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Evolution of Hawaiian Ferns and Fern Allies in Relation to Their Conservation Status1

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Evolution of Hawaiian Ferns and Fern Allies in Relation to Their Conservation Status1 Pacific Science (1995), vol. 49, no. 1: 31-41 © 1995 by University of Hawai'i Press. All rights reserved Evolution of Hawaiian Ferns and Fern Allies in Relation to Their Conservation Status1 WARREN HERB WAGNER, JR. 2 ABSTRACT: Evolutionary and conservational differences between Hawaiian pteridophytes and angiosperms involve differences in life histories (free-living generations, fertilization, and spore dispersal). Very high base chromosome numbers characterize the homosporous pteridophytes. Long-distance spore dispersal took place mainly from Old WorId and pantropical ancestors, ac­ counting for some 80% of the taxa. The ratio of native pteridophyte to angio­ sperm taxa in Hawai'i averages roughly 1: 6, much higher than in continental floras with 1: 14. Two hundred twenty-four pteridophyte taxa, including hy­ brids and naturalizations, are known in Hawai'i. The 170 native orthospecies inC'lude endemics (highly variable taxa with polymorphies involving one or more characters, monophyletic species swarms, and solitary endemics) as well as nonendemics. Hybrid nothospecies compose an important additional com­ ponent, as do naturalized orthospecies. Most of the hybrids are sterile inter­ mediates that propagate by vegetative means; sexual hybrids are rare. The per­ centage ofnaturalized species is only one-fourth that of angiosperms. Hawaiian pteridophytes have evolved much more slowly than the angiosperms, as shown by lower endemism (75% versus 91 % overall and relatively fewer one- or two­ island endemics) and much smaller species swarms (average 1.5 versus 16.0 de­ scendants from each introduction in the 20 most species-rich genera, re-' spectively). Anticipated listing of Hawaiian rare and endangered fern species will probably comprise ca. 17% of the natives, including four believed to be extinct. Naturalized species compose only one-fourth of the percentage in an­ giosperms, and very few are pests. Habitat destruction by humans and feral mammals is the major conservation problem. Although artificial spore banks and whole-plant culture may help save some rare pteridophytes, the most promising procedure is establishment of natural preserves. COMPARING THE PATTERNS of Hawaiian pter­ In this essay I have tried to establish a broad idophytes with their flowering plant counter­ view as a framework for more detailed in­ parts reveals numerous differences, especially vestigations. Most of the observations re­ in their relative numbers, their endemism ported here are based on intensive studies by (both overall and island-by-island), the num­ the author with the help of Florence S. ber and size of monophyletic species swarms, Wagner over the past 8 yr, together with a incidence of polyploidy, and extent of hy­ number of other individuals. We have also bridization, all of which bear upon our un­ relied heavily on substantive contributions in derstanding of their evolutionary processes. particular groups, such as Elaphoglossum (Anderson and Crosby 1966), Cystopteris (Blasdell 1963), Ophioglossum (Clausen 1 Project supported by NSFB5R90, Survey and In­ 1954), Thelypteridaceae (Holttum 1977), ventory for Hawaiian Pteridophyte Flora. Manuscript accepted 27 April 1994. Marsilea (Johnson 1985), Deparia (Kato 2 Department of Biology, The University of Michigan, 1984), Pteris (W. H. Wagner 1949, 1968), Ann Arbor, Michigan 48109-1048. and Diellia (W. H. Wagner 1952, 1953) My 31 32 PACIFIC SCIENCE, Volume 49, January 1995 Hawaiian research was actually begun in common in the Islands, viz. Selaginella ar­ 1947, with the help of Lincoln Constance, buscula (Kaulf.) Spring; this is also the only Annie M. Alexander, and Harold St. John. one that is polymorphic with many varia­ The ferns and fern allies differ radically tions, some of which have been named. In from seed plants in their life history biology. North America, the percentage of hetero­ It is not surprising, therefore, that there are sporous pteridophytes is more than eight strong differences in their evolutionary pat­ times as great. Because of the low incidence terns, and this is well illustrated by their dif­ ofheterospory, the following discussion deals ferences in evolution on oceanic islands, such only with homosporous pteridophytes, and as those of Hawai'i. Pteridophytes have a the major basis for comparison will be the distinctive alternation of independent free­ indigenous species. living generations: the familiar spore-pro­ A poorly understood feature of all homo­ ducing plants that are dominant and long­ sporous pteridophytes is the number of chro­ lived, and the tiny gamete-producing plants mosomes (Wagner and Wagner 1980). The that are inconspicuous and short-lived. In base numbers range mainly from 20 to 70, flowering plants, the gamete-producing gen­ much higher than those in flowering plants. eration has become parasitic on the spor­ Some ofthe largest genera in Hawai'i display ophyte and only the diploid stage is free. such numbers (e.g., Asplenium with x = 36, Ferns and fern allies reproduce simply by and Dryopteris with x = 41). Polyploid spe­ wind-blown spores, but flowering plants re­ cies are frequent, as in the dryopteroid ferns, quire transfer by pollen grains to the ovaries with n numbers of 41, 82, 123, and 164. The where the embryonic seed or ovules occur importance of these high numbers is still not and where fertilization takes place on the fully understood. It has been suggested that plant. In pteridophytes, fertilization requires the polyploid base numbers arose in antiq­ merely layers of water on the substrate in or uity and gene-silencing effectively diploidized through which the ciliated sperm can swim the genome, so that the paleopolyploids are from the male sex organs to the female or­ genetically no more heterozygous than typi­ gans. In flowering plants the process is much cal flowering plants (Haufler 1987). Neo­ more complicated and specialized: the sperm polyploids may occur within species or be must be transferred by pollen tubes. The derived from sterile hybrids between species. whole process of pollination in flowering The latter situation involving hybridization plants is mediated mainly by the behavior of between two known parental species produc­ volant animals, especially insects (primarily ing allopolyploids seems to be rare among Lepidoptera and Hymenoptera) and birds, Hawaiian pteridophytes, unlike those of the latter especially in the Tropics. Thus there North America and temperate Asia, where are profound differences in the life cycles of such allopolyploids are frequent to common, pteridophytes and angiosperms, and these no at least in certain genera. doubt bear upon the differences in their is­ The immigration of pteridophytes to Ha­ land evolution. wai'i has been primarily due to the long-dis­ Most pteridophytes are homosporous, but tance dispersal of spores. The majority of several groups are heterosporous and have native Hawaiian pteridophytes, estimated to male and female spores, which store food be over half of the taxa, appear to have their implanted in them by the parent plants. The closest affinities in the Old World. Of the re­ native heterosporous orders represented in mainder, some 60% are pantropical, and less the Hawaiian flora are Selaginellales (spike­ than 20% are New World in their relation­ mosses, two species), Isoetales (quillworts, ships. Even though some spores could be one species), and Marsileales (water clovers, carried among the feathers of migrating one species). Why these heterosporous pter­ birds, the overwhelming pattern has surely idophytes are so few and have evolved so lit­ been by wind because spores are readily air­ tle in Hawai'i is unexplained. Only one ofthe borne. Presumably, a majority of spores have heterosporous species is widespread and the ability to produce gametophytes that can Hawaiian Ferns: Evolution and Conservation-WAGNER 33 become under certain conditions bisexual, derived from single original introductions thus making it possible to have intra­ that diverged into two or more monophyletic gametophytic mating. Many spores germi­ species; solitaries are single isolated species nate and form female gametophytes, which, presumably resulting by direct descent from if not fertilized for a long period, may pro­ original ancestors or surviving branches of duce male organs and male gametes capable ancient swarms. The native nothospecies in­ of fertilizing eggs on the same gametophytes. clude taxa that originated by local hybrid­ Thus a single spore from thousands of kilo­ ization involving native and (or) recently in­ meters away could start a whole colony. The troduced species. Only one nothospecies is ages of the current high islands (i.e., those thus far demonstrated to have resulted from with well-developed rain forest) range from hybridization that took place outside of Ha­ ca. 5.7 to 0.5 million yr old. Most native wai'i. Naturalized describes those species species occur on all the major islands, with known to have been introduced into the ar­ only a minority of approximately one in six chipelago and established mainly in the last species one- or two-island endemics. The lat­ century by Western commerce. Numbers of ter more localized species are probably either each of these groups are shown in Table 1. relicts of once widespread species, species of Patterns of biodiversity in Hawaiian pter­ highly specialized habitats, or species of re­ idophytes in many respects suggest various cent arrival. underlying evolutionary processes. These The mode of long-distance dispersal by patterns
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