First Report of Yamadaella caenomyce (Liagoraceae, Rhodophyta) from the Atlantic Ocean, with Descriptive Notes and Comments on Nomenclature

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1 Caribbean Journal of Science, Vol. 34, No. 3-4, , 1998 Copyright 1998 College of Arts and Sciences University of Puerto Rico, Mayagüez First Report of Yamadaella caenomyce (Liagoraceae, Rhodophyta) from the Atlantic Ocean, with Descriptive Notes and Comments on Nomenclature MICHAEL J. WYNNE 1 AND JOHN M. HUISMAN 2 1 Department of Biology and Herbarium, University of Michigan, Ann Arbor, Michigan mwynne@umich.edu 2 School of Biological Sciences and Biotechnology, Murdoch University, Murdoch, Western Australia 6150, Australia huisman@possum.murdoch.edu.au ABSTRACT. Specimens of a liagoroid red alga forming imbricating clusters in the shallow subtidal at Boca Chica, Bahía de Andrés, Dominican Republic, are described and identified as Yamadaella caenomyce (Decne.) I. A. Abbott (Liagoraceae, Nemaliales). Yamadaella is a monotypic genus with the following distinguishing features: inflated terminal cortical cells, straight, three-celled carpogonial branches, and diffuse gonimoblast filaments. Yamadaella caenomyce has a wide distribution throughout the tropical Indo-Pacific Ocean, but its presence in the Atlantic Ocean was not previously confirmed. INTRODUCTION The benthic marine algae of the Caribbean are known from the works of Taylor (1960), Littler et al. (1989), and Wynne (1986, 1998). The species occurring in the Dominican Republic are known from the accounts by Børgesen (1924), Almodóvar and Bonnelly de Calventi (1977), Díaz- Piferrer (1978), Almodóvar and Alvárez (1980), Montero et al. (1982, 1983), and Rosado (1993). The red algal genus Yamadaella, a member of the Liagoraceae (Nemaliales), was thought to be restricted to the tropical/subtropical Indian and western Pacific Oceans (Kraft, 1989). An indication that the genus might occur outside its reported distribution was the identification of a syntype specimen of Liagora annulata J. Agardh from Guadeloupe as Y. caenomyce (Decne.) I. A. Abbott by Abbott (1990), but she questioned the provenance of the specimen, thus discounting the occurrence of Yamadaella from the Atlantic. The discovery of a population of Y. caenomyce growing in a shallow water habitat of the Dominican Republic is thus significant and establishes the occurrence of the genus outside of the Indo-Pacific. MATERIALS AND METHODS Collection information is the following: Boca Chica, Bahía de Andrés, 26 km east of Santo Domingo, Dominican Republic (Greater Antilles): 30.ix.1993, legit M. J. Wynne 9846, monoecious, in shallow subtidal (1 m depth). Voucher specimens deposited in the following herbaria: MSM, MICH, MURU, PC, and US. The specimens were initially preserved in 5% formalin/sea-water and later processed as herbarium specimens. Portions of plants were removed and decalcified in dilute acetic acid, then washed, and stained in a mixture of 1% aniline blue/1% acetic acid/60% Karo syrup/38% distilled water. The extremely tough consistency of the decalcified thalli required that the axes be squashed between two glass slides in order to separate the filaments. Whole-plant photographs (Figs. 1, 2) were taken with a 35- mm camera using Kodak T-MAX 100 film. The line-drawings (Figs. 3-7) were prepared with the aid of a camera-lucida. Herbarium abbreviations are according to Holmgren et al. (1990), whereas MURU refers to the herbarium of Murdoch University, Australia. Authors of cited species are according to Brummitt and Powell (1992). The following collections of Yamadaella caenomyce in MICH were examined for comparison: SOMALIA. Ten miles north of Mogadiscio: 23.ix.1962, leg. G. Papenfuss & R. Scagel PR-III-35. Sar Uaule (Chisimaio): 10.vi.1973, leg. G. Sartoni. HAWAII. Halape 280

YAMADAELLA CAENOMYCE FROM ATLANTIC OCEAN 281 FIGS. 1 AND 2. Yamadaella caenomyce. Habit. (MW 9846). Natural size. Beach area, Hawaii Volcanoes National Park, Island of Hawaii: 30.vii.1963, leg. W.

2 YAMADAELLA CAENOMYCE FROM ATLANTIC OCEAN 281 FIGS. 1 AND 2. Yamadaella caenomyce. Habit. (MW 9846). Natural size. Beach area, Hawaii Volcanoes National Park, Island of Hawaii: 30.vii.1963, leg. W. Gilbert On offshore reef platforms, Hau ula, Oahu: iv.1946, leg. I. Abbott MAURITIUS. Blue Bay Lagoon: 8.v.1951, leg. R. Vaughan TAIWAN. South side of Nan Wan, Pingtong Hsien: 13.iv.1971, leg. Y.-M. Chiang heavily calcified distal portions. The calcification is confined to the cortical regions (assimilatory filaments) of the axes. A conspicuous feature of the axes is their transversely rugose nature, that is, the axes showed annular constrictions in both young and mature portions. Cortical filaments are dichotomously branched, with narrow elongate cells terminating in swollen, tear-drop-shaped cells (Fig. 3), 8-10 mm in width and mm in length. These terminal cells are distally enlarged. The specimens are monoecious. One to several spermatangial mother cells are produced from the subterminal cell in the cortical filaments. The spermatangial mother cells bear one to several spermatangia (Fig. 4). Carpogonial branches (Fig. 5) are threecelled, straight, and borne on inner cortical supporting cells. Although the carpogonial branches are not abundant, their relatively large cell size makes them easy to detect. Gonimoblast filaments arise directly from the fertilized carpogonium (Fig. 6), and a diffuse system of gonimoblast filaments develops. No subsidiary sterile or involucral filaments are associated with these spreading gonimoblast filaments, which terminate in single carposporangia (Fig. 7), 8-10 mm in width and mm in length. Gonimoblast filaments are distinguishable from cortical filaments due to their constituent cells being broader and not as elongate as those of the cortical filaments, and the cells (Fig. 7) that bear the carposporangia being distally truncate. OBSERVATIONS The specimens form imbricating, decumbent clusters in the shallow subtidal. Individual clumps (Figs. 1, 2) measure approximately cm in extent and consist of dichotomously branched, divaricate, three-dimensionally oriented axes, which become connate by frequent secondary connections. The rigid axes are about 1.0 mm diam. in older regions, tapering to mm diam. near the apices. Axes are cylindrical (somewhat compressed when dried) and are heavily calcified with a thick chalky whitish limestone in older regions, but are pinkish to reddish in the less DISCUSSION Yamadaella was established by Abbott (1970) on the basis of a unique combination of features. Its heavily calcified thallus is similar to that of some species of Liagora, but Yamadaella differs in the production of a straight three-celled carpogonial branch that is apparently a modified vegetative filament, as opposed to the mostly curved, accessory carpogonial branches of Liagora. The abundant calcification separates Yamadaella from the non-calcified Nemalion, which has similar straight carpogonial branches invariably more than three cells in length (Kraft, 1989). Perhaps the most strik-

3 282 M. J. WYNNE AND J. M. HUISMAN FIGS Yamadaella caenomyce. Fig. 3. Medullary filament and cortical fascicle with inflated terminal cells. Fig. 4. Spermatangia borne singly or in pairs on elongate spermatangial mother cells. Fig. 5. Three-celled carpogonial branch. Fig. 6. Gonimoblast filaments arising from the carpogonium. Arrow indicates attachment point of the trichogyne. Fig. 7. Diffuse gonimoblast filaments with immature, terminal carposporangia. All drawings from MW 9846, #4. Abbreviations: c.br: carpogonial branch; c.f: cortical fascicle; g: gonimoblast filament; m.f: medullary filament; sp: spermatangia; sp.m: spermatangial mother cell; su: supporting cell; tr: trichogyne.

4 YAMADAELLA CAENOMYCE FROM ATLANTIC OCEAN 283 ing feature of Yamadaella is seen following fertilization, when the carpogonium produces a loose system of branching gonimoblast filaments without any associated sterile filaments. Spermatangia are also produced in a distinctive manner, namely, from stalk cells (= spermatangial mother cells) produced on the subapical cells of the cortical filaments. In addition to these distinctive reproductive features, Yamadaella is unique among the calcified Liagoraceae in the presence of relatively enlarged and clavate or wedge-shaped terminal cells of cortical filaments. In addition to the detailed study of Yamadaella caenomyce provided by Abbott (1970), Yoshizaki (1980) also followed the pre- and post-fertilization development in some detail. His account essentially agreed with that of Abbott, differing only in one detail. Instead of the carpotetrasporangia reported by Abbott, Yoshizaki observed that the loosely organized gonimoblast filaments terminated in carposporangia. Although some authors (Abbott, 1945; Yoshizaki, 1980) have described this alga as being dioecious, other authors (Abbott, 1970; Kraft, 1989) have observed this taxon to be monoecious, or protrandrous. Our observations showed it to be monoecious. According to Jaasund (1977), Yamadaella caenomyce in Tanzania occurs in the intertidal zone at a higher level than species of Liagora, and it can be recognized in the microscope by the terminal cell of assimilatory filaments being relatively large and triangular in profile. Cribb (1983) stated that Great Barrier Reef populations occur on boulders and are never permanently submerged. Kraft (1989) referred to Yamadaella as forming pulvinate, mat-forming thalli anchored by numerous holdfasts on mid- to high-intertidal reef flats. These depictions of this species are certainly true for the material from the Dominican Republic. Our material agrees with the descriptions of Yamada (1938), Tseng (1941), Abbott (1970), and Cribb (1983), who characterized the surface of Y. caenomyce as being transversely rugose or with annulations. The specific epithets of L. rugosa and L. annulata [the former regarded by Abbott (1970) as conspecific with Y. caenomyce, the latter regarded herein as a tax. syn. pro parte (see below)] allude to the surface appearance. The Dominican Republic specimens agree with these published descriptions in most respects, differing only from that of Abbott (1970) (but not of Yoshizaki, 1980) in the production of carposporangia as opposed to carpotetrasporangia. Given the overriding similarities between all published descriptions, it seems likely that this feature is variable between populations. Weber-van Bosse (1921) reported a cotype of Liagora caenomyce (in the Hauck Herbarium), comparing it with specimens collected on the Siboga Expedition which she assigned to this species. She stated that the species was distinguishable by the rugose, annulate fronds with smooth, nonpowdery calcification, and that sections of the frond showed uniform, cylindrical, not very broad filaments with relatively thick walls in the central portion. She pointed out that the same structure occurred in L. rugosa Zanardini (Zanardini, 1851), in material assigned to L. annulata J. Agardh (J. Agardh, 1876) by Grunow, and also in Harvey s Friendly Island Exsicc. No. 47 (as L. viscida ). Abbott (1990) later discovered that this Harvey s Friendly Island Exsicc. No. 47 was part of J. Agardh s syntype of his L. annulata (J. Agardh, 1876) (see below). Yamada (1938) treated L. intricata Butters (Butters, 1911) and L. holstii Zeh (Zeh, 1912) as conspecific with Yamadaella [Liagora] caenomyce. At the same time Yamada placed L. rugosa Zanardini (Zanardini, 1851) and L. annulata J. Agardh (J. Agardh, 1876) as possible taxonomic synonyms. Børgesen (1942, 1952) recognized Liagora rugosa from Mauritius but did not agree with the suggestion made by Weber-van Bosse (1921), and later by Yamada (1938), that L. rugosa was probably conspecific with L. caenomyce. In her designation of a lectotype for Liagora annulata, Abbott (1990) said that the choice of a suitable specimen was difficult because of J. Agardh s vague reference to the syntype localities being ad insulas Indiae occidentalis et in calidore pacifica. No specimen had been labelled as type in the Agardh Herbarium in LD. According to Abbott, a syntype specimen (LD 32413) from Guadeloupe is identifiable as

5 284 M. J. WYNNE AND J. M. HUISMAN Yamadaella caenomyce. Because that species (and genus) was not known outside of the Indian and Pacific Oceans, she doubted the provenance of the collection. Because the syntype specimen from the South Pacific (Harvey s Friendly Is. exsicc. no. 47) was monoecious, she discounted that specimen from consideration, regarding it as conforming to her concept of L. fragilis Zanardini [= L. valida Harv.]. She selected an old and decomposed specimen collected by Mrs. F. Curtiss from Florida as the lectotype of L. annulata. The determination of the present collection from the Dominican Republic as Y. caenomyce supports the acceptance of the provenance of one of the syntypes of L. annulata as being from the West Indies (Guadeloupe) and the treatment of J. Agardh s (1876) L. annulata as being based upon disparate elements (Liagora valida and Yamadaella caenomyce). The following treatment incorporates the taxonomic judgments of Yamada (1938) and Abbott (1970): Yamadaella caenomyce (Dec.) I. A. Abbott (1970) Basionym: Liagora caenomyce Decne. (Decaisne, 1842) tax. syns.: L. rugosa Zanardini (1851), fide Abbott (1970) L. annulata J. Agardh (1876), pro parte (specimen from Guadeloupe, LD 32413), fide Abbott (1970) L. intricata Butters (1911), fide Yamada (1938) L. holstii Zeh (1912), fide Yamada (1938) Acknowledgments. MJW wishes to thank Dr. Michael L. Smith of the Center for Marine Conservation, Washington, D.C., for the invitation to attend a workshop in Santo Domingo, at which time the collections were made. He also thanks the Center for Marine Conservation for defraying most of the travel expenses. David Bay, Department of Biology, University of Michigan, kindly took the photographs used in Figs. 1 and 2. JMH thanks the Australian Biological Resources Study for financial support. LITERATURE CITED Abbott, I. A The genus Liagora (Rhodophyceae) in Hawaii. Occas. Papers Bernice P. Bishop Museum 18: Abbott, I. A Yamadaella, a new genus in the Nemaliales (Rhodophyta). Phycologia 9: Abbott, I. A A taxonomic assessment of the species of Liagora (Nemaliales, Rhodophyta) recognized by J. Agardh, based upon studies of type specimens. Crypt. Bot. 1: Agardh, J. G Species genera et ordines... (Vol. 3: Epicrisis systematis floridearum). vii pp. Lipsiae. Almodóvar, L. R., and V. Alvárez Adiciones a la flora marina bentónica macroscópica de la República Dominicana. Centro de Investigaciones de Biología Marina Contribuciones 8, Universdidad Autónoma de Santo Domingo, República Dominicana. 8 pp. Almodóvar, L. R., and I. Bonnelly de Calventi Notas sobre las algas marinas bentónicas macroscópicas de la República Dominicana. Centro de Investigaciones de Biología Marina, Universidad Autónoma de Santo Domingo, República Dominicana. pp Børgesen, F Plants from Beata Island, St. Domingo. Collected by C. H. Ostenfeld, (Botanical Results of the Dana-Expedition , No. 1). Dansk Bot. Arkiv 4(7): Børgesen, F Some marine algae from Mauritius III. Rhodophyceae Part 1 Porphyridiales, Bangiales, Nemalionales. Det Kgl. Danske Videnskabernes Selskab, Biologiske Meddelelser 17(5) [1] pp., 2 pls. Børgesen, F Some marine algae from Mauritius. Additions to the parts previously published, IV. Det Kgl. Danske Videnskabernes Selskab, Biologiske Meddelelser 18(19). 72 pp., 5 pls. Brummitt, R. K., and C. E. Powell (eds.) Authors of Plant Names. 732 pp. Royal Botanic Gardens, Kew. Butters, F. K Notes on the species of Liagora and Galaxaura of the central Pacific. Minnesota Bot. Studies 4: , pl. 24. Cribb, A. B Marine Algae of the Southern Great Barrier Reef Rhodophyta. Australian Coral Reef Society Handbook No. 2. Watson Ferguson, Brisbane. 173 pp. Decaisne, J Mémoire sur les Corallines ou Polypiers califères. Ann. Sci. Nat. Bot., Paris, sér. 2, 18: Díaz-Piferrer, M Las investigaciones ficológicas del Caribe: la flora marina de la República Dominicana. Moscosoa 1(3):1-9. Holmgren, P. K., N. H. Holmgren, and L. C. Barnett Index Herbariorum. Part I: The Herbaria of the World, 8th edn. International Association for Plant Taxonomy, New York Botanical Garden, Bronx, New York. x pp. Jaasund, E Marine algae in Tanzania VII. Bot. Mar. 20: Kraft, G. T Cylindraxis rotundatus gen. et sp. nov. and its generic relationships within the Liagoraceae (Nemaliales, Rhodophyta). Phycologia 28:

6 YAMADAELLA CAENOMYCE FROM ATLANTIC OCEAN 285 Littler, D. S., M. M. Littler, K. E. Bucher, and J. N. Norris Marine Plants of the Caribbean. A Field Guide from Florida to Brazil. Smithsonian Institution Press, Washington, D.C., 263 pp. Montero, M., I. Bonnelly de Calventi, and L. R. Almodóvar Las algas marinas de la laguna de Boca Chica, Bahia de Andres, D. N. Ciencia (Domincan Republic) 6: Montero, M., I. Bonnelly de Calventi, and L. R. Almodóvar Las algas marinas de la laguna de Boca Chica, Bahía de Andrés, D. N. Publ. Universidad Autónoma Santo Domingo 311: Rosado, G. A Las algas marinas de la República Dominicana. In: Biodiversidad Marina y Costera en la República Dominicana. Centro de Investigaciones de Biología Marina, Fondo Mundial para la Naturaleza. Santo Domingo, pp Taylor, W. R Marine algae of the eastern tropical and subtropical coasts of the Americas. University of Michigan Press, Ann Arbor, ix pp. Tseng, C. K Studies on the Chinese species of Liagora. Bull. Fan Inst. Biol., Bot. Ser., 10: Weber-van Bosse, A Liste des algues du Siboga. II. Rhodophyceae. Première partie. Protoflorideae, Nemalionales, Cryptonemiales. Siboga-Expeditie Monographie 59b. Leiden. Pp , 3 pls. Wynne, M. J A checklist of benthic marine algae of the tropical and subtropical western Atlantic. Can. J. Bot. 64: Wynne, M. J A checklist of benthic marine algae of the tropical and subtropical western Atlantic: first revision. Nova Hedwigia Beiheft 116: iii pp. Yamada, Y The species of Liagora from Japan. Sci. Pap. Inst. Algol. Res. Hokkaido Univ. 2: 1-34, pls Yoshizaki, M Morphology and taxonomy of the Japanese representatives of Nemaliales (4). Thallus structure and reproductive organs of Yamadaella cenomyce. J. Jap. Bot. 55: Zanardini, G Algae novae vel minus cognitae in mari rubro a Portiero collectae. Flora, Regensburg 34: Zeh, W Neue Arten der Gattung Liagora. Notizbl. K. Berlin Bot. Gart. Mus. 5:

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