Journal of Plankton Research Vol 13 no 5 pp. 1093-1099, 1991 Marine phytoplankton: how many species in the world ocean? A.Sournia, M.-J. Chretiennot-Dinet1 and M.Ricard2 Observatoire Odanologique de Roscoff, do Laboratoire de giologie, Museum national d'histoire naturelle, 43, rue de Buff on, 75005 Paris, Observatoire Odanologique de Banyuls, Laboratoire Arago, 66650 Banyulus-sur-mer and 2 Laboratoire de cryptogamie, Musi-urn national d'histoire naturelle, 12, rue de Buffon, 75005 Paris, France Do we classify what we see or see what we classify? Griffiths (1989) Introduction The number of extant species and genera of the marine phytoplankton has long been unknown, despite its obvious (not only academic) interest in ecology, phycology and evolution studies. The reason is that no synopsis of the plankton flora existed at the world scale. The two more extensive surveys available in the taxonomical literature thus far were not entitled to fill this need: (i) the botanical volume of the Nordisches Plankton edited at the beginning of this century by Brandt and Apstein (1980) with contributions by C.Apstein, H.H.Gran, C.Lemmermann, O.Paulsen and N.Wille dealt mostly with North Atlantic and adjacent seas; and (ii) the field covered by the Rabenhorst's Kryptogamen-Flora von Deutschland, Osterreich und der Schweiz, which came later (Hustedt, 19271966; Gemeinhardt, 1930; Schiller, 1930, 1931-1937; Geitler, 1932), is much larger than its modest title would imply but, in any case, this flora is ~60 years old. The other taxonomical works are limited both in the phycological dimension (i.e. they deal with only one or a few algal groups) and in the geographical dimension (i.e. they deal with a given region or ocean). Since the Rabenhorst's series, none of the algal classes (or whatever rank is attributed to the diatoms, dinoflagellates, and so on) has benefited a treatment at the world scale as far as marine phytoplankton is concerned, if one expects an exhaustive but noncritical, illustrated catalogue of the living and fossil silicoflagellates (Loeblich et al., 1968). Note that the freshwater phytoplankton is more favoured on this respect (Huber-Pestalozzi, 1938-1972; Bourrelly, 1973-1985, 1988; Ettl et al., 1978-. . .). There do exist some mentions of total species numbers of marine phytoplankton in the recent literature but these seem to rely on approximate estimates or © Oxford University Press 1093 Downloaded from http://plankt.oxfordjournals.org/ by guest on September 11, 2014 Abstract. Towards the end of the 1980s, living plankton flora of the world ocean amounted to 474504 genera and 3444—4375 species if one neglects the increase rate of taxa during the latest years In the above figures, the lower estimate is that of the 'reliable' taxa (of practical value for identification tasks), whereas the higher estimate includes the insufficiently known or doubtful organisms, and synonyms are excluded. The frequency distribution of the numbers of species per genus confirms the general hyperbolic law, which implies that a relatively large number of genera are uni- or paucispecific. A.Soumla, M.-J.Cbrltfcnnot-DiiKt and M.Rtcard unpublished census. For instance, the number of living species of dinoflagellates has been evaluated as 1000 (Tappan, 1980), 1000-1500 (Steidinger, 1983) or 2000 (Taylor, 1987; Margulis et al., 1990). A synopsis of the genera of the world ocean has been recently published which indicates the number of species of each genus (Sournia, 1986; Ricard, 1987; Chr6tiennot-Dinet, 1990). An answer may thus be given and some comments provided. The data Results The census is summarized on Table I. Some notes must be added for certain classes. (i) The relatively wide range of species numbers in most of the nanoplanktonic classes arises mostly from the fact that electron microscopy is now routinely used for these groups but the relevant information is lacking for many ancient taxa. 1094 Downloaded from http://plankt.oxfordjournals.org/ by guest on September 11, 2014 The Atlas du Phytoplancton Marin considers 15 classes in the marine phytoplankton, all of which are treated in the same way (although three authors are involved); these are the Cyanophyceae, Dictyochophyceae, Dinophyceae and Raphidophyceae (Sournia, 1986), the Bacillariophyceae (Riocard, 1987) and 11 other, mostly nanoplanktonic classes among them being the Prymnesiophyceae (Chr6tiennot-Dinet, 1990). This classification has been followed here for obvious reasons but it does not pretend to be sounder than any of the recent classifications such as those of Levine et al. (1980), Parker (1982), Lee et al. (1985), Puytorac et al. (1987) or Margulis et al. (1990). The precision as regards the number of species in a given genus is very variable as it depends on the proportion of the species which has been poorly described or which remains 'doubtful' for one reason or another to the eyes of the specialist. This reservation does neither include the strictly taxonomical uncertainties nor the failings to the nomenclature rules (Greuter et al., 1988) because a taxonomical statement is ascribed to each alga in the Atlas, how appropriate it may prove to be in the future (in other words, a given organism cannot be counted twice in different parts of the Atlas). Because of the uncertainty about species numbers, the following census considers either a number or a range, depending on the genus considered; in the latter case, the lower number is that of the taxa which look presently reliable and have a practical value to the taxonomist in charge of identifying a species, while the higher number includes the insufficiently known or doubtful species, synonyms excluded. The authors are aware of several new entries or taxonomical propositions which have been published during the last years or months but, for the sake of clarity, such recent information is not taken into consideration, so that the reference level remains that of the Atlas as it was published. How many marine phytopJankton species in the world ocean? Table I. Numbers of genera and species of the living marine phytoplankton, as compiled from Sournia (1986), Ricard (1987) and Chretiennot-Dinet (1990) Classes Genera Species 1 23-34 40-41 12-13 4 1 106-121 94-124 56-73 6-9 77 87 1 115-131 7-8 1 13 78 4 3 8 865-999 500-784 1-3 1424-1772 35-36 3 95-128 239-298 4-5 6 9-13 TotaJ 474-504 = 489 ± 15 3444-4375 = 3910 ± 465 (ii) The mutual delimitations of the Chlorophyceae and Prasinophyceae are particularly amenable to changes in the near future, with new classes being possibly added (0.Moestrup, personal communication). (iii) The Diatomophyceae are subdivided here into their two orders because of the well-known ecological and evolutionary implications of this taxonomical delimitation. The particularly wide ranges for the species numbers result from the presence (or dominance, among the Pennales) of tychoplanktonic diatoms whose ascription to either plankton or benthos is utterly questionable. Because of this fundamental ambiguity, the estimation of genera and species is particularly unprecise in the case of diatoms. (iv) Among the Dinophyceae, no effort has been made to distinguish the freeliving heterotrophic and mixotrophic organisms from the autotrophic ones (see Larsen and Sournia, 1991) but the parasitic and symbiotic genera have been omitted. Discussion The uncertainty about the total numbers of genera and species may reach 3.1 and 11.9% respectively. This indicates that practices in taxonomy are such that genera are more firmly established and/or that they are felt as more reliable to taxonomists than species are. Comparisons can be made with the freshwater phytoplankton on the account of the census provided by Bourrelly (1985) in the second edition of his Algues d'Eau Douce, from which the total numbers of genera and species reach 1173 and 14 900 respectively. For many classes, however, biases are introduced by inclusion of multicellular and/or benthic organisms among the freshwater 1095 Downloaded from http://plankt.oxfordjournals.org/ by guest on September 11, 2014 Chlorarachniophyceae Chlorophyceae Chrysophyceae Cryptophyceae Cyanophyccae Diatomophyceae Central es Pennales Dictyochophyceae Dinophyceae Euglenophyccae Eustigmatophyceae Prasinophyceae Prymnesiophyceae Raphidophyceae Rhodophyceae Tribophyceae A.Soomla, M.-J.Chrttfcnnot-Dtnet and M.Ricard Number of genera 200 -i All classes of marine phytoplankton 150 - 100 - 50 - 100 1000 Number of species per genus Fig. 1. Frequency distribution of the numbers of species per genus for the whole plankton flora of the world ocean (lower and higher estimates as defined in the text). 1096 Downloaded from http://plankt.oxfordjournals.org/ by guest on September 11, 2014 genera. If the comparison is restricted to classes whose members are essentially planktonic and which have been given the same taxonomical acceptance, then the comparative diversity of the marine and freshwater phytoplankton seems to differ widely depending on classes. The continental plankton would thus contain many more chrysophytes (159 genera and 860 species) and euglenophytes (55 genera and 1100 species) but many fewer dinoflagellates (32 genera and 240 species). A picture of the biological diversity can be provided by the frequency distribution of species numbers per genus. It was soon recognized by Willis (1922) that this distribution is not linear but rather hyperbolic, which means that a relatively high number of genera comprise a few or only a single species. Willis dealt mostly with flowering plants and, briefly though quite demonstratively, with several groups of animals. His findings have been recently verified by Griffiths (1989) as regards several groups or protista. The latter work includes a regional synopsis of freshwater algae but does not consider marine phytoplankton (neither partially nor totally). The present study makes it thus possible to extend Willis's laws to the marine plankton flora. The frequency distribution of species among genera, resulting from the present data, is shown in Figure 1; although Griffiths (1989) uses arithmetic scales, a logarithmic scale was felt preferable for the abscissae. A 'hollow curve' (Willis, 1922) is found again. At the height of the curve, 182-195 genera, i.e. more than one-third of the total flora (38.4-38.7%), are shown to be monotypic (i.e. consisting of a single species each). A strikingly identical proportion (38.6%) was found by Willis (1922) for the flowering plants of the world, 4853 of them out of a total of 12 571 being monotypic (as taken by Willis from the 1919 edition of his Dictionary). The 'tail' of the curve on Figure 1 shows very few genera having >50 species each. From How many marine pbytoplankton species in the world ocean? Number of genera 10 10 100 1000 100 1000 Minimum or exact number of species per genus Fig. 2. Comparative frequency distribution of the numbers of species per genus for the dinoflagellates (top) and the diatoms (bottom) 1097 Downloaded from http://plankt.oxfordjournals.org/ by guest on September 11, 2014 the above figures, in so far as this can be estimated from the numbers of species per genus, biological diversification appears to be very low. The shoulder and the peak at 5 and 10 species per genus result from the artefact that many genera of tychoplanktonic diatoms have been ascribed the approximate number of 'say', 5 or 10 planktonic species (Figure 2, bottom). The curve of the minimal or exact species numbers and that of the maximal numbers do not differ significantly in shape from each other (Figure 1). Differences among classes are exemplified by the comparison of the Bacillariophyceae and the Dinophyceae (Figure 2). The present census of the marine plankton flora is obviously liable to two limitations. (i) It is already underestimated, even before being actually published, due to the increase rate of taxa in the literature. Defining these rates for the various classes or for the whole plankton flora would deserve a special study but an order of magnitude has been provided by VanLandingham (1967): 'New diatoms [either recent or fossil, planktonic or benthic, and freshwater or marine] are being described at a rate of approximately one per day or about A-Sournta, M.-J.Chretieniiot-DiDrt and M.Rkard Acknowledgements The thoughtful comments of two anonymous reviewers are gratefully acknowledged. References Anderson,D.M. (1990) Toxin variability in Alexandnum species In Gran61i,E- (ed.), Toxic Marine Phytoplankton. Elsevier, New York, pp. 41-51. Bounelly.P. (1973-1985) Les algues d'eau douce. Initiation a la systtmatique (2eme edition revue et corrigee). I. Les algues vertex (1973). II. Les algues jaunes et brunes (1981). III. Les algues bleues et rouges, les Engltniens, Ptridmiens et Cryptomonadtnes (1983). Boubee, Pans. Bourrelly.P. (1988) Compliments. Les algues d'au douce. Initiation a la systtmatique Tome I. Les algues vertes. Soc. nouv. Edit Boubee, Paris. Brandt.K. and Apstein.C. (eds) (1908) Nordisches Plankton Botanischer Ted. XVIII, 1-124; XIX, 1-146; XX, 1-29; XXI, l^M); XXII, 1-5. Upsius & Tischer, Kiel and Lepizig. Campbell.L., Shapiro.L.P., Haugen.E.M. and Morris.L. (1989) Immunochemical approaches to the identification of the ultraplankton: assets and limitations. In Cosper.E M. et al. (eds), Novel Phytoplankton Blooms. Springer, Berlin, pp. 39-56. Chretiennot-Dinet,M.-J. (1990) Atlas du phytoplancton mann. Vol. 3. Chlorarachnwphyctes, Chlorophycies, Chrysophydes, Cryptophydes, Euglinophydes, Eustigmatophydes, Prasinophycies, Prymntsiophydes, Rhodophyctes, Tribophycies. Editions du CNRS, Paris. Ettl.H., Gerloff,J., Heynig.H. and MollenhauerJ). (eds) (1978-. . .) SOsswasserflora von Mitteleuropa. Gustav Fisher, Stuttgart, Jena. Geitler.L. (1932) Cyanophyceae von Europa unter Beriicksichtigung der anderen Kontinente. In Rabenhorst's Kryptogamen-Flora von Deutschland, Oesterreich und der Schweiz, Vol. 14 Akad. Verlag, Leipzig, pp. 1196. Gemeinhardt.K. (1930) Silicoflagellatae. In Rabenhorst's Kryptogamen-Flora von Deutschland, Oesterreisch und der Schweiz, Vol 10 (2), pp. 1-87. Greuter.W. et al. (eds) (1988) International Code of Botanical Nomenclature Adopted by the Fourteenth International Botanical Congress, Berlin, July-August 1987. Regnum vegetabile, 118 Koeltz Scientific Books, Koenigstein. Griffiths.A.J. (1989) The protistan landscape Prog. Protistol., 3, 1-20. Huber-Pestalozzi.G. (1938-1972) Das Phytoplankton der Susswassers. Systematik und Biologie In Thienemann.A. (ed.), Die Binnengewasser. Schweizerbart'Verlags., Stuttgart, Vol. 16(1), pp. 1342, pi. 1-66. Hustedt.F. (1927-1966) Die Kieselalgen Deutschlands, Osterreichs und Schweiz mit Beruksichtigung der iibngen Lander Europas sowie der angrenzenden Meeresgebiete. In Rabenhorst's Kryptogamen-Flora von Deutschland, Oesterreich und der Schweiz, Vol. 7: 1 [1-5] (1927-1930); 2 [1-6] (1931-1959); 3 [1-4] (1961-1966). Akad. Verlag, Leipzig. 1098 Downloaded from http://plankt.oxfordjournals.org/ by guest on September 11, 2014 320 per year. New diatom genera are being described at a rate of about 3 or 4 per year'. Note that a plot of the increase rate through time, starting at the early days of planktology, may allow a simple extrapolation of the 'true' number of taxa in the oceans to be made, provided that the resulting trend would be a rather regular one. This exercise has not been carried out yet but it can be attempted, in the case of the dinoflagellates at least, as a catalogue of the new taxonomic entries of the marine planktonic Dinophyceae is currently up-dated (Sournia, 1991, and references therein). (ii) The count is worth what the Linnean classification is worth. The delimitation of many genera and species, and the validity of the taxonomical criteria are widely questioned. At least two current perspectives of planktology, viz. picoplankton ecology and the identification of toxic species, tend to emphasize infraspecific or even clonal variability by means of immunochemical or genetical approaches (e.g. Campbell et al., 1989; Anderson, 1990). How many marine phytoptankton species in the world ocean? Received on December 17, 1990; accepted on March 20, 1991 1099 Downloaded from http://plankt.oxfordjournals.org/ by guest on September 11, 2014 Larsen,J. and Sournia.A (1991) The diversity of heterotrophic dinoflagellates. 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In Rabenhorst's Kryptogamen-Flora von Deutschland, Oesterreich und der Schweiz, Vol. 10 (2), Akad. Verlag, Leipzig, pp. 89-273. Schiller^I. (1931-1937) Dinoflagellatae (Peridineae) in monographischer Behandlung. In Rabenhorst's Kryptogamen-Flora von Deutschland, Oesterreichs und der Schweiz, Vol 10 (3)- Teil 1 [ 1 3] (1931-1933); Teil 2 [1-4] (1935-1937). Akad. Verlag, Leipzig. Sournia.A. (1986) Atlas du phytoplancton marin. Vol. 1 Introduction, Cyanophydes, Dictyochophycies, Dinophyctes et Raphidophycees. Editions du CNRS, Paris Sournia.A (1991) Catalogue des especes et taxons lnfraspecifiques de Dinoflagelles marins actuels publics depuis la revision de J.Schiller, V: Compldment Ada Protozoologica, in press. Steidinger.K.A. (1983) A re-evaluation of toxic dinoflagellatc biology and ecology Di Round,F.E and Chapman,D.J. (eds), Progress in Phycological Research Elsevier, Bristol. Vol. 2, pp 147188. Tappan.H. (1980) The Paleobwlogy of Plant Protists. Freeman, San Francisco TaylorJF.J.R. (1987) General group characteristics; special features of interest; short history of dinoflagellate study. In Taylor^F.J R. (ed ), The Biology of Dinoflagellates Blackwell Scientific Publications, Oxford, pp. 1-23. VanLandingham.L. (1967) Catalogue of the Fossil and Recent Genera and Species of Diatoms and their Synonyms. A Revision of F.W.Mills' An Index to the Genera and Species of the Diatomaceae and their Synonyms. Part I. Acanthoceras through Bacillana. Cramer, Lehre WillisJ.C. (1922) Age and Area a Study in Geographical Distribution and Origin of Species Cambridge University Press, Cambridge.