The Liagoraceae (Rhodophyta: Nemaliales) of the Hawaiian Islands.1: First Record of the Genus Gloiotrichus for Hawai'i and

the Pacific Ocean1

John M. Huisman and Isabella A. Abbott2

Abstract: Gloiotrichus fractalis Huisman & Kraft is documented for the first timefrom the island of Hawai'i, Hawaiian Islands, which also represents the firstrecord for the Pacific Ocean. The single specimen on which the record is basedis 12 cm in height, extremely mucilaginous, with percurrent primary axes andirregularly arranged lateral branches. Carpogonial branches are borne on thebasal one to three cells of cortical fascicles; when mature they are five to eightcells long and straight. Before fertilization, cells of the carpogonial branch pro­duce several lateral branches similar in morphology to cortical filaments. Afterpresumed fertilization the zygote (= postfertilization carpogonium) dividestransversely and gonimoblast initials are produced trom both of the resultantcells. Mature carposporophytes are spherical, with terminal carposporangia anda fusion cell formed from the cells of the carpogonial branch and basal cells oflateral filaments. The Hawaiian specimen is identical in virtually all respects tothose from the Indian Ocean type locality in the Houtman Abrolhos Islands ofWestern Australia.

THE MONOTYPIC GENUS Ghiotrichus waserected by Huisman and Kraft (1994) forplants collected from the central west coast ofAustralia. Distinguishing features include anextremely mucilaginous habit, elongate car­pogonial branches bearing secondary lateralbranches, production of the gonimoblastfrom both cells of the transversely dividedzygote, and formation of a postfertilizationfusion cell comprising cells of the carpogonialbranch. Thus far the genus is known onlyfrom the Pelsaert and Easter groups of theHoutman Abrolhos, a cluster of mainly coraloffshore islands situated at a latitude of 28­29° S (see Huisman 1997).

Recently a specimen referable to Gloio­trichus and seeIningly identical to G. fractalis

1 Research supported by the David and Lucile Pack­ard Foundation. Manuscript accepted 25 October 2002.

2 Department of Botany, University of Hawai'i at.Manoa, 3190 Maile Way, Honolulu, Hawai'i 96822.

Pacific Science (2003), vol. 57, no. 3:267-273© 2003 by University of Hawai'i PressAll rights reserved

was collected from the island of Hawai'i inthe Hawaiian Islands. This represents the firstrecord of the genus outside the immediatevicinity of its Indian Ocean type locality. Adescription of the Hawaiian specimen and acomparison between it and the Australianspecimens are presented here.

This contribution is the first in a proposedseries describing various members of theLiagoraceae of Hawai'i. All will follow a sim­ilar format, and some will include emendedgeneric and species descriptions.

MATERIALS AND METHODS

The specimen was collected while scuba div­ing. Portions of the plant for InicroscopicalexaInination were decalcified in IN HCI,stained in 1% aniline blue, then mounted in a50% corn syrup (Karo, CPC International)solution and lightly squashed to separate thefilaments. Herbarium specimens and slidepreparations are held in BISH. Herbariumabbreviations follow Holmgren et al. (1990).Slide preparations were examined with a Ini­croscope (Olympus BX3) and photographedusing a digital camera (Olympus Dll).

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RESULTS

Genus Gloiotrichus Huisman & KraftEur. J. Phycol. 29: 74 (1994).Type: G. fractalis Huisman & Kraft

GENERIC DESCRIPTION: Thalli (game­tophytes) upright, epilithic, soft, and lubri­COUS, with a discoid holdfast and percurrentaxes with regularly or irregularly producedlateral branches. Axes terete, multiaxial, ofuniform diameter with attenuate apices, andlightly calcified around the medulla. Medullacomposed of longitudinal filaments and cor­tex of subdichotomously divided anticlinalfilaments with occasional rhizoidal filamentsissuing from basal cells. Distal cells of corticalfascicles ellipsoid to spherical, proximal cellselongate. Plants monoecious. Spermatangialbranches arise on subterminal cortical cells,become much branched, and when maturebear terminal spermatangia. Carpogonialbranches arise on basal 1-3 cells of corticalfascicles, are 5-8 cells long, straight, and bearsecondary lateral filaments of similar appear­ance to normal cortical filaments on mid­branch cells. Postfertilization carpogonium(= zygote) divides transversely, with bothderivatives producing the gonimoblast. Car­posporophytes compact, with apical carpo­sporangia and a fusion cell formed from cellsof carpogonial branch and basal cells of sec­ondary lateral filaments. Tetrasporophytesunknown.

Gloiotrichus fractalis Huisman & KraftEur. J. Phycol. 29: 74 (1994).

SPECIMEN EXAMINED: 'Au'au Pt., Ha­wai'i, epilithic at 15 m depth,S April 2002,M. Hughes, KM 5414 (Figure 1).

HABIT AND VEGETATIVE STRUCTURE: Thethallus is 12 em high, extremely lubricous,and has several percurrent axes that are ir­regularly laterally branched (Figure 1). Allaxes are terete, lightly calcified around themedulla, and with calcification suspended inthe mucilage (Figure 2), with the main axes1-2 mm diam. and lateral branches to 1 mmdiam. The medulla is composed of longitudi-

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nally aligned filaments (Figure 3) plus adven­titious filaments that arise from the basal cellsof cortical fascicles. Cells of the medullaryfilaments are elongate, 10-12 /lm diam. nearthe apex, and up to 170 /lm diam. in olderportions. Cortical fascicles are 200-300 /lmlong and are borne on subisodiametric basalcells; they are subdichotomously branched,with the distal two to four cells unbranched(Figure 4). Lower cells of cortical fascicles areelongate, with progressively more distal cellsbecoming ellipsoid or subspherical (to 25 /lmdiam.), the penultimate cell generally thebroadest of the filament, and the apical cellsubspherical (Figure 4). Small cells withdarkly staining contents (Figure 4) or hairsare borne singly or in pairs on the apical cellsof cortical filaments. These appear to be reg­ularly shed because remnant walls are gener­ally visible (Figures 4, 5). Cortical filamentsthat arise from adventitious filaments areoften unbranched and more slender thantypical filaments. Most cells have a deeplylobed plastid and a conspicuous central py­renoid (Figure 5).

REPRODUCTION: The specimen is mo­noecious, with ovoid spermatangia 3-5 /lmin length formed on much-divided branchesarising from the outer cells of cortical fila­ments (Figure 6). Carpogonial branches(Figure 7) are straight, five- to eight-celled,and arise from the basal or suprabasal cells ofcortical fascicles, or directly from rhizoidalfilaments (Figure 8), with most cells proximalto the carpogonium and hypogynous cells ul­timately bearing lateral filaments resemblingvegetative filaments (Figure 9). Initiation ofthe lateral filaments begins in the proximalportion of the branch and progresses distally.Generally the cell below the carpogonium(= hypogynous cell) is slightly broader thanlower cells and remains naked (Figure 9). Thelower cells of the carpogonial branch oftenbear secondary carpogonial branches, partic­ularly when the primary carpogonial branchhas not been fertilized. After presumed fertil­ization the zygote divides transversely. Theorigin of the gonimoblast was not clearly seenbecause no immediate postfertilization stageswere present in the material and once post­fertilization fusion of the carpogonial branch

Gloiotrichus in Hawai'i . Huisman and Abbott

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FIGURES 1-6. Gloiotrichus fmctalis Huisman & Kraft. All KM 5414. 1. Herbarium preparation of specimen fromHawai'i. Scale = 2 em. 2. Apex of branch showing calcification around the medulla and lying loose in the mucilage.Scale = 500 ~m. 3. Apex of decalcified branch showing multiaxial construction and anticlinal cortical fascicles.Scale = 100 ~m. 4. Detail of cortical filaments. A slightly offset small cell can be seen at the apex of one filament (ar­row) and empty walls where these cells have been shed (arrowhead). Scale = 40 ~m. 5. Detail of small cells at apices ofcortical filaments. Scale = 20 ~m. 6. Spermatangial clusters formed at the apices of cortical filaments. Scale = 40 ~.

cells commences it is difficult to follow theprocess. Based on the morphology of theprefertilization carpogonial branch, in whichthe hypogynous cell is generally naked andslightly broader than lower cells (see arrow in

Figure 9), and assuming the cells indicated inFigures 10 and 11 are also the hypogynouscells, it appears that the gonimoblast arisesfrom both cells of the divided zygote (i.e., allcells distal to the hypogynous cell). A fusion

Gloiotrichus in Hawai'i . Huisman and Abbott

cell (Figures 10-12) is formed from cells ofthe carpogonial branch and lower cells ofthe lateral branches, with the distal portionof the lateral branches often being shed.Mature carposporophytes (Figure 12) are185-250 !lm diam., with terminal, clavate toobovoid carposporangia measuring 30-40 by15-20 !lm.

DISCUSSION

The Hawaiian specimen of Gloiotrichus frac­talis displays all of the features consideredcharacteristic for the genus, including theproduction of an elongate carpogonial branchthat bears lateral branches of normal corti­cal appearance and the formation of a fusioncell comprising the cells of the carpogonialbranch (Huisman and Kraft 1994, Huisman2000). Unfortunately the immediate post­fertilization development could not be ob­served clearly in our material, which hadabundant carpogonial branches but very fewcarposporophytes, so the production of thegonimoblast from both cells of the trans­versely divided zygote could not be ascertainedwith absolute certainty. Because Huisman andKraft (1994) regarded this feature to be ofgeneric significance, an explanation of thestages observed in the Hawaiian specimen iswarranted. The development of the carpogo­nial branch includes the production of lateralbranches from cells proximal to the hypogy­nous cell (= the cell below the carpogonium),as can be seen in Figure 9 (the arrow indicatesthe hypogynous cell). If the stages of post­fertilization development follow those de­scribed by Huisman and Kraft (1994), thezygote would subsequently divide transverselyand the gonimoblast arise from both of thecells produced. Thus later stages would showa naked cell (the hypogynous cell) subtending

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the gonimoblast. If we follow the progress ofthe hypogynous cell in our material, it ap­pears to subtend the gonimoblast (Figure 11,arrow indicates hypogynous cell), whichtherefore has arisen from both cells of thedivided zygote and the process agrees withthat described by Huisman and Kraft (1994).Some potentially confusing stages are pres­ent, however. The young carposporophytedepicted in Figure 10 shows a carpogonialbranch with two naked cells below the goni­moblast, which, if the proximal of the twonaked cells (arrowhead) is interpreted as thehypogynous cell, would suggest that thegonimoblast is arising from only the distal cellof the divided zygote (i.e., the cell indicated isthe proximal cell of the divided zygote). Whatappears to be shown in Figure 10, however, isthat the laterals on the subhypogynous cellhave been shed (their original point of at­tachment is indicated by a couple of pro­trusions). Thus the cell indicated in Figure 10is the hypogynous cell and the gonimoblast isarising from all cells distal to it. All of thepostfertilization stages seen in our material,therefore, can be interpreted as agreeing withthe description of Huisman and Kraft (1994).

As indicated by Huisman and Kraft (1994),Gloiotrichus shows similarities to TrichogloeaKiitzing, but differs in the morphology of thelateral branches on the carpogonial branch,with those of Trichogloea being highly modi­fied (Huisman and Kraft 1994: fig. 11, Abbott1999: figs. 18C,E, Huisman 2000:35), whereasthose of Gloiotrichus are similar to vegetativefilaments (Huisman and Kraft 1994: figs. 7-9,Huisman 2000:31), and also in the productionof the gonimoblast in Trichogloea from bothcells (as opposed to only the upper cell inGloiotrichus) of the divided carpogonium.Moreover the architecture of the sperma­tangial branches further distinguishes Gloio-

FIGURES 7-12. Gloiotrichus fractalis Huisman & Kraft. All KM 5414. 7. Developing carpogonial branches.Arrow indicates an immature branch. Scale = 40 Ilm. 8. Carpogonial branch arising from a rhizoidal filament.Scale = 40 Ilm. 9. Mature carpogonial branch with lateral filaments. Arrow indicates the hypogynous cell. Scale = 40Ilm. 1O. Young gonimoblast at an early stage of fusion-cell formation. Arrow indicates the hypogynous cell. Lateralbranches on the subhypogynous cell (arrowhead) apparently have been shed. Scale = 20 Ilm. 11. Young gonimoblast ata stage comparable with that shown in Figure 9. Arrow indicates the hypogynous cell. The lateral branches on thesubhypogynous cell are still present. Scale = 40 Ilm. 12. Mature carposporophyte with fusion cell (arrow) formed fromthe cells of the carpogonial branch. Scale = 40 Ilm.

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trichus from Trichogloea, with those of the lat­ter produced in whorls on intercalary corticalcells.

Huisman and Kraft (1994) designated thesmall cells that are formed distally on theouter cortical cells (see Figure 5 and cellsindicated in Figure 4) as "glandular" cellsdue to their appearance resembling that of"gland" cells (also known as vesicular cells) inother red algae. However, because no glan­dular function has been demonstrated forthese cells it is perhaps best not to conferthem with any particular role. As can be seenin Figure 4 (arrowhead), the contents of thesecells are often shed, leaving behind a remnantwall. This type of behavior is most often seenin reproductive cells such as monosporangia.Although we cannot speculate as to the roleof these cells, a couple of observations arepertinent. First, their contents are homoge­neous in appearance, with perhaps only a fewsmall vacuoles, and stain darkly (compare thedistal cells shown in Figure 5 with those sub­tending them). This type of appearance issuggestive of what are known as "gland" cellsin other red algae (e.g., Coelarthrum [seeHuisman 1996]), but (in Gloiotrichus at least)it is also found in actively growing cells suchas the apical cells of developing carpogonialbranches. Second, in identical positions onthe Australian specimens of Gloiotrichus (butnot well developed in the Hawaiian plant) areoccasional hairs. These are elongate, withdistally inflated tips containing cytoplasmidentical in appearance to that of the smallcells. At the base of the hairs are often rem­nant wall collars, indicating that the hairseither arise within the remnant walls of thesmall cells or are themselves shed, leavingbehind a portion of their wall. These smallcells and hairs are present in many membersof the Liagoraceae (e.g., see Huisman andKraft 1994: fig. 30, where remnant walls arevisible on outer cells of Ganonema helmin­thaxis Huisman & Kraft; and Huisman andSchils 2002: fig. 19, where the cells can beseen on Trichogloea requienii (Montagne)Kiitzing). Given the similarities between thecells and the hairs, it is possible that they areperforming the same function. If so, it is un­likely that they are reproductive cells, which

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never take the form of hairs. What thenmight their function be? We cannot spec­ulate, but an ultrastructural examination orchemical analysis of these cells would cer­tainly be of interest.

Gametophytes of Gloiotrichus fractalis inAustralia are found during the austral springand summer, presumably overwintering asthe (as yet unknown) filamentous tetra­sporophyte. The Hawaiian plant was like­wise collected during the boreal spring. Thegrowing periods of the two collections are,therefore, not synchronous. Given this, plusthe large geographical separation of the Ha­waiian and Australian collection localities, itis almost certain that they are reproductivelyisolated. Molecular and culture studies wouldbe of interest in ascertaining whether thisisolation has been long-standing and hasresulted in reproductive incompatibility orgenotypic variation not expressed morpho­logically, or conversely whether either popu­lation is a recent introduction.

ACKNOWLEDGMENTS

We thank Marc Hughes, the collector of thespecimen, and Karla McDermid (Universityof Hawai'i at Hilo) for bringing it to ourattention. Gerry Kraft (University of Mel­bourne) reviewed the manuscript and madenumerous helpful suggestions.

Literature Cited

Abbott, I. A. 1999. Marine red algae of theHawaiian Islands. Bishop Museum Press,Honolulu.

Holmgren, P. K., N. H. Holmgren, and L. C.Barnett. 1990. Index herbariorum. Part I:The herbaria of the world. 8th ed. NewYork Botanical Garden, New York [Reg­num Vegetabile, Vol. 120].

Huisman, J. M. 1996. The red algal genusCoelarthrum Borgesen (Rhodymeniaceae,Rhodymeniales) in Australian seas, includ­ing the description of Chamaebotrys gen.nov. Phycologia 35:95-112.

---. 1997. Marine benthic algae of theHoutman Abrolhos Islands, Western Aus-

Gloiotrichus in Hawai'i . Huisman and Abbott

tralia. Pages 177-237 in F. E. Wells, ed.The marine flora and fauna of the Hout­man Abrolhos Islands, Western Australia.Western Australian Museum, Perth.

---. 2000. Marine plants of Australia.University of Western Australia Press,Nedlands.

Huisman, J. M., and G. T. Kraft. 1994.

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Studies of the Liagoraceae (Rhodophyta)of Western Australia: Gloiotrichus fractalisgen. et sp. nov. and Ganonema helminthaxissp. nov. Eur. J. Phycol. 29:73-85.

Huisman, J. M., and T. SchiIs. 2002. A re­assessment of the genus Izziella Doty(Liagoraceae, Rhodophyta). Cryptogam.Algol. 23:237-249.