ZOOSYSTEMATICA ROSSICA

ISSN 2410-0226 Zoological Institute, Russian Academy of Sciences, St Petersburg ▪ https://www.zin.ru/journals/zsr/ [ onl ine] 0320-9180 Vol. 29(2): 213–237 ▪ Published online 20 October 2020 ▪ DOI 10.31610/zsr/2020.29.2.213 [ print] RESEARCH ARTICLE

Classification and evolution of the burrowing sea anemones (Anthozoa: Actiniaria: Athenaria): a review of the past and current views Классификация и эволюция закапывающихся актиний (Anthozoa: Actiniaria: Athenaria): обзор прежних и современных представлений

N.Yu. Ivanova Н.Ю. Иванова

Natalia Yu. Ivanova, Zoological Institute, Russian Academy of Sciences, 1 Universitetskaya Emb., St Petersburg 199034, Russia. E-mail: [email protected]

Abstract. The opinions of systematists about the classification and evolution of burrowing sea anemones have repeatedly changed over the long-term study of Actiniaria. Four stages can be distinguished over the course of the classification history. Each system was characterised by the use of mainly one particular fea- ture. These features were: (1) characters of the external morphology, (2) arrangement of the mesenteries, (3) presence or absence of the basilar muscles and (4) molecular markers. The views on the origin and the evolution of the burrowing sea anemones were also altered more than once, that led to the emergence of several hypotheses. The burrowing sea anemones were considered as a primitive group or, on the contrary, as more advanced descendants of large hexamerous actinians. Резюме. Представления исследователей о классификации и эволюции закапывающихся актиний неоднократно менялись в течение длительного времени изучения Actiniaria. В процессе формирования классификации можно выделить четыре этапа. Каждый из них характеризовался использованием в основном одного признака, на который опирались авторы при построении своей системы. К этим признакам следует отнести: (1) черты внешнего строения, (2) распо- ложение мезентериев, (3) наличие или отсутствие базилярных мускулов и (4) молекуляр- ные маркеры. Представления о происхождении и эволюции закапывающихся актиний также неоднократно изменялись, что привело к появлению нескольких гипотез. Закапывающиеся морские анемоны рассматривались в качестве примитивной группы или, наоборот, как более продвинутые потомки крупных гексамерных актиний. Key words: burrowing anemones, comparative morpho-anatomical analysis, taxonomic characters, clas- sification, evolution, Athenaria Ключевые слова: закапывающиеся актинии, сравнительный морфо-анатомический анализ, таксономические признаки, классификация, эволюция, Athenaria ZooBank Article LSID: urn:lsid:zoobank.org:pub:2B001412-4B70-4E12-BB97-54D620F6D12F

Introduction huge amount of work in an attempt to build a nat- ural classification that reflected the evolution of The classification of the burrowing sea anemo- this group. The first researchers (Milne-Edwards nes has a long history dating back more than 150 & Haime, 1857; Gosse, 1858, 1860) relied main- years. During this time, researchers conducted a ly on the external features of the burrowing sea

© 2020 Zoological Institute RAS and the Author(s) N.Yu. Ivanova. Classification and evolution of the burrowing sea anemones anemones to arrive at a classification. Later it be- to represent a polyphyletic group (Hand, 1966; came clear that anatomical characters were more Schmidt, 1972, 1974). stable and reliable characters (Hertwig, 1882; Following the contemporary trend in the nat- McMurrich, 1893). ural sciences, many specialists had high hopes of The transition to a classification based on in- solving the difficult problems of phylogeny and sys- ternal features was associated with a detailed tematics based on molecular genetic studies. Un- study of the successive development of the mes- fortunately, as evident from the new higher-level enteries by Hertwig & Hertwig (1879). It became classification for Actiniaria proposed by Rodríguez soon clear, however, that relying solely on the ar- et al. (2014), these issues are still far from being rangement of the mesenteries led to the union of resolved. Firstly, that classification yields a com- unrelated polyps and to the separation of close- bination of completely dissimilar forms. For exam- ly related forms (Beneden, 1897). According to ple, the edwardsians and the endocoelantheans are Carlgren (1898, 1900, 1905), the most important placed in one order: apart from sequence similarity, feature in classifying the burrowing sea anemones however, these sea anemones have no other common is the absence of the basilar muscles. Over time, his features in either structure or biology. Secondly, system was improved, developed, and published in placing some burrowing sea anemones, which lack the monograph “A survey of the Ptychodactiaria, acontia, together with the thenarian polyps that Corallimorpharia and Actiniaria” (1949). Carl- possess them, in the superfamily Metridioidea, was gren’s (1949) classification was universally accept- explained by loss of the acontia. Thirdly, when us- ed and was used by all researchers until recently. ing one set of markers, the position of many genera In the second half of the 20th century, however, in the scheme reflected a particular phylogenetic Carlgren’s system was increasingly though not to relationship, whereas using other markers yielded reflect the phylogeny of Actiniaria, and the bur- a quite different result. That cast doubt on the ap- rowing sea anemones were ultimately considered plicability of the method itself.

Fig 1. Early sea anemone division based on characters of their external morphology. a, burrowing sea anemones, elongated forms with a rounded aboral end or physa; b, large attached sea anemones with a well-developed, flat, adhesive and muscular pedal disc. After Gosse (1860).

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1. Development of classification of 1.2. Transition to the classification based the burrowing sea anemones on internal features: the succession of arising mesenteries 1.1. Classification based on external morphological features The system of all Anthozoa, including the sea anemones, was later based on features of the inter- The taxonomists of the mid-19th century re- nal organization of the polyp (McMurrich, 1893). lied on external features to construct the classi- fication of sea anemones. They separated the bur- Haime (1854) was the first to point out the impor- rowing forms from the remaining representatives tance of anatomical features, but only Hertwig & based on their elongated body shape and absence Hertwig (1879) began to use them in constructing of a pedal disc (Fig. 1a, b). Milne-Edwards & their classification. Having traced the formation Haime (1857) placed these anemones inside of the of mesenteries in the sea anemones, the zoanthids, subfamily Actininae in section “Actinines pivo­ and the octocorals, Hertwig & Hertwig (1879) tantes”, defining them as “species whose base is considered that the arrangement of mesenteries very small and body is very elongated” (Fig. 2). In and the development of their muscles (but not constructing his system, Gosse (1860) also relied their number as Ehrenberg (1834) and Haeckel on the presence or absence of a sticky pedal disc. (1866) believed) should be regarded as the most Accordingly, he isolated the worm-like anemones important taxonomic characters. along with the cerianthids from other anemones Hertwig & Hertwig (1879) and many subse- in the family Ilyanthidae (Gosse, 1858). Verrill quent researchers demonstrated that, in the early (1864) was among the first zoologists to draw at- stages of development, sea anemones are bilateral­ tention to internal features of the polyp, indicating ly symmetrical animals. This is underlined by the the number of mesenteries (“internal lamellae”) in presence of eight primary mesenteries, which are a description of the species. Nonetheless, as diag- symmetrical with respect to the plane of a flat- nostic features for distinguishing genera and fami­ tened pharynx. First, in anemone larvae, two lies, Verrill mainly used external features: body ventro-lateral mesenteries are formed to the right shape, surface structure, tentacles number, etc. and left of the flattened pharynx, making up the Klunzinger (1877) also used the elongated body bilateral pair (“couple”) (Fig. 3a). They divide the and rounded or pointed proximal end of the body body cavity into a smaller part located on the con- without a well-differentiated pedal disc as diag- ventionally ventral side, and a large portion on the nostic characteristics. conventionally dorsal side. The next mesenteries

Fig 2. The position of burrowing sea anemones (in bold) in Milne-Edwards & Haime’s (1857) classification of coral polyps.

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Figs 3–6. The succession of arising mesenteries, schematic transversal section. 3, the first type;a , the first cou- ple (ventro-lateral mesenteries); b, the second couple (dorsal directive mesenteries); c, the third couple (ventral directive mesenteries); d, the fourth couple (dorso-lateral mesenteries); 4, the second type; a, the first couple (ven- tro-lateral mesenteries); b, the second couple (dorso-lateral mesenteries); c, the third couple (ventral directive mesenteries); d, the fourth couple (dorsal directive mesenteries); 5, Edwardsia stage; 6, arising of the fifth and sixth couples of lateral mesenteries. c, column; phx, pharynx; rm, retractor muscle; vlm, ventro-lateral mesenteries; dlm, dorso-lateral mesenteries; vdm, ventral directive mesenteries; ddm, dorsal directive mesenteries; V, fifth couple of lateral mesenteries; VI, sixth couple of lateral mesenteries.

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Figs 7–9. The succession of arising mesenteries, schematic transversal section. 7, Halcampa stage; 8, formation of the secondary mesenteries; 9, formation of the tertiary mesenteries. c, column; phx, pharynx; rm, retractor muscle; I, mesentery pairs of the first cycle; II, mesentery pairs of the second cycle; III, mesentery pairs of the third cycle.

( Zoosystematica Rossica, Vol. 29, No. 2, pp. 213–237 217 N.Yu. Ivanova. Classification and evolution of the burrowing sea anemones are formed in a similar mode, namely in bilateral pairs. This encompasses a pair of dorsal directive, ventral directive and dorso-lateral mesenteries (Fig. 3b–d). Sometimes the sequence of pair de- velopment differs (Fig. 4a–d). The stage of eight primary mesenteries was called the Edwardsia stage by McMurrich (1889) (Fig. 5). Among the eight primary mesenteries, the dorsal and ventral me­senteries, which grow to the narrow sides of the flattened pharynx, are termed directive mes- enteries. The location of retractor muscles on the mesenteries also determines the bilateral symme- try of the anemone body: in the directives they face outwards, towards the exocoels, whereas in the lateral mesenteries they face towards the ventral pair of directives (Fig. 5) (Haddon, 1889; McMurrich, 1889; Bourne, 1900; Duerden, 1899; Panikkar, 1937; Grebelny, 1982; Berking, 2007; Malakhov, 2016). After development of the first eight mesenter- ies, one mesentery appears on the ventral side of each lateral mesentery, with a retractor muscle facing to it. This yields four lateral pairs (“pairs”). Fig. 10. Early description of a mismatching number These four mesenteries remain rudimentary in of tentacles and mesenteries in Edwardsia. c, column; some burrowing anemones (Fig. 6) (Edwardsi­ phx, pharynx; rm, retractor muscle; pt, primary tenta- idae Andres, 1881) but reach the size of the pri- cles; st, secondary tentacles. After Andres (1881). mary mesenteries in all others. At this stage (the Halcampa, the Halcampula or the Halcampoides “Edwardsien” were a special group. In their way stage) the polyp already has twelve mesenteries, of life, they resemble the ceriantharians, but their which constitute the first hexamerous cycle and internal organization more closely resembles that make the animal radially symmetrical (Fig. 7). of other sea anemones. Nonetheless, the presence Subsequently, mesentery formation occurs in or- of eight mesenteries in Edwardsia de Quatrefages, dinary pairs consisting of adjoining mesenteries, 1842, as well as a mismatching number of tenta- with retractor muscles facing each other. The cles and mesenteries (Fig. 10), led Hertwig & Her- number of mesenterial pairs increases according twig (1879) to place the edwardsians in a separate to the rule: 6+6+12+24+48 ... (Figs 8, 9) (Her- group, unlike the system of Milne-Edwards & twig, 1882; Haddon, 1889; Bourne, 1900; Pax, Haime (1857) or Gosse (1860). 1914; Grebelny, 1982; Malakhov, 2016). Like Hertwig & Hertwig (1879), Andres (1881) noted that the edwardsians are a special group. 1.3. Classification based on mesentery According to Andres, the edwardsiids are octome- arrangement rous and characterised by a discrepancy between Studying the development of the mesenteries in the number of tentacles and endocoels/exocoels. soft corals and sea anemones, Hertwig & Hertwig In most anemones, one tentacle corresponds to (1879) first noted the similarity between certain each endocoel (the space between two mesenteries worm-like anemones, namely the edwardsians, of the same pair), and one tentacle to each exocoel and the octocorals. Both groups feature, there are (the space between different pairs). In Edward- eight mesenteries, and their arrangement through- sia, each endocoel formed by a pair of directive out the life of the polyp determines the bilateral mesenteries communicates with one tentacle, and symmetry of the body. The authors concluded that each lateral chamber communicates with two or

218 ( Zoosystematica Rossica, Vol. 29, No. 2, pp. 213–237 N.Yu. Ivanova. Classification and evolution of the burrowing sea anemones three tentacles (Fig. 10) (Andres, 1881). Based on these characters, Andres (1883) joined these polyps into the family Edwardsinae Andres, 1883, but other worm-like polyps were combined with large anemones into the family Actininae Andres, 1883, which was subdivided into five subfamilies. Thus, unlike other researchers (Milne-Edwards & Haime, 1857; Gosse, 1860), Andres (1883) began to split the burrowing sea anemones into a larg- er number of groups rather than putting them in one family (Ilyanthidae). He still relied more on external features, distributing the burrowing sea anemones among different subfamilies: Halcam- pidae Andres, 1883, Siphonactinidae Andres, 1883 (now Haloclavidae Verrill, 1899), Phellidae Andres, 1883, Ilyanthidae, Heteractidae Andres, 1883, Mesacmaeidae Andres, 1883, whereas the subfamilies Phellidae and Heteractidae includ- ed the burrowing forms and sea anemones with a pedal disc (Fig. 11) (Andres, 1883). Studying the “Challenger” collection, R. Her- twig (1882), based on the number and arrange- ment of the mesenteries, proposed to divide Ac- tiniaria into six tribes: Hexactiniae, Paractiniae, Fig 11. The position of burrowing sea anemones (in bold) in Andres’s (1883) classification of sea anemones Monauleae, Edwardsiae, Zoantheae, Ceriantheae. sensu lato. Only three of them, Hexactiniae, Paractiniae and Edwardsiae, included anemones without a pedal disc. The tribe Edwardsiae was characterised by seemed to him more attractive because it relied the presence of only eight mesenteries: two pairs on a more solid foundation. Nonetheless, external of directive mesenteries and four unpaired mesen- characters should not be ignored because they can teries (Fig. 5). The remaining burrowing anemo- be used as valuable auxiliary elements. Danielssen nes were included by Hertwig (1882) in the tribe used such a combination of external and internal Hexactiniae because they had at least six (usually features in his monograph on the sea anemones more) pairs of mesenteries and then increasing in collected by the Norwegian North Atlantic Expe- multiples of six (Figs 7–9). The tribe Paractiniae dition. He described several species of burrowing included forms in which the number of anti­meres sea anemones from the North Atlantic and estab- did not increase in multiples of six. Based on the lished a new family of Andvakiidae Da­nielssen, shape of the aboral body end, Hertwig (1882, 1890 inside the tribe Hexactiniae. He also recog- 1888) divided Hexactiniae into forms with and nised the new tribe Aegireae Danielssen, 1890, without a pedal disc. The polyps, which had no which included the family Aegiridae Da­nielssen, pedal discs, constituted two families, Ilyanthidae 1890, in which he placed Fenja mirabilis Dan- and Siphonactinidae. The representatives of the ielssen, 1890 and Aegir frigidus Danielssen, 1890 first did not have conchula, in contrast to the sec- (both species have now been synonymised with ond, which did (Hertwig, 1882, 1888). Halcampoides purpureus (Studer, 1879). Danielssen (1890) and McMurrich (1891, Faurot (1895) contributed significantly to the 1893), like other zoologists, followed the classifi- development of the taxonomy of burrowing sea cation of Hertwig (1882, 1888). Danielssen (1890) anemones. He revealed that Edwardsia in fact appreciated the works of his predecessors (e.g. has more than eight mesenteries (Fig. 6). Faurot Gosse, 1858, 1860), but Hertwig’s classification discovered that Edwardsia beautempsi de Quat-

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Fig 12. The position of burrowing sea anemones (in bold) in Bourne’s (1900) classification of Zoantharia sensu lato. refages, 1842, in addition to eight macrocnemes Bourne’s (1900) classification, like Hertwig’s (large perfect mesenteries), also developed eight (1882, 1888), separated the edwardsians from microcnemes (very underdeveloped and which all other burrowing anemones into the order Ed- long remained unnoticed by other morphologists). wardsiidea, which he placed together with the or- The presence of additional mesenteries explained ders Cerianthidea, Antipathidea, Zoanthidea and the presence of sixteen tentacles and made it pos- Proactiniae in the grada Paramera, which united sible to reject the opinion of early researchers that forms with primitive bilateral symmetry. Bourne the number of tentacles in this genus exceeds the placed the remaining burrowing sea anemones number of mesenteries. Although Faurot did not together with large hexamerous sea anemones in trace the order of appearance of additional mesen­ the grada Cryptoparamera. The latter included teries, he considered it quite probable that they polyps whose primary bilateral symmetry is sub- appear in the exocoels, as in all the hexactinians. stituted by radial development of the second and This discovery of microcnemes in Edwardsia, in succeeding cycles of mesenteries. Bourne placed Faurot’s opinion, showed the inconsistency of iso- these sea anemones in the order Actiniidea, groups lating these anemones in a separate branch (Fau- A. Hexactiniae and B. The burrowing forms were rot, 1895). placed in the families Ilyanthidae and Polyopidae. Beneden (1897) considered Faurot’s (1895) As a significant diagnostic feature, Bourne used discovery of the rudimentary mesenteries to be the presence of a rounded aboral end of the body. the most important event for the taxonomy of sea Based mainly on the number of mesenteries and anemones. In recognition of this fact, he conside­ tentacles, he distributed them into the subfami- red it impossible to separate the edwardsians from lies Halcampinae, Ilyanthinae, Peachiinae in the the hexactinians as had been proposed by Her- fami­ly Ilyanthidae (Fig. 12) (Bourne, 1900). twig (1882, 1888) because there is no significant Somewhat later, Delage & Hérouard (1901) difference between the two groups. The adapta- proposed a curious system. In the suborder tion to different habitat conditions should not play Hexactinidae, the authors placed large polyps at- a significant role, especially since the remaining tached to hard substrates in the tribe Actinina. burrowing sea anemones are placed in the same The burrowing forms were encompassed in the tribe as the attached polyps. Based on mesentery tribes Edwardsina and Halcampina, whose rep- development, Beneden’s (1897) system placed all resentatives differed in the number of the mesen- sea anemones in the suborder Actiniaria, order teries making up the first and the second cycles. Hexactiniaria and subclass Zoanthactiniaria. The tribe Edwardsina included the families Ed-

220 ( Zoosystematica Rossica, Vol. 29, No. 2, pp. 213–237 N.Yu. Ivanova. Classification and evolution of the burrowing sea anemones wardsinae and Protantheinae. Edwardsinae were ally used for the sea anemones and scleractinians, defined as forms in which only the first eight mes- but not for the antipatharians and ceriantharians. enteries are well developed, whereas mesenteries Bourne felt that since the edwardsians did not of the second cycle are confined to the most dis- have six pairs of the first cycle of mesenteries, the tal part. Protantheinae were also characterised names “Hexacorallia” and “Dodecacorallia” did by eight well-developed mesenteries, and by mi- not reflect this. For a subclass that included the cromesenteries that form a more or less complete edwardsians, the name Zoanthactiniaria proposed second cycle developed along entire length of the by Beneden (1897) would be more appropriate. column. The tribe Halcampina included polyps Even though a detailed study of polyp anatomy characterised by the first two complete cycles and and mesentery arrangement clearly indicated that sometimes by an incomplete third cycle. Delage the edwardsians belong to Actiniaria, Bourne & Hérouard referred three families to this tribe. continued to consider this group separately from These are Halcampinae, whose polyps are charac- the remaining sea anemones, referring them to the terised by a first cycle of twelve macromesenteries order Edwardsiaria, subclass Zoanthactiniaria. and whose second cycle is either absent or consists Bourne (1916) united the other sea anemones in of micromesenteries (genera Halcampa, Halcam- the suborder Actiniaria and placed them in the poides Danielssen, 1890, Peachia etc.), Monauli- order Dodecactiniaria, subclass Zoanthactini­ nae (genus Scytophorus Hertwig, 1882), previ- aria. Thus, he insisted on the independence of the ously considered by Hertwig (1882) in the rank edwardsians based on a detailed study of the se- of tribe, and Holactininae with a single genus Gy- quence of mesenteries and tentacles arising in sev- ractis Boveri, 1893 (Delage & Hérouard, 1901). eral edwardsiid species. His observations showed Hickson’s (1906) system recognizes two or- that the succession of appearance of four lateral ders: Edwardsiidae and Actiniaria. The order micromesenteries and tentacles within the genus Edwardsiidae encompassed the edwardsians and Edwardsia varies. On this basis, he denied any the protantheans based on the presence of only homology of the mesenteries of the fifth and sixth eight perfect mesenteries. The other burrowing bilateral pairs in Edwardsia and other anemones. sea anemones were placed along with attached po­ Moreover, a correspondence of the six primary ten- lyps in the order Actiniaria because they had more tacles to exocoels and the two directive tentacles than eight perfect mesenteries. to endocoels is typical for most anemones, whereas Later, Carlgren (1908) divided all coral po­ in some Edwardsia all eight primary tentacles cor- lyps, Anthozoa, based on the number of primary respond to the endocoels (Bourne, 1916). mesenteries into three subclasses: Hexacoral- Stephenson (1920, 1921, 1922) in his “On lia, Octocorallia, and Dodecacorallia. The first the Classification of Actiniaria” adhered to the subclass, Hexacorallia (sensu Carlgren only), Bourne’s (1916) system. Stephenson (1921) was characterised by the presence of six primary similarly separated the edwardsians in the or- mesen­teries and later also by a varying number of der Edwardsiaria, subclass Zoanthactiniaria. metamesenteries. Only the ceriantharians and the He united the remaining forms, as suggested by antipatharians were attributed here. The subclass Bourne (1916), in the suborder Actiniaria, order Octocorallia included polyps with eight bilateral Dodecactiniaria, subclass Zoanthactiniaria. The protomesenteries. In the third subclass, Dodeca- further division of the sea anemones by Stephen- corallia, he placed polyps with twelve protomes- son was partly consistent with Carlgren’s (1898, enteries, usually also having a different number of 1900) system. Stephenson (1922) also separated metamesenteries, arranged bilaterally or radially. the tribe Nynantheae within the suborder Ac- This subclass encompassed the orders Zoantha- tiniaria, but unlike Carlgren (1898, 1900) sub- ria (= Zoanthida), Actiniaria and Madreporaria divided this tribe into four subtribes: Athena­ (= Scleractinia). ria, Endocoelactaria, Mesomyaria, Endomyaria. Bourne (1916) did not agree with the names Some burrowing sea anemones were located in the of taxa proposed by Carlgren (1908). According families Halcampidae and Ilyanthidae in the sub- to Bourne, the name Hexacorallia was tradition- tribe Athenaria. One burrowing form, Andresia

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Fig 13. The position of burrowing sea anemones (in bold) in Stephenson’s (1920, 1921, 1922) classification of coral polyps. partenopea (Andres, 1883), however, was isolated elongated body and a rounded aboral end, but in the family Andresiidae Stephenson, 1922 inside lacking basilar muscles, made up Athenaria Carl- of the subtribe Endomyaria along with polyps that gren, 1898 (Fig. 16). That group corresponded have an endodermal sphincter (Fig. 13). to “Actinines pivotantes” and was largely con- sistent with Ilyanthidae, but did not include the 1.4. Classification based on presence or ceriantharians. Carlgren included the edward- absence of basilar muscles sians in Athenaria as a family Edwardsidae. The remaining burrowing sea anemones were distri­ The next important step in building an ana- buted among the families Halcampomorphidae tomical classification of the sea anemones was Carlgren, 1900, Halcampactidae Carlgren, 1900, the use of a new attribute proposed by Carlgren Halcampidae, Andvakiidae, and Ilyanthidae. Lat- (1898, 1900), the presence of basilar muscles. The er, Carlgren (1905) used other names to refer to fibers of the basilar muscles pass along the me­ these groups–Basilaria (for Thenaria) and Abasi- sentery accretion line to the base on both sides laria (for Athenaria)–emphasizing that shape of of the mesogloeal plate of the mesentery (Figs 14, the proximal end is less important and that the 15). The basilar muscles constrict edges of a pedal main distinguishing feature is the pre­sence of disc to its center and promote crawling. All anem- basilar muscles in the first group and their ab- ones with basilar muscles and a pedal disc, as a sence in the second (Figs 14, 16). Both these rule, inhabit solid substrates. They were united groups, Thenaria and Athenaria, were united in by Carlgren into a new taxon, Thenaria Carlgren, the tribe Nynantheae Carlgren, 1898 (suborder in 1898. At that time the burrowing forms with an Carlgren, 1949).

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Figs 14–15. Mesentery musculature of Thenaria. 14, position of different muscles on mesentery, viewed from the exocoelic (left half) and endocoelic (right half) side, vertical section; 15, position of basilar mus- cles of mesentery, vertical section. c, column; t, tenta- cle; phx, pharynx; mshp, marginal sphincter; ms, mar- ginal stoma; m, mesentery; mf, mesenterial filament;b , base; rm, retractor muscle; tm, transversal muscle; pbm, parieto-basilar muscle; bm, basilar muscle. After Carl- gren (1905) and Stephenson (1928).

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Fig 16. Mesentery musculature of Athenaria, vertical section. a, viewed from the exocoelic side; b, viewed from the endocoelic side. c, column; t, tentacle; ph, physa; phx, pharynx; g, gonads; mf, mesenterial filament; tm, transversal muscle; rm, retractor muscle; pm, parietal muscle. After Carlgren (1905).

224 ( Zoosystematica Rossica, Vol. 29, No. 2, pp. 213–237 N.Yu. Ivanova. Classification and evolution of the burrowing sea anemones

McMurrich (1904) did not agree with Carl- the length of the inner and outer tentacles as well gren’s (1898, 1900) system. He noted that, al- as in the presence or absence of nemathybomes and though Carlgren’s classification is based on a sta- physa. Furthermore, he established a new fami- ble character, such a division leads to association ly Limnactiniidae Carlgren, 1921, whose polyps of unrelated forms and separation of relatives. Mc- lacked either a sphincter and or tentacles. He pre- Murrich also noted that the relationship between served the family Andvakiidae, characterised by a a pedal disc and muscles is so close that it is impos- mesogloeal sphincter and acontia. Beyond this, he sible to modify one without changing the other. proposed a new family Halcampactiidae Carlgren, Furthermore, from his point of view, it would be 1921 with acontia but without a sphincter. The more correct to refer not to the absence of a pedal family Halcampidae joined forms with a simple or disc, but to its modification into a physa. In this double mesogloeal sphincter, but without acontia. case, the parietal muscles should be considered as Halcampoididae Appellöf, 1896 included polyps homologous with the basilar muscles. Avoiding the without a sphincter or with a very weak endoder- system proposed by Carlgren (1898, 1900), Mc- mal one. Carlgren (1921) also retained the family Murrich mainly followed Andres’ (1883) classifi- Ilyanthidae because its representatives exhibited cation. Inside the order Actiniaria, he separated an endodermal sphincter. the suborder Actininae, which united the burrow- Afterwards, as a result of many years of dis- ing sea anemones and the polyps with a well-de- cussion between Carlgren and Stephenson, Carl- veloped pedal disc, which were placed by him into gren (1949) published the system that has become different families. McMurrich (1904) considered widespread and still serves as the basis of the Ac- the edwardsians in the rank of a family and en- tiniaria classification. In this system, Carlgren larged this family by placing Cactosoma chilense distinguished within the infraorder Athenaria (McMurrich, 1904) in it. nine families, namely Edwardsiidae, Halcampoi- In the fundamental work on the anemones didae, Haloclavidae, Andresiidae, Halcampidae, collected during the Ingolf Expedition, Carlgren Limnactiniidae, Haliactinidae, Octineonidae (1921) continued to follow the classification pro- and Andvakiidae. As before (1921), when classi- posed by him in 1898 and 1900. He emphasised fying the burrowing sea anemones, Carlgren re- that the main feature that distinguished Athe- naria (Abasilaria) from Thenaria (Basilaria) was the absence of the basilar muscles in the first group. The earlier researchers (Milne-Edwards & Haime, 1957; Gosse, 1858, 1860; Verrill, 1864; Klunzinger, 1877; Andres, 1883; Hertwig, 1882, 1888) attached great importance to the shape of the proximal end, placing the burrowing sea anemones in a separate group. However, the ab- sence of basilar muscles was a more important feature for combining these polyps because the shape of the proximal end can vary considerably, although many of these sea anemones were un- doubtedly characterised by a rounded proximal end (Carlgren, 1921). He considered the pres- ence or absence of a sphincter and its structure, as well as the presence or absence of acontia, as the main features for division of Athenaria into families. Thus, he distinguished the family Ed- wardsiidae with two subfamilies, Edwardsiinae Fig 17. The position of burrowing sea anemones (in and Milne-Edwardsiinae, whose representatives bold) in Carlgren’s (1949) classification of Actiniaria lacked a sphincter but differed from each other in with some modifications by Fautin (2013).

( Zoosystematica Rossica, Vol. 29, No. 2, pp. 213–237 225 N.Yu. Ivanova. Classification and evolution of the burrowing sea anemones lied mainly on characters such as presence or ab- can be distinguished. Each stage is characterised sence of a sphincter and acontia. Later, Carlgren by a key feature that underlies the system. (1956) added another family, Galatheanthemidae, The first period of classification dates back whose polyps were characterised by a very strong to the mid-19th century and is associated with mesogloeal sphincter and a strong cuticle, forming Milne-Edwards & Haime (1857), Gosse (1858, a tube. Carlgren’s (1949) system was adopted for 1860), and Klunzinger (1877). This period is a long time by a number of researchers (e.g. Hand characterised by allocating the burrowing sea & Bushnell, 1967; Manuel, 1977; Fautin, 1988; anemones into a separate group, mainly based on Sanamyan & Sanamyan, 1998; Gonzalez-Muñoz their elongated body shape and rounded aboral et al., 2012) and, with minor modifications, was end (Fig. 1a, b). By attaching such great impor- available on the “Hexacorallians of the World” tance to external features, the researchers com- website (Fautin, 2013) (Fig. 17). bined unrelated forms; for example, Gosse (1860) placed the burrowing sea anemones together with 1.5. Classification based on molecular markers the ceriantharians. The second stage is associated with the onset Adopting a system based on molecular markers of anatomical studies by the German zoologists was suggested by Rodríguez et al. (2014). They R. Hertwig and O. Hertwig. The discovery of proposed a completely new classification, in which eight perfect mesenteries (Fig. 5) in members of Actiniaria is divided into two suborders, Anen- the family Edwardsiidae led them to be separat- themonae and Enthemonae. The representatives ed from all the other burrowing sea anemones. of Carlgren’s (1949) Athenaria were distributed In turn, the latter were combined with large at- within the composition of both suborders and set- tached polyps (Hertwig & Hertwig, 1879). Some tled on very distant branches. The suborder Anen- researchers (e.g. Bourne, 1916; Stephenson, 1920, themonae united the superfamily Edwardsioidea 1921, 1922) supported this separation of the bur- Andres, 1881 with one family of the burrowing rowing forms until the 1920s, even though the sea anemones Edwardsiidae and the superfamily uniformity of the mesenterial development in the Actinernoidea Stephenson, 1922. This suborder, both edwardsians and all the other hexamerous according to Rodríguez et al., includes the actin- sea anemones was already shown in the late 19th iarians with a unique arrangement of mesenteries century (see Faurot, 1895). that differs from the most typical hexamerous ar- The use of the basilar muscles by Carlgren rangement with mesenterial pairs arising in exo- (1898, 1900, 1905, 1949) in creating the system coels. The remaining burrowing sea anemones are of anemones opens its third stage. Carlgren (1898, placed in the suborder Enthemonae and distribut- 1900, 1949) established the infraorder Athena­ ed among the three superfamilies Actinostoloidea ria, which combined the burrowing forms with- Carlgren, 1932, Metridioidea Carlgren, 1893, and Actinioidea Rafinesque, 1815 (Rodríguez et al., out basilar muscles (Fig. 16), and the infraorder 2014; Gusmão et al., 2019). Members of Enthem- Thenaria, whose representatives had such mus- onae, according to Rodríguez et al. (2014), have cles (Figs 14, 15). However, subsequent detailed mostly hexamerous cycles with pairs of mesenter- analy­sis of morpho-anatomical characters and ies arising in the exocoels. the description of new species led some specialists (e.g. Schmidt, 1972, 1974) to assume a polyphyly of Athenaria and to reject the absence of basilar 1.6. Four steps in the development of muscles as a key feature for isolating all the bur- the burrowing sea anemone classification rowing sea anemones in a single group. My review of the establishment of the classifi- At present, animal systems based on molec- cation of burrowing sea anemones underlines the ular markers are very popular and considered result of laborious work devoted to the study of to be comprehensive. In the classification of the the morphology and anatomy of these animals. burrowing sea anemones, the use of molecular Based on the views and assumptions of research- methods opened the next, fourth stage. However, ers, four steps in the formation of the classification recent changes in the anemone classification show

226 ( Zoosystematica Rossica, Vol. 29, No. 2, pp. 213–237 N.Yu. Ivanova. Classification and evolution of the burrowing sea anemones that they cannot be considered as exhaustive or respectively). Stephenson (1935) also noted that successful. This is clearly evident in the new high- Halcampa could have only eight macrocnemes in er-level classification for Actiniaria proposed by the first mesenterial cycle. Moreover, eightEd - Rodríguez et al. (2014). These researchers sub- wardsia mesenteries were found in Condylanthi- divided the order Actiniaria into the suborder dae Stephenson, 1922, in representatives of the Anenthemonae and the suborder Enthemonae. genus Segonzactis Riemann-Zürneck, 1979 (see Rodríguez et al. (2014) noted that their findings Riemann-Zürneck, 1979; Dimitris & Chariton, highlight the inadequacy of the previous classifi- 2002). Thus, the differences in the developmen- cation of the order Actiniaria. Nonetheless, from tal processes of mesenteries in edwardsiids and the perspective of morphology, anatomy, process- endocoelanthids, as well as the discovery of eight es of development, behaviour, and lifestyle, a new Edwardsia mesenteries in representatives of oth- system based on molecular markers must also be er families, make it impossible to combine these considered insufficient. Rodríguez et al. (2014) sea anemones into the suborder Anenthemonae. remark that their findings based on the DNA se- Finally, the edwardsiids differ considerably from quence data correspond neatly with several mor- the endocoelanthids in other features of anatomy, phological trends observed in the order Actiniaria. morphology, behaviour and lifestyle. For example, they proposed uniting the edward- The remaining burrowing forms (apart from sian and endocoelanthean sea anemones in the sub- Edwardsiidae) were placed by Rodríguez et al. order Anenthemonae because these actiniarians (2014) and by Gusmão et al. (2019) in the subor- have a unique mesentery arrangement that differs der Enthemonae along with the sea anemones of from the most typical hexamerous arrangement the remaining Carlgren’s groups and distributed with pairs of mesenteries arising in exocoels. Such among three superfamilies: Actinostoloidea, Met- a characteristic of the suborder is highly doubtful. ridioidea, and Actinioidea. This new division of In the endocoelanthean sea anemones, when the the burrowing sea anemones confirms the assump- first twelve mesenteries (six couples) are devel- tions of previous researchers about the polyphyly oped, all the subsequent pairs appear in the lateral of Athenaria (e.g. Hand, 1966; Schmidt, 1974). endocoels with longitudinal muscles oriented as in The system proposed by Rodríguez et al. (2014), directives. Of course, this is a unique arrangement however, joins completely dissimilar sea anemo­ not found in any other group. Nonetheless, the ed- nes into one group, and their dissimilarity goes wardsians do not share this uniqueness with the beyond morpho-anatomical characters. Although endocoelanthean sea anemones. As early as 1895, the burrowing forms have several common struc- Faurot showed that the edwardsians have the same tures with the remaining actiniarians, they are mesentery organization as numerous hexamerous characterised by features inherent only to them. sea anemones. The edwardsians also have six pairs This leads to indistinctness and diffusiveness of of mesenteries that constitute the first cycle; the the superfamily diagnoses. mesenteries of the next cycles also appear in pairs Accordingly, the methods of classification in exocoels. The differences are that the edward- based on molecular markers clearly require signifi- sians have only eight perfect macrocnemes; later- cant improvement. Importantly, different markers al mesenteries (microcnemes) that make up them give different results, as is clearly evident from the pairs are not fully developed. Microcnemes arise position of the mysterious Relicanthus daphneae only in the most distal part of the column (see Fig. (Daly, 2006). Rodríguez et al. (2014) selected two 4 in Sanamyan et al., 2015). Moreover, eight Ed- nuclear and three mitochondrial genes with multi- wardsia mesenteries are also found in other rep- ple analytical methods, which did not allow find- resentatives of Carlgren’s Athenaria. For example, ing a precise position for Relicanthus in the Acti­ the arrangement of mesenteries in Octineon sueci- niaria system. As the result, the authors had to cum Carlgren, 1940 (Octineonidae Fowler, 1894) rank this animal as incerti ordinis. In a subsequent and Limnactinia Carlgren, 1921 (Limnactiniidae publication based on numerous complete nucleo- Carlgren, 1921) resembles that of the edwardsians tide sequences of mitochondrial DNA, however, (see Sanamyan et al., 2018; Carlgren, 1921, 1927, the taxonomic status of Relicanthus daph­neae was

( Zoosystematica Rossica, Vol. 29, No. 2, pp. 213–237 227 N.Yu. Ivanova. Classification and evolution of the burrowing sea anemones changed: it was returned to the order Actiniaria corresponding to Edwardsia mesenteries, and in the rank of the suborder Helenmonae Daly et four weak ones forming pairs with four lateral Rodríguez, 2019 (Xiao et al., 2019). mesenteries. Like Hertwig (1882), Boveri (1890) The use of the molecular markers to clarify the considered Halcampa Gosse, 1858 to be a transi- systematic position of some burrowing sea anemo- tional form between Edwardsia and hexactinians. nes has also led to unexpected changes. For exam- Regressive development seemed unlikely to him. ple, Haloclava Verrill, 1899 in the newly present- McMurrich (1891), discussing issues of anemo­ ed scheme (see Fig. 2 in Rodríguez et al., 2014) ne phylogeny, also wrote that representatives of was placed within the clade Actinioidea, but one the order Actiniaria descended from ancestors species Haloclava producta (Stimpson, 1856) and close to modern Edwardsia. He believed that a another Haloclava sp. were moved apart. Later, form similar to but different from the scyphozoan however, H. producta took a position close to rep- larva should be placed at the root of the Anthozoa resentatives of the clade Metridioidea (Xiao et al., tree. From this ancestor, a transition occurred to a 2019). Another genus, Halcampoides, was orig- polyp with octomerous symmetry, which gave rise inally (Rodríguez et al., 2014) placed inside the to Edwardsia and all Alcyonaria. Since the stage clade Metridioidea, but later (Xiao et al., 2019) with eight mesenteries was described in the on- became very distant from representatives of that togeny of all non-skeletal coral polyps, including clade. the ceriantharians and zoantharians, McMurrich Thus, at present, I consider that abandoning (1891) thought that their origin was associated the traditional classification of Actiniaria (Carl- with an Edwardsia-like form. Considering the de- gren, 1949; Fautin, 2013) built on morpho-ana- velopment of the first hexamerous cycle of mesen­ tomical characters and founding it based on mo- teries, he also described the stage in which four lecular markers is premature. lateral mesenteries reach a pharynx and in which smaller mesenteries that form pairs with them do 2. Views on the evolution of not reach it, i.e. remain imperfect. Although no the burrowing sea anemones adult sea anemone with this structure is known, this stage represents an important period in evo- 2.1. The burrowing sea anemones are lution. It gave rise to the genera Scytophorus Her- a primitive group, from which all other twig, 1882, Gonactinia Sars, 1851 and Oractis anemones originate McMurrich, 1893, forming the group Protactin- Based on the study of mesentery development iae Carlgren, 1891, whose representatives had an in different anthozoan groups, researchers (Her- incomplete second cycle of mesenteries. Moreo- twig & Hertwig, 1879; Hertwig, 1882; Boveri, ver, an important feature of Protactiniae was the 1890) assumed that the edwardsians are closest preservation of bilateral symmetry. They gave rise to the ancestral forms and that all other anemo- to hexamerous anemones, in which, upon com- nes originate from them. In the earlier stages of pletion of development of the second mesenterial ontogenesis, all sea anemones are bilaterally sym- cycle, radial symmetry replaces the original bilat- metrical animals. The edwardsians, however, stop eral symmetry. However, forms belonging to the at the eight–mesentery stage and retain this type genus Halcampa disturbed the strictness of the of symmetry throughout their lives. In the further phylogenetic scheme. Some members of this ge- developmental process the remaining anemones nus had only six pairs of mesenteries and could be turn to radial (mainly hexamerous) symmetry considered more primitive. Other Halcampa spp. by completing the lateral pairs and by developing and representatives of closely related genera also paired mesenteries of the next cycles in the exo- exhibited secondary imperfect mesenteries. This coels (Hertwig & Hertwig, 1879; Boveri, 1890). would make them more advanced. The first of Boveri (1890) examined Halcampa chrysanthel- these, according to McMurrich, could be close to lum (Peach in Johnston, 1847) in detail. Although Scytophorus, Gonactinia and Oractis, but this was it forms twelve mesenteries as in hexactinians, unlikely because all species of the genus Halcampa they are unevenly developed: eight strong ones, were very similar to each other and differed sig-

228 ( Zoosystematica Rossica, Vol. 29, No. 2, pp. 213–237 N.Yu. Ivanova. Classification and evolution of the burrowing sea anemones nificantly from the three other genera. Therefore, number of mesenteries that have undergone spe- Halcampa and closely related genera with second- cialization. The first cycles consisted of sterile ary mesenteries most likely originate from hex- perfect mesenteries with weak muscles; imper- actinians due to a stopped development that led fect fertile mesenteries formed subsequent cycles to the reduction of the second cycle of mesenteries (Stephenson, 1920, 1921). Thus, Stephenson also (McMurrich, 1891). separated Edwardsia from the other anemones As noted above, Carlgren (1898, 1900) pro- and considered the halcampids to be more primi­ posed dividing the sea anemones into Thenaria tive forms that gave rise to all large hexamerous and Athenaria based on the presence of basilar polyps. Nevertheless, he cautiously assumed that muscles in the former and their absence in the lat- the edwardsians still belong to the Nynantheae ter. Carlgren (1905) considered this presence to be (according to Carlgren’s (1898, 1900) suborder, a more advanced trait that arose later in evolution, including Athenaria and Thenaria), in which some and was characteristic of “higher” anemones with mesenteries became rudimentary and form only a well-developed flat pedal disc (Figs 14, 15). The bilateral couples. The histological structure of Ed- absence of basilar muscles, in contrast, is a primi­ wardsia also shows similarities with Nynantheae tive character of “lower” Actiniaria–Athenaria. (Stephenson, 1920, 1921, 1922). Greater mobility and elongated body shape con- tributed considerably to the development of lon- 2.2. The burrowing sea anemones originate gitudinal muscles on the mesenteries in Athenaria from large hexamerous actinians (Fig. 16). These retractor muscles are homologous to those of other anemones. Carlgren believed that Faurot (1895) revealed that Edwardsia in fact the parietal muscles, lying on one side of the mesen­ had more than eight mesenteries. His work largely tery, were the modified parieto-basilar muscles, changed the notions about evolution within Ac- and those on the other side were part of the longi- tiniaria and sought to find common and distinc- tudinal muscles of the mesentery. Importantly, the tive features of “Actinines pivotantes” and “Hex- musculature of the Athenaria mesenteries did not actinies” using embryology and anatomy data. have a homologue to the basilar muscles of higher Although the author did not consider the relation- anemones (Figs 14–16) (Carlgren, 1905, 1921). ship of different groups of anemones, he showed Stephenson (1920, 1921, 1922) wrote that a po- that all have a common organization plan, which tential ancestor for all Anthozoa was a small plank- changes from group to group. He suggested that tonic organism characterised by eight mesenteries Edwardsia, like Halcampa or Peachia Gosse, 1855, and bilateral symmetry. Several forms could have showed a stoppage in development, but more pro- derived from it and given rise to all the anthozo- nounced. In Faurot’s thinking, his discovery by an groups. With regard to the anemones, Ste- of microcnemes in Edwardsia showed the incon- phenson (1921) believed that Edwardsiaria were sistency of isolating these anemones in a separate the first to separate from the common stem; they branch, and the groundlessness of their affinity to acquired a burrowing lifestyle and became worm- the ancestral form (Faurot, 1895). like. The main branch led to the appearance of a Beneden (1897) agreed that the description Halcampa-like organism, from which most anem- of the micromesenteries by Faurot (1895) in Ed- ones originated. According to Stephenson (1920, wardsia beautempsi and Edwardsianthus pudi- 1921), primitive forms were small and had few cus (Klunzinger, 1877) negated the assumption mesenteries, the macrocnemes, which performed about the primitiveness of Edwardsia. Van Bened- all the functions and had mesenterial filaments, en reco­gnised the Edwardsia species as repre- gonads and muscles1. The evolution of anemones sentatives of Hexactiniaria whose development was marked by a tendency to increase the size of stopped, that retained only the eight perfect mes- the individual and, accordingly, to develop a large enteries and became sexually mature. Since these

1I reserve the right to use the terms “gonads” and “organs” following their traditional application in the literature on sea anemones (e.g. Sanamyan et al., 2018).

( Zoosystematica Rossica, Vol. 29, No. 2, pp. 213–237 229 N.Yu. Ivanova. Classification and evolution of the burrowing sea anemones species have a total twelve primary mesenteries, scleractinians (Scleractinia = Madreporaria). Ac- as do hexactinians, and in addition an incomplete cordingly, the first sea anemones (which lost their second cycle of mesenteries, van Beneden con- ability to form a skeleton) could, in the late stages sidered it impossible to separate the edwardsians of ontogenesis, develop a pedal disc with muscles. from all other anemones and to regard them as an These muscles enabled them to attach to a sol- ancestral form. The presence of even rudimentary id substrate, a characteristic of higher anemones. mesenteries did not allow Edwardsia to be con- Thus, in Hand’s interpretation, it is more correct to sidered as a transitional form from an ancestor to consider Thenaria, whose members have numerous hexactinians because, according to van Beneden, mesenteries, to be closer to the ancestor than Athe- these mesenteries could hardly be preserved until naria. Hand also concluded that Haeckel’s (1966) the present. Consequently, the edwardsians origi- interpretation of evolution, from simple to complex nated from the hexamerous anemones with a large (from a few to many mesenteries), is incorrect in number of mesenteries and tentacles, as evidenced the case of sea anemones. Hand was the first to by the presence in the genus of species with many draw attention to the similarity of burrowing sea tentacles and by their hexamerous arrangement. anemones and the polyps of the subtribe Acontiar- They are hexactinians with underdeveloped ia (now the superfamily Metridio­idea), which goes mesen­teries of the fifth and sixth bilateral pairs of beyond the presence of acontia in polyps of both the first cycle and rudimentary mesenteries of the groups. Among Acontiaria, representatives of the second cycle (Beneden, 1897). genera Flosmaris Stephenson, 1920 and Mimetri­ Subsequently, Carlgren & Stephenson (1928) dium Hand, 1961, resemble the athenarian polyps emphasised that the consideration of the genus Ed- in body shape and burrowing lifestyle. Hand there- wardsia by most zoologists as an example of a prim- fore concluded that the burrowing lifestyle and the itive eight-ray form, from which all sea anemones correlated elongation of the body (characteristics originated, is in fact incorrect. On the one hand, of Athenaria) first arose in the acontiarian anemo- Edwardsia has more than eight mesenteries (Fau- nes. In the course of evolution, the latter could lose rot, 1895), and there are no anemones that have a muscular base and develop physa. Therefore, the only eight mesenteries in the adult state. On the athenarians derived from members of Acontiaria. other hand, Gonactinia can be identified as a more The athenarians without acontia, such as Edward- primitive form, with an organization closer to the sia and Halcampoides, lost these organs and at the primitive state than Edwardsia. Unlike Gonactin- same time, began to mature at earlier ontogenetic ia, Edwardsia is in many ways a more specialised stages, therefore reducing the number of mesenter- and advanced form. Its few mesenteries indicate, ies (Hand, 1966). rather, a reduction or cessation of development as- Schmidt (1972) also suggested that Edward- sociated with a worm-like body shape. Moreover, sia cannot be considered primitive because it has Stephenson rejected Bourne’s (1916) assumptions only eight perfect mesenteries. On the contrary, and concluded, based on his own observations, it belongs to the phylogenetically “later”, higher that Edwardsia’s microcnemes adjacent to four lat- anemones. Schmidt (1974) then argued that the eral macrocnemes correspond to the fifth and sixth presence of basilar muscles is neither an advanced couples of other anemones, and that the rest of the nor a primitive feature: these muscles develop in microcnemes arise as ordinary pairs, but not cou- anemones that settle on a solid substrate and are ples (Carlgren & Stephenson, 1928). reduced in the burrowing forms. Thus, the athe- In the second half of the 20th century, with ac- narian anemones may have arisen independently cumulation of new data on anemone diversity, in- in several families due to reduction of the basi- terest in the study of the athenarian polyps was re- lar muscles during a transition to soft sediments. vived. An original view of its origin was expressed Having studied the distribution of nematocysts by Hand (1966). He believed that Athenaria, and certain anatomical traits, Schmidt (1974) long considered as primitive anemones, should be divided the athenarians into two actiniarian su- considered as secondarily simplified forms. In his perfamilies: Endomyaria (now the superfamily opinion, all the sea anemones originated from the Actinioidea), equipped with an endodermal mar-

230 ( Zoosystematica Rossica, Vol. 29, No. 2, pp. 213–237 N.Yu. Ivanova. Classification and evolution of the burrowing sea anemones ginal sphincter muscle, and Mesomyaria (now the forms are considered as primitive, the closest to the superfamily Actinostoloidea), whose mesogloeal ancestor. A number of researchers (see Hertwig marginal sphincter muscle consists of muscular & Hertwig, 1879; Hertwig, 1882; Boveri, 1890; fibers embedded in a thick layer of mesogloea. Carlgren, 1905), however, have explained their Based on the strongly differing structure of the primitiveness in terms of various anatomical fea- edwardsians and the endomyarians, an affinity of tures. For example, Hertwig (1882), based on the these sea anemones as proposed by Schmidt (1972, discovery of only eight mesenteries in Edwardsia, 1974) seems unlikely. Nonetheless, the description considered the edwardsians as being the closest to of a new genus Segonzactis Riemann-Zürneck, the ancestor. He defined the remaining burrowing 1979 (Condylanthidae) became a serious argu- forms (having at least one complete hexamerous ment for conjunction of Edwardsia-like anemones cycle of mesenteries) as transitional between Ed- with Endomyaria (Riemann-Zürneck, 1979). This wardsia and attached hexamerous polyps. Howev- genus differs significantly in morpho-anatomical er, the presence of more than eight mesenteries in features from the remaining condylantids. It has the edwardsians contradicts their relationship to no basilar muscles, and its eight macrocnemes Octocorallia, which are generally considered the are located as in Edwardsia (Riemann-Zürneck, closest to ancestors of all Anthozoa. 1979; Dimitris & Chariton, 2002). Riemann-Zür- Carlgren (1905) also believed that burrowing neck concluded that members of the family Con- sea anemones are a primitive group. Nevertheless, dylanthidae were transitional forms between the in contrast to Hertwig (1882), he relied on the endomyarians and the edwardsians. This view presence or absence of the basilar muscles. Accord- was based on the similarity between Segonzactis ingly, Carlgren (1905) divided the sea anemones and Edwardsia as well as the fact that the fami- into “higher” Thenaria with basilar muscles and a ly presents a combination of features and their well-developed pedal disc and “lower” Athenaria variation between genera (namely dimorphism of without such muscles and with a rounded aboral mesenteries and their number, the distinctness of end. Subsequent researchers questioned Carl- body division, and the presence of basilar muscles gren’s (1905) assumption about the primitiveness and a marginal sphincter). Speculating on a di- and monophyly of the athenarians. This revived rection of the evolution of the group and on the the views of Faurot (1895) and Beneden (1897) ancestral form, Riemann-Zürneck concluded that and established a new hypothesis suggesting that the ancestor was probably very close to a typi- the burrowing sea anemones are advanced forms cal Actinia-like endomiarian sea anemone. One (see Carlgren & Stephenson, 1928; Hand, 1966; branch of descendants is today represented by the Schmidt, 1972, 1974). sea anemones (Athenaria), which reduced the size The first to suspect that burrowing sea anem- and number of mesenteries and specialised in be- ones could have come from large hexamerous po­ coming flexible and contractile animals. They ul- lyps (based on stopped individual development) timately succeeded in conquering a new habitat, were Faurot (1895) and Beneden (1897). This loose sediment. Examples of possible stages of this view was extended by Hand (1966), who suggest- evolutionary trend are evident in Condylanthidae ed that they originate from Acontiaria. As a result (Riemann-Zürneck, 1979). of the transition to life on soft substrates, they lost The growing number of works based on mole­ the basilar muscles, reduced the number of mesen- cular markers increasingly support the polyphy- ly of Carlgren’s Athenaria (e.g. Daly et al., 2002, teries and became mature in the earlier ontogenet- 2008, 2010; Rodríguez et al., 2012, 2014). ic stage. Schmidt (1972, 1974) held a similar opin- ion, the only difference being that the athenarians arose independently from different families of the 2.3. Hypotheses on the origin of the burrowing sea anemones thenarian sea anemones, and not only from Acon- tiaria. Other authors (e.g. Daly, 2002; Rodriguez My review shows two main hypotheses on et al., 2012, 2014) disagree that this group origi- the origin of the burrowing sea anemones. In the nated from anemones with basilar muscles in the framework of the first hypothesis, the burrowing course of adaptation to a burrowing lifestyle.

( Zoosystematica Rossica, Vol. 29, No. 2, pp. 213–237 231 N.Yu. Ivanova. Classification and evolution of the burrowing sea anemones

Based on molecular markers, the researchers 1897 (Actinodendronidae Haddon, 1898), Oulac- (Daly et al., 2008; Rodriguez et al., 2012, 2014) tis concinnata (Actiniidae). Nonetheless, the be- showed the polyphyly of athenarian sea anemones. haviour of many thenarians living in sand is gen- Accordingly, an elongated body, a rounded abo- erally the same as that of settled thenarians: they ral end and the absence of basilar muscles arose are also attached with their pedal disc to a solid (or were lost) multiple times within Nynanthe- substrate (stones, rock, shell fragments, etc.), the ae (Rodríguez et al., 2014). The discovery of sea only difference being that they are hidden in the anemones that both have basilar muscles and a sediment. A burrowing behaviour may well not al- burrowing lifestyle (vs those lacking such mus- ways be necessary for them: at least Oulactis ori- cles and not burrowing) les to the opinion that entalis was rather often found attached to a stone, Carlgren’s (1898, 1900, 1905) division into higher not submerged into sand (Grebelny, pers. comm.; Thenaria and lower Athenaria is incorrect (Daly author’s unpublished data). Thenarian sea anemo- et al., 2002; Rodríguez et al., 2014). To confirm nes do burrow, as shown by O. concinnata (Mag- polyphyly and that incorrectness, the researchers num, 1970; Pickens, 1988), by contracting pari- (e.g. Daly, 2002) usually concentrated on the pres- eto-basilar muscles and peristaltic contractions. ence or absence of the basilar muscles in different First, the parieto-basilar muscles contract and the groups of sea anemones. Nevertheless, the remain- pedal disc is swollen. Then, the column lengthens ing morpho-anatomical features and the burrow- due to relaxation of parieto-basilar muscles and ing behaviour itself are, as a rule, not taken into the passage of a peristaltic wave (the result of con- account, which makes it possible to combine the traction of a circular muscles of body wall) and the athenarian and thenarian sea anemones. pedal disc compresses. This is followed by a grad- Burrowing behaviour is poorly studied and ual relaxation of the disc and new contraction of described only for certain representatives of the parieto-basilar muscles. When the column initial- four athenarian families (Haloclavidae, Halcam- ly plunges into the sediment, the retractor muscles poididae, Halcampidae, Edwardsiidae) and only sharply contract. As a result, the polyp decreases for two representatives of the thenarian polyps: in size and settles in a larger hole. When a solid Oulactis concinnata (Drayton in Dana, 1846), object is reached, the burrowing stops (Magnum, Actiniidae Rafinesque, 1815, andIosactis vaga­ 1970; Pickens, 1988). bunda Riemann-Zürneck, 1997, Iosactinidae In contrast to the thenarians, the burrow- Riemann-Zürneck, 1997 (see Williams, 2003; ing athenarians not only submerge into the sed- Durden et al., 2015). Even based on such insuf- iment but also move inside it, as noted for the ficient data, I consider that the burrowing behav- edwardsiids (see Manuel, 1975; Williams, 2003). iour of the athenarians and thenarians undoubt- Although its behaviour has not been described, edly arose independently. This is supported by a Limnactinia, judging from the absence of tenta- significantly different morphology and anatomy cles in this genus, has probably became completely of the two groups and by the related differences infaunal and no longer appears on the surface of in their burrowing methods (see Ansell & True- the substrate. Furthermore, the burrowing behav- man, 1968; Magnum, 1970; Pickens, 1988; Ansell iour of Athenaria differs significantly from that & Peck, 2000; Williams, 2003). observed in Thenaria, reflecting their distinct In the literature, the term “burrowing” ap- anatomy. As shown for Peachia hastata Gosse, plies to both thenarian and athenarian polyps. 1855 (Haloclavidae) (Ansell & Trueman, 1968), Nevertheless, it has been proposed to call some Halcampoides sp., (Halcampoididae) (Ansell thenarian species the “burying” sea anemones to & Peck, 2000) and Nematostella vectensis Ste- emphasize their difference from the athenarian phenson, 1935 (Edwardsiidae) (Williams, 2003), “burrowing” forms (Williams, 2003). Carlgren’s burrowing involves peristaltic contractions of Thenaria include many sea anemones that live on the column wall which lead to eversion of physa. soft sediments, for example Stichodactyla haddo- With sufficient immersion in the sediment, when ni (Saville-Kent, 1893) (Stichodactylidae Andres, the physa can serve as an anchor, the column is 1883), Actinostephanus haeckeli Kwietniewski, straightened by contraction of the retractor mus-

232 ( Zoosystematica Rossica, Vol. 29, No. 2, pp. 213–237 N.Yu. Ivanova. Classification and evolution of the burrowing sea anemones cles in P. hastata (Ansell & Trueman, 1968) and probably be considered as an evidence for a fur- Halcampoides sp. (Ansell & Peck, 2000) or of the ther independent evolution of various athenarian parietal muscles in N. vectensis (Williams, 2003). families. Moreover, Athenaria should not be con- In addition, the edwardsiids Scolanthus callimor- sidered primitive because the appearance of this phus Gosse, 1853, Edwardsia ivelli Manuel, 1975, group is probably associated with the expansion of and E. claparedii (Panceri, 1869) burrow head- the ecological niche of the order Actiniaria. first into mud, i.e. they burrow by alternately Nevertheless, the athenarian sea anemones extending and introverting the distal end of the share many characters with Thenaria, potentially column, with the tentacles retracted, using a di- indicating the origin of the athenarians from sev- lated scapus wall as a “penetration anchor” (Ma- eral groups of the thenarians. nuel, 1981; Williams, 2003). The only exception Almost all athenarians (except Halcampoides, among the non-athenarians is the abyssal burrow- which has only six pairs of mesenteries, and An- ing Iosactis Riemann-Zürneck, 1997 (Iosactiidae dresia Stephenson, 1921, which has three mesen- Riemann-Zürneck, 1997), which moves below the teric cycles) have a division of mesenteries into surface (see Durden et al., 2015). It can “jump out” macrocnemes and microcnemes. Macrocnemes of its hole by contracting the endodermal circu- are strong, perfect mesenteries that bear retrac- lar muscles and move along the substrate surface tors, filaments and gonads; microcnemes usually (Riemann-Zürneck, 1997). The athenarian sea lack these organs, but can have parietal muscles. anemones have no such ability. Moreover, Iosactis Among the thenarians, differentiated mesenteries may have independently acquired burrowing be- are found in five families: Condylanthidae (Endo- haviour based on the presence of peculiar anatom- myaria), Isanthidae (Mesomyaria), Acontiophori- ical features (sphincter muscles in the proximal dae, Bathyphelliidae, and Isophelliidae (Acontiar- part of tentacles, strong endodermal circular mus- ia). In both groups, microcnemes can appear both cles of the column, altering character, shape and in the distal and proximal parts. Only Andresia size of the longitudinal mesenterial musculature lacks a differentiation into macro- and microc- along the longitudinal extension (Riemann-Zür- nemes, making this unusual polyp resemble most neck, 1997)) and habitation at great depths. thenarians. Hence, based on a few examples, it can be as- Interestingly, Athenaria and Thenaria are not sumed that burrowing behaviour is not associated always characterised by hexamerously arranged with the presence or absence of basilar muscles, mesenteries. Decamerous and octomerous ar- but rely on the use of retractor muscles and the rangements are also common in both groups. Some parieto-basilar or parietal muscles. The basilar thenarians (e.g. Zaolutus actius Hand, 1955) are muscles are involved in attachment/detachment characterised by a weak development of the fifth and creeping, together with endodermal circular and sixth couples of mesenteries (Hand, 1955), so muscles of the pedal disc, lower parts of the retrac- that a bilateral arrangement of mesenteries fur- tor muscles and the parieto-basilar muscles, as was ther enhances their similarity with Edwardsia and shown in Metridium senile (Linnaeus, 1761) (see certain other athenarians. Batham & Pantin, 1951). Another feature that binds the two groups is a Accordingly, burrowing in athenarian sea marginal sphincter muscle, which constricts the anemones should be associated mainly with the distal part of the column. Within each infraorder, parietal and retractor muscles, with a rounded ab- the sphincter may be endodermal, mesogloeal or oral end, and with an elongated body form. These completely absent. Moreover, some representa- features, in turn, are correlated with fewer tenta- tives develop a double mesogloeal sphincter (e.g. cles and mesenteries, the latter divided into mac- Halcampidae and Isanthidae) (see Carlgren, 1949; ro- and microcnemes. Hand, 1955). The presence of the above-mentioned similar One more overlapping feature is the presence features in the athenarians potentially confirms of specialised stinging organs, the acontia. Among their common origin. The presence of several Athenaria, acontia develop in representatives characters that define, rather, individual fami- of three families (Haliactinidae, Octineonidae, lies or genera than the infraorder as a whole can Andvakiidae). Among Thenaria, they occur in 14

( Zoosystematica Rossica, Vol. 29, No. 2, pp. 213–237 233 N.Yu. Ivanova. Classification and evolution of the burrowing sea anemones families, which are combined into the superfamily the mesentery muscles, the separation of mesen- Metridioidea. teries into micro- and macrocnemes, peculiarities Even though small size and a worm-like body of behaviour, in particular how they burrow, and are typical for Athenaria, that group does contain other characters. Considering a larger set of fea- forms that are very similar to the thenarians. Oc- tures allowed me to conclude that the burrowing tineon (Octineonidae) is the most remarkable ex- sea anemones are characterised by a common ori- ample of this likeness: it has a wide, sticky, flat ped- gin and further divergence into the families with- al disc with which it attaches to a solid substrate in the infraorder Athenaria. In this interpretation, (Sanamyan et al., 2018). Vice versa, the thenarian the similarities with certain representatives of anemones of various families can also be buried Thenaria can be explained by convergence. in the sediment and be elongated, in some cases forming a rounded aboral end. As a rule, however, Acknowledgements they still need to attach the base to a hard object. In Athenaria, the development of a clearly defined I am grateful to Dr Elena E. Kostina (Vladivostok) and Dr Ekaterina S. Bocharova (Moscow) for valuable attachment disc is probably an exception. None- comments to the early draft of the manuscript and to theless, it cannot be denied that the athenarians Dr M. Stachowitsch (University of Vienna) for cor- can attach their aboral end to solid objects (see recting the English language. The study was funded Williams, 2003). by the Russian Foundation for Basic Research, project Considering the totality of characters, the athe- No. 19-34-90083. narians are most similar to representatives of the families Condylanthidae (Endomyaria), Isanthi- References dae (Mesomyaria), Acontiophoridae, Bathyphellii- dae, and Isophelliidae (Acontiaria). The athenari- Andres A. 1881. Intorno all’Edwardsia claparedii an sea anemones potentially come from a common (Halcampa claparedii Panceri). Atti dell’ Accade- mia de Lincei, 5: 221–236. ancestor with polyps of these five families. Andres A. 1883. Le Attinie (Monografia). Roma: Coi Tipi der Salviucci. 460 p. Conclusions Ansell A.D. & Peck L.S. 2000. Burrowing in the Antarctic anemone, Halcampoides sp., from Signy An analysis of the systems of athenarian sea Island, Antarctica. Journal of Experimental Marine anemones proposed by various authors reveals Biology and Ecology, 252(2000): 45–55. https:// that each classification scheme was based on only doi.org/10.1016/s0022-0981(00)00232-x one feature, i.e. on the external organization, the Ansell A.D. & Trueman E.R. 1968. The mechanism of arrangement of the mesenteries, the presence of burrowing in the anemone, Peachia hastata Gosse. the basilar muscles, or on a comparison of a few Journal of Experimental Marine Biology and Eco­ molecular markers. Clearly, focusing on only one logy, 2: 124–134. https://doi.org/10.1016/0022- 0981(68)90003-8 specific feature yields heterogeneous groups: in Batham E.J. & Pantin C.F.A. 1951. The organization every case it separates similar and joins unrelated of the muscular system of Metridium senile. Quar- forms. A detailed analysis of the recently proposed terly Journal Microscopical Science, 92(1): 27–54. classification (Rodríguez et al. 2014), which many Beneden E. van. 1897. Les Anthozoaires de la authors consider to be a replacement for the tradi- “Plankton–Expedition” (Die Anthozoen der tional system, confirms this conclusion. I consider Plankton–Expedition). Ergebnisse der Plankton– that an integrated approach is currently need- Expedition der Humboldt–Stiftung, 2: 1–222. ed to develop a natural classification that would Bourne G.C. 1900. VI. – The Anthozoa. In: Lanke- include both morpho-anatomical features and ster E.R. (Ed.). A Treatise on Zoology. Part II. The Porifera and Coelenterata: 1–84. London. https:// molecular markers, supported by data on behav- doi.org/10.5962/bhl.title.1018 iour, embryology, etc. Solving the problem of the Bourne G.C. 1916. A description of five new species of origin of Athenaria calls for taking into account Edwardsia, Quatr., from New Guinea, with an ac- not only their elongated shape and rounded body count of the order of succession of the micromesen- end, the absence of the basilar muscles, but also teries and tentacles in the Edwardsidae. Zoological

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Received 8 April 2020 / Accepted 20 August 2020. Editorial responsibility: T.N. Dautova, A.V. Frolov

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