Morphogenesis of T edania gurjanovae Koltun (Porifera)

GERALD J. BAKUS1

DURING THE COURSE of a study of the marinesponges of the San Juan Archipelago, Wash­ington, the discovery of several specimens ofT edania gurjanovae Koltun (Koltun, 1958 :65 ,fig. 20 ) was of special interest because of theopportunity provided to observe its larval meta­morphosis. This species had been known pre­viously only from the eastern part of the TatarStrait, off Sakhalin, USSR, at depths of 60 to100 m (Koltun, 1958, 1959) . The presentspecimens (No. 30, 58, 90, 112, lot 163) weredredged in depths of 73 to 198 m in PresidentChannel and San Juan Channel, San Juan Archi­pelago , Washington, and now reside in thiswriter's personal collection. An account of themorphology, larval metamorphosis, ecology, andtaxonomy of the Washington population isgiven here.

The suggestions and criticisms offered by Dr.Dixy 1. Ray, Dr. Paul Illg, Dr. Melville Hatch,Dr. Standish Mallory, and Dr. Willard Hart­man are appreciated. Many others contributedto this study . Support was given by the NationalScience Foundation during the summers of1958, 1959, and 1961, and the facilities at theUniversity of Washington Friday Harbor Lab­oratories were used. Translations from Russianto English of both sponge distribution recordsand a description of T edania gurjanovae Koltunwere made by Dr. Gordon Orians.

ADULT MORPHOLOGY

Tedania gurjanovae is an amorphous encrust­ing sponge that shows a tendency to macerateafter being dissected or upon being collected inbroken pieces and preserved. It commonly meas­ures up to 12 mm thick but broken pieces ofNo. 163 attained a size of up to 4 cm by 3 cmby 2 ern. These fragments probably represented

1 Allan Hancock Foundation, University of South­ern California, Los Angeles, California. Manuscriptreceived July 2, 1962 .

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portions of a larger specimen. Specimen No. 90is an encrusting form that intermittently coversplates of Balanus and measures up to 1 mmthick.

The color in life ranges from very light cin­namon to Lido (Maerz and Paul, 1950: pI. 12,D-4, F-5; pI. 13, C-3 ). In alcohol it is beige tonearly white. The species is odorless so far asis known.

The sponge surface may be smooth but oftenis gently to roughly undulated (Fig. 1). It isfeltlike to the touch. The consistency is mod­erately soft and spongy. The surface may beslippery because of detritus and production ofmucus . The dermal anatomy is considerably ob­scured in some preserved specimens and ob­servations on living material are useful. Osculesmay be absent but, if present, are usually numer­ous, irregularly distributed, open at the bodysurface, and measure up to 1 mm in diameter.Some oscules have an accumulation of hastatetornotes around their periphery. Pores areabundant and range from 21 to 68p. in greatestdiameter. In No. 163 they were no longer ob­served after about one hour in the preservative,ind icating that they had closed.

The derm al membrane measures from 20 to25 !L thick. Hastate tornotes (Fig. 2b ), arrangedmore or less perpendicular to the body surface,occur immediately below the dermal membrane.They are loosely distributed and often simulateshort wisps of commercial glass wool. Groups ofabout 10 perpendicular tornotes occasionallyoccur. In a few regions tornotes are almostparallel to the sponge surface. Hastate tornotesand styles ( Fig. 2a) sometimes penetrate up to50 !L beyond the dermal membrane.

The endosomal mesenchyme ranges frombeing loose and fluffy to cotton-like. Style tractsextend toward and sometimes penetrate thebody surface . The tracts measure from 34 to 55!L in diameter and the styles are united by smallamounts of spongin. Numerous hastate tornotesand some styles are found irregularly distributed

T edania gttrjanovae-BAKUS

FIG. 1. Tedania gurianovae Kolrun ( X ~) . Small sample, Specimen No. 58 . Largesampl e, Specimen N o. 112 , encru sting on Modiolus.

59

throughout the endosome. Onychaetes (Fig. 2c­e) occur both scattered and in trich odragmata.Excurrent canals measure up to 500 }.t in diame­ter, whereas smaller canals range down to 83 }.t

in diameter. Canals are moderately numerous.The spicules and their dimensions are listed

in Table 1. The mean dimensions of each spiculecategory of specimen No. 30 and 112 are basedon 10 measurements, and each size range isrepresented by 1 minimum and 1 maximummeasurement.

The styles are often curved. Occasional ju­venile styles were observed. Hastare tornotessometimes have very slightly inflated ends.Onychaetes are straight or slightly curved andoccur in two size ranges. The smaller forms (1)tend to be prominently roughened, whereas thelarger sizes ( II ) are only 'slightly rugose (Fig.2c-e). Juvenile onychaetes also occur. Onemeasurement is 81 X 1 }.t. Onchaetes are oftenfound in trichodragmata measuring from 60 to

100 }.t thick.

ECOLOGICAL NOTES

T edania gurjanovae is collected chiefly froma biotic community of lamellibranchs (mussels )and barnacles. In some specimens the endosomeis contaminated by a few sand grains .

Biological associates include: N o. 30, T.gurjanovae partly encrusting on barnacles (B ala­ntts) with another sponge (Halichondria ) , allof which are encrusting on the carapace of acrab; No. 58, T . gurjanovae encrusting arounda barnacle (Balanus) with attached polychaetetubes ( Fig. 1) ; No . 90, T . gurjanovae encrust­ing on barnacles (Balanus ); No. 112, a fewforaminifera on the sponge surface, T. gurjano­vae encrusting on a mussel (Modiolus modiolusLinnaeus) and surrounding a barnacle (Balanus)and several large polychaete tubes (Fig. 1);No. 163, one large endosomal polychaete tube.Koltun ( 1959: 156) reported that Tedania gur­janovae is frequently found encrusting on thevalves of scallops (Chlamis).

60

Author

Specimen N o.

D epth and Habit at

Style :LengthWidth

H astate Tornore :LengthWidth

Onychaete I :LengthWidth

Onychaete II :LengthW idth

PACIFIC SCIENCE, Vol. XVIII, January 1964

TABLE 1

SPICULE MEASUREMENT (in p.) OF Teda nia gurjano vae KOLTUN

Bakus Bakus Kolrun, 1958

30 112 2974

192 m rock-shell bottom 110-128 m rock-shell bottom shell bottom

296-324-33 5 318- 340- 373 260-3439- 11- 12 10-12-13 8-1 4

204- 226-24 8 222- 236-252 202- 2805-6-7 4- 6-7 4- 8

40-75- 91 58-69-89 77- 1572.2-2.7-3.5 2.2-2.6-3.0 3-4

142-168- 265 150- 174-265 197- 3121.5-1.7-1.8 1.2-1.4-1.6 2

LARVAL METAMORPHOSIS

The dissection of a specimen of a sponge(lot No . 163 ) .pn",26 July 1959 revealed livingembryos attached by the posterior end to theparental mesenchyme ( Fig. 3a) . Motile ciliawere distributed over the entire surface exceptfor the posterior pole. A minute region at theanterior end was very slightly pigmented. Bothembryos and subsequently released larvae werecream colored. The larvae were typical paren­chymulae, roughly oblong in shape, and meas­ured from 500 p. long by 332 p. in mid-lengthdiameter to 576 p. by 433 p: In released larvaethe anterior pole had very short cilia; cilia werelacking on the posterior end (Fig. 3b). Else­where the cilia were longer and of approximatelyequal dimensions. Several larvae contai ned oneor two visible parental ( ? ) spicules passingthrough their mesenchyme . This had no ap­parent effect on their swimming behavior. Thepresence of spicules in larvae of Demospongiaeis common . Ali (1956 :558-559 ), in a study onthe development of Lissodendoryx similis Thiele,found that the larvae conta ined both micro­scleres and megascleres and in greater densitythan found in the adult.

Larval spiculation was studied in preservedembryos. A mature embryo, ready to leave the

parent sponge, contains several hundred ony­chaetes 'of both adult size groups, bur . the ma­jority are of the smaller category (I) . More­over, there are about 25 to 35 conspicuouslytapering and mildly echinated acanthosryles thatmeasure about 120 p. in length by 10 p. in basalshaft diameter or 5 p. in mid -shaft diameter.Both onychaetes and acanrhosryles are concen­trated into a dense packet near one pole, thoughmany onychaetes occur elsewhere throughoutthe larva. Since the larval acanthostyles ap­parently do not occur in the adult they mayundergo further change to the stylote configura­tion. The late embryonic spicule distr ibution of

.T edania gurjanovae looks something like that ofthe T . charcoti embryo as figured by Burton(1932:362, fig. 471). Burton (1932 :361) re­poned that acanrhostyles are the first spiculesto appear in embryos of T . charcoti Topsentand that they become convened into smoothstyles as developm ent progresses. Further growthis indicated by a segregation of styles in a neatbundle at the "aboral pole of the embryo" anda rapid increase in numbers of rhaphides . Burtonbelieves that rhaphides are probably the pro­totypes of adult onychaetes.

The larvae swam with the anterior end di­rected forward and completed spiral gyrations .

Tedania gurjanovae-BAKUS

One larva was observed swimming with theposterior pole directed forward. It was notunusual for natatory parenchymulae to pausefor several minutes on the bottom of the glassfinger bowl.

There appeared to be no obvious negat iveor positive phototaxis. Levi (1956: 119 ) notedthat the larvae of Haliclona indistincta ( Bower­bank ) showed no particular taxis. Larvae ofLissodendoryx similis (Ali, 1956 :557) andMycale syrinx ( 0 . Schmidt ) (Wilson, 1935:287 ) have shown negative phototaxis. Whetheror not sensory cells are associated with thisbehavior is unknown at the present time (Jones,1962 :13-14). Further observations on larvalbehavior are discussed by Jones (1962 :13-14,49- 50) . Ali (loc. cir.) and Wilson (loc. cit.)both reported that some sponge larvae swimupwards then adhere to the water surface filmand eventually die or disperse into scatteredfragments and disintegrate. .

Four larvae were removed from their attach­ment to the parent and placed in a finger bowlof sea water to observe-settling behavior. Twoof the larvae were fixed to the bottom of thefinger bowl 6 hr later; of the remaining larvaeone appeared to be caught in the water surfacefilm, the other attached to the bottom of thefinger bowl after about the 7th hr. A few larvaeappeared to have a slightly invaginated pos­terior pole just prior to fixation on the glasssubstratum ( Fig. 3c) .

Larvae of Lissodendoryx similis (Ali, 1956:575 ) commence attachment to a substratum

61

after about 40 hr ; almost 24 hr of this periodis spent swimming near the water surface. Sexuallarvae of Esperella sordida ( Bowerbank ) (De­lage, 1892: 370) swim for about 20 hr, whereasthose of Mycale syrinx remain mot ile for 1 to3 days (W ilson, 1935:295 ). Some larvae ofMycale syrinx rotate on a substratum for aslong as 10 days before fixation. The duration ofthe larval peri od of Halisarca metschnik oviLevi is 2 days, and that of Halisarca dujardiniJohnston, less than 1 day (Levi, 1956 :79).Asexual larvae of Esperella fibrexilis Wilson(W ilson, 1894: 298 ) swim freely for 1 to 2days, whereas, those of Callyspongia diffusa( Ridley ) (Sivaramakrishnan, 1951 :287) shownatatory activities for only 6 to 8 hr. It is knownthat within a single species of marine animalthe planktonic period varies considerably withtemperature, the availability of food, and theproper substratum (Thorson, 1957 :482 ; Moore ,1958 :314 ). T edania gurjanovae apparently hasa brief swimming period, at least under labora­tory conditions.

In the present study, as a parenchymula larvaattached to the glass substratum by the anteriorend, the ciliary beat slackened in frequ ency andwithin 10 to 15 min all cilia appeared to bemotionless. Approximately 30 min after fixationthe typical larval habitus became completelydisorganized. The mesenchymal cells collapsedfrom their original position and spread into aflat light-yellow circular plate measuring about600 p- in diameter ( Fig. 3d ). Segregation andspreading of cells cont inued. At 3 hr of age the

c==-----------::=::> a

c::=================::=:: b

~ .. .~.. .. ,." c d

. .~e

FIG. 2. Spiculati on of T edania gurjanouae Koltun. a, Style, X 37 5; b, tornote, X 375; C, onychaete I,X 560; d, end of onychaete I, X 1260 , note the echinations; e, onychaete II , X 375 , note the comparativelyfiner echinatio ns.

62 PAOFIC SOENCE, Vol. XVIII, January 1964

b O c d e

FIG. 3. Larvae and metamorph osis of Tedania gur;anovae Koltun. a, Sketch of a living embryo obliquelyjoined to parent al mesenchyme, X 32. It is nearly ready to detach as a parench ymula larva; b, Sketch of anatatory parenchymula, lateral view, X 46. N ote the parental ( ? ) style and onychaete piercin g the larva.c, Sketch of a parenchymula showing a slightly invaginated posterior pole, lateral view, X 16. d, Sketch show­ing from above a spherical mass of mesench ymal cells (pa tte rn ) resulting fro m fixation of a larva to a glasssubstratum for about 30 min, X 14. e, Sketch mad e from above the same larva after a fixation period of 3hr, X 18. Mesenchymal cells occupy the cortical region ( patte rn ) and are encompassed by a transparent bandof syncytium-like protoplasm.

disc measured 1065 ft in diameter and consistedof an internal subspherical light-yellow mass800 ft in diameter surrounded by a transparentband of protoplasm containing no observablecell boundaries ( Fig. 3e) . The rate of develop­ment in T edania gur jano1!ae during the earlystages of metamorphosis seems to be consider­ably more rapid than that described for Lis­sodendoryx similis (Ali, 1956 ) . The length oftime necessary for T edania gurjanovae to reachhistological maturity was not determined in thepresent study. Wilson (1935 :295) reported thatthe formation of choanocyre chambers and canalsin some cultures of M ycale syrinx occurredwithin 3 to 4 days after discharge of the larvaefrom the parent, and Levi (1956:81) notedthat the histogenesis of Halisarca du jardini intoa functi onal rhagon took about 2 days afterlarval fixation.

At 1 day of age the juvenile encrustationrevealed several small styles that were irregularlyscattered in the mesenchyme. These may stillhave been the embryonic acanthostyles, butwith the 112.5 X magnification of a dissectingmicroscope echinations were not apparent. At7 days of age the styles were showing someevidence of orientation perpendicular to thesubstratum. After 13 days most of the styles,especially in the center of the disc, were orientedperpendicular to the substratum. Hastate tor­notes were observed for the first time . A verythin dermal membrane with scattered mesen­chymal cells constituted the sponge surface.The endosome was translucent and archeocyteswere concentrated at the sponge base and around

perpendicular megascleres. The sponge had al­most doubled in thickness since the seventhday of attachment. No oscules were observed.At 19 days of age the colonies were almostunchanged except for increased thickness . Onespecimen had formed a fistule about 1.5 mmhigh.

The colonies were last observed on 28 August1959 (at an age of 33 days). They had remainedrelatively minute. The largest two sponges meas­ured roughly 1.5 mm by 0.75 mm and 2.0 mmby 0.75 mm in diameter. Their thickness did notexceed 2 mm. N one of the specimens showedevidence of oscule form ation. Perhaps in culturethese sponges remained in a diminutive condi­tion because their environmental conditionspresent in the laboratory differed from thei rnatural deeper water habitat.

TAXONOMIC DISCUSSION

The holotype of T edania gurjano vae Koltunis specimen N o. 2974, Zoological Institut, Akad­ernia Nauk, Leningrad, USSR. The habitat,habitus , and natural color of this species asreported by Koltun (1958 :65 ) closely resemblethat of local San Juan representatives. Thespicule morphology and size are also very simi­lar to local forms except that the onychaetes arelonger and more rugose in the Russian specimen.The endosomal anatomy is too briefly describedto make a useful comparison. Koltun (1959 :156) states : "The main skeleton is in appear­ance like an irregular net of organized bund lesof spines."

Tedania gurjanovae-BAKUS

Burton (1932:345) recognized the VancouverIsland specimen of Tedania tragilis Lambe (seeLambe, 1895:136) as 1 of the 24 valid speciesof its genus . De Laubenfels (1961 :197) col­lected Tedania tragilis from a depth of 50 to60 m, northeast of Blakeley Island (San JuanArchipelago) . I examined the holotype (USNMNo. 7401) of Tedania tragilis Lambe and foundthat it differs from specimens discussed in thispaper in the following features: the spiculationis larger and onychaetes are often erraticallycurved. The short-size category of onychaetes islacking. The hastate tornotes often have slightlyinflated ends that may be microspined. Sometornotes have one end hastate and the otherrounded or subtylote. Style tracts are moreabundant and interstitial styles are irregularlydistributed, although some meshes do occur.The holorype is dry and exceptionally fragile.The specimens from the San Juan Archipelagodescribed in this paper are placed tentatively inTedania gurjanovae Kolrun,

SUMMARY

The adult morphology, larval metamorphosis,biological associates, taxonomic status, and dis­tr ibution of T edania gurjanovae Koltun are de­scribed. This species has been dredged from arock-shell substratum on the continental shelfand apparently ranges from the San Juan Archi­pelago in the northeast Pacific to Tatar Straitin the northwest Pacific. The larval nararoryperiod is 6 to 7 hr . Metamorphosis involves acomplete collapse of the larva into an amorphousmass somewhat platelike in over-all shape, withinwhich many cells can be seen. Segregationoccurs; this results in a core of inner cells(archeocytes) and an outer transparent layer ofprotoplasm not shown definitely to be cellular.Development continues to a miniature adult­like habitus which is reached after about 2 to 3weeks.

REFERENCES

ALI, M. A. 1956. Development of the monaxo­nid sponge Lissodendoryx similis Thiele. J.Madras Univ. B, 26(3) :553-581.

BURTON, M. 1932. Sponges. Discovery Reports6:237-392.

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DELAGE, Y. 1892. Ernbryogenie des Eponges .Developpement Post-larvaire des EpongesSiliceuses et Fibreuses Marines et d'EauDouce. Arch. Zool. Experim. 10(2) :345­498.

DE LAUBENFELS, M. W. 1961. Porifera of Fri­day Harbor and vicinity. Pacific Sci. 15(2) :192-202.

JONES, W. C. 1962. Is there a nervous systemin sponges? BioI. Rev. 37:1-50.

KOLTUN, V. M. 1958. Siliceous sponges (Cor­nacuspongida) from the southern region ofthe Kurile Islands and waters , washed up onsouthern Sa k h alin. Issledovania Dalnevos­tochnh Morei SSSR 5:42-77. [In Russian.]

--- 1959. Silicospongin sponges of theNorthern and Far Eastern Seas of the USSR­Keys to the fauna of the USSR. OpredeliteliPo Faune SSSR 67: 1-227. (In Russian .]

LAMBE, 1. M. 1895. Sponges from the westerncoast of North America. (1894) Proc. andTrans. Roy. Soc. Can. 12 (4) :113-138 .

LEVI, C. .1956. Etude des Halisarca de Roscoff.Embryologie er Systematique des Dernospon­ges. Arch . Zool. Exp. Gen . 93:1-181.

MAERZ, A., and M. R. PAUl. 1950. A Dic­tionary of Color. McGraw-Hill Book Co., Inc.,New York. 208 pp.

MOORE, H . B. 1958. Marine Ecology. J. Wileyand Sons, New York. 493 pp.

SIVARAMAKRISHNAN, V. R. 1951. Studies onearly development and regeneration in someIndian marine sponges . Proc. Indian Acad.Sci. 34:273-310.

THORSON, G. 1957. Bottom communities. In:Hedgpeth, J. W. (ed.), Treatise on MarineEcology and Paleoecology, Vol. 1. Ecology,Geol. Soc. Amer . Mem . 67:461-534.

WILSON, H . V. 1894. Observations on the gem ­mule and egg development of marine sponges.J. Morph. 9:277-406.

--- 1935. Some critical points in the meta­morphosis of the halichondrine sponge larva.J . Morph. 58:285-345.