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Association between Dentitheca habereri (Cnidaria: Hydrozoa) and twozoanthidsC. G. Di Camillo a; M. Bo a; S. Puce a; G. Bavestrello a
a DiSMar, Università Politecnica delle Marche, Ancona, Italy
First published on: 18 January 2010
To cite this Article Di Camillo, C. G., Bo, M., Puce, S. and Bavestrello, G.(2010) 'Association between Dentitheca habereri(Cnidaria: Hydrozoa) and two zoanthids', Italian Journal of Zoology, 77: 1, 81 — 91, First published on: 18 January 2010(iFirst)To link to this Article: DOI: 10.1080/11250000902740962URL: http://dx.doi.org/10.1080/11250000902740962
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Association between Dentitheca habereri (Cnidaria: Hydrozoa) and twozoanthids
C. G. DI CAMILLO*, M. BO, S. PUCE, & G. BAVESTRELLO
DiSMar, Universita Politecnica delle Marche, Ancona, Italy
(Received 19 June 2008; accepted 9 January 2009)
AbstractDentitheca habereri is a leptomedusan hydroid forming large colonies on the fringing reefs of the Bunaken National Park(North Sulawesi, Indonesia). The hydroid is generally associated with two zoanthid species, Parazoanthus gracilis andParazoanthus sp. Colonies lacking zoanthid epibionts are rare and generally smaller (8–10 cm). When associated withParazoanthus sp., the hydroid colonies are fan-shaped and may exceed 1 m in width. In contrast, when D. habereri iscolonised by the large polyps of Parazoanthus gracilis, the host colonies are smaller and the branching is irregular.
Keywords: Dentitheca habereri, zoanthids, epibiosis, distribution
Introduction
Hydroids often live as epibionts on other organisms
or, conversely, act as a substrate for both vagile and
sessile species (Bavestrello et al. 1996; Zintzen et al.
2008). These associations often lead to very close
relationships ranging from mutualism to parasitism
(Boero & Bouillon 2005; Puce et al. 2008).
Although large hydroid colonies are often a suitable
substrate for smaller hydroids, they rarely host other
cnidarians, particularly anthozoans. In the Adriatic
Sea, the octocoral Cornularia cornucopiae and occa-
sionally small anemones can surround the base of
the stalk of Eudendrium colonies, but no exclusive
relationship with the host appears to be established
(Di Camillo, unpublished).
Zoanthids are common epibionts of different
organisms (Acosta et al. 2005; Sinniger et al.
2005) including gorgonians and black corals (West
1979), but relationships with hydroids are poorly
documented (Table I). Parazoanthus gracilis lives on
the thecate hydroid Dentitheca habereri, Parazoanthus
tunicans is associated with Plumularia sp.,
Parazoanthus dichroicus grows on Plumularia ramsay,
Parazoanthus douglasi on an unidentified hydroid,
and a Parazoanthus or Epizoanthus species is
associated with the aglaopheniid Macrorhynchia
philippina (Haddon & Shackleton 1891; Duerden
1900; Stechow 1909, 1913; Tischbierek 1929; Van
Gemerden-Hoogeveen 1965; West 1979; Inaba
1982; Muirhead & Ryland 1984; Ryland &
Muirhead 1993; Hirohito 1995; Burnett et al. 1997;
Sinniger et al. 2005). Moreover, Calder (personal
communication) observed that Dentitheca habereri
from the Indo-Pacific Ocean and D. dendritica from
the Caribbean Sea are covered by undetermined
zoanthids (Table I). Finally, Billard (1913, Planche
II, Fig. 23) shows the hydroid Plumularia crater
partially covered by a zoanthid, but this association
was not mentioned in the text. These data show that
the only hydroids known as hosting zoanthids belong
to the closely related families Plumulariidae and
Aglaopheniidae, suggesting a certain degree of
specialisation in this relationship.
The first hydroid species recorded associated to a
zoanthid was Dentitheca habereri (Stechow 1909),
but the correct interpretation of this association had
a complex story. Plumularia (5Dentitheca) habereri
was described by Stechow (1909) based on material
collected in the Sagami Bay by Haberer in 1903.
The author misunderstood the association with
the zoanthid, describing numerous, small and
*Correspondence: C. G. Di Camillo, Dipartimento di Scienze del Mare, Universita Politecnica delle Marche, Via Brecce Bianche, I-60131 Ancona, Italy.
Tel: +39 071 2204649. Fax: +39 071 2204650. Email: c.dicamillo@univpm.it
Italian Journal of Zoology, March 2010; 77(1): 81–91
ISSN 1125-0003 print/ISSN 1748-5851 online # 2010 Unione Zoologica Italiana
DOI: 10.1080/11250000902740962
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unbranched hydroid colonies growing on a large
gorgonian. In 1892, Inaba had already described an
unidentified Plumularia from Misaki (Sagami Bay),
depicting this hydroid partially covered by an
epibiont he identified as a sponge. In 1913,
Stechow considered Inaba’s hydroid as belonging
to D. habereri and reinterpreted the type material
of this species as being a large, branched and
Table I. Survey of associations reported in literature (numbers indicate records shown in Figure 4).
Hydroid Zoanthid Localities Author and year No.
Plumularia habereri Parazoanthus gracilis Ebisina, Misaki (Sagami Bay) Carlgren 1934 1
Plumularia habereri Parazoanthus gracilis North Sulawesi (Indonesia) Sinniger et al. 2005 2
Plumularia habereri Parazoanthus gracilis
(Epizoanthus cnidosus)
Ito, Sagami bay (Japan) Tieshbierek 1929 3
?Plumularia habereri Not specified Curacao, Carribean Van Gemerden-Hoogevan 1965 4
Plumularia habereri var.
mediolineata
Not specified Indonesia Billard 1913 – Planche III,
Fig. 31
5
Plumularia habereri Not specified (identified
as a gorgonian)
Between Ito and Hatsushima,
Sagami bay (Japan)
Stechow 1909 and 1913 6
Plumularia habereri Not specified (identified
as a sponge)
Wagamura, Shishigahana,
Misaki (Japan)
Inaba 1892 7
Dentitheca habereri Parazoanthus gracilis Between Ito and Hatsushima,
Sagami bay (Japan)
Stechow 1923b 8
Dentitheca habereri Parazoanthus gracilis Sagami bay (Japan) Hirhoito 1995 9
Dentitheca habereri With undetermined
zoanthids
Off Normanby Island,
Papua New Guinea
Calder, personal communication 10
Dentitheca habereri With undetermined
zoanthids
Kapalai Island, Malaysia Calder, personal communication 11
Dentitheca habereri With undetermined
zoanthids
Tulear, Madagascar Gravier-Bonnet, personal
communication
12
Dentitheca habereri With undetermined
zoanthids
Tulear, Madagascar Pichon 1978 (Thesis) 13
Dentitheca dendritica With undetermined
zoanthids
Long Cay, Lighthouse Reef,
Belize
Calder, personal communication 14
Dentitheca dendritica With undetermined
zoanthids
West Palm Beach, Florida,
USA
Calder, personal communication 15
Plumulariid Parazoanthus gracilis
(Sidisia gracilis)
Misaki, Sagami bay (Japan) Lwowsky 1913 16
Plumularia sp. Parazoanthus tunicans Pedro Bank, Jamaica Duerden 1900 17
Plumularia sp. Parazoanthus tunicans Off La Parguera, Puerto Rico West 1979 18
Not specified Parazoanthus tunicans Utila (Honduras) Sinniger et al. 2005 19
Plumularia ramsay Parazoanthus dichroicus Channel between Mer
and Dauar (Torres Strait)
Haddon & Shackleton 1891 20
Not specified Parazoanthus dichroicus Bowden (Torres Strait) Burnett et al. 1997 21
Not specified Parazoanthus douglasi Albany Pass, Cape York
(Torres Strait)
Haddon & Shackleton 1891 22
Macrorhynchia philippina Parazoanthus or
Epizoanthus sp.
Cleveland Bay
(off Townsville, Australia)
Muirhead & Ryland 1984;
Ryland & Muirhead 1993
23
Plumularia crater ? Indonesia Billard 1913 – Planche II, Fig. 23 24
Plumularia habereri var.
attenuata
? Damar, Indonesia Billard 1913: 42, figs 34–38. 25
Plumularia habereri var.
elongata
? Borneo Billard 1913: 44, fig 35–37. 26
Plumularia habereri var.
subarmata
? North Ubian, Indonesia Billard 1913: 45, fig 38. 27
Plumularia habereri var.
mucronata
? Borneo Billard 1913: 46, fig 60,
pl 2 fig 24.
28
Plumularia ?habereri ? Baia di Cartagena, Colombia Florez Gonzalez 1983 29
Dentitheca habereri ? Guam, Micronesia Kirkendale & Calder 2003 30
Plumularia habereri ? Herald Pass, Great
Astrolabe reef, Fiji
Ryland & Gibbons 1991 31
Plumularia habereri ? Kei Islands - Samalon Island
near Ujungpandang, Sulawesi,
Schuchert 2003 32
Dentitheca habereri ? Europa Island Gravier-Bonnet, personal
communication
33
82 C. G. Di Camillo et al.
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polysiphonic hydroid colony that did not grow on
the sponge, but was instead covered by it. In 1923,
Stechow transferred his species to the genus
Dentitheca, finally recognising that the hydroid was
covered by the zoanthid Parazoanthus gracilis which
had been identified by Ferdinand Pax (Stechow
1923a).
The latter species was described by Lwowsky
(1913) as Sidisia gracilis on material collected by
Doflein in 1904 at Misaki (Sagami Bay) living on an
unidentified plumulariid hydroid. The image (Taf.
19) shows a colony very likely belonging to D.
habereri. Carlgren (1913) re-examined the descrip-
tion and drawings of Sidisia gracilis made by
Lwowsky (1913) and suggested that the zoanthid
was in all probability a Parazoanthus species.
Another specimen originating from the Haberer’s
collection and growing on a colony of D. habereri was
described by Tischbierek (1929) as Epizoanthus
cnidosus. Carlgren (1934) synonymised Epizoanthus
cnidosus with Parazoanthus gracilis and described a
Parazoanthus gracilis specimen from Ebisina (Misaki,
Sagami Bay) that was associated with D. habereri.
Billard (1913) published an illustration (Planche
III, Fig. 31) of a portion of D. habereri from
Indonesia (Pulu-Missa, Makassar, South Sulawesi)
showing small, rounded warts covering the basal
part of a branch. These structures could be
zoanthids growing on the hydroid skeleton,
although they were not mentioned in the text. Van
Gemerden-Hoogeveen (1965) studied three colo-
nies identified as D. habereri from Curacao
(Caribbean) partly covered with zoanthids, remark-
ing that the distal parts of stems, branches and
hydrocladia were free of epibionts.
Dentitheca habereri is a common hydroid on the
coral reefs of the Bunaken Marine Park (North
Sulawesi, Indonesia) where it forms large, branched
colonies generally associated two species of
Parazoanthus. The aim of this work is to describe
the relationship between this hydroid and its
epibionts.
Materials and methods
Samples of Dentitheca habereri were collected from
different sites in the Bunaken National Marine Park
(Figure 1) by SCUBA diving from November 2004
to March 2007. The reefs of the Bunaken archipe-
lago are typical fringing reefs composed of a shallow,
mainly sandy reef flat colonised by few species, the
edge of the reef, characterised by foliaceous and
branched stony corals generally subjected to strong
currents, and vertical walls with canyons and caves
showing the greatest hydroid abundance (Di
Camillo et al. 2008).
Before sampling, the colonies were photographed
and measured. Small specimens were collected
entirely, while portions were cut from large, fan-
shaped colonies. After sampling, living specimens
Figure 1. Map of sampling sites.
Association between Dentitheca habereri and two zoanthids 83
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were examined with a microscope for the identifica-
tion; drawings were made, and pictures and mea-
surements of the hydroid and their epibionts were
taken. Afterwards, the samples were fixed using 4%
neutralised formaldehyde.
For scanning electron microscopy analysis, small
portions of the hydroid were rinsed with distilled
water, then dehydrated in a graded ethanol series
and dried by means of a critical point dryer. Samples
were coated with gold-palladium in a Balzer Union
sputter-coater and examined with a Philips XL20
SEM.
Several pieces of the hydroid hosting zoanthids
were taken off and prepared to obtain resin sections.
First, samples were dehydrated in a graded ethanol
series, than embedded in Technovit 8100 resin.
Sections (10 mm) were mounted on slides and then
stained with toluidine blue; finally slides were
enclosed using Eukitt.
During February 2007, six colonies of D. habereri
associated with two species of zoanthids were tagged
and measured to obtain data on the growth rate of
the associations. Unfortunately, in January 2008
only one colony was still alive. For this specimen,
area, maximum width and maximum height were
determined from underwater photographs using the
ImageJ software and the growth rate was thereby
calculated.
Results
Description of Dentitheca habereri
Family Plumulariidae McCrady, 1859
Genus Dentitheca Stechow, 1919
Dentitheca habereri (Stechow, 1909)
Figures 2, 3. Table II.
Plumularia habereri Stechow 1909: 77, pl 6 fig 4;
Stechow 1913: 10 and 91, figs 59,60; Ryland &
Gibbons 1991: 532: fig. 5; Schuchert 2003: 211,
fig. 60;
?Plumularia habereri van Gemerden-Hoogeeveen
1965: 60, figs 34–36.
?Plumularia habereri Florez Gonzalez 1983: 121,
figs 38,39.
Dentitheca habereri Stechow 1920: 41; Stechow
1923a: 227; Stechow 1923b: 18; Hirohito 1995:
259, fig 87a–c; Kirkendale & Calder 2003: 167 and
179; Pichon 1978: 432.
Plumularia habereri var. attenuata Billard 1913: 42,
figs 34–38.
Plumularia habereri var. elongata Billard 1913: 44,
figs 35–37.
Plumularia habereri var. subarmata Billard 1913: 45,
fig 38.
Plumularia habereri var. mediolineata Billard 1913:
45, fig 39, pl 3 fig 31.
Plumularia habereri var. mucronata Billard 1913: 46,
fig 60, pl 2 fig 24.
Material examined
Bunaken National Marine Park, North Sulawesi,
(Indonesia): Bualo, 20–25 m; Sachiko, 40 m; Siladen,
20–50 m; Mandolin, 25 m; Depan Kampung, 5–
30 m; Likuan, 5–30 m; Mike’s Point, 5–30 m.
Other examined material
Coel. No. 4059, Zoologisch Museum Amsterdam,
Plumularia habereri var. mediolineata, type v/d var.,
Billard – Siboga Expedition, Stat. 80. – Nr. 4781
Sammlung Haberer – Zoologische Staatssammlung
Muenchen (portion of the type material of P.
habereri described by Stechow 1909).
Figure 2. Dentitheca habereri. A, young colony not yet colonised
by epibionts; B, hydrotheca in lateral view; C, hydrotheca in
frontal view; D, particular of the hydrocladial apophysis; E,
gonothecae. Scale bars: A, 1 cm. B–D, 100 mm. E, 200 mm.
84 C. G. Di Camillo et al.
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Description
Large colonies, fan-shaped, reaching 70 cm in height
and 107 cm in width; branched up to the fourth
order; lateral branches arising from apophyses on the
auxiliary tubes. The smallest colonies (5–6 cm in
height) branched up to second order. Hydrocaulus
and main branches rigid, strongly polysiphonic;
perisarc of the tubes very thick; distal portions of
the branches monosiphonic; each tube bearing
nematothecae arranged in rows. Apophyses of
variable length, a mamelon and two nematothecae
visible on the basal part of each apophysis; a
transverse node separates the apophysis from the
branch. The first internode bearing a variable
number of nematothecae depending on its length,
the nematothecae sometimes arranged in couples.
The remaining internodes generally not segmented;
nodes, when present, transverse. Internodes bearing
alternate hydrocladial apophyses associated with two
nematothecae and a mamelon.
Hydrocladia with up to 16 uniseriate hydrothecae;
the internodes showing several internal ribs; nodes
indistinct; each internode with one hydrotheca and
three nematothecae (one median inferior and two
lateral).
Hydrothecae cylindrical, deep, the adcauline wall
completely adnate. Thecal margin almost straight or
slightly sinuous in the adcauline side and lowering
towards the adcauline side. Abcauline wall curved; a
Figure 3. SEM pictures of Dentitheca habereri. A, hydrotheca in lateral view; B, particular of a lateral nematotheca; C, portion of a fertile
colony showing gonothecae; D, particular of a gonotheca. Scale bars: A, D, 200 mm. B, 50 mm. C, 2 mm.
Table II. Measurements of D. habereri (mm).
Portions Dentitheca habereri
Diameter of cauline internodes (small colonies) 13–360
Diameter of cauline internodes (big colonies) up to 6000
Length of hydrocladial internode 450–470
Diameter of hydrocladial internode 60–120
Hydrothecae Diameter of hydrothecal margin 100–120
Length of adnate adcauline wall 190–200
Nematocysts Microbasic mastigophores 8.75–1063.75–5
Microbasic mastigophores 562.5
Lateral Upper chamber 22.5–25
Nematothecae Lower chamber 42.5–45
Median inferior Upper chamber 22.5–25
Nematothecae Lower chamber 42.5–45
Association between Dentitheca habereri and two zoanthids 85
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fold is often present just above the half height. The
internal fold is sometimes absent (see remarks). The
median inferior nematotheca placed on a promi-
nence of the internode, not reaching the theca base;
lateral nematothecae not reaching the thecal margin.
All nematothecae movable and two-chambered: the
upper chamber conical, the walls straight; the inner
wall of the upper chamber emarginate.
Gonothecae arising from the hydrocladial apo-
physes, large, tapered to base, and distally truncated;
the lateral walls curved.
Measurements (mm): see Table II.
Colour: Stems and branches shining brown,
hydrocladia brownish.
Ecology
Colonies of D. habereri were observed along vertical
cliffs from 10 to 50 m depth, but they are more
abundant from 20 to 40 m depth. This species was
mainly found in sites exposed to strong currents.
Remarks
In some specimens, the hydrocladia are shorter,
bearing nine or fewer hydrothecae, and the inter-
nodes generally do not contain internal ribs. The
hydrothecae of these colonies are cylindrical or
campanulate, and the distal hydrothecae are deeper
than the proximal ones. Moreover, these thecae are
slightly smaller (length of adnate adcauline wall 130–
160 mm; diameter of hydrothecal margin 90–
100 mm) and lack an intrathecal fold.
The distributions of Dentitheca habereri and other
hydroids associated with zoanthids are shown in
Figure 4 and Table I. The descriptions of the two
specimens reported from the Caribbean Sea (Van
Gemerden-Hoogeveen 1965; Florez Gonzalez 1983)
do not match with the characters of D. habereri and
their attribution must be considered doubtful.
Unfortunately the comparison of our specimens
with the original material was impossible because
the samples are lost. Therefore it seems likely that D.
Figure 4. Distribution of Dentitheca habereri and records of the associations reported in literature between hydroids and zoanthids. Number
correspondences are shown in Table I.
86 C. G. Di Camillo et al.
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habereri has an Indo-Pacific distribution and the
Caribbean hydroids associated with zoanthids
belong to a different species.
Associated zoanthids (Table III)
The systematics of the zoanthids associated with
hydroids appears very complex. Studies based on
molecular analyses (Sinniger et al. 2005) suggest that
these species probably belong to a separate clade.
Based on morphological criteria, in the Bunaken
Marine Park Dentitheca habereri was found associated
with two different zoanthids: Parazoanthus gracilis and
Parazoanthus sp.
Parazoanthus sp. is characterised by polyps with a
viscid surface; they are small and delicate (Table III),
with a dark red scapus and yellow tentacles
(Figure 5A–C). Foreign bodies are scarce, limited
to the capitular ridges and visible only when the
polyps are closed. This species is clearly different
from P. gracilis in colour and size of the polyps and in
the scarcity of incorporated particles.
Parazoanthus gracilis (Lwowsky, 1913) is charac-
terised by large polyps (Table III) with a long scapus
(Figure 5D–F). The coenenchyme and the polyps
are completely incrusted by calcareous sand grains
and sponge spicules that render the consistency of
the coenenchyme brittle. The tentacles are generally
dark brown, sometimes yellow. The debris coat
makes the polyps grey-coloured, but the inner
coenenchyme is dark brown. The colonies are not
viscid. The comparison with the zoanthid covering
the type material of D. habereri (Stechow, 1909)
identified as P. gracilis (Lwowsky, 1913) by
Ferdinand Pax (Stechow 1923a) revealed that the
polyps of our specimen are larger.
Figure 5. A–C, Underwater pictures of Dentitheca habereri hosting Parazoanthus sp. A, a large, fan-shaped colony; B, detail of A; C,
Parazoanthus sp. covering the hydroid up to the apex and leaving free the hydrocladia; D–F, underwater pictures of Dentitheca habereri
hosting Parazoanthus gracilis. D, colony of a hydroid with epibiontic zoanthids; E, detail of D; F, detail showing Parazoanthus gracilis
covering hydrocladia. G–I, Resin sections of D. habereri associated with zoanthids. G, longitudinal section of specimen covered with
Parazoanthus sp. Note the living coenosarc inside the hydroid skeleton (arrows); H, detail; I, transverse section of D. habereri covered with
Parazoanthus gracilis. White arrow, hydroid coenosarc; z, zoanthid tissue; s, hydroid skeleton.
Association between Dentitheca habereri and two zoanthids 87
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In the Bunaken area, colonies of D. habereri not
associated with zoanthids were small and rare, but
small colonies with few branches were found covered
with zoanthids. In the associations with both
zoanthid species, the hydroid portions covered by
the epibiont are alive as was demonstrated by the
sections showing living coenosarc within the hydroid
skeleton (Figure 5G–I).
The colonies of D. habereri associated with
Parazoanthus sp. were more numerous than those
associated with P. gracilis, representing about 70% of
all colonies. Generally, only one of the two epibionts
was present on the same hydroid colony. However,
we found a large colony of D. habereri that was
widely covered by Parazoanthus sp. but also had a
small portion covered by P. gracilis.
Parazoanthus sp. forms a continuous layer around
the hydrocaulus and the polysiphonic branches of
the hydroid colonies. In thinner portions, the
epibiont covers the main axis and grows up to
the distal apex of the branches, always leaving the
hydrocladia free (Figure 6A–C). The polyps of
the zoanthid are arranged alternately above and
below the axis. The hydroid branches protrude from
the covered areas and show living polyps. Such
covered hydroid colonies are fan-shaped, with
branches arranged almost in one plane, and reach
69 cm in height and 107 cm in width.
Dentitheca habereri forms smaller colonies when
hosting P. gracilis than when covered by
Parazoanthus sp., reaching only 31 cm in height
and 36 cm in width. Such colonies are not
fan-shaped because the branching is irregularly
three-dimensional. During their growth, the colonies
of P. gracilis cover both branches and hydrocladia,
but leave the terminal, ramified hydroid portions
free (Figure 6D,E).
The only one of the D. habereri colonies tagged in
March 2007 and still alive in January 2008 was
associated with Parazoanthus sp. Comparison of the
photographs from the two times indicates a growth
of 2.44 cm in height and 0.74 in width, with an
increase of the total surface of 63.53 cm2.
Discussion
Dentitheca habereri from Bunaken Marine Park is
almost always associated with a zoanthid: only a few
small hydroid colonies, 8–10 cm high, were recorded
free from epibiont. However, colonies less than 8 cm
high can also be covered by zoanthids: therefore,
larvae of the epibiont zoanthids settle on young
colonies of D. habereri. The zoanthids were never
observed on other substrata, suggesting that, at least
for the latter partner, the association is compulsory.
Owing to the exploitation of the hydroid skeleton
for mechanical support, the zoanthids effectively
transform themselves into erect branching organ-
isms, whilst avoiding the energetic cost of producing
their own skeleton. The advantage of this strategy for
a passive filter feeder is that, by rising well above the
substratum into faster flowing water, a larger volume
will be filtered. It remains unclear if the hydroid
benefits from this association, but it is possible that
the very large cnidae of the zoanthid provide extra
protection against predators.
Table III. Comparison of the zoanthids considered in the paper.
Parazoanthus gracilis
(present work)
Parazoanthus sp.
(present work)
E. cnidosus
Tishbierek 1929
(original description)
S. gracilis Lwowsky
1913 (original
description)
P. gracilis as
described by
Carlgren (1934)
Colour of scapus Grey Dark red – – yellowish
Colour of tentacles Generally dark brown Yellow – – –
Height of polyps (mm) 2–5 0.5–1 1.25 4.05 4.05
Diameter of polyps (mm) 1.6–3 1.6–3 1–2.8 1.8–3 3.05
Number of capitular ridges 16 12 – 18–21 16–19
Number of tentacles 32 22–24 – – 34–38
Number of mesenteries 32 ? 32 36–42 34–38
Larger nematocysts (mm) 40–47.5617.5–22.5 35–42.5615–17.5 42–52614–16 35–38615–16 44–48619–22
Colony consistence Brittle Viscid ? ? ?
Incorporated particles Coenenchyme and
capitular ridges
Scarce, limited to
the capitular ridges
Coenenchyme and
capitular ridges
Coenenchyme and
capitular ridges
Coenenchyme and
capitular ridges
Exceptions One specimen with
yellow tentacles
One specimen with
more inclusion
scattered on the
column
– – –
Locality North Sulawesi North Sulawesi Ito (Sagami Bay),
collector: Haberer
Misaki (Sagami Bay),
collector: Doflein
Ebisina, Misaki
(Sagami Bay),
collector: Gislen
88 C. G. Di Camillo et al.
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Although several hydroid species are exploited as
substratum by numerous organisms, this is uncom-
mon in species of Plumulariidae and Aglaopheniidae
that are always completely devoid of sessile epibionts
probably for the cleaning function of the widespread
nematophores (Allman 1864; Gravier-Bonnet
2004). In the case of D. habereri, it remains unknown
how the zoanthids are able to overcome the larval-
repelling role of the nematophores.
Several zoanthids are known as epibionts of
different species of branched cnidarians such as
gorgonians and antipatharians. Generally, in these
associations the colonisation leads to the death of the
host. The extreme example of this strategy occurs in
the genus Savalia living on gorgonians. When the
host is completely killed by its epibiont, the zoanthid
becomes able to produce its own skeleton deposited
on that of the sea fan, the combined skeleton
becoming extremely thick (Zibrowius 1985).
The relationship with Dentitheca is peculiar
because it seems that a sort of equilibrium is reached
between the two partners: in contrast to the
parasitism observed in the case of anthozoan
colonisation, we never found a colony of Dentitheca
completely covering and or having been killed by the
zoanthid. This is probably due to a structural
difference of gorgonians and hydroids as the
coenosarc is protected inside the perisarc tubes and
thus not in direct contact with the epibiont tissues.
In contrast, in the branched anthozoans, epibiontic
zoanthids directly contact the cellular coenenchyme
that covers the internal organic skeleton.
The relative growth of the epibiont and the host is
different in the two species of zoanthids. In
Parazoanthus gracilis, the fast growth of the hydroid
allows the distal regions with living polyps to
continuously escape from the overgrowth by the
zoanthid. The zoanthid never reaches the extremities
of the branches. In the case of Parazoanthus sp., the
relationship is more complex. This zoanthid grows
only on large branches and never covers the
hydrothecal openings. Also the influence of the two
zoanthids on the final size and shape of the hydroid
colonies differs. While the colonies infested by
Parazoanthus sp. are unusually large and charac-
terised by a fan shape and numerous ramifications,
those with P. gracilis are smaller (about one-third in
the maximal size), irregular, and with a simpler
Figure 6. A–E, Modality growth. A, colony of the hydroid covered with Parazoanthus sp.; B, enlargement of a portion; C, particular of the
distal extremities of branches showing that the zoanthid colonises the main axes leaving free the thin hydrocladia bearing polyps; D, colony
of the hydroid covered with Parazoanthus gracilis; E, particular of D.
Association between Dentitheca habereri and two zoanthids 89
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ramification pattern. This is probably due to the
different size of the polyps of the zoanthids: the
small-sized polyps of Parazoanthus sp. are able to
colonise only the branches avoiding the hydrocladia,
while the large-sized polyps of P. gracilis completely
envelop both branches and hydrocladia. Moreover,
the thin layer of Parazoanthus sp. is easily perforated
by the growing new branches, while the thick coat of
P. gracilis, embedded with abundant sediment,
probably hampers the growth of new branches.
In both cases, the result of the epibiosis is a
cooperative relationship allowing the production of a
composite organism that, especially in the case of
Parazoanthus sp., reaches unusual sizes. The two
covering strategies of the zoanthids described here
could be considered different steps in a process of
transformation of a parasitic epibiosis in a mutualis-
tic relationship.
Acknowledgements
We would like to thank Dr Bernhard Ruthensteiner
(Zoologische Staatssammlung Muenchen) for his
helpfulness and for supplying type material of
Dentitheca habereri plus related literature. We are
grateful to Dr Dale Calder and Dr Nicole Gravier-
Bonnet who provided with records of plumulariids
associated with zoanthids, and to Professor John
Ryland for bibliographic data and his constructive
criticism. Thanks to Dr Frederic Sinniger for his
comments on the manuscript and his suggestions.
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