Harmful algal blooms are often almost monospecific events. Correctly assessing the precisetaxonomic identity of the causative organism thus becomes crucial in deciding whether knowledge on toxicology, physiology and ecology gained from similar blooms can be reliably applied to the species at hand. Resolution of the species concept in harmful algae has become a profound issue of discussion at conferences dealing with toxic phytoplankton.
WHAT IS A SPECIES?
While genera are more or less subjective taxonomic units that attempt to reflect close relationships, species are supposed to be evolving biological units (see Taylor 1993, for a discussion of the history of development of this concept). This has been the basis for the Biological Species Concept with species boundaries defined according to the ability of organisms to interbreed and produce viable offspring. While readily applicable to Metazoan animals, there are problems with plants where some apparently distinct species successfully hybridise (often with weakly viable offspring) and in particular with protists for which sexual fusion is infrequent or apparently absent. For dinoflagellates, for example, sexuality has been documented for only about 10% of species (see Chapters 11 and 20) and accordingly very few attempts have been made to use sexual interbreeding for strain and species definition (see Beam & Himes 1982 for Crypthecodinium cohnii; Blackburn et al. 1989 for Gymnodinium catenatum; Anderson et al. 1994 for Alexandrium tamarense). These studies have revealed the existence of morphologically similar natural populations that are reproductively isolated, analogous to the “sibling species” concept known from animal studies. For most harmful algal species, however, the usual mode of proliferation is by asexual fission and sexuality in addition to genetic recombination serves a special purpose in the life cycle of these organisms (cyst formation and survival in dinoflagellates; auxospore formation and cell enlargement in diatoms). For permanently asexual organisms, only discontinuities in morphological or biochemical characters can be used to constitute species boundaries.
TAXONOMIC CRITERIA USED FOR IDENTIFICATION AND CLASSIFICATION
Morphology of an organism is the complex expression of its genotype, subject to phenotypical change due to the environment, life cycle transformations and other influences. Morphological traits and biogeographical distributions of organisms continue to be considered as the primary means for traditional species classification. Through examination of thousands of individuals one needs to develop an understanding of what are conservative characters useful for taxonomy and what are highly variable characters. Cultured cells can have more variable morphology than field material, and considerable care should be exercised in basing new species descriptions exclusively on cultured material. For diatoms, useful conservative taxonomic features include
strutted/ labiate/occluded process patterns and diatom valve markings (number of striae; areolae in 10 l.trn) (Chapter 17). For armoured dinoflagellates thecal plate patterns are the most
diagnostic, with hypothecal characters being more conservative than epithecal ones (Chapter 15). For less ornate unarmoured dinoflagellates and especially nanoplanktonic and pica planktonic taxa (such as Aureococcus anophagefferens) ultrastructure of chloroplasts, pyrenoids, flagellar roots etc. have become indispensable morphological adjuncts. In addition, non-morphological characters such as lipid, pigment and toxin biochemistry, immuno cytological traits, chromosome number and DNA content (e.g. for Gymnodinium cf. nagasakiense; Partensky et al. 1988), and more recently nuclear or plastid DNA sequences are now being increasingly used to aid in species recognition. While marine phytoplankton species have remained morphologically conservative they can have accumulated significant genetic variability. Looking alike does not necessarily mean genetically identical, and looking different does not mean genetically isolated (Taylor 1993). Morphospecies designations therefore sometimes can be of limited use for ecological purposes. The dinoflagellate Alexandrium tamarense is known to exist as toxic and non-toxic strains, bioluminescent and nonbioluminescent populations, and cold-water and warm-water forms. In some cases the use of biochemical, molecular, and physiological data has corroborated morphotaxonomy (e.g. arguments for the synonomy of A. minutum and A. Zusitanicum; Costas et al. 1995), while in other cases apparent conflicts have inspired a revaluation of traditional species discrimination (e.g. the Phaeocystis pouchetii complex; Medlin et al. 1994; the elevation of Pseudo-nitzschia multiseries to species level; Manhart et al. 1995) or provoked further debate on the species concept in unicellular algae. While the presence of a ventral pore in the first apical plate of the dinoflagellate Alexandrium tamarense has been widely accepted as a stable taxonomic character (Balech 1995) discriminating this species from A. fundyense, Anderson et al. (1994) demonstrated that cultured clones of the two taxa were sexually compatible. Furthermore, Scholin and Anderson (1994) working with the same A. tamarense “species complex” found that ribosomal RNA sequences of isolates clustered more logically on the basis of geographic origin than morphotaxonomy.
GENERAL COMMENTS ABOUT TAXONOMIC NOMENCLATURE
The science of taxonomy seeks to delimit stable groups of individuals that share common traits. The correct name for a phytoplankton species should fulfil stringent requirements as spelled out by the International Code of Botanical Nomenclature (ICBN; most widely used for algae), International Code of Zoological Nomenclature (ICZN; sometimes used for dinoflagellates and euglenoids which have a large proportion of colourless species) or the International Code of Nomenclature of Bacteria (used for cyanobacteria).The aim of these codes is to produce nomenclatural stability. Under the ICBN, for species descriptions after 1 Jan.1958 there is a requirement for a written description of the essential characters, an illustration, a Latin diagnosis and a designation of type material. The name must not have been used previously in that rank for a member of the Plant Kingdom (if it had it would be referred to as a homonym) and it must have priority, being published before any other name applied within the same rank to the same organism (others being referred to as synonyms). More and more, the practice of Iodging permanent mounts in a museum or herbarium is being replaced by the designation of
light or electron micrographs as holotypes, while with (cyano)bacteria pure cultures can serve as types (Stanier et al. 1978). The recommendation by the ICBN that names above the level of genus should be typified (e.g. the class Prymnesiophyceae based on the genus Prymnesium) has not been generally accepted (i.e. leaving the name Haptophyceae as a valid alternative, Chapter 16). When new combinations result from transferring species from one genus to another, the species name should be retained, unless it has already been used with the genus to which the species is brought, in which case a new species name must be provided. After 1 Jan. 1953, the basionym (the combination under which the species first appeared) must be cited, withpublication details provided. An author’s name in parentheses means that since the original description of the taxon its name has been changed. There are important procedural differences between the ICBN and ICZN (e.g. requirement or not for a Latin diagnosis), and neither the ICBN nor ICZN recognize as homonyms those names proposed under one code but preoccupied under the other. This can lead to absurd situations in which a scientist declaring him/herself a zoologist can be precluded from using names a botanist can use (Patterson and Larsen 1992). A proposal (Taylor et al. 1987) to resolve these nomenclatural problems was not accepted at the Berlin Botanical Congress. There are also differences between botanists and zoologists in the recognition of infraspecific categories. Botanists use the terms variety (often conceived as small differences in genotype) and form (a response of an organism with the same genotype to a different environment), although the meaning of these terms is not agreed upon, while zoologists only recognize the term subspecies, which carries with it a notion of geographic isolation and lack of interbreeding which is difficult to apply to marine phytoplankton with virtually unlimited dispersal options. Palaeontologists working with fossil dinoflagellate cysts by consensus have chosen to treat them as form genera under the ICBN. When a dinoflagellate taxon has both a fossil (e.g. Polysphaeridium zoharyi) and modern representation (Pyrodinium bahamense; Chapter 20), then the name-carrier should preferably be the living organism, since this provides the most complete information (Wall & Dale 1968). This would necessitate, however, the official conservation of e.g. the genus Gonyaulax Diesing 1866 against the older equivalent cyst name Spiniferites Mantel1 1850. An attempt to produce a unified classification of living motile dinoflagellates and fossil dinoflagellate cyst taxa has been prepared by Fensome et al. (1993).
Name changes always cause concern and confusion to non-specialists, but reflect the ever developing scientific understanding of natural relationships among organisms. Two examples are provided to illustrate the taxonomic principles described above. The diatom Pseudonitzschia australis Frenguelli 1939 was classified as a section within the genus Nitzschia by Hasle (1965). Since the name N. australis was preoccupied, the new name Nitzschia pseudoseriata Hasle was introduced. Recently Pseudo-nitzschia was revived for species with step-wise overlapping colonies (Chapter 17) thus necessitating a return to the name P. australis. Another example is the toxic dinoflagellate Gonyaulax tamarensis Lebour 1925, which once it was recognised that its thecal plate pattern (4 apicals, no intercalaries) did not fit in the genus Gonyaulax, was relegated for a number of years to either the poorly defined genus Alexandrium Halim 1960, or Gessnerium Halim 1967 (based on an erroneously optically reversed Alexandrium) or Protogonyaulax (based on absence of contact between the first apical plate homologue with the apical pore complex [PO]; Taylor 1979). This confusion was eventually resolved by a reexamination of material of the type species Alexandrium minutum from the type locality in Alexandria Harbour, Egypt (Balech 1989), which revealed the variable nature of the contact between 1’ and PO and thus indicated that Protogonyaulax could not be maintained (Chapter 15). The dinoflagellate organism in question now should be called Alexandrium tamarense (Lebour) Balech. To alleviate the problems of ever-changing taxonomy of harmful phytoplankton, it is recommended: (1) to study type-material or, if this is not available, collect and reexamine material from the type locality; (2) establish and curate type specimen collections using permanent mounts and/or photomicrographs (which is required by the codes), but also include video tapes and preferably living cultures; and (3) incorporate life cycle features e.g. cysts in species descriptions (Steidinger 1990). Original names as far as possible should be retained until complete information is available on the existing available and valid genera.
ANDERSON, D.M.; KULIS, D.M.; DOUCETTE, G.J.; GALLAGHER, J.C.; BALECH, E.
(1994). Biogeography of toxic dinoflagellates in the genus Alexandrium from the
northeastern United States and Canada. Mar. BioZ. 120: 467-478.
BALECH, E. (1989). Redescription of Alexandrium minutum Halim (Dinophyceae): type
species of the genus Alexandrium. Phycologia 28: 206-2 11.
BALECH, E. (1995). The genus Alexandrium Halim (Dinoflagellata). Sherkin Island Marine
Station, Cork, Special Publication.
BEAM, C.A.; HIMES, M. (1982). Distribution of members of the Crypthecodinium cohnii
(Dinophyceae) species complex. J. Protozool. 29: 8-15.
BLACKBURN, S.I.; HALLEGRAEFF, G.M.; BOLCH, C.J. (1989). Vegetative reproduction
and sexual life cycle of the toxic dinoflagellate Gymnodinium catenatum from Tasmania,
Australia. J. Phycol. 25: 577-590.
COSTAS, E ; ZARDOYA, R.; BAUTISTA, J.; GARRIDO, A.; ROJO, C.; LOPEZ-RODAS
(1995). Morphospecies vs.genospecies in toxic marine dinoflagellates: an analysis of
Gymnodinium catenatum I Gyrodinium impudicum and Alexandrium minutum / A.
Zusitanicum using antibodies, lectins and gene sequences. J. Phycol. 31: 801-807.
FENSOME, R.J.; TAYLOR, F.J.R.; NORRIS, G.; SARJEANT, W.A.S.; WHARTON, D.I.;
WILLIAMS, G.L. (1993). A classification of living and fossil dinoflagellates. Amer.
Mus. Nat. Hist., Micropal. Special Publ. 7. 351 pp.
HASLE, G.R. (1965). Nitzschia and Fragilariopsis species studied in the light and electron
microscopes. II. The group Pseudonitzschia. Skr. Norske Vidensk.-Akad. Oslo. I. Mat.-
Nut. KZ. Ny Serie 18, l-49.
MANHART, J.; FRYXELL, G.A.; VILLAC, M.C.; SEGURA, L.Y. (1995). Pseudonitzschia
pungens and P. multiseries (Bacillariophyceae): nuclear ribosomal DNAs and
species differences. J. Phycol. 31: 421-427.
MEDLIN, L.K.; LANGE, M; BAUMANN, M.E.M. (1994). Genetic differentiation among
three colony-forming species of Phaeocystis: further evidence for the phylogeny of the
Prymnesiophyta. Phycologia 33: 199-2 12.
PARTENSKY, F.; VAULOT, D.; COUTE, A.; SOURNIA, A. (1988). Morphological and
nuclear analysis of the bloom-forming dinoflagellates Gyrodinium c$ aureolum and
Gymnodinium nagasakiense. J. Phycol. 24: 408-415.
PATTERSON, D.J.; LARSEN, J. (1992). A perspective on protistan nomenclature. J.
Protozool. 39( 1): 125- 13 1.
SCHOLIN, C.A.; ANDERSON, D.M. (1994). Identification of group- and strain-specific
genetic markers for globally distributed Alexandrium (Dinophyceae). I. RFLP analysis of
SSU rRNA genes. J. Phycol. 30, 744-754.
STANIER, R.Y.; SISTROM, W.R.; HANSEN, T.A.; WHITTON, B.A.; CASTENHOLZ,
R.W.; PFENNIG, N.; GORLENKO, V.N.; KONDRATIEVA, E.N.; EIMHJELLEN,
K.E.; WHITTENBURY, R., GHERNA, R.L.; TRUPER, H.G. (1978). Proposal to
place the nomenclature of the cyanobacteria (blue-green algae) under the rules of the
International Code of Nomenclature of Bacteria. Znt. J. Syst. Bacterial. 28: 335-336.
STEIDINGER, K.A. (1990). Species of the tamarensis / catenella group of Gonyaulax and the
fucoxanthin derivative-containing gymnodinioids. In: E. Graneli et al. (eds), Toxic
Marine Phytoplankton, pp. 11-16. Elsevier Science Publishing Co.
TAYLOR, F.J.R. (1979). The toxigenic gonyaulacoid dinoflagellates. In: Taylor, D.L.and
Seliger, H.H. (eds), Toxic Dinoflagellate Blooms. Elsevier North Holland, N.Y., pp.45-
TAYLOR, F.J.R. (1993). The species problem and its impact on harmful phytoplankton
studies, with emphasis on dinoflagellate morphology. In: Smayda, T.J. & Shimizu, Y.
(eds), Toxic Phytoplankton Blooms in the Sea. Elsevier, New York. pp 81-86.
TAYLOR, F.J.R.; SARJEANT, W.A.S.; FENSOME, R.A.; WILLIAMS, G.L. (1987).
Standardisation of nomenclature in flagellate groups treated by both the Botanicai and
Zoological Codes of Nomenclature. Syst. ZooZ. 36: 79-85.
WALL, D.; DALE, B. (1968). Modem dinoflagellate cysts and evolution of the Peridiniales.
Micropaleontology 14: 265-304.