Gracilariopsis silvana sp. nov., G. hommersandii sp. nov., and G. cata-luziana sp. nov., Three New Species of Gracilariaceae (Gracilariales, Rhodophyta) from the Western Atlantic
Gracilariopsis silvana sp. nov., G. hommersandii sp. nov., and G. cata-luziana sp. nov., Tres especies nuevas de Gracilariaceae (Gracilariales, Rhodophyta) para el Atlántico Occidental
Carlos Frederico D. Gurgel1,3, Suzanne Fredericq1, and James N. Norris2
1Department of Biology, University of Louisiana at Lafayette, Lafayette, LA 70504-2451, USA.
2U.S. National Herbarium, NHB 166, National Museum of Natural History, Botany Section, Smithsonian Institution, P.O. Box 37012, Washington, D.C. 20013-7012, USA.
]]> 3Current address: Universidade Federal do Rio de Janeiro, CCS, Instituto de Biologia, Departamento de Botânica, sala A1-094, RJ, Brasil, 21940-900.
Recibido: 16 de julio de 2002.
Aceptado: 10 de diciembre de 2002.
Abstract
Species of Gracilariopsis are typically characterized as slender, elongate, cylindrical fronds with varying degrees of branching that exhibit less habit diversity than species of Gracilaria. Of the thirteen currently known species of Gracilariopsis worldwide, ten have been described from the Pacific Ocean and the Gulf of California, and three from the Atlantic Ocean and the Caribbean Sea. Sequence analysis of chloroplast-encoded rbcL provides sufficient phylogenetic signal for species level resolution in Gracilariopsis, and for assessing the intrageneric evolutionary relationships. Results showed the identification of previously described species and the delineation of three new western Atlantic species: Gp. silvana sp. nov. from Venezuela, is the first of the genus to be characterized by flattened, strap-shaped thalli that are sparingly or profusely, subdichotomously or irregularly pinnately branched up to 4(-6) orders; Gp. hommersandii sp. nov., from Panama and Venezuela, is a cylindrical, stringy unbranched to branched species, that sometimes bear short, uncinate branchlets, formed mostly apically or along the axes, and often hooked-up to adjacent thalli; and, Gp. cata-luziana sp. nov., from Campeche Bay, Gulf of Mexico, is also cylindrical and stringy, but with very slender, delicate, and much elongated, loosely and profusely branched thalli, up to 40 cm tall, that have a medulla of few, large cells. Parsimony analysis inferred from rbcL sequences of 22 taxa worldwide supports the distinctness of these new species. This study indicates species diversity in Gracilariopsis, now with sixteen species worldwide, including six in the Atlantic Ocean, has been underestimated, and the diagnosis of the genus must be expanded to include flattened species.
Key words: Gracilariopsis, Gracilariaceae, new species, rbcL, phylogeny, Western Atlantic.
Resumen
]]> Las especies de Gracilariopsis están caracterizadas típicamente por frondas delgadas, elongadas y cilíndricas con grados diversos de ramificación, que exhiben una diversidad menor de hábitos que las especies de Gracilaria. De las trece especies actualmente reconocidas de Gracilariopsis a nivel mundial, diez han sido descritas para el Océano Pacífico y Golfo de California y tres para el Atlántico y Mar Caribe. El análisis de secuencias de nucleótidos del gen codificante rbcL, en cloroplasto, brindan información filogenética suficiente, a nivel de especie, para inferir las relaciones evolutivas intragenéricas en Gracilariopsis. Los resultados mostraron la identificación de especies descritas previamente y la delineación de especies nuevas para el Atlántico occidental: Gp. silvana sp. nov. de Venezuela, es la primera dentro del género caracterizada por talos aplanados y acintados, ramificados subdicotómicamente o de manera pinada irregular. La ramificación puede ser profusa o esparcida hasta 4 (6) órdenes; Gp. hommersandii sp. nov. de Panamá y Venezuela posee talos cilíndricos, fibrosos ramificados o no, algunas veces con ramitas cortas uncinadas que se desarrollan apicalmente o a lo largo de los ejes y que con frecuencia se aferran a otros talos cercanos y Gp. cata-luziana sp. nov. proveniente de la Bahía de Campeche, Golfo de México, también cilíndrica y fibrosa pero con talos muy delicados, delgados y alargados, ramificados profusamente o escasamente de hasta 40 cm de longitud, con una médula de pocas células grandes. Un análisis de parsimonia, a partir de secuencias del gen rbcL, de 22 taxa mundiales respalda la distinción de estas tres especies nuevas. El presente estudio indica que la diversidad específica en Gracilariopsis, ahora con 16 especies en todo el mundo, incluyendo seis para al Atlántico, ha sido subestimada y que la diagnosis del género debe ser ampliada para incorporar a especies aplanadas.Palabras clave: Gracilariopsis, Gracilariaceae, especies nuevas, rbcL, filogenia, Atlántico occidental.
Introduction
Members of the red algal genus Gracilariopsis Dawson (1949:40) (Gracilariaceae Nägeli 1847:240; Gracilariales Fredericq et Hommersand 1989a:225) are typically characterized as slender, elongate cylindrical fronds with varying degree of branching, and a range of habit types considered to be less diverse than those of Gracilaria Greville nom. cons. (1830:liv,121). This thallus uniformity, coupled with a lack of obvious discriminating macro-features, complicates species identification. Gracilariopsis (=Gp.) was separated from members of Gracilaria (=G.) primarily on reproductive differences in the internal anatomy of the cystocarp.
The genus Gracilariopsis [generic type: Gracilariopsis sjoestedii (Kylin) Dawson 1949:404] is characterized by the absence of 'nutritive filaments' (=tubular nutritive cells), connecting the gonimoblasts to the pericarp, a broad-based gonimoblast of small cells, and by the superficial arrangement of spermatangia. In contrast, Gracilaria [generic type: G. compressa (C. Agardh) Greville 1830:liv, typ. cons.5] possesses 'nutritive filaments' and spermatangia arranged in pits. The presumed generic type for years was Gracilaria verrucosa (Hudson) Papenfuss (1950:195; =Fucus verrucosus Hudson 1762:470) from southern England.
Later Papenfuss (1967) in studying material he identified as 'G. verrucosa' reported tubular nutritive cells present in some specimens and absent in others, and considered the two genera indistinct, placing Gracilariopsis in synonymy with Gracilaria.
Detailed morphological studies of Gracilariopsis sjoestedtii (Kylin) Dawson [=Gp. lemaneiformis sensu Abbott 1983; non Gp. lemaneiformis (Bory) Dawson, Acelto et Foldvik 1964] from California by Fredericq and Hommersand (1989a,b) resulted in their resurrecting Gracilariopsis. While noting the generic characters used by Dawson (1949) for Gracilariopsis, i.e., the absence of multinucleate tubular nutritive cells in the cystocarp and the superficial arrangement of the spermatangia, Fredericq and Hommersand (1989a,b; 1990) also emphasized another feature: that the gonimoblast cells become linked to gametophytic cells of the cystocarp floor by means of secondary pit connections through gonimoblast conjunctor cells. Several genetic studies have corroborated the taxonomic validity of Gracilariopsis (e.g., Goff and Coleman 1988, Kapraun 1993, Kapraun et al. 1993, Goff et al. 1994, Bellorin et al. 2002, Gurgel et al. 2003). While many taxonomists recognize Gracilariopsis as distinct from Gracilaria (e.g., Ohmi 1958; Yamamoto 1975; Fredericq and Hommersand 1990; Womersley 1996, Silva et al. 1996), others have treated them as one, i.e., Gracilaria (e.g., Gargiulo et al. 1992; Abbott 1995, 1999; Terada & Ohno 2000).
Gurgel et al. (2003) recently provided a molecular phylogenetic study inferred from maximum parsimony and maximum likelihood analyses of chloroplast-encoded rbcL sequences, along with nomenclatural and taxonomic changes, based on twenty-two specimens of Gracilariopsis encompassing ten of the currently recognized species worldwide (7 from the Pacific; 3 from the Atlantic), and three out-group species. Of these studied taxa (Gurgel et al. 2003) six were recognized to be undescribed species, but a formal description was not provided.
Ten species of Gracilariopsis have been described from the Pacific Ocean (Table 2): Gp. andersonii (Kylin) Dawson (1949), [the correct name for the generitype Gp. sjoestedtii Kylin 1930, see Gurgel et al. 2003 for nomenclatural note from central, California]; Gp. chorda (Holmes) Ohmi (1958) from Japan; Gp. costaricensis Dawson (1949) from Costa Rica; Gp. heteroclada (Zhang et Xia) Zhang et Xia in Abbott et al. (1991) from the Philippines; Gp. lemaneiformis (Bory) Dawson, Acleto et Foldvik (1961) from Peru; Gp. megaspora Dawson (1949; Norris 1985) from Sonora, Gulf of California; Gp. nganii Pham-Hoàng (1969) and Gp. phantietensis Pham-Hoàng (1969) both from Viêtnam (Nguyen 1992); Gp. panamensis (W. Taylor) Dawson (1949) from Panama; and Gp. rhodotricha Dawson (1949) from Pacific Mexico and Viêtnam (Dawson 1954; Nguyen 1992). Sequence analyses of rbcL revealed two other unidentified Pacific taxa of Gracilariopsis (Gurgel et al. 2003; herein): Gp. sp. 1 (Table 1) from southern Australia and the Gulf of California; and Gp. sp. 3 (Table 1) from China and Japan.
]]> Fewer species have been described for the Atlantic Ocean (Table 2). Dawson (1953) first reported a Gracilariopsis from the southern Caribbean and considered it close to but distinct from "Gp. sjoestedtii." Gracilariopsis tenuifrons (Bird et Oliveira) Fredericq et Hommersand (1989b) is a species originally described from Maceió, Brazil (Bird and Oliveira 1986, as 'Gracilaria tenuifrons'). Fredericq and Hommersand (1989b) first identified another Gracilariopsis from the eastern Atlantic, a species later recognized as Gp. longissima (Gmelin) Steentoft, Irvine et Farnham (1995) from Kent, southern England. More recently a new western Atlantic species, Gp. carolinensis Liao et Hommersand in Gurgel et al. (2003), was described from North Carolina. An economically important species, Gp. 2 (Table 1), of the local agar industry of western South Africa and Namibia (Stegenga et al. 2002, as 'Gp. lemaneiformis;' Wakibia et al. 2001, as 'Gp. sp.'), was shown, based on rbcL sequence analyses (Gurgel et al. 2003; herein), to also be an unknown taxon.Our comparative studies of three unknown Atlantic species (Table 1; Gurgel et al. 2003: as 'Gp. sp.' from Venezuela; 'Gp. aff. panamensis' from Caribbean Panama and Venezuela; and 'Gp. sp.' from the Gulf of Mexico) revealed them to be distinct from any currently known species of Gracilariaceae (e.g., Taylor 1960, Wynne 1998), nor did they match with photographs of type specimens (PC!, NY! or BM!) of Schramm and Mazé (1865, 1866). Therefore we herein describe them as new species, based largely on the analysis of chloroplast encoded rbcL sequences, and broaden the description of the genus to include a flat species.
Material and methods
Morphology. Voucher specimens were fixed and stored in 5% Formalin/seawater, and/or pressed and air-dried on herbarium sheets and deposited in LAF, Alg. Coll. US and UC (herbarium abbreviations follow Holmgren et al. 1990). Specimens were photographed on a Zeiss Stemi 2000-C dissecting scope (Carl Zeiss Inc., Thornwood, NY, USA) attached to a Minolta 35mm camera (Minolta Corporation USA, Ramsey, NJ, USA). Some were scanned into the computer either as 'wet' (liquid-preserved) specimens, or directly from a herbarium sheet using a Microtek ScanMaker III scanner (Microtek International, Hsinchu, Taiwan). Cross-sections for morphological studies were hand-made using stainless steel razor blades, and then stained in a 3% aniline blue solution (Tsuda and Abbott 1985) for 10-15 minutes. The stain was fixed with 1 drop of 3% acetic acid, rinsed with distilled water and then mounted in a 50% KaroTM corn syrup/distilled water solution with phenol added as a preservative. Photomicrographs were taken with a Polaroid DMC Ie digital camera (Polaroid, Inc., Cambridge, MA, USA) attached to an Olympus BX60 (Olympus, Melville, NY, USA). Images were edited and assembled in plates using Photoshop v.5.0 (Adobe Systems Inc., San Jose, CA, USA).
Molecular Phylogeny. Silica gel-dried specimens and extracted DNA samples were deposited in the Seaweed Laboratory at the University of Louisiana at Lafayette, and stored at -20ºC. DNA samples were prepared using the DNeasy Plant Mini Kit (QIAGEN, Valencia, CA, USA), or were submitted to a CTAB-Cesium Chloride DNA procedure (Freshwater and Rueness 1994). Plastid-encoded rbcL was selected to infer a phylogeny for Gracilariopsis. PCR and sequencing primers used in this study were FrbcL start, F7, F57, F492, F577, F753, F993, R753, R1381 and RrbcS start as listed in Freshwater and Rueness (1994) and Hommersand et al. (1994). Protocols for gene amplification, automated sequencing and alignment are identical to those given in Lin et al. (2001) and Gurgel et al. (2003).
Partial rbcL sequences were produced from 22 recently collected samples of Gracilariopsis. Collection information (Table 1) includes specimen locality, date and collector's name, percentage of rbcL gene sequenced, and GenBank accession numbers (see also Gurgel et al. 2003). Melanthalia obtusata (Labillardière) J. Agardh and Curdiea coriacea (Hooker et Harvey) J. Agardh from New Zealand, and C. crassa Millar from southern Australia were chosen as outgroup taxa based on their close phylogenetic relationship with the ingroup in global searches of the Gracilariaceae (data not shown).
Phylogenetic analysis was performed with PAUP* v.4.0 beta 10 (Swofford 2002) for Macintosh using maximum parsimony (MP). Because the first 40 base pairs (bp) were missing in many sequences, the phylogenetic analysis was restricted to the last 1427/1467 bp of rbcL. Maximum parsimony trees were inferred from: 1) heuristic searches of 5000 replications of random sequence addition (Fitch 1971) using, unordered, only the phylogenetically informative characters, under the Fitch criterion of equal weights for all substitutions; 2) Tree Bisection Reconnection (TBR), saving multiple trees (MULTREES) but holding 20 trees at each step; and, 3) STEEPEST DESCENT. Support for all nodes (bp) for all trees was assessed by bootstrap analysis (Felsenstein 1985) on the data set using 3000 replicates and "as is" sequence addition, as implemented in PAUP*.
Results
]]> Gracilariopsis silvana Gurgel, Fredericq et J. Norris, sp. nov. (Figs 1-16 (2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15))
Holotype. #US Alg. Coll. -204316 (Fig. 1). Venezuela: Playa Barranquilla, Estado Falcón, 14 vii 1999, coll. C. F. D. Gurgel, J. E. Conde and C. Carmona, # FG-37. Isotypes: LAF; UC.
Paratype. Venezuela: La Vela de Coro, Estado Falcon, 13 vii 1999, coll. C. F. D. Gurgel, J. E. Conde and C. Carmona #FG-13 (#US Alg. Coll. -204317).
Etymology: This species is named in honor of Dr. Paul C. Silva (Herbarium, University of California at Berkeley) on the occasion of his 80th birthday, and to celebrate his groundbreaking contributions to the taxonomy and nomenclature of the algae. In choosing the epithet, "silvana", we follow Stern (1973:294) who noted Lindley (1832) had suggested that when the epithet is to compliment the person it should be rendered in the adjectival form.
Latin diagnosis: Thalli plerumque 14-16 (-20) cm alt., 1-3 cm. lat. Thalli juniores plerumque solitarii tenues delicatique, vetustiores crassi cartilagineique uterque exorientes haptero parvo oributalato, interdum haptera anastomosantia. Thalli complanati omnino, interdum undulati. Axes principales ligulati, dichotomi, subdichotomi, polychotomi vel ramosi irregulariter. Ramificatio abunde, rami longi apicem versus. Rami numquam constricti basi, maximam partem orti margine, apicibus fractorum thallorum sed intersum mediregionibus laminae axium principalium.
Description: Thalli flattened throughout, strap-shaped (Figs. 1-5), sometimes slightly undulated (Figs. 1, 3), 14-16 (-20) cm tall, 1-3 cm wide, (275-) 488 (-600) m thick, red, pinkish red, sometimes with yellow regions. Young plants usually solitary and thin, arising from small, rounded holdfasts (Figs. 3, 5-6). Older thalli thick, cartilaginous, borne on wart-like irregular holdfasts formed from the coalescence of neighboring holdfasts (Figs. 1, 7) from which new juvenile uprights (Fig. 7) may arise. Main axes sparingly (Fig. 1) or profusely (Fig. 5) subdichotomously or irregularly branched for up to 4 (-6) orders; branches gradually decreasing in width distally (Fig. 5). Lateral branches not constricted at base, curved upward, irregularly pinnate, mostly arising from thallus margin (Figs. 1-5), damaged tips, and the mid-region of main axes (Figs. 1-2). Apices variable, acute to roundly blunt. Gradual transition in cell size between a medulla composed of 5-6 (-9) layers of large, laterally compressed, thin-walled central cells (250-) 330 (-400) µm by (60-) 105 (-140) µm (Figs. 9-10), to an outer cortex composed of 1-3 layers of isodiametric cells, 7.5-10 µm diameter (Fig.11). Cortical gland cells present, rounded in surface view.
]]> Cystocarps hemispherical (Fig. 8), scattered on lower and upper surfaces of main axes, 1-2mm diameter and slightly constricted at base where protruding from thallus (Figs. 12-13), with a centrally located, occasionally rostrate ostiole (Fig. 12). Carposporangia organized in tightly packed branched files. Pericarp composed of 12-14 cell layers, 150-165 µm thick, pericarp cells (Fig. 14) distally squarish becoming star-shaped to rounded below to accommodate for cystocarp expansion. Cystocarps wide-based (Figs 12-13); gonimoblasts at maturity completely filling cystocarp cavity and composed of small, regular thin-walled cells, 3-5 µm diameter. Carpogonial fusion cell not pronounced. Transition zone at base of cystocarp (within lower carposporophytic region), composed of elongated cells corresponding to former subcortical cells that expanded upon schizogenous formation of cystocarp cavity directly distally to these cells; terminal gonimoblast conjunctor cells subsequently fusing downward onto these enlarged cells to form secondary pit connections. As the cystocarp expands laterally, degenerating carpogonial branches may become incorporated and are seen as darkly staining multinucleate cells (Figs 15, 16). Spermatangial and tetrasporangial specimens not seen.Gracilariopsis hommersandii Gurgel, Fredericq et J. Norris, sp. nov. (Figs. 17-23, 26-30)
Holotype. #US Alg. Coll. -204312 (Fig. 19). Republic of Panama: cystocarpic thallus, on rock in shallow water, 0.75 m depth, Fort Randolph, Colón City, Bahía Limon, Provincia Colón, (Caribbean Panama), 26 iii 1999, coll. B. Wysor, #BW-00197. Isotypes: LAF.
Paratypes. Venezuela: Los Roques Archipelago: Los Francisky Island, coll. C. F. D. Gurgel, # FG-02, # FG-05, 4 vii 1999; Madrisky Island, coll. C. F. D. Gurgel, # FG-06, 7 vi 1999; and, Crasky Island, coll. C. F. D. Gurgel, # FG-07, # FG-08, 7 vii 1999. Venezuela: La Encrucijada, Peninsula Paraguana, Estado Falcon, 13 vii 1999, coll. C. F. D. Gurgel, #FG-18 (#US Alg. Coll. 204313).
Etymology: This species, "hommersandii", is named in honor of Dr. Max H. Hommersand (University of North Carolina at Chapel Hill) whose contributions to algal systematics, including the Gracilariales have greatly enhanced our knowledge of the red algae.
Latin diagnosis: Thalli flavi, saepe subrosei basi, interdum pallidivirides, erecti aut prostrati, 20-45 cm long., cartilaginei, graciles laevigatique, exorientes haptero discoideo. Plures thalli plerumque fasciculati simul eodem haptero inconspicuo. Thalli plerumque ramosi non profuse, saepe solum compositi axium linerarium rectorum ramis. Apices acuminati, uncinati vel compositi 1-4 unciformium ramulorum, 0.5-0.8 cm long, deorsum extensorum formatorum antea fractorum apicum crescentium. Interdum superae partes axium spiratae circum alios axes contiguos. Ramuli minuti retroanastomosantes axem formantes regiones locales circulares annuliformes.
]]> Description: Thalli 20-45 cm long, 1.0-2.3 mm diameter, terete, stringy, slender, cartilaginous, smooth, sparingly (Figs. 17-18) to profusely (Fig. 19) branched. One to several yellowish thalli (Fig. 19), sometimes pale-green or often pinkish at the base, arise above a small, discoid holdfast (Figs. 17-18). Thalli > 30 cm often composed solely of straight linear axes with branching towards the base limited to a few sparse, branches. Apices either acuminate (Fig. 17), or uncinate (Figs. 20-21), comprised of one-to-four hook-like branchlets, 0.5-0.8 cm long, spreading downward. Uncinate branchlets originating on axes below tend to coil around both adjacent axes (Fig. 22) or around their own axis, forming localized ring-like regions (Fig. 18) arrow. Medulla 6-7 cell layers, of large vacuolate, thick-walled, roundish cells, (175-) 244 (-284) µm by (125-) 165 (-225) µm (Figs. 26, 28, 30). Transition between medulla and subcortex abrupt; subcortex composed of evenly spaced, slightly anticlinally elongated cells, (6.0) 8.8 (-10) µm by (3.8-) 5.0 (-7.5) µm, with innermost subcortical cells the largest and thick-walled (Fig. 28). Outermost cortical cells of distal most 3-6 cell layers radially elongated, (5.0) 7.5-8.8 (-10) µm by 3.8-5.0 µm.Cystocarps hemispherical, protruding (Fig. 23), scattered along axes, slightly constricted at base, 0.8-0.9 mm tall, 0.9-1.0 mm wide. Pericarps (Fig. 27) of mature cystocarps composed of 9-10 cell layers, 125 µm to 240 µm diameter; composed of evenly-spaced, rounded-ellipsoidal cells, 6.25-8.75 µm by 7.5-11.25 µm, with cell walls 3.75-8.75 µm thick. Central gonimoblasts composed of tightly packed files of evenly-sized, roundish cells filling the cystocarp cavity (Figs. 26-27, 29). Carpogonial fusion cell not pronounced. Inner pericarp cells at base of cystocarp cavity (Fig. 27), 31.25-43.75 µm by 18.75 µm diameter. Spermatangial and tetrasporangial specimens not seen.
Gracilariopsis cata-luziana Gurgel, Fredericq et J. Norris, sp. nov. (Figs. 31-36)
Holotype. #US Alg. Coll. -204314 (Fig. 31). México: protected sandy beach near lagoon [19º 03.31' N; 96º 00.44' W], 2 miles west of Anton Lizardo (close to Veracruz), Estado Veracruz, Campeche Bay, Gulf of Mexico, coll. C. F. D. Gurgel, # FG-204, 10 ii 1999. Isotypes: LAF
Etymology: The adjectival ending, -ana, is chosen (Stern 1973:294; Lindley 1832) for "cata-luziana", named in honor of Professors Catalina Mendoza and Luz Elena Mateo-Cid (Escuela National de Ciencias Biológicas, Instituto Politécnico Nacional, México D.F.), who have greatly enhanced our floristic knowledge of the marine algae of México. Following Art. 60.9 of the ICBN (Greuter et al. 2000), we use the hyphen to indicate that the given names of these two phycologists, Catalina and Luz, are formed independently.
Latin diagnosis: Thalli dumales compositi aliquot specimeninum intricatorum. Individua specimena gracilia, 25 cm long., usque ad 6 cm alt. Segregati axes principales cartilaginei, filo metallico similis, teretes ad paucicompressi, aliquot ramulis irregularibus ad subdichotomos, ramosis profuse. Ramificatio pro parte maxima alternata, irregularis, interdum duo ramis insertis in eadem regionem. Rami tenuissimi, lineares leviter constricti basi distributi omnino thallo descrescentes in apices acutatos.
Description: Habit bushy, up to 25 (-36) cm long, with clumps up to 6 cm broad, composed of several distinct thalli mostly entangled to each other (Fig. 31). Individual main axes wiry, thin, delicate in texture, terete to slightly compressed, mostly 25-30 (-36) cm long by (373-) 447 (-555) µm thick. Main axes laterally bearing elongate, mostly alternate, linear, simple side branches, slightly constricted at the base, may produce an order of very thin branch initials (Fig. 31). Two lateral branches may originate from same insertion point (Fig. 35). Branch initials spine-like, distributed all over thallus at wide 45º-90º angles, tapering into acute tip, mostly of two sizes, 2.5 and 4.0 cm long. Hair cells rare. Cortical region composed of two distinct layers of pigmented cells. Cells of outer cortical layer typically refringent, of variable shape (Figs. 32-34, 36), but mostly rounded, (5.0) 7.5 (-8.5) µm by 4.5-5.0 µm, or spherical or squarish, (7.0) 10 (-12.5) µm by (6.5-) 7.5 (-10) µm. Subcortex composed of spherical to anticlinally elongated larger cells, (6.25-) 13 (-21.25) µm by (9.4-) 12 (-23.75) µm, rich in floridean starch. Transition zone between medulla and subcortex abrupt. Medulla composed of one central cell (Fig. 32), 250-330 µm diameter, or up to five large central vacuolate cells (Figs 33-34, 36) as seen in transverse section. A single-celled medulla is the result of collapsing cell walls of contiguous medullary cells. A two-celled inner medulla comprises slightly compressed cells, 125 µm by 200 µm (Fig. 34). When composed of 3-4 cells, inner medullary cells measure 66.5 µm by 135 µm. The subcortex is composed of (13.75-) 14.2 (-21.25) µm by (12.5-) 13.75 (-15) µm, radially or anticlinally compressed cells, rich in floridean starch. Cystocarpic, spermatangial and tetrasporangial specimens not seen.
]]> Discussion and taxonomic conclusion
The distinctness of the new western Atlantic members Gracilariopsis silvana, Gp. hommersandii and Gp. cata-luziana at the species level is corroborated by the rbcL analysis (Fig. 37; Table 1 & Gurgel et al. 2003: as 'Gp. sp.,' 'Gp. aff. panamensis,' and 'Gp. sp.'). Molecular results show Gp. heteroclada from the Philippines as the most basal species in the data set followed by Gp. silvana and Gp.hommersandii and an as yet undescribed species (Gp. sp. 3) from Japan and China. Despite the absence of bootstrap support values at the deeper nodes in the Gracilariopsis tree, these four species always grouped basally in the phylogenetic analyses.
The four haplotypes of Gp. hommersandii confirm the phenotypic variation in overall habit shape displayed by members of this species in the Caribbean, ranging from pseudodichotomously branched thalli typical of Caribbean Panama (Fig. 19) to unbranched or sparsely branched specimens collected in Venezuela (Figs. 17-18). The range of genetic variation present among the Gp. hommersandii haplotypes, is minimal at 0-0.07% sequence divergence ("p" distance), confirming that specimens with such divergent habit in fact belong to the same species.
The eastern Pacific Gp. lemaneiformis from Peru, Gp. costaricensis from Costa Rica, and the recently described western Atlantic Gp. carolinensis (Gurgel et al. 2003) form a well-supported clade (bp = 91) sharing similar cystocarp features. Gurgel et al. (2003) also showed that Gp. carolinensis is morphologically and genetically more closely related to Gp. lemaneiformis than it is to Gp. andersonii. Gracilariopsis andersonii stands alone in the Gracilariopsis phylogram.
Gracilariopsis cata-luziana is a sister taxon to Gp. tenuifrons, and both species form a well-supported clade (bp = 95) (Fig. 37). Gracilariopsis sp. 2 from Namibia corresponds to an undescribed species.
The most derived and well supported clade (bp = 92) is composed of Gp. longissima and Gp. sp. 1. Gracilariopsis sp. 1, collected from Lake Butler, is apparently an invasive species in southern Australia (=Womersley 1996: 29-31, figs. 8A-F, as 'Gp. lemaneiformis'), and is shown to be the same entity as specimens from the Baja California Norte coast of the Gulf of California (=Pacheco-Ruíz et al. 1999, as 'Gp. lemaneiformis') (Fig. 37; Table 1). Two entities that may be separate taxa have both been misidentified as 'Gp. longissima' in Europe; one species is from the Mediterranean, and the other is in the northeastern Atlantic
Based solely on external habit, the distinction between Gracilariopsis silvana and flat species of Gracilaria from the Caribbean and Gulf of Mexico may not be readily apparent, especially when dealing with small, immature or non-reproductive specimens. Specimens of Gp. silvana that lack the characteristic abundance of marginally inserted branches on their strap-shaped thalli may superficially resemble specimens of Gracilaria curtissiae J. Agardh (1885: 61; type locality: Florida, lectotype LD!), G. cuneata Areschoug (1854: 351; type locality: vicinity of Pernambuco, Brasil; syntypes S!), or misidentified specimens from Venezuela (Rodriguez de Rios 1986, as 'G. textorii'). However, fully grown specimens of Gp. silvana are easily distinguished from G. curtissiae by possessing narrower and thinner blades that may bear abundant and irregular pinnate branches curved slightly upwards. On the other hand, G. curtissiae usually has thicker (0.5-1.0 mm) blades, sometimes with distinct di- to tripartite (palmate) branches radially distributed along the margin. The medullary region of G. curtissiae is composed of fewer (3-4 cell layers across) but larger, less compressed central cells, and a sharp medullary-cortex transition. Cortical gland cells were never seen in Gp. silvana, but they are conspicuous in Gp. curtissiae. Gracilariopsis silvana represents the first report of a truly flat-foliose species of Gracilariopsis.
Gracilariopsis hommersandii is most likely a common member of Caribbean sandy beach habitats of the upper subtidal. Usually, several distinct thalli grow closely together forming isolated clusters of entangled, long, cylindrical axes. Occasionally, a few short, hook-like branchlets are formed near the apices, probably the result of regenerated grazed, damaged or fragmented tips, and in the mid portion of the axis, where they hook up to adjacent thalli, keeping the entire cluster together. Such uncinate branchlets were also observed in an isotype specimen of Gp. chorda (BM!; Enoura, Japan, coll. Prof. Saida #6, March 1894). Specimens of Gp. hommersandii from exposed shores in Venezuela (e.g., La Encrucijada) are thicker and seldom branched, whereas those from calm, protected bays and sea-grass beds of Thalassia testudinum (e.g., Francisky Is., Los Roques Archipelago) are thinner, more delicate, sometimes more branched and beset with more distal uncinate branchlets.
]]> Unbranched specimens of Gp. hommersandii collected at the islands of Los Roques Archipelago may superficially resemble Gp. panamensis (W. Taylor) Dawson (see: G. panamensis Taylor 1945:231, pl. 76, figs. 1-4) from Pacific Panama, with a recorded range from Costa Rica to the Galápagos Islands. Gracilariopsis hommersandii may be a sister species to Gp. panamensis, and the rise of the Panamean Isthmus 3.1-3.6 million years ago (Vermeij and Rosenberg 1993, Haug and Tiedemann 1998) would probably be the vicariant event responsible for their isolation and subsequent speciation. Examination of Gracilariopsis panamensis (isotypes: UC!; #US Alg. Coll. -56496!) shows it differs from Gp. hommersandii in being longer, up to 165 cm long, lacking the hook-like branchlets, and in possessing a more narrow-based cystocarp in which the gonimoblasts extend farther vertically, and have a pericarp with more anticlinally elongated cells (Figs 24, 25). Dawson's (1953) report of a southern Caribbean species of Gracilariopsis might also be Gp. hommersandii.Gracilariopsis cata-luziana is described from specimens collected from a single locality in Campeche Bay, southern Gulf of Mexico, and may be endemic to that region. Clusters of specimens are attached to coarse sand by small rounded holdfasts. Among the newly described western Atlantic species of Gracilariopsis, Gp. cata-luziana is morphologically and genetically the closest to Gp. tenuifrons (Bird et Oliveira) Fredericq et Hommersand (see: Gracilaria tenuifrons Bird and Oliveira 1986: figs. 2-3). Both species possess exceedingly slender, delicate, stringy thalli, grow to about 40 cm tall, and are loosely and profusely branched. Entangled axes are common, and ultimate branches are short and filiform. Both species are typical of protected bays and turbid waters, sometimes inhabiting areas subjected to eutrophication, and occurring in shallow waters about one meter depth where they readily colonize loose debris and other substrata, often with their basal portions buried in fine sediment. Gracilariopsis cata-luziana is readily distinguished from Gp. tenuifrons in being more delicate, with main axes that are brittle when wet and easily break-up when dried.
Population studies on certain species of marine organisms in the southern Gulf of Mexico reveal some degree of uniqueness when compared to populations of the same species from other areas, and that southern Gulf region seems to promote the isolation needed for speciation to take place (Reed and Avise 1990). The geographic structure of the Gulf of Mexico, especially its southern embayment configuration (e.g., Campeche Bay) may be similarly acting as the vicariant event that has isolated Caribbean and Gulf of Mexico populations into two ancestrally related species, Gp. tenuifrons and Gp. cata-luziana.
Results also found three other undescribed species (Table 1): Gp. 2 from Namibia; Gp. 3 from Japan and China; and Gp. 1, which is reportedly an invasive species in southern Australia (Womersley 1996, as 'Gp. lemaneiformis') and is also found in the Gulf of California (Pacheco-Ruíz et al. 1999, as 'Gp. lemaneiformis'). These taxa await additional data for final taxonomic diagnosis. All are characterized by being terete, sterile, stringy, and by thriving in protected shallow embayments with thalli commonly drifting close to the shore. Because of their high biomass in Namibia (Stegenga et al. 1997, as 'Gp. lemaneiformis') and in the Gulf of California, Mexico (Pacheco-Ruiz et al. 1999, as 'Gp. lemaneiformis') these species have been used in their local agar industries.
This study has shown that rbcL gene sequence analysis provides sufficient phylogenetic signal for species level resolution in the genus Gracilariopsis, for the identification and delineation of new and previously described species, and for assessing the evolutionary relationships within the genus. The lack of distinct vegetative and reproductive characters and the high degree of morphological similarity among many species of Gracilariopsis may be the reason that genetically distinct species were not previously recognized on the basis of their morphology alone.
Prior to this study, there were only three species of Gracilariopsis described for the Atlantic Ocean, namely Gp. longissima (Steentoft et al. 1995) from the eastern Atlantic, and Gp. tenuifrons (Fredericq and Homnersand 1989b) and Gp. carolinensis (Gurgel et al. 2003) from the western Atlantic. Our results reveal that species diversity of Gracilariopsis, now with at least six species in the Atlantic Ocean and sixteen species recognized worldwide (Table 2), has been underestimated. The genus is also expanded to include flattened species.
Acknowledgments
Much of this work was submitted as part of the Ph.D. dissertation by C. F. D. Gurgel (2001) to the Department of Biology, University of Louisiana at Lafayette. We thank B. Wysor, M. H. Hommersand, W. Nelson, A. J. K. Millar, D. W. Freshwater, S. M. Lin, C. Acleto, L. Liao, J. Zertuche-Gonzáles, H. B. S. Womersley, K. S. Cole, A. R. Andria Gonzales, W. F. Farnham, and A. Renoux for material used in this study. We especially thank M. Hommersand and L. Liao for their interest and support in this study. For comments on this manuscript we thank K. E. Bucher and D. H. Nicolson for discussion on nomenclature. This study was funded in part by a Smithsonian Institution and Link Foundation Graduate Summer Internship at the Smithsonian Marine Station at Fort Pierce, FL; Sigma Xi Graduate Grant-in-aid for Research; Phycological Society of America Hoshaw Travel Award and Grant-in-aid for Research to CFG; and, a US Department of Energy grant DE FG02-97ER122220, NURC-NOAA grant NA96RU-0260, and a Smithsonian Institution Postdoctoral Fellowship (1988-1989) to SF. This study represents Smithsonian Marine Station Contribution number 536.
]]> References
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Notas
4Gracilariopsis sjoestedtii [basionym: Gracilaria sjoestedtii Kylin 1930:55; type locality: "biologischen Station" (=Hopkins Marine Station of Stanford University), Agazzi (=west) beach of Mussel Point, Pacific Grove, California] is now considered to be a taxonomic synonym of Gp. andersonii (Grunow) Dawson 1949:43 [basionym: Cordylecladia andersonii Grunow in Piccone 1886:62] (Gurgel et al. 2003).
5Conserved generic type, Gracilaria compressa (C. Agardh) Greville 1830:liv [basionym: Sphaerococcus compressus C. Agardh 1822:308; type locality: Cádiz, Spain] (see: Steentoft et al. 1991; Silva 1994:263; Silva et al. 1996:917-918); is a taxonomic synonym of G. bursapastoris (Gmelin) Silva 1952:265 [basionym: Fucus bursapastoris Gmelin 1768:121] (Silva et al. 1996:157).
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