Classification and evolution of the burrowing sea anemones (Anthozoa: Actiniaria: Athenaria): a review of the past and current views

2020·4.2 MB·

by  N. Yu. Ivanova

ZOOSYSTEMATICA ROSSICA
I S S N Zoological Institute, Russian Academy of Sciences, St Petersburg ▪ https://www.zin.ru/journals/zsr/
2410-0226
[online] Vol. 29(2): 213–237 ▪ Published online 20 October 2020 ▪ DOI 10.31610/zsr/2020.29.2.213
0320-9180
[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).
214 ( Zoosystematica Rossica, Vol. 29, No. 2, pp. 213–237
N.Yu. Ivanova. Classification and evolution of the burrowing sea anemones
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-
Haime (1854) was the first to point out the impor-
fication of sea anemones. They separated the bur-
tance of anatomical features, but only Hertwig &
rowing forms from the remaining representatives
Hertwig (1879) began to use them in constructing
based on their elongated body shape and absence
their classification. Having traced the formation
of a pedal disc (Fig. 1a, b). Milne-Edwards &
of mesenteries in the sea anemones, the zoanthids,
Haime (1857) placed these anemones inside of the
and the octocorals, Hertwig & Hertwig (1879)
subfamily Actininae in section “Actinines pivo-
considered that the arrangement of mesenteries
tantes”, defining them as “species whose base is
and the development of their muscles (but not
very small and body is very elongated” (Fig. 2). In
their number as Ehrenberg (1834) and Haeckel
constructing his system, Gosse (1860) also relied
(1866) believed) should be regarded as the most
on the presence or absence of a sticky pedal disc.
important taxonomic characters.
Accordingly, he isolated the worm-like anemones
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.
( Zoosystematica Rossica, Vol. 29, No. 2, pp. 213–237 215
N.Yu. Ivanova. Classification and evolution of the burrowing sea anemones
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.
216 ( Zoosystematica Rossica, Vol. 29, No. 2, pp. 213–237
N.Yu. Ivanova. Classification and evolution of the burrowing sea anemones
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
me senteries, 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-
Fig 11. The position of burrowing sea anemones (in
tiniaria into six tribes: Hexactiniae, Paractiniae,
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 anti meres sea anemones from the North Atlantic and estab-
did not increase in multiples of six. Based on the lished a new family of Andvakiidae Da nielssen,
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 Da nielssen,
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-
( Zoosystematica Rossica, Vol. 29, No. 2, pp. 213–237 219
N.Yu. Ivanova. Classification and evolution of the burrowing sea anemones
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- fami ly 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-
mesen teries 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
( Zoosystematica Rossica, Vol. 29, No. 2, pp. 213–237 221
N.Yu. Ivanova. Classification and evolution of the burrowing sea anemones
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 pre sence 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).
222 ( Zoosystematica Rossica, Vol. 29, No. 2, pp. 213–237