Phuket mar. bioI. Celll. Res. Bull. 68: 11-19 (2007)

SCHIZAMMINA ANDAMANA N. SP., A LARGE FORAMINIFERAN(pROTOWA, GRANUWRETICULOSA) FROM TIlE SHELF

WEST OF THAILAND

Ole SecherTeodaI' and Tomas CedhagenZ

lZoological Museum, The Stale Museum ofNatural History, University ofCopenhagen,Universitetsparken JJ, DK~2JOO Copenhagen @,

Denmark rE-mail: ostendal@Snm.ku.dk)J Departmellt ofMarine Ecology, Biologicallnstitllte, University ofAarlllls, Finlondsgode 14,

DK-8200 lrlllls N, Denmark (E-mail: cedlwgen@bioJogy.au.dk)

ABSTRACT: A new species of Scliizammina is described from the mid-shelfofthe Andaman Sea atdepths between 60 and 85 m. The test is agglutinating, up to about 30 mm high, and consists ofdichotomously branching tubes. Tube diameter varies between 0.8 and 1.2 mm. The most closelyrelated species are S. allal/tideae, S. fiwcata, and S. galatlieae. Schizammina andomolla n. sp. wasthe dominant macrofauna organism at some stations and its cytoplasm contained centric diatoms,indicating that it is a filter feeder on sedimenting primary production.

INTRODUCTION

The Thai-Danish BIOSHELF project1996-2000 in the Thai Economic Exclusive Zoneof the Andaman Sea comprised 12 transectsperpendicular to the coast. Sampling in these wascarried out during a number of cruises with the'RN Chakratong Tongyai', using different kindsof gear at depths from 40 10 900 m (Aungtonya etal. 2000, Tendal et al. unpubl.).

During the last two cruises in 2000 it wasnoticed, when sorting some ofthe samples on deck,that a schizamminid foraminiferan lives in the mid­shelf area. Inspection of the literature andcomparison with specimens in the collection ofthe Zoological Museum in Copenhagen ofall earlierdescribed members of the family indicated thatthe BIOSHELF specimens represent a new speciesof the genus Schizammilla.

The species is here formally described asSchizommina olldama"a n. sp. and its occurrenceis discussed and compared to Ihe distributionpanems of other species of the family.

MATERIALS AND METHODS

See Aungtonya et al. (2000) for the list ofsampling stations. The samples were immediately

fixed in formalin (c. 4%) in seawater with anaddition of disodium tetraborate (borax). Theywere later transferred to 80% alcohol.

Individuals intended for histology werefint transferred to distilled water through a fallingalcohol series, then to a 5% aqueous solution ofhydrochloric acid (HCI) for I h in order to removecalcareous particles, and finally to 30%hydrofluoric acid (HF) for 24 h in order to removesiliceous mineral grains. The individuals werewashed in distilled water, brought through a seriesof increasing alcohol concentrations (30, 50, 70,80%) and finally stored in 80% alcohol. They wereembedded in Epon. Sections, 3 /lm thick, weremade using a Jung microtome fitted with a glassknife. They were stained with toluidine blue forabout 2 min and differentiated in 96% alcohol andthe coverslips were mounted with Gurr.

Individuals used for scanning electronmicroscopy were transferred from alcohol toacetone and dehydrated by the use of aD ElectronMicroscopy Sciences 850 critical point drier. Theindividuals were mounted, broken or entire, onstubs and coated with gold-palladium in anEdwards S ISOB sputter coater for 5 minutes, andstudied in a scanning electron microscope(CamScan MaXim 2040 S) at the University ofAarhus, Denmark.

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Phulcet mar. bioi. Cellt. Res. Bull.

Some individuals were dried in order toallow the exttaction ofDNA, but this method failed.

FAMILYSCIIIZAMMINIDAEN0RVANG,1961

Diagnosis: Test free, large (2-10 cm maximumdimension) and either plate-like or formingdichotomously branching tubes. Agglutinated wallthick and firmly cemented. Interior non-septate,consisting of large, nattened space or lumen oftube system. Aperture simple, oval or circular.(After Lee et 01.2000, abbreviation of the originaldiagnosis by N0rvang, 1961).

Scope: Schizamminidae comprises two genera,Schizammina Heron-Alien and Earland, 1929 withseven species and Jlll/iene//a Schlumberger, 1890with three species. A third genus, Astrorhizinellawith one species, A. plO/lata, was described bySaidova in 1970 and placed in the family, a positionkept in her monograph on Pacific benthicForarninifera (1975) and other papers, and byBeljaev (1983, 1989). A. planata has thecharacteristics ofaxenophyophore and wastransferred to the genus Psammina by Tendal(1996), a view confirmed in a reinvestigation ofthe original material by Kamenskaya and Saidova(1998).

History aDd present status of genera andspecies: The first genus of the family (asunderstood nowadays) to be described wasJullienella Schlumberger, 1890 with the typespecies J. Joetida by monotypy. It was found bya French expedtion off West Africa and firstbelieved by the bryozoan specialistJules Jullien tobe a bryozoan. Next came Schizamm;1/a Heron­Alien and Earland, 1929 with type species S.labyrinthica and one other species, S. Jureata,based on material taken by the British' Discovery',offWest Africa as well. Meanwhile, Pearcy (1908)had described Botellina pinnata from materialprovided by the South African 'Pieter Faure' inthe Indian Ocean ofT South Africa. The specieshad a remarkable fate, being divided by N0rvang(1961) into two species, lIIlliellella pearcyiN0rvang, 1961 and SclJjzammino pinnota (Pearcy,

1908). Buchanan (1958; 1960), during a surveyof the fauna off Ghana, found some of the earliernamed species, and described S. arborescens.N0rvang (1961) investigated a rich material partlytaken by the Danish 'Atlantidc' (1945-1946) and'Galathea' (1950-1952) expeditions, partlycollected by the Danish zoologist Th. Mortensenin South Africa in 1929, comprising all the species,and added three new ones, S. atlantideae, S.galatheae and S. reticlllum. A third species ofJullienella, J. zealal/dica, was described fromNew Zealand by Hayward and Gordon (1984).

RFSULTS

Sc!lizammi"a a"dama"a n. sp.(Figs. 1-5)

Material examined:St. C-2. I February 2000. 9°00' N, 97°55' E. 60ffi. Rectangular dredge. Few specimens!fragments. Alcohol.St. J-3. 26 February 2000. 7°15' N, 98°35' E-7°12'N, 98°34' E. 79-79 m. Agassiz trawl. Numerousspecimens/fragments. Alcohol.SI. J-3. 26 February 2000. 7°15' N, 98°35' E. 78m. Sand. Hyperbenthic sledge. Hundreds ofspecimens/fragments, Dry.SI. 1-48. 23 February 2000. 7°14' N, 98°37' E­7°16' N, 98°42' E. 76 m. Hundreds of specimens/fragments (including the holotype and sixparatypes). AlcohoLSI. K-3. 29 February 2000. 7°00' N, 98°41' E­7°01' N, 98°43' E. 83-81 m. Agassiz trawl. Fewspecimens/fragments. Dry.St. L-3. 29 February 2000. 6°45'N, 98°43' E- 6°46'N, 98°41' E. 83-84 m. Agassiz trawl. Fewspecimens/fragments. Alcohol.St. L-3. 29 February 2000. 6°45' N, 98°45 'E. 82­81 m. Sandy mud with shell fragments.Hyperbenthic sledge. Few specimens/fragments.Alcohol.

Description of holotype:The holotype is reddish brown and about

15 mm high. It brancbes dichotomously four timeswith good distance between branching points, anda pronounced thickening of the branches just

13

SCHlZAMMlNA ANDAMANA N. SP. FROM THE SHELF WEST OF THAILAND

below these. Large mineral grains are conspicuouson the test surface (Fig. 2A).

Deposition of type specimens:The holotype is deposited at the Phuket

Marine Biological Center, Reference Collection(PMBC No. 24587). Six paratypes are depositedin the collection of the Zoological Museum, SNM,Copenhagen (ZMUC PRO 11 toZMUCPRO 16).

General description:Largest specimens 2-3 cm in length,

consisting of a repeatedly dichotomously dividedtube system with 5 or 6 dividing points, and 2-6mm between them. Tubes between points slightlyconical with thickest part distally, and 0.8-1.2 mmin outer diameter, mostly just around I mm (Fig.IA-Z).

The branching pattern is characteristic ina way most clearly seen in large specimens (> 1.5cm). The first dichotomy is at a large angle, closeto 90°, the following at the same or a smaller angle.The first two branches curve slightly outwardsand branch again, but the following pairs ofbranches are unequally developed, one of themprolonging the original branch in a gentle curve,the other not dividing, but ending blindly, pluggedwith loose sand grains and fine particles. After 4­5 divisions repeating the pattern of prolongationand curving, the 'main branch' almost forms acircle. The branching pattern is not always thisstrict; the other or both branches in a division maydevelop, resulting in a more straight part of thetest, which itself can be dichotomously dividedseveral times. The branching is essentially in oneplane, but slight twisting ofsingle branches out ofthat plane is seen now and then.

The tube wall consists of quartz grains,up to c. 500 Ilm in diameter, but mostly 200-250Ilm, set in a matrix of organic cement. The largemineral grains extend all the way through the wall.The outer test surface consists of minute mineralgrains which often form a rim or smooth surfacearound the margin of the larger grains (Fig. 3A).Channels for the cytoplasm are found betweensome of the larger mineral grains. Such channels

often expand into larger hollow structures justbelow the test surface, but do not seem to penetratethe surface itself.

The test colour is red~orange¥brown,

except at the tips of the branches where it is white(Fig. 2A, D). The colour changed when individualswere put in a weak hydrochloric acid (HO)solution. A greenish or yellow¥greenisb substancewas given ofIto the liquid. The test turned whitishwith some greenish cement remaining between themineral grains (Fig. 2B). This treatment made iteasier to observe the distribution of the mineralgrains on the outer test surface.

The test lumen is a longitudinal channelalong the centre of the test axis (Fig. 3B, D). Anorganic lining was observed in the lightmicroscopic sections. It is often seen on one sideonly, but in some sections it was found all theway around the cytoplasm (Fig. SA, B). Thedifferences are probably fixation artifacts.

The cytoplasm is not a uniform cell bodyas in many other foraminiferans, but a kind ofcompressed network of numerous compactedgranuloreticulopodia. Consequently, this cellorganisation resembles to some extent the outerpart of the cytoplasm in ToxisarcolI syllsucidicaCedhagen and Pawlowski, 2002 (Fig. 21). Thecytoplasm surface towards the mineral grains istherefore nol smooth but has numerous irregularholes and cavities (Fig. 3C).

The cytoplasm is full of stercomata (Fig.3C) and also contains several centric diatoms. Theolder (lower) parts of the test lumen are entirelyfilled with stercomata and the active cell parts seemto be located at the tips of the branches (Fig. 2B,D).

The nucleus is up 10 100 Ilm in diameter(Fig. SA). Its margin can be irregular and on someof the slides it is located in a structure resemblinga vacuole. However, this is probably a fixationartifact. The nucleus contains numerous nucleoliand most of them arc concentrated towards itsperiphery, as in many other species (e.g., Cedhagenand Pawlowski 2002).

Free granuloreticulopodia of the shapetypical for foraminiferans were found at the tip of

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Phuket mar. bioI. Cellt. Res. Bull.

a branch (Fig. 4).The tcst is usually free from other

organisms but a few species have been observedon it, primarily on the older parts. An undescribedciITiped (Cedbagen and Heeg, unpubl.) andbryozoan colonies are frequently found. Rareepizoans are gastropod egg cases, hydroids, andother agglutinating foraminiferans.

Distribution:The species has so far been recorded

between 6°4S'N and 9°N, and can probably befound as scattered fragments also in samples fromthe two more northern transects. The bathymetricdistribution is, for the lime being, established asthe depths between 60 and 85 rn, on sandy mudwith shell fragments. It can be the dominantmacrofauna organism in some localities (Fig. 2C).

E

yJ

oBA

Figure 1. SchizamminQ andamollQ n.Sp. Specimens collected at the type locality (Andaman Sea,BIOSHELF station J-48). Scale bar:: 5 mm.

15

SCH1ZAMMINA ANDAMANA N. SP., FROM THE SHELF WEST OF THAiLAND

c 0Figure 3. Schizammi/lQ aI/dOli/alia n.Sp. SEM photos. A. Side view of branch with larger mineralparticles surrounded by a matrix of finer particles. The upper part is broken and a part of the cytoplasmfilling the lest lumen is exposed. B. Transverse view ofbroken branch showing the test lumen (TL). C.Cytoplasm surface that was attached to a mineral particle. Its structure is 'spongy', like a compressednetwork of reliculopodia. The round structures are stercomata. D. Enlargement of B showing testlumen (TL) and mineral particle covered by cement (Cm). The central cytoplasm has fallen out butextensions of the cytoplasm (Cp) project between the mineral grains and spread out just under theouter surface of the test. Scale bars: A & B = 100 Ilm; C = 10 Ilm; D = 50 Ilm.

c 0Figure 2. Sc},izamm;nQ andamOIlQ ".sp. A. Holofype, from BJOSHELF station J-48. B. Part of testwhere sediment particles have been dissolved aDd the cement connecting them is stained with toluidineblue. C. Small part ofsledge sample J-48 as it appeared on the deck immediately following collection.D. Tip of branch where sediment particles have been dissolved. The lighter branch tip contains theactive cytoplasm and the brown interior consists of stercomata. Scale bars: A = 5 mm; B & 0 = 500

"m.

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Phuket mar. bioI. Cent. Res. Bull.

Figure 4. Schizammina andamana n.sp. SEM photo of granuloreticulopodia at branch tip. Masses ofdetritus and finer particles are gathered at lhe surface. Scale bar = 100 J.lrn.

Figure S. Schizammina QndamollQ n.sp. Light microscopic images of 'soft partS'. A. N :: nucleuswith numerous nucleoli; S = hole after dissolved sand grain; OL:: organic lining. B. Transverse sectionof branch showing the general organisation of the organism; S = hole after dissolved sand grains; QL= organic lining; Cm = cement with finer mineral particles; Cp "" cytoplasm. Scale bars = 100 J.lrn.

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SCHIZAMMINAANDAMANA N. SP.. FROM THE SHELF WESTOF THAILAND

DISCUSSION

SystematicsSchizammina alldamana agrees with the

diagnosis of the gcnus as given and discussed byNrarvang (1961). The differences to four of theother seven species of the genus, S. arborescensBuchanan, 1958, S. labyrinthica Heron-Alien &Earland 1929, S.pimlata (Pearcy, 1908) and S.reticulum N0rvang, 1961, are very obvious, beingfound in dimensions, branch form or branchingpattern.

Distinguishing between S. andamana andthe laSlthree species, S. atlantideae Nervang, 1961,S. furcata Heron-Alien & Earland, 1929 and S.galatlleae Nrarvang, 1961, is more subtle since thedimensions and branch form are much the same.and the branching patterns vary in a lesspronounced way. It might even be that with moregeographic regions represented by samples and abetter knowledge ofvarialion, the four species mayin the future be united under the name ofS.fllrcafa,a point of view mentioned by Nrarvang (1961) indiscussing relationships between S. fllrcata and S.galathelle. For the time being these slightlymorphologically different but geographic wellseparated populations are considered valid species.

The worst problem for the comparisonof samples comes from the fragmentation causedby the mechanical handling during sampling,washing and sorting. It obscures the branchingpattem, and older and younger parts are not easilydistinguished. Likewise, it can make it difficult toclarify whether one or more species arerepresented in the catch.

The main difference compared to S.atlallfideae is that the latter is a smaller « 20 mmmaximum length) species. The branching patternis furthermore more zig-zag-like because somebranches to both sides remain short andunbranched. The branch diameter in S atlantideaeis 1.0-1.2 mm. The tube wall has several layers,is about 250 ""m thick, and the material is silly(20-50 Jlm grains), with only few finer grains inthe interstices.

Likewise, S. furcara seems to be a smaUerspecies (rarely> 20 nun maximum length). Thebranching pattern is dichotomous with a rather

long distance (ab. 10 mm) between the first twobranching points and smaller but constant distancesbctween the later ones. Branchings are few andpredominantly on one of the sides, the branchesoften curving slightly outwards, although not tothe degree seen in S. andamana. The branchesare coarser than in S. alldamana, the branchdiameter, although varying from 0.8-1.2 mm,mostly being over 1 mm and rarely reaching 1.5mm. The tube wall is single layered, 250-350 Jlmthick, and the material is sandy (250-350 Jlmgrains), with a filling of silty particles in theinterstices on the outside.

S. galatheae is poorly known, tbe originalmaterial being scanty and fragmented. It is of aspecial importance because it, being found offTranquebar, southeast India, is so far thegeographically nearest species to the Andaman Sea.The branching pattern is regularly dichotomouswith short distances bctween branching points.The branch diameter is 1.2-1.6 mm. The tube wallis single layered, 200-250 Jlm thick, and thematerial is sandy (200-250 ""m grains), with theinterstices between grains filled with large amountsof organic cement.

Geographic distributionHayward and Gordon (1984), Nervang

(1961) emphasize that the species ofSchizamminidae all have regional, restricteddistribution areas. The best examples, supportedby numereous records, are Ju/liel/ella foetidafound off West Africa, Schizammilla pillllata and1. pearcyi known from eastern South Africa, andJ. zealandica from off New Zealand.

In the case ofS. andamalla this restrictedregional distribution is the eastern shelf of theAndaman Sea. A qualified guess is tbat the speciesoccurs at mid-shelf depths in the area of seasonalupwelling. The nol1;hem limit ofdistribution couldbe in the Gulf of Martaban, influenced byfreshwater and particle outflow from theIrrawaddy delta. To the south the specialhydrographical conditions of the Malacca Strait(strong currents, effects of breaking internalwaves. change in sediment composition andstructure) might be limiting.

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P}lIIkel mar. bioI. Cent. Res. Bull.

ACKNOWLEDGEMENTS

We thank DANlDA for supporting theBIOSHELF project well. Somchai Bussarawit,Charatsee Aungtonya and their colleagues at theReference Collection of the Phuket MarineBiological Center are thanked for their indefatigable

and extended help. Likewise, the crew of RJV'Chakratong Tongyai' are heartily thanked for theirpatience, helpfulness and good spirits during ourstays onboard. Susanne Perersen, University ofAarhus, helped sectioning and light microscopicpreparations specimen preparation for SEM.

REFERENCES

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Beljaev, G.M.1983.Animals and plants, previously unknown to science, described from the RN 'Vityaz'collections. pp. 268-323, part IV. In: The research vessel 'Vitiyaz' and her expeditions 1949­1979. "Nauka". Moscow. 388 p. (In Russian)

Beljaev, G.M. 1989. Deep-sea oceanic trenches and their fauna. Institute of Oceanology. A cademy ofSciences of the USSR. Nauka, Moscow. 255 p. (In Russian)

Bllchanan, J.B. 1958. The bottom fauna communities across the continental shelf off Accra, Ghana(Gold Coast). Proc. Zool. Soc. Land. 130: I-56.

Buchanan, J.B. 1960. On Julliellella and Schizammi1la, two genera of arenaceous Foraminifera fromthe tropical Atlantic, with a description ofa new species. Journal ofLinnean Society of LondonZoology. 44: 27fj-277.

Cedhagen, T. and J. Pawlawski. 2002. Toxisarcoll sYlIsf/icidica n. gen., n. sp., a large monothalamousforaminiferan from the west coast of Sweden. Journal of Foraminiferal Research. 32: 351­357.

Hayward, B.W. and D.P. Gordon. 1984. A new species of the agglutinated foraminifer Julliellella(Schizamminidae) from New Zealand. Journal of Foraminiferal Research. 14: 11-114.

Heron·Allen, E. andA. Earland. 1929. Some new Foraminifera from the South Atlantic I. Journal oflheRoyal Microscopical Society. 49: 102-108.

Kamcnskaya, O.E. and Kh.M. Saidova. 1998. Redescription of Psammilla plallata (Saidova, 1970), ahadal xenophyophore from the Kurile·Kamchatka Trench. Pp. 125-128. In: A.P. Kuznetsovand D.N. Zezina (eds.) Benthos of the High Latitudc Regions. Moscow. 137 p. (In Russianwith English summaries).

Lee, J.J., J. Pawlowsky, J.P. Debcnay, J. Whittaker, F. Banner, A.1. Gooday, D.S. Tendal, J. Hayncsand W. W. Faber. 2000. Class Foraminifera. Pp. 877-951. In: J.1. Lee, G.F. Leedale and P.Bradbury (eds.): An illustrated guide to the Protozoa, vol. Il. Sociely of Protozoologists,Lawrence, Kansas. 1492 p.

Norvang, A. 1961. Schizamminidae, a new family of Foraminifera. Atlantidc Report. 6: 169-201.Pearcy, EG. 1908. On the genus Botellilla (Carpenter), with a description ofa new species. Transactions

of the South African Philosophical Society. 17: 185-194.Saidova, Kh.M. 1970. Benthic foraminifers in the Kurile-Kamchatka Region based on the data of the

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Saidova, Kh.M. 1975. Bcnthonic Foraminifera of the Pacific Ocean, part I-Ill. Academy ofSciellccsof the USSR. P.P. Shirshov Institute. Moscow, 586 p. (In Russian)

SCHlZAMMINA ANDAMANA N. SP, FROM THE SHELF WESTOFTHA1LAND

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Malllt.Scripr received: August 2005Accepted: September 2007