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The Prostrate System of the Gelidiales: Diagnostic and Taxonomic Importance

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The Prostrate System of the Gelidiales: Diagnostic and Taxonomic Importance Article in press - uncorrected proof Botanica Marina 49 (2006): 23–33 ᮊ 2006 by Walter de Gruyter • Berlin • New York. DOI 10.1515/BOT.2006.003 The prostrate system of the Gelidiales: diagnostic and taxonomic importance Cesira Perrone*, Gianni P. Felicini and internal rhizoidal filaments (the so-called hyphae, rhi- Antonella Bottalico zines, or endofibers) (Feldmann and Hamel 1934, 1936, Fan 1961, Lee and Kim 2003) and a triphasic isomorphic life history, whilst the family Gelidiellaceae (Fan 1961) is Department of Plant Biology and Pathology, University based on 1) the lack of hyphae and 2) the lack of sexual of Bari-Campus, Via E. Orabona 4, 70125 Bari, Italy, reproduction. Two distinct kinds of tetrasporangial sori, e-mail: [email protected] the acerosa-type and the pannosa-type, were described * Corresponding author in the genus Gelidiella J. Feldmann et Hamel (Feldmann and Hamel 1934, Fan 1961). Very recently, the new genus Parviphycus Santelices (Gelidiellaceae) has been pro- Abstract posed to accommodate those species previously assigned to Gelidiella that bear ‘‘pannosa-type’’ tetra- Despite numerous recent studies on the Gelidiales, most sporangial sori and show sub-apical cells under- taxa belonging to this order are still difficult to distinguish going a distichous pattern of division (Santelices 2004). when in the vegetative or tetrasporic state. This paper Gelidium J.V. Lamouroux and Pterocladia J. Agardh, describes in detail the morphological and ontogenetic two of the most widespread genera (which have been features of the prostrate system of the order with the aim confused) of the Gelidiaceae, are separated only by basic of validating its diagnostic and taxonomic significance. features of cystocarps (cf. Santelices 1988, 1990). The Observations were made on fresh, liquid preserved and genus Pterocladiella Santelices et Hommersand was later cultured thalli. The morphology of the attachment system established to segregate from Pterocladia those species and the characteristics of rhizoid ontogeny have proven with distinct carposporophyte developmental characters to be useful diagnostic and taxonomic characters. Spe- (Santelices and Hommersand 1997). cies belonging to Gelidium, Pterocladia and Pterocla- However, the presence of internal rhizoidal filaments in diella bear true attachment organs consisting of cells of some thalli or axes of the Gelidiaceae has been ques- both exogenous and endogenous origin. In the family tioned, so it should not be taken for granted (Perrone Gelidiellaceae, in contrast, attachment to the substratum 1994). In certain habitats, in fact, both small thalli and is effected by single independent exogenous rhizoids. small species belonging to either Gelidium or Pterocla- The attachment rhizoids of the Gelidiales, both exoge- diella are known to assume a prostrate habit bearing nous and endogenous, are of the same cell type, and are uprights with a few, or, very often, without any internal the so-called hyphae, historically considered typical of rhizoids at all, such as Pterocladiella melanoidea the family Gelidiaceae only. A new subdivision of the (Schousboe ex Bornet) Santelices et Hommersand and Gelidiales into three families is proposed here, with the G. pusillum (Stackhouse) Le Jolis on southeastern coasts amendment of both Gelidiellaceae and Gelidiaceae, and of Italy (Perrone 1994) as well as Pterocladiella minima the Pterocladiaceae fam. nov. (Guiry et Womersley) Santelices et Hommersand in Aus- tralia (Guiry and Womersley 1992). In this latter form they Keywords: attachment; Gelidiales; Pterocladiaceae; can hardly be distinguished from species belonging to rhizoids; rhizines; taxonomy. the family Gelidiellaceae. The apical growth pattern as well as an evident axial cell row throughout the erect axes, described as characteristic of Parviphycus, are also Introduction present in some genera of the family Gelidiaceae (Rico and Guiry 1997, pers. observ.). In addition, the absence Diminutive species, as well as juvenile and dwarf plants of gametophytic thalli in the Gelidiellaceae can no longer of gelidialean macroalgae are difficult to identify, espe- be maintained, since Sreenivasa Rao (1974) observed cially when vegetative. This can seriously flaw floristic meiotic divisions during tetraspore formation, and and ecological works, especially because in some geo- Kapraun et al. (1994) reported diploid and haploid nuclear graphic areas entire populations of Gelidiales are known DNA amounts in tetrasporophytes and presumptive to propagate only vegetatively, or to be, at most, tetra- gametophytes in G. acerosa. Furthermore, male game- sporic (Fan 1961, Dixon and Irvine 1977, Guiry and tophytes were described in G. acerosa (Santelices 1997a) Womersley 1993). Tetrasporangial sorus characteristics and Parviphycus tenuissimus (J. Feldmann et Hamel) alone do not permit either generic or specific assignment Santelices (as G. tenuissima) (Rico et al. 2002). (Maggs and Guiry 1987, Guiry and Womersley 1992, The pannosa-type tetrasporangial arrangement, attrib- Kraft and Abbott 1998). uted to Parviphycus (as tenuissima-type), can also be The Gelidiales sensu Kylin (1923) consists of two fam- observed in other Gelidiaceae, such as Pterocladiella ilies, Gelidiaceae and Gelidiellaceae. The family Gelidia- melanoidea, Pterocladiella minima, Pterocladiella calo- ceae is characterized by typical unicellular thick-walled glossoides (Howe) Santelices and Capreolia implexa Gui- 2006/54 Article in press - uncorrected proof 24 C. Perrone et al.: The prostrate system of the Gelidiales ry et Womersley as well as in young tetrasporangial sori G. vagum Okamura and G. elegans Ku¨ tzing (Shimada et of Pterocladia lucida (Brown ex Turner) J. Agardh, Pte- al. 1999), G. samoense (Santelices et al. 2004), Acantho- rocladiella capillacea (S.G. Gmelin) Santelices et Hom- peltis japonica Okamura, Ptilophora subcostata (Oka- mersand, Pterocladiella bartlettii (W.R. Taylor) Santelices, mura) Norris and Capreolia implexa (Shimada et al. Pterocladiella caespitosa (Kylin) Santelices and some 1999)x. Shimada et al. (1999) generated an SSU phylog- Gelidium species (Norris 1992b, Guiry and Womersley eny in which three major species clades were resolved, 1993, Adams 1994, Rico and Guiry 1997, Kraft and (1) the Gelidiella clade, (2) the Pterocladia/Pterocladiella Abbott 1998, Santelices 1998, pers. observ.). Therefore, clade and (3) the Gelidium-complex clade. These clades the generic assignment of vegetative or tetrasporic geli- were shown to correlate with each kind of attachment dioid thalli in a turf where creeping axes of clonal geli- system, suggesting that the rhizoidal attachment ontog- dioid algae are entangled and sometimes anastomosed eny reflects a phylogenetic trend within the order is not possible (Perrone 1994). Gelidiales. Finding diagnostic vegetative characters has often This paper describes in detail the morphological and been the goal of morphological research on the Geli- ontogenetic features of the prostrate system of the Geli- diales (Okamura 1934, Stewart 1976, Akatsuka 1981, diales with the aim of validating their diagnostic and tax- 1986, Rodrı´guezand Santelices 1987, 1988). All the veg- onomic significance. etative characters taken into consideration, however, have been more or less correctly criticized and evaluated as unreliable (Dixon 1958, Maggs and Guiry 1987, Norris 1992a, Felicini and Perrone 1994, Kraft and Abbott 1998). Materials and methods The prostrate system of the Gelidiales has been con- sidered interesting from both a diagnostic and a taxo- nomic point of view, since preliminary observations on The following taxa were collected frequently from the some Mediterranean species of Gelidiella, Parviphycus Apulian coasts (Adriatic and Ionian Seas): Parviphycus (as Gelidiella), Gelidium and Pterocladiella (as Pterocla- antipae, Gelidiella lubrica (Ku¨ tzing) J. Feldmann et Hamel, dia) indicated that the attachment system features could Parviphycus tenuissimus, Gelidium spinosum (S.G. Gme- be useful for distinguishing between the genera. While lin) Silva, Gelidium pusillum, Gelidium spathulatum investigating the rhizoid ontogeny in some Mediterranean (Ku¨ tzing) Bornet, Gelidium crinale (Turner) Gaillon, Pte- species of Gelidiella, de Gregorio and Perrone (1994) rocladiella capillacea and Pterocladiella melanoidea. emphasized that only one kind of attachment rhizoid Fresh material was preserved in formalin-seawater, dried could be observed in the genus, i.e., single independent on herbarium sheets and also kept in stock cultures for rhizoids. Until then, this kind of attachment system had 30–40 days under natural light and temperature condi- been described only in Parviphycus antipae (Celan) San- tions in order to observe the prostrate system growth and telices (as Gelidiella antipae Celan); the few examples of morphogenesis. Liquid-preserved material was also ‘‘peg-like’’ holdfasts described in Gelidiella acerosa examined, as follows: (Forsska˚ l) J. Feldmann et Hamel, Gelidiella lubrica (Ku¨t- ● Gelidiella/Parviphycus: G. acerosa, sterile and tetra- zing) J. Feldmann et Hamel and Parviphycus tenuissimus sporic, 1994, Port Okha, India (sent by Dr. Vijayarag- (as Gelidiella pannosa) (Hatta and Prud’homme van Reine havan); sterile and tetrasporic, 1995, Queensland, 1991, Norris 1992b) result from misinterpretation of the Australia (sent by Dr. M. Hommersand); sterile and tet- rhizoidal clump morphology. rasporic, 1995, Taiwan (sent by Dr Mei Lin); G. lubrica, The same conclusions were
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