Some Delesseriaceae (Ceramiales, Rhodophyta) new to the southwestern Atlantic

Algumas Delesseriaceae (Ceramiales, Rhodophyta) novas para o sudoeste do Atlântico

Some Delesseriaceae (Ceramiales, Rhodophyta) new to the southwestern Atlantic

PAULO A. HORTA¹,² and EURICO C. OLIVEIRA¹

(received: May 10, 2000; accepted: August 22, 2001)

ABSTRACT- (Some Delesseriaceae (Ceramiales, Rhodophyta) new to the southwestern Atlantic). Up to now 18 species of Delesseriaceae have been referred to the Brazilian coast, nine of which belong to the subfamily Delesserioideae. Here we report for the first time the occurrence of Apoglossum gregarium (Dawson) Wynne, Branchioglossum minutum Schneider and Hypoglossum anomalum Wynne & Ballantine collected by SCUBA diving on islands of the south and southeastern coast of Brazil. This report is an indication that the subtidal has been undersampled on the southwestern Atlantic.

RESUMO - (Algumas Delesseriaceae (Ceramiales, Rhodophyta) novas para o sudoeste do Atlântico). Até agora 18 espécies de Delesseriaceae (Rhodophyta) foram citadas para a costa brasileira, dentre as quais nove pertencentes à subfamília Delesserioideae. Aqui reportamos, pela primeira vez, a presença de Apoglossum gregarium (Dawson) Wynne, Branchioglossum minutum Schneider e Hypoglossum anomalum Wynne & Ballantine coletadas através de mergulho autônomo em ilhas do sul e sudeste do Brasil. Esta é mais uma contribuição mostrando que a biodiversidade algal do infralitoral é ainda pouco conhecida no Atlântico Sul Ocidental.

Key words - Delesseriaceae, Apoglossum, Branchioglossum, Brazil, Hypoglossum

Introduction

The family Delesseriaceae (Ceramiales, Rhodophyta) has more than 90 genera divided into two subfamilies (Wynne 1996). In the subfamily Delesserioideae procarps are located on the primary cell row near the blade tip, whereas in the Nitophylloideae procarps are randomly distributed over the blade surface (Maggs & Hommersand 1993).

Among the 18 species of Delesseriaceae referred to Brazil (cf. www.ib.usp.br/algamare-br, based on Oliveira Filho 1977, Cordeiro-Marino & Guimarães 1981, Yoneshigue 1985, Bouzon 1989) nine belong in the Delesserioideae, assigned to the genera Caloglossa (Harv.) G. Martens, Cottoniella Børgesen, Hypoglossum Kützing, Platysiphonia Børgesen, and Taenioma J. Agardh.

Although the flora of the southeastern coast of Brazil is the best known in the country, most of the information is based on collections from the intertidal and on relatively few dredgings. Here we refer for the first time to the Brazilian coast and southwestern Atlantic species of the genera Hypoglossum, Apoglossum J. Agardh, and Branchioglossum Kylin.

The three genera dealt with here have a similar morphology. The genus Apoglossum, however, is distinct from Hypoglossum and Branchioglossum because not all initials of third order rows reach the blade margin, whereas in Hypoglossum and Branchioglossum the initials of all the third-order cell rows do reach the margin (Wynne 1988, Maggs & Hommersand 1993). In Branchioglossum primary branching is marginal, by conversion of a distal second-order cell row into a primary initial, whereas in Hypoglossum primary branching is endogenous and produced from the midrib (Millar & Wynne 1992).

Material and methods

Sampling was made by SCUBA dives, in different sites, depths and occasions at the southeastern coast of Brazil. Material preserved in formalin 4% in seawater was stained with aniline blue 1%, acidified with 1 N HCl, and mounted in 50% Karo Syrup. The photographs were taken on a standard Leica microscope. The studied specimens are deposited at the Phycological Herbarium of the University of São Paulo, Brazil (SPF).

Results and Discussion

Apoglossum gregarium (Dawson) Wynne Bull. Southern California Acad. Sci., 84: 164. 1985.

Basionym: Hypoglossum gregarium Dawson, 1966, J. Ariz. Acad. Sc. 4, p. 65, figure 6c; Phrix gregarium (Dawson) Stewart, 1974, Phycologia 13: 147.

Synonym: Membranoptera spatulata Dawson, 1950, Am. J. Botany 37: 157, figure 15.

Studied material: São Paulo, Rapada Island (23°26' S, 44°54' W), 02/04/99, 9 m deep, on rhodoliths, PH 28; Castilho Island (25°17' S, 47°57' W), 13/01/99, PH 11 (tetrasporic), 12 m deep, epilithic. Coll. P. Horta.

Plants consisting of delicate erect monostromatic blades, except at the midrib, 2.5-6.4 mm long and 0.6-2.5 mm wide, attached by a compact discoid rhizoidal system (figure 1). A light rhizomatous cortication is present at the basal portion (figure 2); apex emarginate (figure 3); lateral microscopic veins can be seen on older blades (figure 4). Axial cells 76-135 mm long and 11-20 mm in diameter; lateral pericentral cells, 48-155 mm long and 15-30 mm in diameter, do not divide transversely except in portions within the tetrasporangial sori. Continuous tetrasporangial sori distributed along midrib, 0.95-1.6 mm long and 0.14-0.30 mm at the widest portions; tetrasporangia tetrahedrally divided 30-36 mm in diameter (figures 5-7). Spermatangial sori separated by sterile cells (figure 8). Female plants were not found.

Apoglossum gregarium is distinct from A. ruscifolium (Turner) J. Agardh, a species already reported from the Atlantic (Schneider & Searles 1991, Maggs & Hommersand 1993, Coppejans & Kling 1995, Stegenga et al. 1997), by its smaller thallus and tetrasporangia size. Besides that, A. ruscifolium has spermatangial sori as a series of narrow striae running diagonally from the midrib towards the blade margins (Wynne 1984).

Other related species are Apoglossum spathulatum (Sonder) Womersley & Shepley and A. unguiculescens Millar. Both can be distinguished from A. gregarium by having lateral branches produced from the central midrib (Wynne 1984, Millar 1990), whereas in A. gregarium they arise from a cylindrical basal axis or from decumbent fragments (Ballantine & Wynne 1985).

Our plants are very similar to A. gregarium studied by Ballantine & Wynne (1985) from the Caribbean and Gulf of Mexico, Sartoni & Boddi (1993) from the Mediterranean, Wynne (1985) from California and Pacific Mexico, Wynne & Norris (1991) from South Africa, and by Schneider (2000) from Bermuda, being equally corticated by rhizoids in the basal portions and with spermatangial sori separated by sterile cells.

Branchioglossum minutum C.W. Schneider Nova Hedwigia, 24: 92, figures 13, 15, 16. 1974.

Studied material: Santa Catarina, Tacami Island (28°21' S, 48°36' W), 17/01/99, 8-15 m deep, PH 42-44; São Paulo, Rapada Island (23°26' S, 44°54' W), 02/04/1999, 10 m deep, on rhodoliths, PH - 39. Coll. P. Horta.

Pink delicate plants, 3-12 mm in height and 350-2260 µm in width. Thallus erect or prostrate, monostromatic blade presenting an evident central midrib, corticated at the basal portion; all cells of second-order rows bearing third-order rows; attached to the substract by a rhizoidal disk; oblanceolate to linear-lanceolate blades produce branches at the margin from the terminal cells of the second-order cell rows, with irregular, opposite or occasionally alternate disposition; apices pointed, occasionally obtuse (figures 9-11); thallus margin undulated, presenting multicellular rhizoids (figure 21). Axial cells 78-166 µm in length and 19-60 µm in diameter, surrounded by pericentral cells.

Tetrasporangia tetrahedrally divided, 15-40 (56) µm in diameter, arranged in contiguous rounded sori along the midrib, 330-700 µm long and 300-530 µm wide (figure 12). Male plant with spermatangial sori diagonally located, confluent or interrupted when young, on both sides of the midrib, occupying the distal half or almost the whole extension of the male frond (figures 13-17). Female plant with four-celled carpogonial branch (figure 19) produced from the midrib; cystocarps (figures 18, 20) 220-605 µm in diameter at the base; carpospores spherical 20-39 (54) µm in diameter.

The distribution of tetrasporangia in groups of scattered circular sori in Branchioglossum pygmaeum Wynne & Norris (Wynne & Norris 1991), from South Africa, distinguishes it from our specimens. On the other hand, B. epiphyticum Millar et Wynne presents holdfasts produced submarginally in association with lateral blades, or rarely from the blade apices (Millar & Wynne 1992), what differs from our material.

Our specimens present several similarities with Branchioglossum bipinnatifidum (Montagne) Wynne from the eastern Pacific. However, B. bipinnatifidum differs from our plants in the location of the tetrasporangial sori which are in an intermediate portion between the margin and the midrib (Abbott & Hollenberg 1976, Wynne 1988). Branchioglossum nanum Inagaki is also distinct from our plants by having elongate tetrasporangial sori, in only one or two rows on both sides of the midrib (Millar & Wynne 1992), whereas B. minutum presents rounded tetrasporangial sori contiguous with the midrib.

Branchioglossum spiniferum Yoshida & Mikami differ from our plants because not all secondary cell rows give rise to third-order cell rows (Yoshida & Mikami 1992).

Branchioglossum minutum differs from Frikkiella pseudoprostrata (Ballantine & Wynne) Wynne & Schneider (Wynne & Schneider 1996), described by Ballantine & Wynne (1987, as B. pseudoprostratum) for in Frikkiella not all the cells of the second-order rows produce third-order rows. Besides, in oposition to Branchioglossum, in Frikkiella branches are initiated from marginal cells.

Branchioglossum prostratum Schneider, in spite of having about the same morphology and dimensions as our material, can be distinguished for having scattered spermatangial sori. However, Wynne (1988) concluded that variations in the height and margin of the blade and the location of the tetrasporangial sorus are not discrete criteria for distinction between Branchioglossum bipinnatifidum (Montagne) Wynne and B. woodii (J. Agardh) Kylin. Wynne's observation leads us to question the maintenance of Branchioglossum minutum (table 1) because of the variability we found within populations at Tacami and Rapada Island, in addition to the information presented in the literature (Schneider 1974, Schneider & Searles 1975, Schneider & Searles 1991). The finding of scattered spermatangial sori in some plants of the Brazilian populations indicates that this criterion should be more critically evaluated.

Hypoglossum anomalum Wynne & Ballantine J. Phycol., 22: 185. 1986.

Studied material: São Paulo, Queimada Grande Island (46°41' W, 24°29' S), 27/08/97, PH 81-87, 8-12 m deep, 11/11/97, PH 88-90, 08-16 m deep, epilithic. Coll. P. Horta.

Rosy delicate plants with undulated blade, monostromatic except at the midrib; thallus prostrate, dorsiventral, 20 mm long and 2 mm wide. Frequent anastomoses and multicellular rhizoids arising from abaxial face of the midrib or blade margin attaching to other blades and producing an entangled aspect. Opposite pairs of branches originating from the axial cells of the midrib but emerging at an intermediary position between the margin and the midrib (figures 22-30).

Fertile plants were not found, which perhaps is an indication that the species is at its southern limit of distribution, propagating only vegetatively.

This species differs from the two other species of Hypoglossum referred to Brazil by the pattern of blade construction. Hypoglossum hypoglossoides (Stackhouse) Collins & Hervey, referred to Oliveira Filho (1969) and Yoneshigue (1985) as Hypoglossum tenuifolium (Harvey) J. Agardh var. carolinianum Williams, although having all the cells of the second-order rows producing third-order rows, branches from the midrib, whereas H. tenuifolium (Cordeiro-Marino & Guimarães 1981) does not produce third-order rows from every cell of the second-order rows.

In spite of the Brazilian specimens being a little smaller than the type material (Wynne & Ballantine 1986) the diagnostic presence of the branch primordia initiated endogenously (Wynne 1994, Wynne & Norris 1991) supports our identification. None of the taxa described for other regions by Womersley & Shepley (1982), Wynne & Kraft (1985), Yoshida & Mikami (1986), Ballantine & Wynne (1988), Wynne (1989), Wynne et al. (1989), Wynne (1994) and Abbott (1996) fit the attributes of the Brazilian plants better than H. anomalum, previously described for Guadeloupe, Puerto Rico, Florida, South Africa and Indian Ocean (Wynne & Ballantine 1986, Wynne & Norris 1991, Wynne 1989).

This paper is a first contribution reporting the results of a new effort to survey the infralittoral benthic seaweed flora of Brazil, so far based mostly on intertidal sampling. The finding of the three new references of Delesserioideae algae reported in this paper is an indication that other taxa may be found in other groups as well. This will certainly enlarge the list of species that are known for this part of the world and will supply new evidence to test the biogeographic hypothesis put forward to explain the origins and affinities of the Brazilian seaweed flora as discussed by Taylor (1955), Joly (1965), and Oliveira Filho (1977).

Acknowledgements - This research was supported by FAPESP (process: 98/05776-5). E. Oliveira acknowledges a CNPq scholarship. We thank Professor M. Wynne for a careful revision of the manuscript and Dr. C.W. Schneider for his remarks regarding the identification of Branchioglossum prostratum.

2. Corresponding author: [e-mail]

• ABBOTT, I.A. 1996. New species and notes on marine algae from Hawaii. Pacific Science 50:142-156.
• ABBOTT, I.A. & HOLLENBERG, G.J. 1976. Marine Algae of California. Stanford University Press, Stanford.
• BALLANTINE, D.L. & WYNNE, M.J. 1985. Platysiphonia and Apoglossum (Delesseriaceae, Rhodophyta) in the tropical western Atlantic. Phycologia 24:459-465.
• BALLANTINE, D.L. & WYNNE, M.J. 1987. Notes on the marine algae of Puerto Rico. III. Branchioglossum pseudoprostratum new species and B. prostratum Schneider (Rhodophyta: Delesseriaceae). Bulletin of Marine Science 40:240-245.
• BALLANTINE, D.L. & WYNNE, M.J. 1988. The life history and development of Hypoglossum rhizophorum (Delesseriaceae, Rhodophyta) in culture, a new deep-water species from the Caribbean. Journal of Phycology 24:812.
• BOUZON, Z.L. 1989. A ocorręncia de Cottoniella filamentosa (Howe) Břrgesen no sul do Brasil. Ínsula 19:191-198.
• COPPEJANS, E. & KLING, R. 1995. Flore algologique des côtes du nord de la France et de la Belgique. Jardin Botanique National de Belgique, Meise.
• CORDEIRO-MARINO, M. & GUIMARĂES, S.M.P.B. 1981. Novas referęncias para a flora marinha de profundidade do Brasil. Rickia 9:61-70.
• JOLY, A.B. 1965. Marine flora of the tropical and subtropical Western South Atlantic. Anais da Academia Brasileira de Cięncias 37:279-282.
• MAGGS, C.A. & HOMMERSAND, M.H. 1993. Seaweed of the British Isles. v. 1. Rhodophyta. Part 3A. Ceramiales. HMSO Publications, London.
• MILLAR, A.J.K. 1990. Marine red algae of the Coffs Harbour region, northern New South Wales. Australian Systematic Botany 3:293-593.
• MILLAR, A.J.K. & WYNNE, M.J. 1992. Branchioglossum epiphyticum sp. nov. (Delesseriaceae, Rhodophyta), with a discussion of the generic bounderies between Branchioglossum and Hypoglossum Phycologia 31:231-239.
• OLIVEIRA FILHO, E.C. 1969. Algas marinhas do sul do Estado do Espirito Santo (Brasil). I - Ceramiales. Boletim da Faculdade de Cięncias e Letras da Universidade de Săo Paulo 343:1-277.
• OLIVEIRA FILHO, E.C. 1977. Algas marinhas bentônicas do Brasil. Tese de livre docęncia, Universidade de Săo Paulo, Săo Paulo.
• SARTONI, G. & BODDI, S. 1993. Apoglossum gregarium (Delesseriaceae, Rhodophyta), a new record for Mediterranean algal flora. Botanica Marina 36:297-302.
• SCHNEIDER, C.W. 1974. North Carolina Marine Algae. III. A community of Ceramiales on a glass sponge from 60 meters. Bulletin of Marine Science 24:1093-1101.
• SCHNEIDER, C.W. 2000. Notes on the Marine Algae of the Bermudas. 5. Some Delesseriaceae (Ceramiales, Rhodophyta), including the first record of Hypoglossum barbatum Okamura from the Atlantic Ocean. Botanica Marina 43:455-466.
• SCHNEIDER, C.W. & SEARLES, R.B. 1975. North Carolina marine algae. IV. Further contributions from the continental shelf, including two new species of Rhodophyta. Nova Hedwigia 24:83-103.
• SCHNEIDER, C.W. & SEARLES, R.B. 1991. Seaweeds of the southeastern United States: Cape Hatteras to Cape Canaveral. Duke University Press, Duke.
• STEGENGA, H., BOLTON, J.J. & ANDERSON, R.J. 1997. Seaweeds of the South African west coast. Contributions from the Bolus Herbarium 18:1-655.
• TAYLOR, W.R. 1955. Marine algal flora of the Caribbean and its extension into neighboring seas. In Essays in the Natural Sciences in honour of Captain Allan Hancock, Los Angeles.
• WOMERSLEY, H.B.S. & SHEPLEY, E.A. 1982. Southern Australian species of Hypoglossum (Delesseriaceae, Rhodophyta). Australian Journal of Botany 30:321-346.
• WYNNE, M.J. 1984. The occurrence of Apoglossum and Delesseria (Ceramiales, Rhodophyta) in South Africa. South African Journal of Botany 3:137-145.
• WYNNE, M.J. 1985. Taxonomic notes on some Delesseriaceae (Rhodophyta) occurring in Southern California and Mexico. Bulletin Southern California Academy of Science 84:164-171.
• WYNNE, M.J. 1988. Notes on Branchioglossum Kylin (Delesseriaceae, Rhodophyta) in the eastern Pacific. Cryptogamie, Algologie 9:53-64.
• WYNNE, M.J. 1989. A reassessment of the Hypoglossum group (Delesseriaceae, Rhodophyta), with a critique of its genera. Helgoländer Wissenschaftliche Meeresuntersuchungen 42:511-534.
• WYNNE, M.J. 1994. The description of Hypoglossum subsimplex sp. nov. (Delesseriaceae, Rhodophyta) from the Florida Keys, Gulf of Mexico. Cryptogamie, Algologie 15:253-262.
• WYNNE, M.J. 1996. A revised key to genera of the red algal family Delesseriaceae. Nova Hedwigia 112:171-190.
• WYNNE, M.J. & BALLANTINE, D.L. 1986. The genus Hypoglossum Kützing (Delesseriaceae, Rhodophyta) in the tropical western Atlantic, including H. anomalum sp. nov. Journal of Phycology 22:185-193.
• WYNNE, M.J. & KRAFT, G.T. 1985. Hypoglossum caloglossoides sp. nov. (Delesseriaceae, Rhodophyta) from Lord Howe Island, South Pacific. British Phycological Journal 20:9-19.
• WYNNE, M.J. & NORRIS, R.E. 1991. Branchioglossum pygmaeum sp. nov. and the new records of other delesseriaceous algae (Rhodophyta) from Natal, South Africa. Phycologia 30:262-271.
• WYNNE, M.J., PRICE, I.R. & BALLANTINE, D.L. 1989. Distinction between Hypoglossum barbatum Okamura, H. minimum Yamada and H. simulans sp. nov. (Delesseriaceae, Rhodophyta). Phycologia 28:28-38.
• WYNNE, M.J. & SCHNEIDER, C.W. 1996. Frikkiella gen. nov. (Delesseriaceae, Rhodophyta) from Bermuda and Caribbean Sea. Systematic Botany 21:77-84.
• YONESHIGUE, Y. 1985. Taxonomie et ecologie des algues marines dans la region de Cabo Frio (Rio de Janeiro, Brésil). Thčse de Docteur, Université de d'Aix-Marseille, Luminy.
• YOSHIDA, T. & MIKAMI, H. 1986. Observations on the morphology of Hypoglossum minimum Yamada and H. geminatum Okamura (Delesseriaceae, Rhodophyta). Japanese Journal of Phycology 34:177-184.
• YOSHIDA, T. & MIKAMI, H. 1992. Branchioglossum spiniferum sp. nov. (Delesseriaceae, Rhodophyta) from north Kyushu, Japan. Japanese Journal of Phycology 40:379-384.

1

. Universidade de São Paulo, Instituto de Biociências, Departamento de Botânica, Caixa Postal 11461, 05422-970 São Paulo, SP, Brasil.

Publication Dates

• Publication in this collection
  31 July 2002
• Date of issue
  Dec 2001

History

• Accepted
  22 Aug 2001
• Received
  10 May 2000