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FAU Institutional Repository http://purl.fcla.edu/fau/fauir This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute. Notice: © 1992 California Sea Grant College Program, University of California. This manuscript is an author version with the final publication available and may be cited as: Kilar, J. A., Hanisak, M. D., & Yoshida, T. (1992). On the expression of phenotypic variability: why is Sargassum so taxonomically difficult? In I. A. Abbott (Ed.), Taxonomy of economic seaweeds: with reference to some Pacific and Western Atlantic species. Volume III (pp. 95-117). La Jolla, CA: California Sea Grant College. TAXONOMY OF ECONOMIC SEAWEEDS With reference to some Pacific and Western Atlantic species Volume Ill Isabella A. Abbott, Editor Results of an international workshop sponsored by the California Sea Grant .. College in cooperation with the Pacific Sea Grant College Programs of . •.: Alaska, Hawaii, Oregon, and Washington and hosted by Scripps Institution of Oceanography (University of California, San Diego), August 1989. ',I .· •· . • A .. .. .... '\.• A Publication of the California Sea Grant College Report No. T-CSGCP-023 ON THE EXPRESSION OF PHENOTYPIC VARIABILITY: WHY IS SARGASSUM SO TAXONOMICALLY DIFFICULT? John A. Kilar, M. Dennis Hanisak, and Tadao Yoshida Abstract Anatomical and physiological variation is inherent in all living organisms, originating at both the genotypic and the phenotypic levels. In the morphologically complex phaeophyte Sargassum, characters exhibit variability on several scales: (1) temporal, (2) intraindividual, (3) interindividual, (4) environmental, and (5) interlocality (geographical). Taxonomic inconsistencies result from haphazard measurements of variation and from species descriptions that describe only part of the plant's anatomical range. Prominent features, such as blade shape and size, are used almost exclusively to distinguish taxa but are highly variable. Polymorphs increase between-plant variation and, in some cases, make species descriptions inadequate. The search for stable characters or suites of characters is further complicated by developmental cycles, low-occurrence traits, environmental variates (polymorphisms and polyphenisms), and genetic differences among populations. Variation at the phenotypic and genotypic levels must be understood before an acceptable species concept can be developed. Introduction Phycologists have long realized the functional role of the "biological species" but have often pondered its artificial nature, recognizing the difficulty in describing variability in a single, meaningful description. Some investigations have considered local populations, not the abstract species, to be the fundamental unit of nature, claiming that gene flow is rarely strong enough to unite populations into an integrated species (Ehrlich and Raven 1969). Although methods of reproduction and life history are important, vegetative organization plays a more significant role in delimiting marine algae (Papenfuss 1955). In the genus Sargassum, morphological features are highly differentiated, exhibiting temporal as well as within- and between-plant variability. In this paper, problems associated with the taxonomy of Sargassum are identified on the basis of observations of the Floridian and Bahamian floras and the published literature. Patterns in trait variation are elucidated, problems associated with haphazardly measuring such variations are listed, and a framework to resolve taxonomic inconsistencies is established. Sargassum, with more than 400 described species, has the largest number of taxa in the Phaeophyta (Yoshida 1983) and occurs throughout most major oceans (the exception is the Antarctic [Nizamuddin 1970]). Its life history is typical of the Fucales, that is, haplobiontic; the organism is diploid in chromosome constitution. Asexual spore production is unknown, but free-floating pelagic species reproduce by thallus fragmentation. Annual (Tsuda 1972, Ang 1985), pseudoperennial (Ang and Trono 1987, Fletcher and Fletcher 1975a, De Wreede 1976, Prince and O'Neal 1979, Prince 1980), and perennial (Paula and Oliveira 1982, De Ruyther van Steveninck and Breeman 1987) life histories have been reported. Sargassum contributes significantly to coastal-zone biomass worldwide, fringing many temperate, subtropical, and tropical shores. The alga dominates many shallow-water habitats and is presently the deepest occurring brown alga: 200 m depth (S. hawaiiensis Doty et Newhouse [Magruder 1988]). Similar to the "kelps" in northern latitudes, nearshore and pelagic populations of Sargassum play critical roles in the life histories of many animal and plant species, providing them with a substratum, protection against predation, and a concentration of food (Mukai 1971 , Dooley 1972). Two free-floating species, S. fluitans B0rgesen and S. natans (Linnaeus) J. 95 ··· L R ····················· ········ V Fig. 1. Axis morphology of primary branches of Sargassum. V = vesicle; L = blade; R = receptacle; S = axis or stem. Meyen, are the "keystone species" of the largest marine community in the world, the Sargasso Sea (Taylor [1975] recognizes a third species: S. pusillum Taylor) . The questions of whether the derivation of these pelagic species is entirely a matter of past evolution and whether they should be dealt with as independent taxa or merely as phenotypic variations of a sessile species-one of the oldest questions in marine biology (Krummel 1891 , Winge 1923, Parr 1939, Ryther 1956)-are still unanswered since variation in their morphology is not well understood or documented. In addition to its large number of described species, Sargassum is one of the most anatomically complex genera in the Phaeophyta. It consists of leaf-like blades, stems (axes), vesicles, fruiting branches, and a holdfast (Fig. 1 ). All features exhibit considerable latitude in form, size, or numbers. Blades are the principal light-harvesting organs in Sargassum (Fagerberg et al. 1979) and range from linear to lanceolate to ovate with entire, serrate, or highly dentate margins (Fig. 2). Furthermore, blades can be flat, 96 A B D 2cm l ) G .�,, (c Fig. 2. Blade morphology of Sargassum polyceratium. A, Linear blades with nearly entire margins. B, Linear, bifurcated blade. C, Lanceolate, bifurcated blade. D, Linear blades with serrate margins. E, Linear-lanceolate blades. F, Ovate blades. G, Recurved, ovate blades. recurved, undulate, or inflated. Such variability is understandable between taxa; however, it can occur within a single taxon (Howe 1920, Magruder 1988, Kilar and Hanisak 1989). Similar in appearance to the stomata on higher-plant leaves, cryptostomata occur on most plant features, and the arrangement and size of cryptostomata on blades are of taxonomic importance (e.g., S. platycarpum Montagne). In the western Atlantic, main axes are terete with or without acute spines that may be deciduous. Vesicles are common in these algae; their function is to support the thallus upright in the water column. Some of the features of the vesicle are among the most erratic and some others among the most stable: Alated (winged) vesicles exhibit a seasonal pattern, whereas the diameters of mature vesicles are nearly invariable (Ang and Trono 1987, Kilar and Hanisak 1988). Sexual structures are contained in modified blades called receptacles (Fritsch 1945), and their form and arrangement are as diverse as the somatic features are (Fig. 3). Although the number of different characters would seem to be sufficient to distinguish taxa, it is often exceedingly difficult to do so (Taylor 1960). Phenotypic Expression Temporal. Plant morphology changes with the age of the plant and its primary laterals. The number of laterals arising from the main or perennial stem (Jephson and Gray 1977, Umezaki 1986) and the degree of branching (Womersley 1954) are age related characters. Blades of older plants, especially when reproductive, may have blades narrower than normal (Taylor 1960); studies of pseudoperennials, S. polyceratium Montagne (Kilar and Hanisak 1988) and S. muticum (Yendo) Fensholt (Kane and Chamberlain 1978, Critchley 1983a), and the annual S. cristaefolium C. Agardh (Soe-Htun 97 0 receptacle Hermaphrodite S. vulgare' 0 i conceptacle r;J e erconceptacle s. lyceratium rili endula2 Androgynous S. S. WO� fjj S. hystrix [i] S. acinarium Androdioecious � 1••1 S. stenophyllum filipendula Dioecious 3 �·• loor 1••1 pteropleuron fluitans ThaNus Fragmentation S. S. natans Fig. 3. Modes of reproduction and distribution of sex organs in Caribbean species of Sargassum (after Sawada 1958). With the exception of Sargassum polyceratium, all other androgynous species were determined from samples collected during a single month rather than over an annual growth cycle (Kilar and Hanisak, unpublished data). 1From Paula (1978) as Sargassum vulgare var. foliosissimum. 2Collection site in the Indian River Lagoon. 3Collection site in the Homosassa River. and Yoshida 1986) support this observation. In the perennial S. stenophyllum Martius, alterations in blade morphology are not as pronounced because laterals of similar morphology form throughout the year. Changes are more evident in annuals and pseudoperennials; newly produced blades become smaller in size and breadth as the frond matures, and older, broader blades are lost from the plant (Ang 1985, Soe-Htun and Yoshida 1986, Ang and Trono 1987, Kilar and Hanisak 1988). Blade senescence and loss are observed in vitro and in situ for many taxa (e.g., Norton 1977a,