Cliona minuscula Schönberg, Grass & Heiermann, 2006, sp. nov.

Remarks on Cliona minuscula, sp. nov. and a discussion of a species complex of bioeroding sponges that only contain tylostyles as skeletal elements

Species of the genus Cliona that only contain tylostyles

The newly described species of a bioeroding sponge from Orpheus Island contains only tylostyles as skeletal elements. The arrangement of spicules and the manner in which the sponge erodes identifies it as a Cliona. Comparison with 15 other species of this genus that also contain only tylostyles showed that this sponge has not previously been described (Tab. 2). One of the species that we considered was C. caesia nov. comb.. Additional samples obtained since the original description support the transfer from Pione to Cliona. Variable oxeas previously found in C. caesia were not present in most of the new samples and are likely to be contaminations or kleptospicula (Schönberg unpublished data). It was also noted that dark bodies in tissue preparations previously described as ‘pigment granules’ (Schönberg 2000) are symbiotic dinoflagellates. C. caesia thus becomes available for the present comparison.

A number of species have not been considered as they have previously been synonymised with C. celata (Tab. 3). Topsent (1900) further synonymised C. alderi and C. dissimilis with C. celata, however, these two species are presently regarded as valid (Rützler & Stone 1986; Fromont et al. 2005) and were included in the comparison. C. celata itself was considered, even though it has occasionally been observed with an additional spicule type, with raphides. Only C. celata without raphides is used for comparison, and it has been discussed that specimens with and without raphides belong to different species (e.g. Rosell & Uriz 2002). Some other species were not considered, because the original descriptions were insufficient and revised descriptions were unavailable (Tab. 3). Two other species were not included, although they only contain tylostyles and other authors described them as Cliona, but their status as bioeroders is unconfirmed (Tab. 3). All the above species are dissimilar to our present specimens or are invalid. Details for taxonomic decisions are given below.

Sample Dimension Minimum Mean Maximum SD

QM G322595 length 180.0 231.1 265.0 21.3

shaft width 2.5 4.4 7.5 1.1

tyle width 4.5 6.9 9.5 1.0

QM G322596 length 182.5 219.5 247.5 15.4

shaft width 2.5 4.5 7.3 0.9

tyle width 5.0 6.7 8.0 0.9

Remarks on Cliona minuscula, sp. nov.

C. minuscula, sp. nov. was distinguished from 15 other clionaid species containing only tylostyles by using available original descriptions and additional references as listed (Tab. 2). The 15 comparison species were grouped based on the similarities of their taxonomic characters. The same grouping and sequence was retained in Table 2 and Figure 4.

C. arenosa, C. californiana, C. celata, C. delitrix, C. dissimilis and C. laticavicola are yellow to orange and have significantly longer tylostyles than C. minuscula, sp. nov. (50–100 µm longer; Fig. 4 A–I). Elongate­oval tyles are usually terminal in C. minuscula. sp. nov., and more spherical and often subterminal in the other six species. C. celata, C. delitrix, C. dissimilis and C. laticavicola have larger erosion chambers, papillar diameters of> 1 mm and larger papillar canals than in C. minuscula, sp. nov. (Tab. 2). C. californiana, C. celata, C. delitrix and C. dissimilis can occur in encrusting growth form, and C. californiana and C. celata may have free­living growth stages, which to date is unknown for C. minuscula, sp. nov. (Tab. 2). Furthermore, C. laticavicola has only been found in the Caribbean and the Atlantic, and C. californiana only in the Western Pacific. There is very little information available on C. arenosa, but some authors have remarked on its affinity to C. celata (e.g. Topsent 1889). C. arenosa has been described as a massive sponge occurring in the North Atlantic at Florida (Schmidt 1870).

A species group encompassing C. ecaudis, C. janitrix, C. kempi and C. macgeachii has tylostyles that are shorter and wider than in C. minuscula, sp. nov. (Fig. 4 J–O). C. ecaudis has two size classes of tylostyles (Topsent 1932), whereas C. minuscula, sp. nov. has only one. C. ecaudis and C. janitrix have larger erosion chambers and papillar sizes than C. minuscula, sp. nov. (Tab. 2). C. kempi and C. macgeachii have small erosion chambers and very small papillar sizes, similar to C. minuscula, sp. nov. (Tab. 2), but can easily be distinguished from C. minuscula, sp. nov. by their ensiform tylostyles (Fig. 4 N–O). Unlike C. minuscula, sp. nov., C. janitrix has tylostyles with subterminal tyles or even stylar modifications, and its tylostyle points are often mucronate, telescoped or stepped (Fig. 4 K–M). With the exception of C. kempi, in which the colour has not been described, all the above species differ in colour from C. minuscula, sp. nov. (Tab. 2), and to date none of them has been reported from the Great Barrier Reef (Tab. 2).

Tylostyle lengths of C. alderi, C. insidiosa, C. millepunctata and C. peponaca resemble those of C. minuscula, sp. nov. (between 180 and 245 µm; Fig. 4 P–V), but the spicule shapes differ. Tylostyles are on average wider in C. alderi, C. insidiosa and C. peponaca than in C. minuscula, sp. nov. (Fig. 4 P–S and V), and more delicate and thinner in C. millepunctata (Fig. 4 T–U). Due to seasonal spicule formation, spicule width may not be a reliable character (Schönberg and Barthel 1997 and 1998), but other spicule characters were found to differ as well. C. alderi and C. peponaca display significant tylar variability, with subterminal and displaced, spherical tyles and modifications to styles (Fig. 4 P–Q and V). Tylostyle shafts are slightly curved in both species. Tyle shape in C. insidiosa is very characteristic (Fig. 4 R–S; ‘heads distally flattened’, Rützler and Stone 1986), with an angular constriction in the neck region. In C. millepunctata, the tylostyle shaft is more curved than in C. minuscula, sp. nov., and can be sinous (Fig. 4 T–U). These characters are atypical for C. minuscula, sp. nov. C. alderi, C. insidiosa and C. millepunctata may be brown like C. minuscula, sp. nov. (only dried colours are known; Tab. 2), but they are likely to be European species (Hancock’s species are mostly from England), which further reduces the chance of conspecifity with C. minuscula, sp. nov. C. peponaca is a richly yellow Caribbean species and clearly distinct from C. minuscula, sp. nov. (Tab. 2).

C. caesia shares a number of characters with C. minuscula, sp. nov. Both species have been sampled from the same site, have very small papillae and erosion chambers, are dark brown, contain symbiotic dinoflagellates, and have predominantly straight tylostyles (Tab. 2). However, in C. caesia tylostyles are longer on average, tyles are distinctly more spherical and often wider than long (Fig. 4 W). Furthermore, C. caesia has two size classes of tylostyles and light blue rings on extended papillae (Tab. 2), which is not the case for C. minuscula, sp. nov.

Species Colour Growth Tylostyle Tylostyle Macrosco­ Occurrence References

form, dimensions form pic erosion

papillae [m] traces

(chambers)

Cliona brown 225.3 x 4.5 shaft +/­ multi­ Orpheus present

minuscula, (contains 0.4 mm x 6.8 straight camerate, Island, study

sp. nov. zooxan­ evenly (N = 2 x tyles chamber central thellae) dispersed 50) terminal form Great mainly oval spherical Barrier 0.6 mm Reef

Species from the C. celata complex that have yellow to orange colours and mostly longer tylostyles

and larger erosion chambers than C. minuscula, sp. nov. Most species of this complex can occur in

different growth forms.

Cliona brown? tylostyles? Florida, N Schmidt

arenosa when dry Atlantic 1870

(Schmidt, (incorpo­

1870) rates

sediments)

Cliona yellow to 256 x 7.8 x tylostyles? Mexico, W

californi­ brownish, papillar 8.3 with Pacific al. 2004

ana pale yellow openings subterminal

(de or brown in 0.2–3.4 tyles

Laubenfels, alcohol mm

1932)

Cliona yellow­ 323 x 9.1 tyles multi­ cosmo­ Hartman

celata orange papillar subterminal camerate, politan 1958

Grant, 1826 openings> 287 x 8.1 and with with Bergquist

1 mm vesicles, relatively 1968 254 x 7 can contain large Rosell and raphides? chambers Uriz 2002 1–8 mm

Cliona orange­red 279 x 8.9 shafts +/­ multi­ Caribbean Pang 1973

delitrix (commen­ large 325 x 10.1 straight, camerate, Rose and

Pang, 1973 salism with papillae tyles chambers 4 Risk 1985 Parazoan­ subtermi­ mm, Lehnert thus nal, oval elongated­ 1993 parasi­ cylindrical

ticus) penetration

depth 3–12

cm

to be continued.

Cliona orange tyles multi­ Arafura Ridley and dissimilis light brown up to 2 mm subtermi­ camerate, Sea Dendy Ridley & in alcohol nal, with spherical, 1886 Dendy, vesicles in regular Ridley 1886 distribu­ 1887

245–325 x tion, Western Hentschel

6–9 1–2 mm Australia 1909 (as C.

celata)

253 x 6.8 x Fromont et

7.8 al. 2005

Cliona orange 349 x 10.2 shafts +/­ large Caribbean Pang 1973 laticavicola 2.5–2.8 straight, galleries

laticavicola mm, tyles with a

Pang, 1973 tend to fuse subterminal diameter up

or further to 16 mm

displaced

Cliona orange 279 x 7.3 shafts +/­ large Caribbean Pang 1973 laticavicola 2.2–2.5 straight, galleries

parva­ mm, do not tyles with a

spiculata fuse subterminal diameter up

Pang, 1973 or further to 16 mm

displaced

Species with tylostyles that are simultaneously shorter and wider than in C. minuscula, sp. nov.

Cliona brown to thin: two size multi­ Tuamotu Topsent ecaudis yellow 130–160 x classes of camerate, Archipel 1932 Topsent when dry 1.0–1.3 x tylostyles, irregular

1932 3–4 A: thin and 1–3 mm

stunted: long, and

68– 75 x B: stunted

2–8 x 5 –5.5 straight or

slightly

curved

Cliona pale to dull 180–210 x robust, multi­ Caribbean, Topsent janitrix yellow 0.1–1.0 8–12 x shafts camerate, Atlantic 1932 Topsent, alive, dried, mm 11–14 straight to with Ocean 1932 in alcohol slightly relatively Pang 1973

and in curving, large

formalin 178 x 8 tyles chambers, Rosell and

terminal, spherical, Uriz 2002

round or similar to

subtermi­ those of C.

nal, points celata

stepped, 2–6 mm

reduced or

mucronate

to be continued.

Cliona not stated 127–205 x shafts multi­ Indian Annandale kempi very small 4.1–8.2 x straight to camerate, Ocean 1915a Annandale, 8.2–12.5 slightly spherical,

1915a curving, marginal

ensiform, and in one

tyles round tier only;

to 2– 7 x 0.5–3

subterminal mm (N.

Namboo­

diri pers.

comm.)

Cliona mustard, 143.1 x 7.1 shafts multi­ Barbados, Holmes macgeachii yellow to minute, curving, camerate, West Indies 2000 Holmes, orange round, ensiform, spherical,

2000 discrete round tyles, can fuse to

0.2 (0.1­ often form

0.5) mm subterminal strings

0.2­1.5 mm

Species, in which tylostyles are shorter than those in C. minuscula, sp. nov., and in which tyle shapes and shaft curvatures differ from those in C. minuscula, sp. nov.

Cliona dried, 219 tyles multi­ Isle of Man Hancock alderi yellowish­ size subtermi­ camerate, 1849 Hancock, brown variable, nal, irregular to Hancock 1849 largest modifica­ spherical, 1867

papillae 0.6 240 x 7 tions as widely Rützler and

mm, widely styles branching, Stone 1986

spaced, run (Hancock: 4.2 mm

in lines two spicule

types)

Cliona brown, 217 robust, multi­ England? Hancock insidiosa when dry small shafts camerate, 1849 Hancock, papillae 250 x 10 straight to with Rützler and 1849 slightly relatively Stone 1986

curving large

tyles round chambers,

branching

5 mm

Cliona not stated, 181 shafts multi­ England? Hancock millepunc­ papillar straight, camerate, 1849 tata size not 210 x 2 curving or branches Rützler and Hancock, stated sinous, are <0.8 Stone 1986 1849 tyles oval mm in

diamter

to be continued.

Cliona rich, 243 x 8.9 shaft multi­ Caribbean Pang 1973 peponaca yellow­ 0.5–1.4 slightly camerate, Pang, 1973 orange mm curving, large,

tyles cylindrical

terminal 0.9–1.5

and mm

subtermi­

nal, round

C. caesia and C. minuscula, sp. nov. share a number of taxonomic characters, but tylostyle shape and length is different in C. caesia, and its blue, papillar ring could not be observed in C. minuscula, sp. nov.

Cliona brown,, 310 x 6.5 x tylostyles multi­ Central Schönberg caesia nov. with 0.5–2 mm 10.5 of two camerate, Great 2000 comb. character­ 150 x 7 x sizes, tyles spherical to Barrier (Schönberg istic blue 9.5 round, irregular Reef, 2000) ring overall: often wider 1–4 mm

(contains 280 x 6.5 x than high

zooxan­ 9

thellae)

Species that co­occur in the holotype of C. minuscula, sp. nov., but clearly differ from the latter by their spicule characters.

Cliona brown in, 261 x 10.7 shafts one Indian Sollas 1878 ensifera alcohol round, x 12.7 curving in irregular Ocean, characters Sollas, 0.5–0.8 necks: 7.5 mid­region, cavity: 9.8 central from 1878 mm (N = 50) ensiform, mm wide, Great present (characters fully tyles round 3.8 mm Barrier study from the formed and slightly high Reef specimen spicules subterminal

QM only:

G322595) 271 x 12.7

x 13.7

necks: 8.7

(N = 37)

microscle­

res: rare

spirasters

to be continued.

Cliona cf. brown,, 335 x 8.5 x shafts irregular, Ternate, Thiele orientalis greyish in round (1.6 12.3 (N = straight to honeycomb Pacific, 1900 Thiele, alcohol mm, N = 50), no slightly ­shaped central characters 1900 (contains 10) to micro­ curving, erosion of Great from (characters zooxan­ irregular scleres round tyles about 2 mm Barrier present from the thellae) (1.1–3.5 found, but predomi­ in height, Reef study specimen mm) spirasters nant leaving

QM are usually substrate

G322595) present unharmed

about 2 mm

on upper

side of

shell and 1

mm on

inner side

of shell

Aka sp. beige in no no shaft with multi­ Central present (characters alcohol protruding tylostyles, subtle camerate, Great study from the fistules oxeas only: curve, large, oval Barrier specimen observed, 131 x 5.3 sometimes chambers Reef QM 0.6–1.0 (N = 50) slightly oriented in

G322595) mm matures angular or parallel

only: anisotrope, with shell

132 x 5.7 tips acutely surface, in

(N = 45) pointed 1 (max. 2)

tier(s)

3.4 x 2.3

mm (N =

10),

connecting

canals

0.2–0.5

mm in

diameter

For all the reasons listed above we conclude that C. minuscula is a new species. Together with the finding of C. ensifera in the same specimen as C. minuscula, sp. nov., and with two previously unrecorded observations of C. mucronata and C. schmidti, the present study extends the number of species of the genus Cliona reported from Australia to 11 species, with 10 of them from the Great Barrier Reef (Tab. 4).