Redescription and new records of Celtodoryx ciocalyptoides (Demospongiae: Poecilosclerida) - A sponge invader in the north east Atlantic Ocean of Asian origin?

Abstract

In 1996 a sponge was found in a well studied area in the Ria of Etel, Brittany, France, that had never been recorded there before. This sponge was later described as a new species and genus, Celtodoryx girardae by Perez et al. (2006), who concluded that it is probably an invasive species. Over several years C. girardae was found to occur successively in the Gulf of Morbihan, France, and Oosterschelde estuary, Netherlands. This sponge is characterized by an extensive spatial broading and therewith it rates today among the dominant benthic megafauna in the shallow waters of the Gulf of Morbihan and Dutch inshore waters. During our recent survey of the Chinese Yellow Sea sponge fauna, we found an abundant species with close morphological similarities to C. girardae. Further taxonomic studies have revealed that both the Chinese and European sponges are in fact conspecific with Cornulum ciocalyptoides described by Burton (1935) from Posiet Bay, Sea of Japan and later recorded from other localities of the North West Pacific (e.g. Koltun, 1971; Sim & Byeon, 1989). In this paper we transfer the species of Burton from Cornulum to Celtodoryx and consequently it becomes the senior synonym of C. girardae. Furthermore, we conclude that Celtodoryx ciocalyptoides was introduced to the North East Atlantic from the North West Pacific with aquaculture of the Pacific oyster Crassostrea gigas as the probable vector. This is probably the first case recorded so far of a sponge species being transferred from one ocean to another by human activity.

Full text

Redescription and new records of Celtodoryx
ciocalyptoides (Demospongiae:
Poecilosclerida)—a sponge invader in the
north east Atlantic Ocean of Asian origin?
daniela henkel and dorte janussen
Forschungsinstitut und Naturmuseum Senckenberg, Senckenberganlage 25, D-60325 Frankfurt am Main, Germany
In 1996 a sponge was found in a well studied area in the Ria of Etel, Brittany, France, that had never been recorded there
before. This sponge was later described as a new species and genus, Celtodoryx girardae by Perez et al. (2006), who concluded
that it is probably an invasive species. Over several years C. girardae was found to occur successively in the Gulf of Morbihan,
France, and Oosterschelde estuary, Netherlands. This sponge is characterized by an extensive spatial broading and therewith
it rates today among the dominant benthic megafauna in the shallow waters of the Gulf of Morbihan and Dutch inshore
waters. During our recent survey of the Chinese Yellow Sea sponge fauna, we found an abundant species with close morpho-
logical similarities to C. girardae. Further taxonomic studies have revealed that both the Chinese and European sponges are in
fact conspecific with Cornulum ciocalyptoides described by Burton (1935) from Posiet Bay, Sea of Japan and later recorded
from other localities of the North West Pacific (e.g. Koltun, 1971; Sim & Byeon, 1989). In this paper we transfer the species of
Burton from Cornulum to Celtodoryx and consequently it becomes the senior synonym of C. girardae. Furthermore, we con-
clude that Celtodoryx ciocalyptoides was introduced to the North East Atlantic from the North West Pacific with aquaculture
of the Pacific oyster Crassostrea gigas as the probable vector. This is probably the first case recorded so far of a sponge species
being transferred from one ocean to another by human activity.
Keywords: Porifera, systematics, taxonomy, Celtodoryx,C. ciocalyptoides,C. girardae, non-indigenous species, aquaculture, vector
Submitted 6 April 2010; accepted 20 June 2010
INTRODUCTION
Invasion and successful colonization of non-indigenous
species is no longer a matter of isolated incidents, but a
regular event in a globalized world. In a strict sense invasions
are neither new nor exclusively human driven phenomena,
but the geographical scale, frequency, and the number of inva-
sive organisms recorded during the past decades have
increased dramatically as a direct consequence of expanded
transportation and commerce (e.g. Wells et al., 1986; di
Castri, 1989; Minchin et al., 2009). Thus the number of
species that have entered new areas through human activity
has increased by orders of magnitude especially during the
last 200 years. This alarming progress is now broadly recog-
nized as a critical element of ecosystem change and a major
threat to global diversity. Although only a small fraction of
the many species introduced outside of their native range
are able to colonize new habitats successfully, their effects
may be dramatic. The biological impacts of invaders on
affected ecosystems and their native faunal and floral com-
ponents are multifaceted and complex (Mack et al., 2000),
including, for example, competition for resources (Usio
et al., 2001), endemic species being lost by hybridization
with invasive species (Rhymer & Simberloff, 1996), alteration
of habitats (Denslow, 2002) and so forth. Additionally, gov-
ernments are faced with drastic economic consequences. For
example, through damage to agriculture, forestry and fisheries
(de Wit et al., 2001), introduced species inflict enormous costs,
estimated at $120 billion per year to the US economy alone
(Pimentel et al., 2005). For marine species a variety of introduc-
tion pathways has been documented: ballast water (Wasson
et al., 2001); biofouling by adhering to ships and floating anthro-
pogenic debris (Barnes 2002a, b; Convey et al., 2002); canals
such as the Suez Canal and the Panama Canal (Golani et al.,
2007); and the aquaculture industries (Wolff, 2005).
In 1996 an unknown sponge species was discovered in the
Ria of Etel, French Brittany, and since 1999 it was repeatedly
recorded in the nearby Gulf of Morbihan. The sponge remained
unidentified until Perez et al. (2006) established a new genus
and species, Celtodoryx girardae, for it and concluded its prob-
ably invasive nature. Shortly afterwards or even simultaneously,
an abundance peak of C. girardae was recorded in several
localities around Oesterschelde, Netherlands (van Soest et al.,
2007). The exact origin of this invader remains unknown so
far, although oyster farms have been assumed to be the probable
introduction source, because spat of the Pacific oyster
(Crassostrea gigas) has been imported from British Columbia
and Japan to the Oosterschelde estuary and the Gulf of
Morbihan since the 1960s. At present C. girardae is part of
Corresponding author:
D. Henkel
Email: dhenkel@senckenberg.de
347
Journal of the Marine Biological Association of the United Kingdom, 2011, 91(2), 347 –355. #Marine Biological Association of the United Kingdom, 2011
doi:10.1017/S0025315410001487

the dominant macrofauna in shallow waters of the Gulf of
Morbihan and Dutch coast and competes successfully with
other macrobenthic organisms, overgrowing some of the
other sessile invertebrates such as other sponges and octocorals
(Perez et al., 2006). Moreover, it is thought to be distributed
within a much wider range than has been recorded so far
(van Soest, personal communication).
During our recent survey of the Chinese Yellow Sea sponge
fauna, we found an abundant species with close morphological
similarities to C. girardae. A detailed morphological and taxo-
nomic investigation revealed that both Chinese and European
sponges are in fact conspecific with Cornulum ciocalyptoides
described by Burton (1935) from the Sea of Japan and later
recorded from other localities of the North West Pacific
(Koltun, 1959, 1971; Hoshino, 1987; Khodakovskaya, 2005).
In this paper we transfer the species of Burton from
Cornulum to Celtodoryx and it consequently becomes the
senior synonym of C. girardae. We confirm the invasive
origin of the North East Atlantic Celtodoryx ciocalyptoides
and document morphological variation between the Atlantic
and Pacific populations.
MATERIALS AND METHODS
The type series of Celtodoryx ciocalyptoides (Figure 1I) was
provided by the Zoological Institute of the Russian Academy
of Sciences, St Petersburg (ZIN RAS), whereas the paratype
of Celtodoryx girardae (Figure 1III) was made available by
the Muse
´um National d’Histoire Naturelle, Paris (MNHN).
Comparative material included a specimen sampled from
the Dutch waters (Figure 1IV), deposited in the ZMA,
Amsterdam, as well as 15 sponges collected by us by
SCUBA diving from four different shallow-water localities
in the Chinese Yellow Sea (Figure 1V) and deposited in
Senckenberg Naturmuseum, Frankfurt am Main (SMF). We
kept our specimens in seawater for several hours after
sampling, then fixed them in 6% formaldehyde and later
transferred them to 96% ethanol. Five specimens were exam-
ined in detail including a study of the skeletal architecture,
SEM documentation and spicule measurements; others were
studied less intensively. Skeletal architecture was observed in
200–400 mm thick sections under a light microscope. The
preparation of sections mainly followed Vacelet (2006) and
included dehydration, embedding in epoxy resin and cutting
using a precise saw with a diamond wafering blade. Spicules
were prepared by dissolution of the sponge organic com-
ponents in nitric acid and then examined and measured
under light microscope after mounting in Canada balsam on
slides and by SEM (CamScan) after sputtering (Sputter
Coater S 150B) of the spicules on stubs. A minimum of 35 spi-
cules of each category in each specimen was measured.
RESULTS
SYSTEMATICS
Class DEMOSPONGIAE Sollas, 1885
Order POECILOSCLERIDA Topsent, 1928
Suborder MYXILLINA Hajdu, van Soest & Hooper, 1994
Family COELOSPHAERIDAE Dendy, 1922
Genus Celtodoryx Perez, Carteron, Vacelet & Boury-Esnault,
2006
Celtodoryx ciocalyptoides (Burton, 1935)
synonyms
Cornulum ciocalyptoides: Burton, 1935: 72 – 73, figure 4;
Koltun, 1959: 25–26, figure 3. Khodakovskaya, 2003: 76,
table 1; 2005: 210, table 1.
Homoeodictya ciocalyptoides: Koltun, 1971: 93, figure 48, plate
XI (3); Hoshino, 1987: 26.
Coelosphaera physa (non-sensu Schmidt, 1875): Sim & Byeon,
1989: 44, plate X. figures 1 – 6.
Celtodoryx girardae: Perez et al., 2006: 205 – 214, figures 2– 3.
Isodictya ciocalyptoides: van Soest 2009.
type material
Two syntypes of Cornulum ciocalyptoides consist of two
fragments in alcohol: Posiet Bay, Sea of Japan; water
depth 3–4 m (ZIN 11137). Collected by Tazasov, 20 August
1926.
Posiet Bay, Sea of Japan, Station 34; water depth 2 m (ZIN
10844). Collected by Tazasov, 24 August 1926. Since Burton
did not constitute a holotype, (ZIN 10844) is herewith desig-
nated as lectotype.
Paratype of Celtodoryx girardae: one specimen in alcohol:
Les Gorets, Gulf of Morbihan, French Brittany; water
depth 7 m (MNHN D JV 93). Collected by B. Perrin, July
2001.
comparative material examined
(ZMAPOR 19826) (1 specimen in alcohol): Wemeldinge,
Oosterschelde, North Sea, 2.5 m, collected by M. de Kluijver
22 August 2005, initially identified as Celtodoryx girardae by
R.W.M. van Soest.
Our material from the Dalian area, Chinese Yellow Sea:
Dalian Wan Bay, Liaoning Province, China 38852′07.84′′N
121841′48.73′′E (9 specimens): (SMF 10851), 3.4 m, 23
August 2006; (SMF 10785), 3 m, 13 September 2006; (SMF
10790), 4.8 m, 13 September 2006; (SMF 10791), 6 m, 13
September 2006; (SMF 10794), 4.5 m, 13 September 2006;
(SMF 10788), 5.9 m, 29 August 2007; (SMF 10792) (examined
in detail), 5.2 m, 29 August 2007; (SMF 10793), 4 m, 29
August 2007; (SMF 10795), 4 m, 13 September 2006.
Fujizhuang Beach, Liaoning Province, China 38852′22.47′′N
121835′45.49′′E (4 specimens): (SMF 10786) (examined in
detail), 3.4 m, 1 September 2006; (SMF 10787), 2.9 m, 1
September 2006; (SMF 10789), 2.9 m, 1 September 2006;
(SMF 10797) (examined in detail), 2.7 m, 1 September 2006.
Er Tuo Islands, Liaoning Province, China 38852′07.47′′N
121835′46.69′′E (1 specimen): (SMF 10796) (examined in
detail), 5 m, 5 September 2006. Lv Shun, Liaoning Province,
China 38843′50.35′′N 121812′44.19′′E (1 specimen): (SMF
10798) (examined in detail), 4 m, 5 September 2007.
diagnosis (emended from perez et al. 2006)
Coelosphaeridae with a plumose to plumoreticulate choano-
somal skeleton of ascending tracts consisting of anisostron-
gyles and tylotes with terminal spines fanning out towards
the surface, loosely connected. Ectosomal skeleton of a loose
tangential arrangement of scattered anisostrongyles/tylotes
and microscleres. Microscleres consist of arcuate isochelae
of two distinct size categories and oxychaetes of one size cat-
egory. Microscleres are distributed randomly within the
choanosome.
348 daniela henkel and dorte janussen

External morphology
Lectotype (ZIN 10844]) of Cornulum ciocalyptoides a frag-
ment of approximately 1.5–2.5 cm in length and 0.8 cm in
width (Figure 2A). Texture soft, surface irregularly tattered.
Colour in ethanol brownish. Paratype (MNHN D JV 93) of
Celtodoryx girardae a fragment of approximately 1.5 – 2 cm
in length and 1.5 cm in width. Texture soft, surface irregular.
Colour in ethanol beige.
Colour of living Chinese specimens quince-yellow to golden
yellow (Figure 2C– F), turning to whitish grey after fixation.
Sponges of encrusting (Figure 2C, E), massive or globular
(Figure 2D) growth form. Most specimens of a rugose,
thickly incrusting base (mean thickness less than 3 cm) with
fistulose surface (Figure 2E, F). Fistules from few millimetres
to 1 cm in length (Figure 2F). No visible oscules on the top
of the fistules in either living or dead specimens. A number
of freshly collected specimens with conspicuous brown spots
on the surface (Figure 2D). Sponge with very soft, non-elastic
texture, easy to cut or tear. Surface smooth, produces large
amounts of mucus after cut off. Living specimens with an
area of less than 20 cm
2
(maximum size for Pacific specimens)
up to 25 m
2
(recorded from Oosterschelde, Netherlands).
Thickness from few centimetres (for all localities) to 50 cm
(recorded for Atlantic specimens). Specimens with incorpor-
ated detritus and sediment particles often associated with rho-
dophytes (Figure 2C, E).
Skeleton
Ectosomal skeleton with a loose tangential arrangement of
single tylote or anisostrongylote megascleres, contains numer-
ous microscleres and abundant foreign material such as
diatoms and sediment particles.
Choanosomal skeleton densely plumose to plumoreticu-
late with perpendicular tracts of megascleres (tylotes or
strongylotes) loosely connected, ending in surface brushes
(Figure 2H). Diameters of bundles with a width range of
35–120 mm. Megascleres do not appear to be localized.
Microscleres loosely distributed within the skeleton.
Spicules
Spicule dimensions presented in the text below are the values
summarized for all specimens. Results for individual speci-
mens are given in Table 1.
Megascleres of two types: (1) corresponds to proper tylote
type, thin, usually shorter (Figure 3C), straight with well
defined equal tyles, with the head either completely covered
by spines (Figure 3C, J) or with smooth heads, then thinner
and longer (Figure 3B, H); underlined numbers indicate
mean values; numbers in parentheses indicate SD: 125 – 210
(+36)–335×1.6 – 4(+1.1)–8 mm, tyle diameter of 2.4 – 4.7
(+1.1)–8 mm; (2) called anisostrongyles hereafter, intermedi-
ate type of style and strongyle, ends often asymmetrical
(Figure 3A, D, F, G & I). They are straight or slightly curved
with less and stronger spines on extremities compared to
tylote type, generally longer and thicker than the other type,
150–290 (+47) – 370×2.4 –7(+1.5)– 12 mm.
Microscleres of two types: (1) arcuate isochelae of two dis-
tinct size categories: (I) 33.6– 49 (+3.6) –62 mm (Figure 3L,
M & N) and (II) 16 – 23 (+1.9) –30 mm (Figure 3O),
reduced forms of isochelae in both categories 43 – 48
(+2.9)–53 mm and 20 – 24 (+1.1) –28 mm (Figure 3K); (2)
oxychaetes: 48– 68 (+5.7) – 87 mm, straight with ends taper-
ing to thin points (Figure 3E).
Length and diameter of spicule categories do not vary
between the specimens of both oceans or within the represen-
tatives of the respective areas.
Distribution and ecology
Records from the North West Pacific: Sea of Japan in the
Posiet Bay and Peter the Great Bay (Burton, 1935; Koltun,
1959, 1971; Khodakovskaya, 2005); Yellow Sea at the west
coast of South Korea near Anhu
˘ng (Sim & Byeon, 1989)
and Chinese Yellow Sea around Dalian (more precisely Lv
Shun, Dalian Wan Bay, Er Tuo Islands and Fujizhuang
Beach, this study). Depth range 2.5 – 16 m.
Records from the North East Atlantic: North Sea,
Oesterschelde, Netherlands (van Soest et al., 2007) and Gulf
Fig. 1. Geographical distribution of Celtodoryx ciocalyptoides (Burton, 1935) in chronology of discovery: (I) ‘Posiet Bay’, ‘Peter the Great Bay’, Russian part of Sea
of Japan; (II) ‘Anhu
˘ng’, South Korean part of the Yellow Sea; (III) ‘Gulf of Morbihan’, Brittany, France; (IV) ‘Oosterschelde’, Netherlands; (V) ‘Dalian’, Chinese
part of the Yellow Sea.
new records of c. ciocalyptoides in the north-east atlantic 349

of Morbihan, French Brittany (Perez et al., 2006).
Depth-range: 4 – 38 m.
The species occurs on rocky substrate, mussel shells and on
soft-bottoms. The morphology of the specimens from the
Pacific Ocean is more or less thinly encrusting with an area
less than 20 cm
2
, whereas in the North East Atlantic Ocean
massive representatives with a mean of 8 – 10 cm and a
maximum thickness of 50 cm covering an area of 25 m
2
were observed (van Soest et al., 2007). Observations by
Perez et al. (2006) in the Gulf of Morbihan indicate that the
more massive forms are restricted to the shallow waters
whereas thinly encrusting forms occur deeper. This phenom-
enon was not observed in the North West Pacific Ocean. In
the Chinese Yellow Sea, Celtodoryx ciocalyptoides was not
recorded below 6 m depth.
All localities were semi-enclosed environments character-
ized by high turbidity and strong hydrodynamic forces.
Water circulation is primarily driven by a semi-diurnal tide.
The water temperatures for all localities are subject to seasonal
variations (from 4– 258C). The temperature differences in the
Chinese Yellow Sea and Sea of Japan are much more pro-
nounced than in Western Europe. The climate in Dalian is
monsoon-influenced, humid, continental, characterized by
humid summers due to the East Asian monsoon, and cold,
windy, dry winters that reflect the influence of the vast
Siberian anticyclone. Regular icing occurs. In contrast, the
Fig. 2. Celtodoryx ciocalyptoides (Burton, 1935): (A) Lectotype of Cornulum ciocalyptoides (ZIN 10844) with (B) original label of Burton; (C) habit in situ (SMF
10796); (D–F) freshly collected; (D) globular with smooth surface (SMF 10794); (E (SMF 10791)–F (SMF 10790)) encrusting with fistulouse surface; (G–H)
cross-section of choanosomal skeleton; (G) fracture of a histological choanosomal cross section (300 mm thick) showing developing embryos (SMF 10787);
(H) cross-section (SMF 10788). Scale bars: (A, F) 0.5 cm; (C, D, E) 1 cm; (G) 0.5 mm; (H) 1.4 mm.
350 daniela henkel and dorte janussen

climate in the North East Atlantic is moderate with relatively
cool summers and mild winters with infrequent icing. All
Chinese localities are isohaline (31– 32.5 ppm), eutrophic
and with low concentrations of silica (SiO
2,
0.01 mmol/m
3
).
According to the description by Burton (1935), C. ciocalyp-
toides exhibits a blackish external layer in preserved condition.
Several specimens from the Chinese Yellow Sea possess patches
of a brownish crust, caused by incorporation of sediment
particles and diatoms. Chinese specimens are often associated
with rhodophytes, which are in some cases completely incor-
porated into the sponge tissue (see Figure 2C, E & G).
Reproduction
Embryos were found in two Chinese specimens ((SMF 10787)
and (SMF 10789)). They are distributed abundantly within the
choanosome (Figure 3). Embryos are round, flattened, 195 –
370 mm wide, slightly orange, containing close-packed cells.
DISCUSSION
Taxonomic remarks
Burton (1935) located his species to Cornulum, which belongs
to the Acarnidae, suborder Microcionina. Koltun (1959) and
Khodarkovskaya (2005) followed this, although in his later
paper Koltun (1971) moved the species to Homoeodictya,
Isodictyidae (formerly Esperiopsidae), suborder Mycalina.
This decision has been accepted until the present study, only
Homoeodictya was synonymized with Isodictya (van Soest
2009). An interesting record came from the South Korean
part of the Yellow Sea. Under the name Coelosphaera physa
(Schmidt, 1875) (Coelosphaeridae, suborder Myxillina),
Sim & Byeon (1989) documented a sponge which strongly
resembled Celtodoryx ciocalyptoides. Their SEM pictures
clearly revealed oxychaetes although these spicules were
referred to as rhaphides. In spite of the lack of data on its skel-
etal structure, the types and dimensions of spicules and ex situ
images of this specimen leave no doubt that it is conspecific
with C. ciocalyptoides. Finally, comparing all Pacific records
of the latter with the detailed documentation of Atlantic
Celtodoryx girardae by Perez et al. (2006) and van Soest et al.
(2007), we can undoubtedly conclude that these belong to
the same species, and this species should better be kept as the
only representative of Celtodoryx known so far, rather than
allocated to Cornulum,orIsodictya or Coelosphaera. For the
sake of completeness and to avoid confusion, it should also
be mentioned that the Atlantic representatives of C. ciocalyp-
toides are sometimes incorrectly referred to Celtodoryx morbi-
hanensis, e.g. in reference lists (Webster, 2007) or in genetic
databases (e.g. NCBI). Celtodoryx morbihanensis is a nomen
nudum.
Sim & Byeon (1989) had some reasons to attribute their
specimen to Coelosphaera, since Celtodoryx does belong to
the Coelosphaeridae. Among other features, this family is
characterized according to van Soest(2002) by ‘a skeletal archi-
tecture of reticulate tracts forming an isodictyal skeleton’.
However, he placed Acanthodoryx Le
´vi, 1961, which possesses
a distinct plumose skeleton, as a subgenus of Lissodendoryx
Topsent, 1892, a genus of the Coelosphaeridae. Lissodendoryx
(Acanthodoryx) fibrosa (Le
´vi, 1961) is the only species of the
subgenus Acanthodoryx and shows the following clear
Table 1. Spicule dimensions in different specimens of Celtodoryx ciocalypoides (Burton, 1935). All values in mm; underlined numbers indicate mean values; numbers in parentheses indicate SD.
SMF 10792 SMF 10797 SMF 10786 SMF 10798 SMF 10796 MNHN D JV 93 ZMA POR 19826 ZIN 10844
Anisostrongyle 255– 293 (+20) – 330 260– 282 (+19) – 325 235– 307 (+36)–370 250 – 286 (+23) –365 150– 293 (+51) – 360 165– 268 (+45) – 320 300– 332 (+17) – 370 190– 273 (+25)–305
×5.6– 7.1 (+1.1) – 9.6 ×2.4 – 6(+1)– 8 ×3.2 – 6.7 (+1.3) – 8.8 ×4.8 – 7.6 (+1.5)–9.6 ×4.8 –6.7 (+1.4)– 8.8 ×5.8 – 8.9 (+1.7) – 12 ×3.2 –7.1 (+1.4)– 9.6 ×3.2 – 8(+1.7)– 10.4
Tylote 170– 207 (+27) – 275 150– 210 (+35)–305 175 – 212 (+18) –275 145– 182 (+19) – 243 125– 208 (+35) – 315 125– 195 (+19) – 220 195– 257 (+45) – 335 170–208 (+45)– 290
×2.4– 4.8 (+0.7) – 4.8 ×1.6 – 3.8 (+1) – 4.8 ×1.6–3.6 (+1.1)– 5.6 ×1.6 – 4(+1.4)–7.2 ×1.6 –4.6 (+1.8)– 8 ×1.6 – 4.2 (+1.1) – 5.6 ×2.4 –3.7 (+1)– 5.6 ×1.5 – 4.5 (+0.9) – 6.5
tyles 3.2– 5.3 (+0.6)– 5.6 tyles 2.4– 3.7 (+1)–4.8 tyles 2.4 –4.8 (+1.1)–6.4 tyles 2.4 –4.8 (+1.5)– 7.2 tyles 2.4 – 5.9 (+1.6) – 8 tyles 2.4–4.3 (+1.3) –6.4 tyles 4– 5(+0.7) – 6.4 tyles 1.5 – 5.7 (+1.1) – 7.2
Isochelae type I 48 – 53 (+3.2) – 62 43– 48 (+4)–59 34 – 48 (+3.4) – 54 43– 47 (+3) – 58 45– 50 (+2.7)–54 40– 48 (+3.3)–54 42 – 49 (+2.8) – 54 48– 51 (+3.2)–56
Isochelae type II 19– 23 (+1.9)–26 21 – 23 (+2) – 27 21– 22 (+1.6) – 27 21– 23 (+1.7) – 26 21 –24 (+1.9)– 27 19– 23 (+2) – 27 16–22 (+1.7) –24 22– 25 (+2)–30
Oxychaete 54– 72 (+3,8) – 74 56 –66 (+3.8)– 75 58– 66 (+4.5) – 75 48– 65 (+6.4)–77 64 – 74.4 (+4.6) – 83 65–74 (+6.7)– 87 61– 69 (+2.9)–72 62 –67 (+3.1)–72
new records of c. ciocalyptoides in the north-east atlantic 351

differences from C. ciocalyptoides:L. (Acanthodoryx) fibrosa has
a plumoreticulate skeleton with acanthostyles rather than the
plumose to plumoreticulate skeleton of C. ciocalyptoides with
tylotes and anisostrongyles, which are exclusively spined on
tips. Furthermore L. (Acanthodoryx) fibrosa lacks oxychaetes,
which are very abundant in the Celtodoryx species. Moreover
L. (Acanthodoryx) fibrosa is exclusively recorded from tropical
coral reefs in the Philippines, while C. ciocalyptoides was found
only in temperate zones. L. (Acanthodoryx) fibrosa is red
whereas C. ciocalyptoides is yellow. Within Coelosphaeridae
the only genus other than Celtodoryx that shares the presence
of oxychaetes is Chaetodoryx, but in the latter the skeleton is
reticulate consisting of choanosomal acanthostyles.
Varieties and their possible ecological
implications
Although skeletal structure, types and dimensions of spicules
from all studied specimens of Celtodoryx ciocalyptoides are
similar, a few minor differences were observed. Burton
(1935) indicated three different size categories of isochelae,
but we found only two distinct types in the type series.
Perez et al. (2006) suggested that tylotes are restricted to the
ectosome and the thicker and longer anisostrongyles to the
choanosome, but we found that megascleres do not appear
to be localized and there are more discrepancies in the
description by Perez et al. (2006). In addition to the original
description, our study shows the presence of thin tylotes
with smooth tyles, which are not abundant but still present
both in the Pacific and in Atlantic specimens.
Moreover, besides proper isochelae, reduced forms were
found, but exclusively in the Chinese specimens. They
appear in both size categories of isochelae, which makes it
likely that these spicules are developmental stages, possibly
due to the growth period and spiculogenesis at the time of col-
lection of the specimens. But why were those stages not found
in the type series, also collected during the same season? In
addition to these reduced forms of isochelae, we also found
pronounced deformations of other spicules not only in C.
ciocalyptoides (Henkel & Janussen, in preparation). All these
facts make it conceivable that they are a result of seasonal vari-
ation, due to fluctuations of both water temperature (Sara
`&
Vacelet, 1973; Simpson, 1978; Jones, 1987; Bavestrello et al.,
1993a) and dissolved silica concentration (Jørgensen, 1944;
Lowenstam & Weiner, 1989; Bavestrello et al., 1993b;
Wiedenmayer, 1994; Maldonado et al., 1999; Mercurio et al.,
2000) in the seawater. Maldonado et al. (1999), for example,
demonstrated for the Mediterranean species Crambe crambe
(Schmidt, 1862) that variations in spicule size and shape cor-
respond to elevated concentrations of Si(OH)
4
under exper-
imental conditions. As a consequence of increased Si(OH)
4
concentrations, several ‘new’ spicule types were found in
great abundances. These results clearly indicate that avail-
ability of the dissolved silica is a limiting factor for structures
of the silica skeleton, not only for sponges, but for all organ-
isms that use Si(OH)
4
for their skeleton (e.g. diatoms and radi-
olarians). The habitat of specimens of C. ciocalyptoides in
China belongs to an environment that is strongly affected
by the East Asian monsoons and riverine inputs.
Particularly the Yellow River, the biggest river system which
empties into the Yellow Sea and Bohai Sea, carries enormous
loads of sediment and dissolved silica. In the course of distinct
drought periods, damming projects and artificial drainage
activities during the last decades, the output of the Yellow
River has decreased by more than 50% compared to the
1960s. Several studies (Zou et al., 2001; Liu et al., 2004)
stated that today’s low dissolved silica concentration in the
Bohai Sea and Yellow Sea is a consequence of this reduction
of freshwater input from the Yellow River and other rivers.
Their conclusion is supported by the results of this study,
because even before the autumn algae bloom, low silica con-
centrations were measured. As ‘diancistra-like’ spicules,
found in the Chinese specimen of C. ciocalyptoides, may be
regarded as derivates of proper isochelae, their presence can
be explained by the reduction of the spicule structure as a
Fig. 3. Spicule types of Celtodoryx ciocalyptoides (SMF 10797) at SEM. Megascleres: (A –D, F–J), anisostrongyles (A, D) with different heads (F, G, I); tylotes (B,
C) with different heads (H, J); microscleres: arcuate isochelae (K –O) of two size categories, large (L, M), small (O); reduced isochela (K); oxychaetes (E). Scale bars:
(A, B, C, D) 30 mm; (F, G, J, K, L, M, N) 10 mm; (E, H, I, O) 5mm.
352 daniela henkel and dorte janussen

response to low values of dissolved silica in seawater.
Additionally, we conclude that extreme variations in tempera-
ture, such as found at our study site in the North West Pacific,
can be the reason for reduced spicule forms as a response to
temperature stress.
The sponge shows a rapid population growth within the
invaded areas. The external morphology of C. ciocalyptoides
varies significantly between representatives from both
Oceans. Celtodoryx ciocalyptoides from the north-west Pacific
localities tends to be encrusting with a limited spatial exten-
sion, while the North East Atlantic specimens are often
massive or thickly encrusting and of large individual size
(Perez et al., 2006; van Soest et al., 2007). Differences in nutri-
ent supply are unlikely due to the fact that all locations are more
or less strongly eutrophic. The varieties in population
dynamics and external morphology may be rather a conse-
quence of different climatic conditions. The extensive range
in temperatures coupled with very cold winter periods may
cause an adverse effect on C. ciocalyptoides growth in
Chinese specimens. Observations by Perez et al. (2006)
support this possibility. A mass mortality in C. ciocalyptoides
populations occurred in the Gulf of Morbihan as a result of a
relatively severe winter in 2003. After this, the sponge popu-
lation recovered but its growth forms were mainly encrusting.
Results of previous studies, based on growth experiments on
several other sponge species from temperate waters, showed
the decrease in sponge population density and individual size
during winter season (Candelas & Candelas, 1963; Barthel,
1986, 1988; Duckworth & Battershill, 2001). Further studies
are needed to confirm this correlation for C. ciocalyptoides.
Celtodoryx ciocalyptoides, an invader
to the North East Atlantic?
According to the Delivering Alien Invasive Species Inventories
for Europe (DAISIE: http://www.europe-aliens.org) currently
more than 1000 marine exotic species have been recorded in
Europe with no records of sponges so far. Mycale armata
Thiele, 1903, a tropical sponge from the Indo-West Pacific,
which was recently introduced to Hawaii, is currently listed
in the Global Invasive Database (http://www.issg.org) as the
only sponge representative. The lack of records of invasive
sponge species does not mean that they do not exist. It is
more likely to be due to the complexity of sponge taxonomy
and deficiency in regular monitoring. Nevertheless, 15
sponge invaders have been described recently for the Dutch
inshore waters, including Celtodoryx ciocalyptoides (van
Soest et al., 2007).
Several characteristics suggest that C. ciocalyptoides is an
invasive species. First of all, C. ciocalyptoides is new to the
North East Atlantic, whereas its original distribution is strictly
localized. According to the findings by Perez et al. (2006) the
dispersal followed a chronological order from the first evi-
dence in 1996 in the Ria of Etel. The sponge strongly prolifer-
ates within populated biotopes, i.e. competes successfully for
space with various other marine invertebrates, such as
Octocorallia and other poriferan species.
Both Perez et al. (2006) and van Soest et al. (2007)
pointed out that aquaculture is the most evident source of
C. ciocalyptoides in Europe. According to Gollasch et al.
(2009), more than 70 invasive species are established in the
North Sea, verifiably introduced by aquaculture activities.
The distribution of C. ciocalyptoides is considered to be
directly related to the transfer of the Pacific oyster C. gigas
to aquaculture farms in lagoons along the French and Dutch
coasts. Although the invasion pathway cannot be easily deter-
mined, previous studies already demonstrated a presumably
causal relationship of the introduction of C. gigas with the
occurrence of non-indigenous species for the North East
Atlantic and the Pacific coast of North America (e.g. Scagel,
1956; Sauriau, 1991; Reise et al., 2002; Wolff & Reise, 2002;
Smaal et al., 2005; Dijkstra et al., 2007).
Taking all these facts into account we conclude that the
North East Atlantic populations of C. ciocalyptoides originated
from the North West Pacific. Our findings confirm the
hypothesis that aquaculture of the Pacific oyster C. gigas
may be the source of the invasion of C. ciocalyptoides.To
our knowledge, C. ciocalyptoides is likely the first verified
‘non-cosmopolitan’ sponge species that has been transferred
from one world ocean into another by human activity.
The results of this study confirm the need for taxonomic
and ecological surveys, especially in poorly investigated
regions, in order to detect potential sources for invasive
species and finally adopt measures to break the transmission
path.
Further investigation should deal with the following
questions: What is the impact of C. ciocalyptoides on
native benthic community? And, do rising water temperature
and mild winters, due to global warming, support
the proliferation of C. ciocalyptoides on coastlines of north-
east Europe?
ACKNOWLEDGEMENTS
The authors owe deep gratitude to Stefanie George and Esther
Novosel for their assistance in sampling. We express our grati-
tude to numerous Chinese students for assistance during our
field surveys. We thank Professor W. Zhang (DICP, China)
and Professor F. Bru¨mmer (Zoological Institute, University
of Stuttgart) for logistical support. We express our warm
thanks to Dr R.W.M. van Soest (Zoological Museum
Amsterdam), Dr T. Perez (Centre d’Oce
´anologie de
Marseille) and Dr Olga Sheiko (Zoological Institute of
Russian Academy of Sciences in St Petersburg) for the pro-
vision of specimens. We wish also to express our deep grati-
tude to Dr J. Gugel (Zoological Institute, University of
Stuttgart) for his scientific support. We also thank anonymous
referees for their constructive comments. This work was sup-
ported by SYNTHESYS (NL-TAF-4600).
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Correspondence should be addressed to:
D. Henkel
Forschungsinstitut und Naturmuseum Senckenberg
Senckenberganlage 25
60325 Frankfurt am Main
Germany
email: dhenkel@senckenberg.de
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