria: Actiniaria) anemones Coelenterata: Ptychodactiaria and Actiniaria). a mobile sea anemone attacking octocorals. South African Antarctic Research Series, 39,1^67. Journal of Zoology,34,190^196. England, K.W. & Robson, E.A., 1984. A new sea anemone from Stephenson, T.A., 1921. On the classi¢cation of Actiniaria. Part South Africa Anthozoa, Ptychodactiaria). Annals of the South II. Consideration of the whole group and its relationships, African Museum, 94,305^329. with special reference to forms not treated in Part I. Quarterly Fautin, D.G., 1999. Cnidaria. Encyclopedia of reproduction,vol.1 Journal of Microscopical Science, n.s., 65,493^576. ed. E. Knobil and J.D. Neill), pp.645^653. San Diego: Stephenson, T.A., 1928. The British sea anemones,vol.1.London: Academic Press. The Ray Society. Hyman, L., 1940. The invertebrates. Vo l . 1. Protozoa through Wedi, S.E. & Dunn, D.F., 1983. Gametogenesis and reproduc- Ctenophora.NewYork:McGraw-Hill. tive periodicity of the subtidal sea anemone Urticina lofotensis Larkman, A.U. & Carter, M.A., 1982. Preliminary ultrastruc- Coelenterata: Actiniaria) in California. Biological Bulletin. tural and autoradiographic evidence that the trophonema of Marine Biological Laboratory,Woods Hole, 165,458^472. the sea anemone Actinia fragacea has a nutritive function. InternationalJournal of Invertebrate Reproduction, 4,375^379. Nyholm, K.-G., 1943. Zur Entwicklung und Entwicklunsbiologie der Ceriantharien und Aktinien. Zoologiska Bidrag fraan Uppsala, 22,87^248. Submitted 15 May 2000. Accepted 7 September 2000.

Journal of the Marine Biological Association of the United Kingdom 2000)