Actiniaria – Sea Anemones - Marine Benthic Fauna of Chilean

Actiniaria – Sea Anemones
Vreni Häussermann & Günter Försterra
215
Actiniaria – Sea Anemones
Phylum Cnidaria
Vreni Häussermann & Günter Försterra
General Introduction
Class Anthozoa
With approximately 1,200 known species in 46 families
worldwide, sea anemones inhabit all oceans and habitats
from the deep sea to coral reefs, and also estuaries.
Especially in cold and temperate waters they can form an
important part of the macro-zoobenthos. Sea anemones
can range in size from a few mm to 1.25 m diameter. The
largest Chilean species can develop an oral disc diameter
between ten and twenty cm but most species, especially
in the fjords, it varies between one and three cm.
External Morphology (Fig. 1)
Sea anemones are benthic sessile polyps without a
skeleton. They are solitary; with the exception of one
colonial species, Cereus herpetodes, which is known
from Chile. The proximal end of a sea anemone is
either rounded, in which case the species is buried in
soft substrate, or forms a more or less well-developed
flat pedal disc, which it uses to attach to hard substrate.
The column is smooth or provided with different
Order Actinaria
Subclass Hexacorallia
Fig. 1
Fig. 1. Schematic drawing of a sea anemone that represents a mesomyarian anemone on the left and an endomyarian anemone on the right (drawing Roman Babuscak, from Häussermann, 2003).
216
structures such as verrucae (see e.g. Parantheopsis
ocellata), tenaculi (see e.g. Phellia exlex), tubercles
(see e.g. Hormathia pectinata), vesicles (see e.g.
Phymactis papillosa), marginal spherules (=acrorhagi,
see e.g. Phymactis papillosa), marginal pseudospherules
(=pseudoacrorhagi, see e.g. Bunodactis spp.), or marginal
projections (see e.g. Isotealia antarctica). It can be subdivided into different regions (scapus and scapulus or
capitulum, e.g. Hormathia pectinata and Metridium
senile lobatum, respectively); and may possess a cuticle
(e.g. Phellia exlex, Hormathia pectinata). The margin
can be separated from the tentacles by a more or less
developed fosse, or be tentaculate (without fosse).
The oral disc (at the distal end) is usually
circular; in some species it can be drawn
out into lobes (e.g. Antholoba achates).
The tentacles are generally simple, hollow,
and usually arranged in hexamerously
alternating cycles. They arise from the
margin and/or the oral disc, and nearly
never possess spherical tips (acrospheres).
Some species possess special fighting
tentacles that can be everted or retracted,
they bear large amounts of special cnidae
used for defence. Colour and markings of
the animals are highly variable.
Fig. 2-7. Histological slides of longitudinal and transverse
sections of Chilean sea anemones.
Fig. 2. Longitudinal section of Anemonia alicemartinae (Family Actiniidae); note endodermal diffuse sphincter (sp) and
basilar muscles (bm); taken from Häussermann & Försterra
(2001). Legend: ac acrorhagus; co column; me mesenteries;
od oral disc; pd pedal disc; t tentacles.
Fig. 3. Longitudinal section of upper part of column of Phymactis
papillosa (Family Actiniidae); from Häussermann (2004). Legend:
ac acrorhagus; ch channel; lm longitudinal muscle of column; m
mesogloea; v vesicle; sp sphincter (endodermal, diffuse)
Fig. 4. Endodermal, circumscribed sphincter (sp) of Isotealia
antarctica (Family Actiniidae).
Fig. 2
Fig. 3
Fig. 4
217
Key to the higher taxa included in this chapter (adapted after Carlgren, 1949)
Taxa with species from the Chilean Fjord Region in bold
Key to the suborders
Phylum Cnidaria
1) a) Ciliated tract of filaments absent.................................................. Protantheae (1 family; only 1 species in Chile)
b) Ciliated tracts of filaments present or absent. Medially fused mesenteries at proximal end of body.....................
................................................................................................................................... Ptychodacteae (2 families)
c) Ciliated tracts of filaments present. With or without basilar muscles...................................................................2
2) a) Mesenteries, after development of first 12 appearing in lateral endocoels, with their longitudinal muscles oriented
as in directives. No basilar muscles........................................................................ Endocoelantheae (2 families)
b) Mesenteries, after development of first 12 appearing in exocoels, as pairs whose longitudinal muscles face one
another.......................................................................................................................Nynantheae (3 infraorders)
Suborder Ptychodacteae
Class Anthozoa
1) a) Column short, smooth without outgrowth. Numerous tentacles simple and not retractile. 1 weak retractor
muscles per mesentery................................................................................................................Ptychodactiidae
b) Column elongate with vesicular outgrowth histologically identical to tentacles. Tentacles absent or only at
margin of disc. 2 weak retractor muscles per mesentery............................. Preactiidae (only 1 species in Chile)
Suborder Endocoelantheae
Subclass Hexacorallia
1) a) Mesenteries divisible into macro- and micronemes; 6 or 19 pairs of macrocnemes. Retractors of macrocnemes
restricted. 1 siphonoglyph..........................................................................Halcuriidae (only 1 species in Chile)
b) Mesenteries not divisible into macro- and microcnemes. Retractors of mesenteries weak; diffuse. 2
siphonoglyphs...................................................................................................................................Actinernidae
Suborder Nynantheae
Order Actinaria
1) a) Basilar muscles absent.......................................................................................................................................2
b) Basilar muscles present............................................................................................... Thenaria (3 superfamilies)
2) a) Aboral end of body rounded; rarely flattened or disc-like. Column rarely with ectodermal muscles and then
only in uppermost part. Muscles of mesenteries strong. Retractors usually strongly restricted to circumscribed;
parietobasilar muscles usually form well differentiated parietal muscle together with columnar part of
longitudinal mesenterial muscles...................................................................................... Athenaria (10 families)
b) Aboral end of body always disc-like; never rounded. Column with longitudinal muscles. Muscles of mesenteries
weak.......................................................................................................................... Boloceroidaria (2 families)
Infraorder Thenaria
1) a) Families without acontia. Sphincter endodermal or absent; exceptionally meso-endodermal to endo-mesogloeal. Endomyaria
b) Families with mesogloeal sphincter, but without acontia................................................................. Mesomyaria
c) Families with acontia or acontoid organs. Sphincter commonly mesogloeal; sometimes absent........ Acontiaria
Superfamily Acontiaria (13 families)
1) a) Sphincter mesogloeal; strong. Acontia with basitrichs only ........................................................ Hormathiidae
b) Sphincter mesogloeal; usually strong; Acontia with basitrichs and p-amastigophores........................................
...........................................................................................Sagartiidae and Metridiidae (only 1 species in Chile)6
Family Sagartiidae (14 genera)
1) a) Column with somewhat modified but adhesive verrucae ........................................................................Cereus
b) Column smooth. ≥1st cycle of mesenteries sterile . .............................................................................Anthothoe
c) Column with tenaculi with strong cuticle; forming stout papillae. Mesenteries (and directives) irregularly
arranged. Retractors of older mesenteries very strong; restricted ............................................................ Phellia
226
Superfamily Mesomyaria (4 families)
1) a) Mesenteries divisible into macro- and microcnemes....................................Isanthidae (only 1 species in Chile)7
b) Mesenteries not divisible into macro- and microcnemes. Arrangement of tentacles regular; in cycles. Younger
mesenteries not bilaterally arranged .............................................................................................Actinostolidae
Family Actinostolidae (23 genera)
1) a) Mesenteries distinctly arranged according to the Actinostola rule. Longitudinal muscles of tentacles and radial
muscles of oral disc mesogloeal. Oral disc not lobed.........................................................................Actinostola
b) Mesenteries not arranged according to Actinostola rule. Longitudinal muscles of tentacles and radial muscles of
oral disc ectodermal or mesogloeal . .................................................................................................................2
2) a) All or all stronger mesenteries fertile. Tentacles without nematocyst batteries or b-mastigophores. ≥12 pairs of
mesenteries perfect. Retractors strong; diffuse. Tentacles rather numerous. Body elongate..................Paranthus
b) The 3 oldest cycles of mesenteries sterile. Oral disc lobed. Sphincter very long ................................ Antholoba
Superfamily Endomyaria (12 families)
Family Actiniidae (55 genera)
1) a) Acrorhagi present in older specimens; in young specimens sometimes absent or very scarce. Sometimes
holotrichs also in other parts of column.............................................................................................................2
b) Acrorhagi absent. Column smooth (apart from marginal projections)................................................................5
c) Acrorhagi absent. Column with verrucae, vesicles or other protuberances........................................................7
2) a) Column smooth; without vesicles or verrucae. Acrorhagi at margin. Tentacles long; imperfectly retractile.
Sphincter not very strong; diffuse to restricted........................................... Anemonia ( North and Central Chile)
b) Column with non-adhesive vesicles, which are simple, compound or branched (more or less weak nematocyst
batteries).............................................................................................................................................................3
c) Column without vesicles, but with adhesive verrucae. With well developed marginal ruff (verrucae at margin
set on small lobes). Sphincter decidedly diffuse.............................Oulactis (North and Central Chile; 2 species)
3) Vesicles distributed over whole or almost whole column; simple or compound. Sphincter well developed;
distinctly diffuse.................................................................................................................................................4
4) a) Acrorhagi with holotrichs and very numerous and long basitrichs.......................................................Phymactis
b) Acrorhagi with holotrichs only.................................................................Phymanthea (North and Central Chile)
5) a) Tentacles with endodermal sphincter at their bases; long; numerous; occupying only outer half of oral disc.
Sphincter diffuse.................................................................................................................................. Bolocera8
b) Tentacles without endodermal sphincters at their base......................................................................................6
6) a) With ring of perforated marginal projections. Body not elongate. Mesenteries of 2 first cycles sterile. Sphincter
circumscribed........................................................................................................................................ Isotealia
b) Without ring of perforated marginal projections. All or all stronger mesenteries fertile. Tentacles very long;
longitudinally ridged with very long basitrichs. Sphincter endodermal; diffuse ............................. Boloceropsis8
7)
Column with verrucae.......................................................................................................................................8
8) a) Body elongate, cylindrical. No distinct sphincter. Most mesenteries perfect. Tentacles short. Verrucae well
developed..................................................................................................................................... Parantheopsis
b) Body as a rule not elongated. All stronger mesenteries, with or without directives, fertile. Outer tentacles shorter
than inner ones. Sphincter more or less curcumscribed to restricted; rarely weak. Verrucae well developed;
sometimes compound in distal part. Marginal pseudoacrorhagi........................................................Bunodactis
6 Metridiidae are described with b-mastigophores and p-amastigophores in the acontia; but examination of the cnidae showed the
presence of basitrichs and p-amastigophores.
7 Another species collected from the fjord region.
8 The cnidome of the examined specimens attributed to the genera Boloceropsis and Bolocera was identical and we found all
transitions from an endodermal sphincters at the tentacle base to no such sphincter. Therefore we cannot separate the species
Boloceropsis platei and Bolocera occidua at the moment.
227
Key to the described anemone species
White threads (acontia) are expelled
Tentacles can be thrown off
0
0
0
1
0(1)
1
0
0
0
0
0
0
0
1
1
1
0
Anthopleura
0
1
0
0
0
0
0
1
0
1
0
0
Bunodactis hermaphroditica
0
1
0
0
0
0
0
0
0
1
0
0
Bunodactis octoradiata
0
1
0
0
0
0
0
1
0
1
0
0
Parantheopsis ocellata
0
1
0
0
0
0
0
0/1
0
1
0
0
Phellia exlex
0
0
0
1
0
0
0
0
0
1
1
0
Hormathia pectinata
0
0
0
1
0
0
0
1
0
1
1
0
Anthothoe chilensis
0
0
1
0
0
0
1
0
0
1
1
0
Acontiaria sp. 2 (brown)
0
0
1
0
0
1
0
0
0
1
1
0
Acontiaria sp. 1 (yellow)
0
0
1
0
0
1
1
0
0
1
1
0
Metridium senile lobatum
0
0
1
0
0
1
0
0
1
1
1
0
Bolocera/Boloceropsis sp.
0
0
1
0
0
0
0
0
0
0
0
1
Actinostola chilensis
0
0
1
0
0
0
0
0
0
1
0
0
Antholoba achates
0
0
1
0
0
0
0
0
1
1
0
0
Paranthus niveus
0
0
1
0
0
0
0
0
0
1
0
0
Paraisanthus fabiani
0
0
1
0
0
0
0
0
0
1
0
0
Halcurias pilatus
0
1
0/1
0
0
0/1
0
0
0
1
0
0
Isotealia antarctica
0
0
1
0
0
0
0
1
0
1
0
0
Gonactinia prolifera
0
0
1
0
0
0
0
0
0
0
0
0
Dactylanthus antarcticus
0
0
0
0
1
0
0
0
0
0
0
0
Phymanthea pluvia
1
0
0
0
0
0
0
1
0(1)
1
0
0
Oulactis concinnata2
0
1
0
0
0
0
0
1 (0)
1(0)
0
0
0
Oulactis coliumensis3
0
1
0
0
0
0
0
1
0
1
0
0
Anemonia alicemartinae4
0
0
1
0
0
0
0
1
0
0 (1)
0
0
Adult with lobed oral disc
0
0
Blistered structures on margin, sometimes
hidden in small depression
0
1
Entire column with irregularly distributed
lobes
0
0
Column with rough, not slimy surface layer,
often covered with detritus, uppermost
column distinct, perfectly clean
1
Cereus herpetodes
Species
Column +-smooth and +- clean
Phymactis papillosa
Column with clear longitudinal rows of
distinctly coloured, often adhesive spots
Tentacles can be completely covered
Reaction to
annoyance
White or yellow longitudinal stripes
Margin
Uppermost part of column distinct, delicate
Column
Entire column completely covered with
blister-like smooth structures
Class Anthozoa
Phylum Cnidaria
Character
Order Actinaria
Subclass Hexacorallia
hermaphroditica
1
1
228
1-4
Common shallow-water species of North and Central Chile, see Häussermann & Försterra (2001) and Häussermann (2003; 2004b).1: 18°
Legend: 0 absent, 1 present, 0(1) generally absent, 1(0) generally present, 0/1 and 1/0 absent or present, num numerous. In columns size and tent
In situ habitus
Brooding species
Fighting tentacles may be present
Present in Peruvian Province (PP)
0
0
0/1
0
0
0
2–3
1
num.
0
1
0/1
0
0
1
0
0
0
2–3
1
num.
1
1
0
0
0/1
0
0/1
0
0
0
1
1
2
96
0
1
0
0
0
0
1
0
0
0
1
1
2
<48
0
1
0
0
0
0
1
0
0
0
0
1 (2)
2
32–48
0
0
0
1
0
1
1
0
0
0
0
1–2
1
96
0
1
0
0
0/1
0
1
0
0
0
0
2
2
≤~100
0
0
0
0
1
0
0/1
0
0
0
0
3
(2)3
96
0
0(1?)
0
0
1
0
0/1
1
0
0
0
2
3
<100
0
1
0
0
0/1
0
0
0
0
1
0
1
2(3)
<100
1
0
0
0
1
0
0/1
0
0
1
0
1
3
<100
0
0
0
0
1
0
0/1
0
0
1
0
1–2
1
num.
1?
0
0
0
1
0
0
0
0
0
0
3
3
<~100
0
0
0
0
1
0
0 (1)
0
0
0
0
3
2
num.
0
0(1?)
0
1
1
0
0
0
0
0
0
3
1
num.
0
1
0
1
0
0/1
1
0
0
0
0
2
3
96
0
1
0
1
0/1
0
0 (1)
0
0
0
0
1
2
<~110
0
0
0
0
0/1
0
1
0
0
0
0
1
2–3
<96
0
0
0
0
1
0
0
0
0
0
0
3
2–3
96
0
0
0
0
1
0
1
0
1
0
0
1
3
<20
0
1
0
0
1
0
1
0
0
0
0
2
1
<20
0
0
0
0
1
0
0
0
0
0
0
3
1
num.
0
1
0
0
0
1
0
0
0
0
0
3
1
num.
1
1
Tentacle number
Pedal laceration
1
0
Length of longest tentacles
Transverse fission
0
Size (OD without tentacles)
In habitat elongate
0
(0)1
Longitudinal fission
Lower colum hidden in sand
Other
features
Entire body visible in situ
General morphology
6 or 12 tentacles closer to mouth
Mode of asexual
reproduction
Several mouth openings on oral disc
Oral disc
0
0
0
1
0/1
0
0
0
0
2
2
96
0
1
0
0
1
0
0
1
0
0
0
2
2
<100
0
1
8°S–33°S; 2:18°S–40°S; 3: 37°S; 4: 18°S–37°S.
tacle number: 1 small/short, 2 medium, 3 large/long.
229
Halcurias pilatus
233
Halcurias pilatus McMurrich, 1893
Subclass Hexacorallia
Class Anthozoa
Phylum Cnidaria
Common name: Orange decameric anemone;
Anémona decamera naranja
Description: External morphology: PD to ~1.5 cm Ø;
OD Ø to ~1.3 cm. Colour generally orange; more rarely
white; base of tentacles white; preserved specimens
whitish. Elongated anemone. Column smooth to slightly
corrugated; covered with white spots (cnida batteries, see
Fig.) in longitudinal lines; in some individuals uppermost
part seems more delicate. Up to 96 long tentacles; outer
considerably shorter than inner; can be fully covered
by column. Contracted shape round to oblong. Internal
morphology: Actinopharynx short; with 1 siphonoglyph.
2 pairs of directives. 10 pairs of mesenteries; all perfect.
Oral stoma. Histology: Sphincter mesogloeal; weak.
Retractors diffuse; restricted to inner half of mesenteries.
All mesenteries fertile. Cnidae: Spirocysts; basitrichs;
p-amastigophores; holotrichs. Possibility for confusion:
In vivo: Other orange, pink, or white anemones.
However, H. pilatus has a long column with white spots
and no acontia. Preserved: Other elongated anemones
(e.g. Paranthus niveus), but the decamerous mesenterial
arrangement and the holotrich batteries (30–45 µm) on
the column (see Fig.) distinguish H. pilatus from all other
anemones from this region.
Habitat: Rocky substratum. Column regularly hidden
in crevices or holes, dead barnacle and coral skeletons.
Depth: 5–821 m. Abundance: In channels locally very
abundant; more rarely in fjords. Generally aggregated.
Distribution: SE Pacific (NPZ–CPZ). Chile: 42°S–50°S.
Biology: Globular reproductive products observed
in the tentacles. Sexes separate, no signs of asexual
reproduction.
Main reference: McMurrich (1893).
Hormathia pectinata (Hertwig, 1882)
Order Actinaria
Common name: Tubercular anemone;
Anémona de tubérculos
Synonymy: Phellia spinifera Hertwig, 1888 (at least pro
parte).
Description: External morphology: To 5 cm high; PD Ø
to ~4 cm. Colour white to light peach-coloured or light
orange; actinopharynx brown to brown-red; preserved
specimens whitish to grey. Column tough; divided into
scapus and scapulus. Scapus with brown cuticle that can
be at least partially lost. Scapulus with tubercles with
small brown, chitinuous cuticle “hats”; with longitudinal
ridges ending in 12 larger coronal tubercles. 96 tentacles;
long; thin; can be fully covered by column. Mesenterial
insertions visible on OD. Mouth opening prominent; lips
thick. No cinclides on column. Internal morphology:
Actinopharynx deeply furrowed. 2 siphonoglyphs. 2
pairs of directives. Oral stoma. Mesogloea thick. Acontia
present. Histology: 48 pairs of mesenteries: 1st cycle perfect
and sterile; 2nd and 3rd cycle fertile. Parietobasilar muscles
strong. Sphincter mesogloeal; strong. Cnidae: Spirocysts;
basitrichs; p-mastigophores (Fig. 8I Introduction);
p-amastigophores. Acontia with basitrichs only (25–
234
29 µm; 54–64 µm; see Fig.). Possibility for confusion:
On first sight other larger Chilean anemones, but due to
the presence of acontia and a cuticle this species is easily
recognizable. Phellia exlex also has acontia and a cuticle
but is smaller, much darker, appears in groups and has
additional p-mastigophores in the acontia.
Habitat: Steep to overhanging rocky walls. Depth: 12–
1,220 m. Abundance: Infrequent in shallow water; most
individuals below 30 m; never in groups. Distribution:
SW Atlantic (Argentina); SE Pacific (NPZ–CPZ); Strait
of Magellan. Chile: 32°S–33°S?; 42°S–53°S. Biology:
Specimens retract very fast due to light or vibration
stimuli. Comments: Typical deep-water emerging species.
Chilean shallow water specimens are considered dwarf
form. This form includes 2 morphs; some individuals
have a very firm PD, while in others it is delicate.
Morphological characters of hormathiids vary strongly,
even within species, and thus species are often difficult
to tell apart. Argentinean specimens often epibiotic.
Possibly also off Central Chile (32°S–33°S, 350–400 m).
Main references: Hertwig (1882); McMurrich (1893);
Riemann-Zürneck (1973).
Hormathia pectinata
235
Phylum Cnidaria
Glossary
Acontium (pl.
Thin threads attached at one end to mesenteries, as a rule below the filaments, while the other
acontia)
end is free. They are laden with extraordinarily numerous nematocysts of variable categories.
Acrorhagus (pl.
Endocoelic structure outside the tentacle crown and adoral to the marginal sphincter
acrorhagi)
(further away from the mouth) in which the epidermis contains holotrichous nematocysts
and epitheliomuscular cells that are vacuolated at their bases (see Fig. 2&3). Called marginal
spherules by Carlgren (1949).
Acrospheres
The globular ends of certain tentacles, laden with numerous nematocysts. They are of
differentcategories in the Corallimorpharia, in the Actiniaria and seemingly in the Madreporaria
Class Anthozoa
also.
Actinopharynx (syn.
Throat, stomodaeum; the tube which leads from the mouth into the coelenteron; formed by
pharynx)
the epidermis.
Basilar muscles
Radial muscles running along both sides of the base of the mesentery, close to the pedal disc.
Present in most of the Actiniaria (see Fig. 2).
Basitrichs
Type of nematocyst. No V-shaped notch at base of unfired shaft; tubule with long proximal and
short distal spines. Rod-like basitrichs are very long and slender.
b-mastigophores
Type of nematocyst. No V-shaped notch at base of unfired shaft; discharged shaft or proximal
tube approximately same diameter as remaining tubule; proximal tubule with prominent
armature.
Capitulum
See Scapus.
Cinclides
Small apertures (or organized soft spots which will rupture readily) in the column through
Subclass Hexacorallia
which acontia can be expelled. Also present in some species without acontia.
Circumscribed
Shape of a muscle. When the muscles are very strongly concentrated and there is only one
mesogloeal lamella (or a few main lamellae close to each other) originating from the main
lamella of the mesentery (see Fig. 4).
Cnidae (see Fig. 8)
Spirocysts (only Anthozoa), nematocysts (all Cnidaria), and ptychocysts (only Ceriantharia).
Cnidom
List of types of cnidae of a species.
Column
Body-wall. Its musculature is usually entirely endodermal, at least in origin. The fibres of the
muscle-sheets on the endodermal face of the mesogloea are placed horizontally, and constitute
the endodermal circular muscle of the column. The column can possess a variety of structures
such as verrucae, vesicles, tubercles and tenaculi.
Diffuse
Shape of a muscle. Muscle with relatively short processes which are based upon a considerable
Order Actinaria
area of the mesoglea (see Fig. 3).
Directives
Pair of mesenteries situated in the directive axis; with their longitudinal muscles (retractors) on
(syn. directive
their outer sides turned towards the exocoels (see Fig. 6B).
mesenteries)
Distal
The upper end of a sea anemone where the oral disc is situated.
Ectoderm (syn.
External body layer; composed of cells (see Fig. 6C).
epidermis)
Endocoel
The space between 2 mesenteries belonging to one and the same pair.
Endoderm (syn.
Internal body layer; lining the body cavity and tentacles; composed of cells (see Fig. 6C).
gastrodermis)
Exocoel
The space between mesenteries belonging to different pairs.
Fighting tentacle
Specialized tentacle with different cnidome compared to regular tentacles; often longer and
(syn. catch tentacle)
in some cases with different colouration; it is inducible and involved in agonistic behaviour
(competition and defense).
262