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Gayana (Concepción)

versión On-line ISSN 0717-6538

Gayana (Concepc.) v.70 n.2 Concepción dic. 2006

http://dx.doi.org/10.4067/S0717-65382006000200012 

Gayana 70(2): 245-251, 2006


First record of a ceramiaceous red algal species, Ceramium stichidiosum, from magellanic region, chile


Primer registro del alga roja Ceramium stichidiosum en la regiOn de magallanes, chile


Andrés Mansilla1, Nelso P. Navarro1 & Mutue T. Fujii2


1Departamento de Ciencias y Recursos Naturales, Facultad de Ciencias, Universidad de Magallanes, Casilla 113-D, Punta Arenas, Chile.

2Instituto de Botânica, Seção de Ficologia, Av. Miguel Estefano 3687, 04301-102 São Paulo, SP, Brasil

Email: andres.mansilla@umag.cl


ABSTRACT

A ceramiaceous red alga, Ceramium stichidiosum J. Agardh was found for the first time in waters of Magellanic Strait, Chile. Thalli are usually epiphytic on other macroalgae such as Mazzaella laminarioides (Bory) Fredericq and Sarcothalia crispata (Bory) Leister. They have fully corticated axes with alternate to dichotomous branches, straight tips and six periaxial cells per each axial cell. This report extends the distribution limit of C. stichidiosum from the X Región de los Lagos (42º 58'S; 74º 19'W) to the XII Región de Magallanes (53°37'S; 70°59'W).

Keywords: Ceramium, Ceramium stichidiosum, Chile, geographical distribution, Rhodophyta, taxonomy.


RESUMEN

La alga roja Ceramium stichidiosum fue encontrada por primera vez en aguas del Estrecho de Magallanes, Chile. Los talos son frecuentemente encontrados epifitando otras macroalgas como Mazzaella laminarioides (Bory) Fredericq y Sarcothalia crispata (Bory) Leister. Se caracteriza por presentar ejes completamente corticados y ramificaciones alternadas a dicótomas, ápices rectos y seis células periaxiales por cada célula central. Este reporte extiende el límite de distribución sur de C. stichidiosum desde la X Región de los Lagos (42º 58'S; 74º 19'W) hasta la XII Región de Magallanes (53°37'S; 70°59'W).

Palabras claves: Ceramium, Ceramium stichidiosum, Chile, distribución geográfica, Rhodophyta, taxonomía.



INTRODUCTION

Ceramium Roth (Ceramiaceae, Rhodophyta) is a cosmopolitan genus that commonly occurs in both hemispheres, on the tropical as well as on polar coasts (Boo & Lee 1994). The genus is characterized by great specific diversity with more than 191 species described all over the world (Boo & Lee 1994, Barreto & Yoneshigue-Valentin 2001, Fujii et al. 2001, Cho et al. 2003). Furthermore, the genus presents a great morphological variability and

taxonomic instability in red algae (Womersley 1978, Boo & Lee 1994, Maggs & Hommersand 1993, Fujii et al. 2001). The most prominent taxonomical characteristics of the genus are the nodal cortication patterns from periaxial cells at upper ends of axial cells forming partial or complete investment; the number and formation pattern of the periaxial cells and their derivatives, apex form, and tetrasporangial patterns (Nakamura 1965, Itono 1972, Boo 1993, Maggs & Hommersand 1993, Boo & Lee 1994, Athanasiadis 1996).

On temperate South American coast, 14 species of Ceramium have been reported. Of these, 13 species occur on the Chilean coast (Ramírez & Santelices 1991), and eight of the species are distributed in the Magellan and Antarctic regions of Chile or are endemic to this region: C. circinnatum (Kützing) J. Agardh, C. diaphanum (Lightfoot) Roth, C. dozei Hariot, C. involutum Kützing, C. rubrum (Hudson) J. Agardh, C. strictum Greville & Harvey, C. ungulatum (Kützing) Hariot, and one unidentified taxon (Ramírez & Santelices 1991).

Ceramium stichidiosum J. Agardh was at first recognized based on collections from Chatham Islands, New Zealand and Tasmania, Australia (J. Agardh 1876). The species is characterized by dichotomously branched thalli with fully corticated axes and tetrasporangial branches referred to stichidia (J. Agardh 1876). Ceramium stichidiosum is mostly found in the sectors of Las Cruces, Pelancura and Los Molles (central Chile) and also occurs in Chiloé and Puerto Montt (southern Chile) (Santelices & Abbott 1978, Ramírez & Santelices 1991, Hoffmann & Santelices 1997).

In this paper, we proposed to extend the range of distribution of Ceramium stichidiosum in the Chilean territory by reporting its occurrence in the Magellan Region (53°37'S; 70°59'O). Here, we report detailed morphology of the species such as cortication pattern, the number and distribution of the periaxial cells, its acropetal and basipetal distribution and the tetrasporangial structures.


MATERIALS AND METHODS

The studied plants were collected in the intertidal zone of the San Juan sector, Magellan Strait, Chile and were immediately fixed in 4% formalin/seawater. Longitudinal and cross sections were made with a stainless steel razor blade under a stereoscopic dissection microscope, and stained with 0.5% aqueous aniline blue solution, acidified with 1% diluted HCl. Photomicrographs were taken with an Olympus BH-2 microscope. Drawings were made with the aid of a Zeiss camera lucida.

All voucher specimens of Ceramium stichidiosum were deposited in the Herbarium of the Institute of Botany in Sao Paulo, Brasil (SP365 652) and in the collection of marine algae in the Faculty of Sciences of the Universidad de Magallanes in Punta Arenas, Chile.




Figure 1. Collection site of Ceramium stichidiosum.

Figura 1. Sitio de recolección de Ceramium stichidiosum.


Study area

San Juan sector, where material was collected, is situated in the region of the Magellan Strait (53°37'S; 70°59'W), approximately 70 km of the city of Punta Arenas, Chile (Fig. 1). The sampling area is characterized by rocky substrates, with stones and boulders. Furthermore, the area is characterized by strong hydro-energetic activity all year round. According to the classification by Köppen, the climate corresponds to the trans-Andean type with degeneration to steppe Dfk'c. The category Df is defined by a uniform distribution of precipitation, with mean annual rainfall between 400 and 620 mm. In this type of climate, precipitation mainly occurs as snow. The mean temperature is around 5.8°C (Pisano 1977). The region is also characterized by a great variation in the amount of daily temperature throughout the year. During winter, less than eight hours of sunshine are registered whereas about 16 hours of sunlight in the summer.


RESULTS

Ceramium stichidiosum J. Agardh, 1876: p. 105

Reference: Agardh, J.G. (1876). Species genera et ordines algarum. Volumen tertium. Part 1. pp. vii + 724 Lipsiae [Leipzig].

Habit: Thalli are purplish to dark red color, up to 4 cm high, forming tufts on rocky substrate or epiphytic on Mazzaella laminarioides (Bory) Fredericq and Sarcothalia crispata (Bory) Leister. The thalli consist of uniaxial filamentous branches, showing alternate to dichotomous patterns. All branches are fully corticated by cortical cells. Apices are straight to slightly incurved (Fig. 2).

In surface view, cortical cells of vegetative structures are continuous throughout the thalli. Cells in the nodes are regular to elongate of 15-25 mm in diameter and 20 mm of length, decreasing in size to acropetal and basipetal directions (Fig. 3). In a nodal cross section, a central cell produces five to six periaxial cells (Fig. 4). The cortex in nodes is formed from the periaxial cells. Each periaxial cell gives rise up to four, primary cortical cells, two acropetal and two basipetal cells. Each primary cortical cells produces two to three small cortical cells; similar pattern is produced by acropetal and basipetal secondary cortical cells. Adventitious branches are sometimes produced from periaxial cells. Rhizoids are disc-shaped and originated from periaxial cells.

Reproductive structures: Tetrasporangia are mostly localized in apical regions of terminal branches, appearing stichidial branches. They are produced from periaxial cells in the nodes (Fig. 5, 6). Tetrasporangia are tetrahedrally divided, measuring 31-46 mm in diameter and completely covered by cortical cells. Male and female thalli were not found in our collections.

Geographical distribution

In central Chile, Ceramium stichidiosum has been reported in Las Cruces, Pelancura and Los Molles (33°30'S; 71°65'W; Hoffmann & Santelices 1997), and in Chiloé (42°58'S; 74°19'W), and Puerto Montt (41°28'S; 73°00'W) by Santelices & Abbott, 1978 and Ramírez & Santelices 1991. The species is restricted to Subantarctic coasts as Southern Pacific South America, New Zealand, and Tasmania (Australia, Fig. 7).


DISCUSSION

This is the first report of the occurrence of C. stichidiosum in the extreme south of Chile. Our recent collections of Ceramium stichidiosum from Magellanic region of Chile correspond in their habit and structure of vegetative thalli and tetraspongial stichidium to the description of J. Agardh (1867). Ramírez and Santelices (1991) listed up seven species of Ceramium in the Magellan region plus an unidentified taxon, which has been found by Avila et al. (1982) and also by Mansilla and Navarro (2003). Among the seven reported species, only C. dozei, C. involutum, C. rubrum, and C. stichidiosum are fully corticated on axes. Ceramium dozei is similar with our species, but is characterized by short adventitious branches on axes (Hariot 1889) and Ceramium involutum and C. rubrum, do not have stichidial branches (Maggs & Hommers 1993, Stegenga et al. 1997).

However, thalli bearing cystocarps or spermatangial clusters were not collected and it is not known whether the sexual thalli occur in other seasons. Considering the occurrence of female thalli bearing cystocarps and males having spermatangia in central Chile (Hoffmann & Santelices 1997), the absence of sexual reproduction of the species in Magellanic region could be regarded a phenomenon due to a short summer for producing sexual reproductive organs. A limited collection could skip to find female and male thalli on intertidal areas because they could occur only in the subtidal zone. Asexual reproduction may be a strategy for maintaining marginal populations in areas where predominate very cold weather conditions. Culture studies for the tetrasporangial thalli of C. stichidiosum may give answers to above considerations.

The diagnostic characters of Ceramium stichidiosum are straight apices and stichidial tetrasporangia (J. Agardh 1867). However, most of fully corticated Ceramium species tend to have straight apices in tetrasporangial thalli, while female and male thalli often have incurved apices (Boo, pers. comm.). Stichidium with tetrasporangia is the most distinguished character for recognizing C. stichidiosum, the character sounding the name of specific epithet (J. Agardh 1867). However, the identity of C. stichidiosum appears not clear because the species is not listed up in marine flora of both New Zealand (Adams 1994) and Australia (Womersley 1998). Instead, Adams (1994) mentioned, in a remark of C. apiculatum, that there might be considerable confusion concerning the corticated species of Ceramium that have variously been identified as C. apiculatum, C. stichidiosum, and C. planum Kützing. In addition, C. stichidiosum var. smithii Laing from Auckland Islands appears to be referable to C. vestitum Harvey (Adams 1994). Ceramium stichidiosum is distributed to Campbell Island in Antarctic region (Papenfuss 1964), Chatham Islands and Snares Islands in New Zealand (J. Agardh 1867), and Tasmania in Australia (J. Agardh 1867). Since Papenfuss (1964), there are no reports of the species in the sub-Antarctic region except this study.



Figure 2-6. Fig. 2. Vegetative thalli of Ceramium stichidiosum. Bar = 500 mm; Fig. 3. Surface view of vegetative thalli showing disposition of cortical cells in nodes and internodes. Bar = 50 mm; Fig. 4. Transversal section of thalli showing six periaxial cells originated from the central cell. Bar = 100 mm; Fig. 5. Transversal section of thalli showing formation of tetrasporangia. Bar = 50 mm; Fig. 6. Stichidial branch showing tetrasporangia around nodes. Bar = 50 mm.

Figura 2-6. Fig. 2. Talo vegetativo de Ceramium stichidiosum. Barra= 500 mm; Fig. 3. Vista superficial de talo vegetativo mostrando la disposición de las células corticales en los nudos e internudos. Barra = 50 mm; Fig. 4. Sección transversal de un talo mostrando seis celulas periaxiales originadas desde la célula central. Barra = 100 mm; Fig. 5. Sección transversal de un talo mostrando la formación de tetrasporangios. Barra= 50 mm; Fig. 6. Estiquidio mostrando tetrasporangios alrededor de los nudos. Barra = 50 mm.




Figure 7. Distribution of Ceramium stichidiosum (black circle) in the world.

Figura 7. Distribución de Ceramium stichidiosum (círculos negros) en el mundo.



In Chile, Levring (1960) first reported the occurrence of Ceramium stichidiosum based on samples collected in Ancud Bay and Reloncavi fjord and marsh. The Chilean distribution ranges from Valparaíso in the north (Santelices & Abbott 1978) to Chiloé Island in the south (Levring 1960).

There have been many floral works in the Falkland, Kerguelen, and South Georgia Islands as well as islands in the extreme south of Chile, like Cape Horn and Diego Ramirez. Species may be not found due to sampling in different seasons, tiny size, its habitat in sub-tidal zones, and the challenge of isolating species that lives as epiphytes or parasites. However, it is surprising that the species has not been reported in the Magellan region because Ceramium stichidiosum was found as an epiphyte on algae of the genera Mazzaella and Sarcothalia, which had been collected extensively over the years without previously reporting the existence of Ceramium stichidiosum.

We suggest that C. stichidiosum has been recently introduced to the Magellan region with the agent of marine transportation. The species possibly entered from the north of Chile or from sub-Antarctic islands by way of currents. The most plausible route of its dispersal is from the north of Chile, given the common traffic of boats from Puerto Montt. If C. stichidiosum were to be found to the south of the Straight of Magellan, such as South Georgia, Diego Ramírez, Falklands or Cape Horn, it is possible that our report is due to natural colonization. However, the species has not been found in the Diego Ramírez Islands (Mansilla & Navarro 2003), South Georgia Islands, and the Falkland Islands (Pedrini 1992, John et al. 1994). Two invasive species have been reported in Chile to date: Codium fragile spp. Tomentosoides (van Goor) P.C. Silva (González & Santelices 2004) and Polysiphonia morrowii Harvey (Kim et al. 2004). Given the development of inter-ocean transport, algae from coastal ecosystems now are threatened by invasive species (Carlton & Geller 1992, McIvor et al. 2002).

Our report shows the need of an extensive revision for the ceramiaceous red algae in the Chilean sub-Antarctic region, not only for morphologically similar species, but also for possible exotic species. Recently frequent marine traffics make many marine organisms including algae to be introduced from other sea to Magellanic region (Kim et al. 2004).

ACKNOWLEDGMENTS

We are grateful to Dr. Sung Min Boo of the Chungnam National University, Korea, for its valuable suggestions and improvement of the manuscript. This work was financed by Ministry of Education of Chile, Mineduc Acuicultura Project and MECESUP MAG0002.


BIBLIOGRAPHY


Adams, N.M. 1994. Seaweeds of New Zealand. An illustrated guide. Canterbury University Press, Christchurch. 360 pp.
        [ Links ]

Agardh, J.G. 1876. Species genera et ordines algarum. Volumen tertium. Part 1. pp. vii + 724 Lipsiae [Leipzig].         [ Links ]

Athanasiadis, A. 1996. Morphology and classification of the Ceramioidae (Rhodophyta) based on phylogenetic principles. Opera Botanica 128: 1_216.         [ Links ]

Avila M., K. Alveal & H Romo. 1982. Comunidades de algas epífitas en Macrocystis pyrifera de Isla Navarino, Chile. Gayana Botánica 38: 3-16.         [ Links ]

Barreto, M.B. & Y. Yoneshigue-Valentin. 2001. Aspectos morfológicos do gênero Ceramium Roth (Ceramiaceae, Rhodophyta) no Estado do Rio de Janeiro. Hoehnea 28: 77-110.         [ Links ]

Boo, S.M. 1993. Intermediately corticated species, Ceramium puberubem (Ceramiaceae, Rhodophyta). Jpn. J. Phycol (sorui) 41: 143-149.         [ Links ]

Boo, S.M. & A.K. Lee. 1994. Ceramium and Campylaephora (Ceramiaceae, Rhodophyta). In: Biology of Economic Algae.( ed I. Akatsuka), pp. 1-33. SPB Academic Publishing, The Hague.         [ Links ]

Carlton, J.T. & J.B. Geller. 1992. Ecological roulette, the global transport of nonindingenous marine organism. Science 21: 78-82.         [ Links ]

Cho, T.O., R. Riosmena-Rodríguez & S.M. Boo. 2003. First record of Ceramium giacconei (Ceramiaceae, Rhodophyta) in the North Pacific: developmental morphology of vegetative and reproductive structures. Botanica Marina 46: 548-554.         [ Links ]

Fujii, M.T., A.L.M. Concentino & S.M.B. Pereira. 2001. Ceramium nitens (Ceramiaceae, Rhodophyta), an uncommon species from Brazil. Rev. Bras. Bot.24 (3): 359-363.         [ Links ]

González, A. & B. Santelices. 2004. A dichotomous species of Codium (Bryopsidales, Chorophyta) is colonizing northern Chile. Rev. Chil. Hist. Nat. 77: 293-304.         [ Links ]

Hariot, P. 1889. Algues. In: Mission Scientifique du Cap Horn. Vol. 5, Paris. pp. 3-9.         [ Links ]

Hoffmann, A. & B. Santelices. 1997. Flora Marina de Chile Central. Ediciones Universidad Católica de Chile, Santiago de Chile, 434 pp.
        [ Links ]

Itono, H. 1972. The genus Ceramium (Ceramiaceae, Rhodophyta) in southern Japan. Botanica Marina. 15, 74-86.         [ Links ]

John, D.M., P.J.A. Pugh & I. Tittley. 1994. Observations on the benthic marine algal flora of South Georgia: a floristic and ecological analysis. Bull. Nat. Hist. Mus. Lond. (Bot.) 24: 101-114.         [ Links ]

Kim M., E.C. Yang, A. Mansilla & S. Boo. 2004. Recent introduction of Polysiphonia morrowii (Ceramiales, Rhodophyta) to Punta Arenas, Chile. Botanica Marina 47: 389-394.         [ Links ]

Levring, T. 1960. Contribution to the marine algal flora of Chile. Lunds Universitets Arsskrift Ny Foljd, Avd. 2, 56 (10): 1-84.         [ Links ]

Maggs, C.A. & M.H. Hommersand. 1993. Seaweeds of the British Isles. v. 1. Rhodophyta, part 3A Ceramiales. HMSO Publications, London.         [ Links ]

Mansilla, A. & N. Navarro. 2003. Contribución al estudio de la flora ficológica de las islas Diego Ramírez (Chile). En: Memorias Curso Internacional de Postgrado y Especialización de Macroalgas en Ambientes Subantárticos (eds Mansilla, A., C. Werlinger & N. Navarro). pp. 85-89.Ediciones Universidad de Magallanes, Punta Arenas.         [ Links ]

McIvor, L., C.A. Maggs, M.D. Guiry & H.D. Hommersand. 2002. Phylogenetic analysis of the geographically disjunct genus Osmundea Stackhouse (Rhodomelaceae, Rhodophyta). Constancea 83: 1-11.         [ Links ]

Nakamura, Y. 1965. Species of the genera Ceramium and Campylaephora, especially those of northern Japan. Scientific Papers of the Institute of Algological Research, Faculty of Science, Hokkaido University 5: 119-180.         [ Links ]

Papenfuss, G.F. 1964. Catalogue and bibliography of Antarctic and subantarctic benthic marine algae. American Geographical Union Antarctic Research Series 1: 1-76.         [ Links ]

Pedrini, A. de G.. 1992. Catálogo de espécies, ocorrência geográfica e bibliográfica das algas marinhas bentônicas das Ilhas Shetland do Sul, Antártica. Archivos do Jardim Botânico do Rio do Janeiro 31: 103-122.         [ Links ]

Pisano, E. 1977. Fitogeografía de Tierra del Fuego-Patagonia chilena. I. Comunidades vegetales entre las latitudes 52 y 56°S. Anales del Instituto de la Patagonia 8: 121-250.         [ Links ]

Ramírez, M.E. & B. Santelices. 1991. Catálogo de las algas bentónicas de la costa temperada del Pacífico de Sudamérica. Monografías Biológicas Nº5, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile. Santiago de Chile, 437 pp.         [ Links ]

Santelices, B. & I. Abbott. 1978. New records of marine algae from Chile and their effect of phytogeography. Phycologia 17(2): 213-222.         [ Links ]

Stegenga, H., J.J. Bolton & R.J. Anderson. 1997. Seaweeds of the South African west coast. Bolus Herbarium, University of Cape Town, Cape Town, 655 pp.         [ Links ]

Womersley, H.B.S. 1978. Southern Australian species of Ceramium Roth Greville (Rhodophyta). Australian Journal of Marine and Freshwater Research 29: 205-257.         [ Links ]

Womersley, H.B.S. 1998. The Marine Benthic Flora of Southern Australia, Rhodophyta. Part IIIC. State Herbarium of South Australia, South Australia. 535 pp.         [ Links ]


Fecha de recepción: 06.12.05

Fecha de aceptación: 05.01.06