Vegetative and reproductive morphology of Gloiocladia repens (C. Agardh) Sánchez et Rodríguez-Prieto comb. nov. (Rhodymeniales, Rhodophyta), with a taxonomic re-assessment of the genera Fauchea and Gloiocladia

Figures & data

Figs 1–7. Gloiocladia repens. Habit. Fig. 1. Habit of the lectotype (LD 25705). Fig. 2. Habit of a fertile male and female gametophyte in the original collection (LD 25704). Fig. 3. Habit of a sterile specimen in the original collection (LD 25702). Fig. 4. Habit of a fertile female gametophyte in the original collection (LD 25703). Fig. 5. Habit of a tetrasporophyte (HGI-A 6320). Fig. 6. Habit of a sterile stipitate specimen (HGI-A 6746). Fig. 7. Detail of the thallus showing marginal haptera and thalli anastomoses (HGI-A 5463). Abbreviations: a: anastomosis; dh: discoid holdfast; h: hapterum; st: stipe. Scale bars: 1 cm (Figs 1–6); 0.5 cm (Fig. 7).

Table 1. Gloiocladia repens. Examined specimens. Locality, legit, date and depth of collection, herbarium identification number and phenology are indicated. All the specimens come from the coasts of Spain

Catalonia
Blanes	L. Polo: 23 May 1976 (HGI-A 2615)
Lloret de Mar	E. Ballesteros: 8 August 2003, 30 m (HGI-A 6623)
Balearic Islands
Cabrera	Ansiola. E. Ballesteros: 23 July 2003, 60 m (HGI-A 6040). Cap Falcó. C. Rodr.-Prieto: 24 May 1996, 50 m (HGI-A 1710). Cova Blava. C. Rodr.-Prieto: 23 May 1996, 30 m (HGI-A 1716). L’Imperial. C. Rodr.-Prieto: 1 May 1996, 50 m (HGI-A 1563). E. Ballesteros: 30 January 1999, 65 m (HGI-A 5759)
Eivissa	Espartar. E. Ballesteros: 14 September 2004, 55 m (HGI-A 6622)
Formentera	E. Ballesteros: 9 May 2004, 59 m (HGI-A 6621, 6334 ♂); 10 May 2004, 55 m (HGI-A 6671)
Mallorca	Cap Catalunya. E. Ballesteros: 18 July 2001, 45 m (HGI-A 5404)
Minorca	Addaia. J.J. Rodr. y Fem.: 25 March 1897, 105 m (RyF 1653 ⊕); 24 October 1899, 90 m (RyF 1654 ♂); 9 November 1899, 90 m (RyF 1656 ⊕); 10 November 1899, 90 m (RyF 1657 ♂, 1658 ♂). Alaior. J.J. Rodr. y Fem.: 29 December 1887, 95 m (RyF 1639 ⊕). Binidalí. J.J. Rodr. y Fem.: 28 May 1897, 95 m (RyF 1661 ⊕). Binisafuller. J.J. Rodr. y Fem.: 3 January 1888, 100 m (RyF 1641 ⊕, 1640 ♂). Cala Coves. J.J. Rodr. y Fem.: 28 September 1893, 75 m (RyF 1630). Canutells. J.J. Rodr. y Fem.: 3 January 1888, 110 m (RyF 1632); 19 January 1888, 110 m (RyF 1633); 4 February 1888, 95 m (RyF 1634 ⊕); 15 September 1890, 95 m (RyF 1635 ⊕); 15 December 1895, 40 m (RyF 1637); 7 January 1896, 55 m (RyF 1638 ⊕). Cap Font. J.J. Rodr. y Fem.: 11 October 1887, 95 m (MA-A 3916); 18 October 1888, 95 m (RyF 1642, MA-A 3915); 21 September 1891, 85/95 m (RyF 1643 ♂); 4 February 1897 (RyF 1644 ⊕); 22 October 1897, 70/80 m (RyF 1645 ⊕). Cap Negre. J.J. Rodr. y Fem.: 29 October 1889, 95 m (RyF 1648); 9 November 1897, 80 m (RyF 1649 ♂). Northern coast. 26 October 1889 (RyF 1646, 1647). Canal de Menorca. C. Rodr.-Prieto: 28 July 1994, 50 m (HGI-A 3242). S. Mallol: 30 August 2003, 84 m (HGI-A 5939). Els Freus. J.J. Rodr. y Fem.: 22 March 1897, 80 m (RyF 1659 ♂). Enderrosay. J.J. Rodr. y Fem.: 18 September 1891, 100 m (RyF 1650 ♂). La Mola. 24 November 1897, 95 m (RyF 1662 ⊕, 1663 ⊕). Maó. J.J. Rodr. y Fem.: 3 September 1887, 90 m (RyF 1624 ⊕); 9 April 1888, 120 m (RyF 1627 ⊕); 19 May 1890 (RyF 1626 ⊕); 26 May 1898, 10 m (RyF 1628 ⊕). Montjofre. J.J. Rodr. y Fem.: 26 March 1897, 80 m (RyF 1660 ⊕). Rafalet. J.J. Rodr. y Fem.: 29 September 1891, 100 m (RyF 1651 ♂)
?	E. Ballesteros: 20 May 2004, 62/67 m (HGI-A 6320, 6625 ⊕)
Columbretes Islands
Escala d’en Rossi	C. Rodr.-Prieto: 11 May 2002, 42 m (HGI-A 5460, 5462 ⊕, 5463 ⊕, 5470 ⊕); 4 June 2005, 42 m (HGI-A 6746, 6752, 6753, 6754, 6755, 6756, 6757, 6745 ♂). C. Rodr.-Prieto and N. Sánchez: 14 September 2002, 40 m (HGI-A 5627, 5628, 5629, 5633, 5634, 5636, 5812); 17 September 2002, 42 m (HGI-A 6170)
La Foradada	C. Rodr.-Prieto: 12 May 2002, 42 m (HGI-A 5476 ⊕)
Manco Libre	C. Rodr.-Prieto and N. Sánchez: 15 September 2002, 40 m (HGI-A 5637, HGI-A 5638 ⊕); 16 September 2002, 43 m (HGI-A 5632, 5631 ⊕). F. Boisset: 16 September 2002, 45 m (HGI-A 6300)
Mascarat	F. Boisset: 15 September 2002, 35 m (HGI-A 6301, 6302 ⊕, 6303 ♂/♀). C. Rodr.-Prieto: 11 May 2002, 35 m (HGI-A 5542 ♂)
Piedra Joaquín	E. Ballesteros: 22 June 1996, 45 m (HGI-A 1793)
?	J.C. Lino: 7 March 2002, 50 m (VAL-A 2135); 7 March 2002, 60 m (VAL-A 2159). F. Boisset: 17 May 2002, 60 m (HGI-A 6299, 6297 ⊕, 6298 ⊕)
Alboran I. sland	I. E. O.: July 1996 (MGC-A 3549). Fauna IV: July 1996 (MGC-A 3564, 3565, 3566)
Andalusia	Cadis. Cabrera (LD 25702, 25703 ♂); (LD 25704 ♂/♀, 25705 ♂) [as Sphaerococcus repens]
Galicia
A Coruña	Mugardos. C. López Varela: 1 September 1998, 12 m (SANT-A 11760 ⊕). M. Domínguez: 17 July 2003, 14 m (SANT-A 14962 ♂)
Lugo	San Ciprián. I. Bárbara, P. Díaz and J. Cremades, 13 July 2005: 6 m (SANT-A 16072); 11 m (SANT-A 16063)
Abbreviation: RyF = Herbarium of J.J. Rodríguez y Femenías.

Figs 8–13. Gloiocladia repens. Vegetative structure. Aniline blue staining. Figs 8, 9. Longitudinal (8) and transverse (9) sections of a sterile individual in the middle part of the plant (HGI-A 5631, 5637). Figs 10, 11. Cortex and subcortex in longitudinal (10) and transverse (11) section (HGI-A 5631, 5637). Fig. 12. Outer cortical cells in a surface view (HGI-A 5629). Fig. 13. Network of subcortical cells showing frequent secondary pit-connections between cells (HGI-A 5637). Abbreviation: spc: secondary pit-connection. Scale bars: 50 µm.

Figs 14–18. Gloiocladia repens. Vegetative structure. Aniline blue staining. Fig. 14. Medullary cells in transverse section showing several secondary pit-connections between them (HGI-A 5463). Fig. 15. Transverse section of the basal part of the thallus showing the development of rhizoidal filaments and secondary medullary cells (HGI-A 5632). Fig. 16. Detail of the rhizoidal filaments connected by secondary pit-connections (HGI-A 5632). Fig. 17. Transverse section of the basal part of the thallus with many secondary medullary cells (HGI-A 5632). Fig. 18. Transverse section of the stipe (HGI-A 1793). Abbreviations: rf: rhizoidal filament; smc: secondary medullary cell; spc: secondary pit-connection. Scale bars: 50 µm (Fig. 14); 100 µm (Figs 15, 17, 18); 25 µm (Fig. 16).

Figs 19, 20. Gloiocladia repens. Light photomicrographs of male reproductive structures. Aniline blue staining. Fig. 19. Transverse section of a fertile area of the thallus showing a spermatangial sorus (HGI-A 6303). Fig. 20. Transverse section of a fertile area of the thallus showing spermatia borne on spermatangial mother cells (LD 25704). Abbreviations: cc: cortical cell, s: spermatium; spmc: spermatangial mother cell. Scale bars: 50 µm.

Figs 21–25. Gloiocladia repens. Light photomicrographs of female reproductive structures and postfertilization stages. Aniline blue staining. Fig. 21. Carpogonial branch (HGI-A 6303). Fig. 22. Procarp at a stage in which the first cell of the auxiliary branch can just be distinguished (HGI-A 6303). Fig. 23. Auxiliary cell branch composed of an auxiliary mother cell and an auxiliary cell with a proteinaceous inclusion (HGI-A 6334). Fig. 24. Young gonimoblast arising from the primary gonimoblast cell. The fusion cell between the carpogonial branch cells can also been seen (LD 25703). Fig. 25. Detail of the fusion cell (HGI-A 6303). Abbreviations: ac: auxiliary cell; amc: auxiliary mother cell; c: carposporangia; cbc: cells of the carpogonial branch; cc: cortical cell; cp: carpogonium; fc: fusion cell; fcab: first cell of the auxiliary branch; fcbc: fused cells of the carpogonial branch; g: gonimoblast; nc: nutritive cell; pgc: primary gonimoblast cell; pi: proteinaceous inclusion; sc: supporting cell; tr: trichogyne; stc: sterile cell; tac: cell of the tela arachnoidea. Scale bars: 25 µm (Figs 21, 22); 50 µm (Figs 23–25).

Figs 26–30. Gloiocladia repens. Light photomicrographs of the female reproductive structures with aniline blue staining. Fig. 26. Detail of stellate nutritive cells (HGI-A 5542). Figs 27, 28. Details of stellate cells of the tela arachnoidea (HGI-A 5542). Fig. 29. Cystocarps (LD 25703). Fig. 30. Detail of the carposporangia going out through the ostiole (HGI-A 5542). Scale bars: 50 µm (Figs 26–28, 30); 5 mm (Fig. 29).

Figs 31–35. Gloiocladia repens. Tetrasporangial development. Fig. 31. Nemathecia in branch surface (HGI-A 6320). Fig. 32. Transverse section of a well-developed nemathecium (HGI-A 5463). Fig. 33. Transverse section of nemathecium with cruciately dividing tetrasporangia (HGI-A 6298). Fig. 34. Transverse section of nemathecium with decussately cruciate dividing tetrasporangia (HGI-A 6302) (aniline blue staining). Fig. 35. Transverse section of nemathecium with irregularly dividing tetrasporangia (HGI-A 6302) (aniline blue staining). Scale bars: 5 mm (Fig. 31); 100 µm (Fig. 32); 25 µm (Figs 33–35).

Figs 36, 37. Gloiocladia repens and Gloiocladia furcata. Tetrasporangial pit-connections with aniline blue staining. Fig. 36. Tetrasporangia of G. repens showing basal pit-connection with cortical filaments (HGI-A 5631). Fig. 37. Tetrasporangia of G. furcata showing lateral pit-connection with cortical filaments (HGI-A 5769). Abbreviations: bpc: basal pit-connection; lpc: lateral pit-connection; t: tetrasporangium; yt: young tetrasporangium. Scale bars: 50 µm.

Fig. 38. Phylogenetic trees resulting from analyses of 18S rRNA gene sequences of Faucheacean species. Accession numbers for previously published sequences are given below species names. Sequences generated in this study are shown in larger font. (A) One of four most parsimonious trees (length = 176; CI = 0.687; RI = 0.580). Inferred branch lengths are shown above branches, parsimony (P) and distance (D) bootstrap proportions are shown below branches. (B) Maximum-likelihood tree (lnL = −3340.58416) with likelihood bootstrap proportions shown above branches.

Table 2. Comparison of the main features of species currently placed in the genus Fauchea and transferred here to Gloiocladia

	G. fryeana (Setchell) Sánchez et Rodríguez-Prieto comb. nov.	G. furcellata (Baardseth) Sánchez et Rodríguez-Prieto comb. nov.	G. furcata (C. Agardh) J. Agardh	G. galapagensis (W.R. Taylor) Sánchez et Rodríguez-Prieto comb. nov.	G. hassleri (M. Howe et W.R. Taylor) Sánchez et Rodríguez-Prieto comb. nov.	G. laciniata (J. Agardh) Sánchez et Rodríguez-Prieto) comb. nov.	G. leptophylla (Segawa) Sánchez et Rodríguez-Prieto comb. nov.
Branch pattern	Dichotomous*	Dichotomous	Dichotomous	Dichotomous	Dichotomous	Dichotomous or subdichotomous	Dichotomous
Outer cortical filaments	Compact	Straight*	Lax, curled at the base	–	–	Lax*	–
Subcortex	–	Present*	Present	Present	Present	Present	Present
Rhizoidal medullary filaments	Present	–	Present	–	–	Present	–
Secondary medullary cells	–	–	Present	–	–	–	–
Spermatangia	–	–	–	Ill-defined areas	–	Sori	–
Plant procarpic	Yes	–	Yes	–	–	Yes	–
Supporting cell	Subcortical cell	–	Subcortical cell	Cortical cell	–	Subcortical cell	–
Cells in carpogonial branch	3	–	3	2 (3?)	–	3	–
Fusion of carpogonial branch cells	Present*	–	Present	–	–	Present	–
Cells in auxiliary cell branch	2	–	2	–	–	2	–
Connecting cell between fused  carpogonial branch cells  and auxiliary cell	Absent	–	Absent	–	–	Present	–
Nutritive cells	Present	–	Present	Present	–	–	–
Tela arachnoidea	Present	–	Present	Present	–	Present	Present*
Components of the fusion cell	Auxiliary mother cell, auxiliary cell, surrounding cells	–	Auxiliary mother cell, lower auxiliary cell, fused cells of carpogonial branch, surrounding cells	–	–	Auxiliary mother cell, auxiliary cell, fused cells of carpogonial branch	–
Fusion cell shape	–	–	Globose	–	–	–	–
Gonimoblast origin	Primary gonimoblast cell*	–	Primary gonimoblast cell	Erect, big and ovoid cell	–	Primary gonimoblast cell*	–
Cystocarp locating	Marginal	–	Marginal	Marginal	Marginal	Marginal, scattered	Marginal
Cystocarp sessile or stipitate	–	–	Sessile	–	Sessile	–	–
Cystocarp coronate	Occasionally	–	Occasionally	Yes	–	Yes	No
Ostiole	Present	–	Present	Present	–	Present	Present*
Tetrasporangia arrangement	Sori/nemathecia	Swollen sori	Slightly raised nemathecia or scattered	Sori	–	Sori (nemathecia*)	–
Situation of tetrasporangia	Subapical	–	Subapical	–	–	–	–
Situation of the pit-connection	–	–	Lateral	–	–	–	–
Division of tetrasporangia	Cruciate or decussate*	Cruciate or decussate*	Cruciate or decussate	–	–	Cruciate	–
References	Sjöstedt, 1926; Sparling, 1957; Abbott & Hollenberg, 1976	Baardseth, 1941	Sánchez, 2005; Sánchez & Rodríguez-Prieto, 2005	Taylor, 1945; Abbott & Hollenberg, 1976	Taylor, 1960	Sparling, 1957; Dawson, 1963	Segawa, 1941
	G. microspora (Bornet ex Rodríguez y Femenías) Sánchez et Rodríguez-Prieto comb. nov.	G. procumbens (Weber-van Bosse) Sánchez et Rodríguez-Prieto comb. nov.	G. profunda (Børgesen) Sánchez et Rodríguez-Prieto comb. nov.	Gloiocladia repens (C. Agardh) Sánchez et Rodríguez-Prieto comb. nov.	G. spinulosa (Okamura et Segawa in Segawa) Sánchez et Rodríguez-Prieto comb. nov.	G. stipitata (Yamada et Segawa) Sánchez et Rodríguez-Prieto comb. nov.	G. xishaensis (B.M. Xia et Y.Q. Wang) Sánchez et Rodríguez-Prieto comb. nov.
Branch pattern	Dichotomous	Distichous	Irregular	Subdichotomous	Dichotomous*	Di- or polichotomous	–
Outer cortical filaments	Lax	–	–	Compact/straight	–	–	–
Subcortex	Present	–	Present	Present	Present	–	Present
Rhizoidal medullary filaments	–	–	–	Present	–	–	–
Secondary medullary cells	–	–	–	Present	–	–	–
Spermatangia	–	–	–	Sori	–	–	Sori
Plant procarpic	–	–	–	Yes	–	–	–
Supporting cell	–	–	–	Mid outer cortical cell	–	–	–
Cells in carpogonial branch	–	–	–	3 + 1 lateral cell	–	–	–
Fusion of carpogonial branch cells	–	–	–	Present	–	–	–
Cells in auxiliary cell branch	–	–	–	2	–	–	–
Connecting cell between fused carpogonial branch cells and auxiliary cell	–	–	–	Absent	–	–	–
Nutritive cells	–	–	–	Present	–	–	Present
Tela arachnoidea	–	–	Present	–	Present	Present*
Components of the fusion cell	–	–	–	Auxiliary mother cell, lower auxiliary cell, fused cells of the carpogonial branch, supporting cell, surrounding cells	–	–	–
Fusion cell shape	–	–	–	Elongated	–	–	–
Gonimoblast origin	–	–	–	Primary gonimoblast cell	–	–	–
Cystocarp locating	Marginal	–	–	Marginal	–	Marginal	Scattered
Cystocarp sessile or stipitate	Sessile	–	–	Stipitate	–	Stipitate	–
Cystocarp coronate	–	–	–	No	Yes	No	–
Ostiole	–	–	–	Present	–	–	Present
Tetrasporangia arrangement	Nemathecia	–	Sori (Very raised  nemathecia*)	Very raised  nemathecia	–	–	–
Situation of tetrasporangia	–	–	–	Subapical	–	–	–
Situation of the pit-connection	–	–	–	Basal	–	–	–
Division of tetrasporangia	Cruciate or decussate*	–	Cruciate or  decussate	Cruciate, decussate  or irregular	–	–	–
References	Bornet, 1890	Weber-van Bosse,  1928	Børgesen, 1944	This work	Norris & Aken, 1985	Yamada, 1941	Xia & Zhang, 1999
Key: *: from the illustrations; –: unknown.

Table 3. Formal transfers to the genus Gloiocladia

Gloiocladia fryeana (Setchell) Sánchez et Rodríguez-Prieto comb. nov.

BASIONYM: Fauchea fryeana Setchell, Univ. Calif. Publ. Bot., 4: 239, pl. 31, figs 13, 14. 1912.

Gloiocladia furcellata (Baardseth) Sánchez et Rodríguez-Prieto comb. nov.

BASIONYM: Fauchea furcellata Baardseth, Results of the Norwegian Scientific Expedition to Tristan da Cunha 1937–1938, 9: 80–81,  figs 41, 42. 1941.

Gloiocladia laciniata (J. Agardh) Sánchez et Rodríguez-Prieto comb. nov.

BASIONYM: Fauchea laciniata J. Agardh, Acta Univ. Lund 21: 40. 1885.

SYNONYMS: Fauchea laciniata f. pygmaea Setchell et N.L. Gardner in Setchell, Univ. Calif. Publ. Bot., 4: 238. 1912.

Fauchea pygmaea (Setchell et N.L. Gardner in Setchell) Kylin, Acta Univ. Lund, 37(2): 27. 1941.

Fauchea media Kylin, Lunds Universitets Årsskrift, Ny Foljd, Andra Afdelningen, 37(2): 27, pl. 10, fig. 24. 1941.

Gloiocladia galapagensis (W.R. Taylor) Sánchez et Rodríguez-Prieto comb. nov.

BASIONYM: Fauchea galapagensis W.R. Taylor, Allan Hancock Pacif. Exped., 12: 246–247, pl. 82, figs 1, 2. 1945.

Gloiocladia hassleri (M. Howe et W.R. Taylor) Sánchez et Rodríguez-Prieto comb. nov.

BASIONYM: Fauchea hassleri M. Howe et W.R. Taylor, Brittonia, 1: 13, fig. 6, pl. 2, figs 2, 3. 1931.

Gloiocladia leptophylla (Segawa) Sánchez et Rodríguez-Prieto comb. nov.

BASIONYM: Fauchea leptophylla S. Segawa, Sci. Pap. Inst. Algol. Res., Fac. Sci. Hokkaido. Univ., 2: 264–265, fig. 10, pl. 58, fig. 1. 1941.

Gloiocladia microspora (Bornet ex Rodríguez y Femenías) Sánchez et Rodríguez-Prieto comb. nov.

BASIONYM: Fauchea microspora Bornet ex Rodríguez y Femenías, Bull. Soc. Bot. Fr., 37: 142, figs 1–4. 1890.

Gloiocladia procumbens (Weber-van Bosse) Sánchez et Rodríguez-Prieto comb. nov.

BASIONYM: Fauchea procumbens Weber-van Bosse, Siboga Exped. Monogr., 59: 459, pl. 11, figs 2, 3. 1928.

Gloiocladia profunda (Børgesen) Sánchez et Rodríguez-Prieto comb. nov.

BASIONYM: Fauchea profunda Børgesen, Det Kgl. Danske Vid. Selsk. Biol. Medd., 19: 11, figs 6–8. 1944.

Gloiocladia repens (C. Agardh) Sánchez et Rodríguez-Prieto comb. nov.

BASIONYM: Sphaerococcus repens C. Agardh, Species Algarum rite cognitae. Vol. 1, part 2: 244–245. 1823.

SYNONYMS: Gracilaria repens (C. Agardh) J. Agardh, Algae maris Mediterranei et Adriatici, 152. 1842.

Dichophycus repens (C. Agardh) Zanardini, Atti del Reale Istituto Veneto di Scienze, Lettere ed Arti, 6: 16, pl. 6, figs a–i. 1847.

Fauchea repens (C. Agardh) Montagne et Bory in Montagne, Exploration scientifique de l’Algérie pendant 1840–42, Sciences naturelles, Botanique, 1, Cryptogamie: 64–67. 1846.

Gloiocladia spinulosa (Okamura et Segawa in Segawa) Sánchez et Rodríguez-Prieto comb. nov.

BASIONYM: Fauchea spinulosa Okamura et Segawa in Segawa, Sci. Pap. Inst. Algol. Res., Fac. Sci., Hokkaido Univ., 1: 84–85, figs 4, 5, pl. 20, fig. 2. 1935.

Gloiocladia stipitata (Yamada et Segawa) Sánchez et Rodríguez-Prieto comb. nov.

BASIONYM: Fauchea stipitata Yamada et Segawa in Yamada, Sci. Pap. Inst. Algol. Res. Fac. Sci., Hokkaido Univ., 2: 200, pl. 44. 1941.

Gloiocladia xishaensis (B.M. Xia et Y.Q. Wang) Sánchez et Rodríguez-Prieto comb. nov.

BASIONYM: Fauchea xishaensis B.M. Xia et Y.Q. Wang, Acta Phytotaxon. Sin., 38: 38, figs 3, 6. 2000.

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