A seed atlas of Hypoxis from eastern North America - BioOne

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(Hypoxidaceae) from eastern North America (east of Texas) was studied with ... seeds of H. sessilis are unique among the eastern North American species in ...

Journal of the Torrey Botanical Society 136(1), 2009, pp. 26–32

A seed atlas of Hypoxis from eastern North America Scott Zona1,2 Department of Biological Sciences, Florida International University, FL 33199

Jeffery Prince, Gabriela Halder, Robert Schwartz, and Rodrigo Vargas Department of Biology, Dauer Electron Microscopy Laboratory, University of Miami, Coral Gables, Miami, FL 33124 ZONA, S. (Department of Biological Sciences, Florida International University, FL 33199), J. PRINCE, G. HALDER, R. SCHWARTZ AND R. VARGAS (Department of Biology, Dauer Electron Microscopy Laboratory, University of Miami, Coral Gables, Miami, FL 33124). A seed atlas of Hypoxis from eastern North America. J. Torrey Bot. Soc. 136: 26–32. 2009.—The micromorphology of the seeds of six species of Hypoxis (Hypoxidaceae) from eastern North America (east of Texas) was studied with low vacuum, scanning electron microscopy using the backscatter detector. The shape of the cells of the seed coat and the configuration of the cuticle appeared characteristic for a particular species. The species may be placed into three main groups. The first group, those with shiny black, papillate cells, includes H. curtissii and H. hirsuta. The second group, those with shiny black, rounded-inflated (colliculate) cells, comprises H. juncea and H. rigida. The third group of H. sessilis and H. wrightii is characterized by brown seeds with wrinkled, detached cuticles. The seeds of H. sessilis are unique among the eastern North American species in having iridescent seed coats. The widespread occurrence of these seed coat characters among both American and African species suggests that phylogenetically informative characteristics of the seed coat of Hypoxis are affected by a high level of homoplasy. Key words: Hypoxis, Hypoxidaceae, morphology, seed, seed coat, SEM.

species and are frequently used in keys to the species. Herndon (2002) noted that some specimens are impossible to identify without seeds, and that as far as possible, all identifications made by other means should be confirmed by examination of seed characteristics. Seed characteristics are, therefore, critical for the identification of species of Hypoxis This report provides clear, detailed images of seeds of the species of Hypoxis from eastern North America.

Approximately 90 species of Hypoxis are known (Govaerts 2007) from southern Africa (where species diversity is exceptionally high), Madagascar, Asia, Indomalasia, Australia, South America, Central America, North America, and the West Indies. Seven species occur in the United States, six of which occur in eastern North America (east of Texas). The species most frequently occur in hydric or seasonally flooded habitats, where they grow as perennial geophytes with slender, grass-like leaves. Seed morphology, specifically the color and conformation of the seed coat, has long been recognized as a character of taxonomic significance in the genus Hypoxis (Hypoxidaceae) (Brackett 1923, Henderson 1987, McVaugh 1989, Herndon 1992, 2002, Wiland-Szyman´ska 2001, 2006). The seeds of Hypoxis are small, generally less than 2 mm in the longest diameter. Although difficult to see without the aid of a microscope, characteristics of the seed are useful in distinguishing

Materials and Methods. The taxonomy of Hypoxis used here follows Govaerts’ (2007) on-line checklist of Hypoxidaceae. Herbarium specimens from the Florida Museum of Natural History, Gainesville, Florida (FLAS) and Fairchild Tropical Botanic Garden, Miami, Florida (FTG) were consulted for this atlas. Seed size and color was measured to the nearest 0.1 mm with calipers under a dissecting microscope. The seed descriptors correspond to those of Beaufort-Murphy (1983). Selected specimens from among those examined were sampled for SEM study. Samples were removed from specimens for scanning electron microscopy with permission of the curators. Samples were processed in the Dauer Electron Microscopy Laboratory, Biology

1 We thank the curators of FLAS and FTG for allowing us access to specimens in their care. This is FIU Tropical Biology Program contribution number 141. 2 Author for correspondence. E-mail: [email protected] fiu.edu Received for publication August 14, 2008, and in revised form November 19, 2008.

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FIG. 1. Hypoxis curtissii, seed (a, c) and papillate cells of the seed coat (b, d). a, b. Morris 3365. c, d. Thomas et al. 35499.

Department, University of Miami, Florida. Non-fixed, uncoated seeds were attached to carbon coated tape on aluminum stubs and viewed with a Jeol 5601 LV Scanning Electron Microscope operated in the low vacuum mode (0.3–0.6 Torr) at 25 kV using the backscatter detector. Results. Hypoxis curtissii Rose in J.K. Small (Fig. 1). Distribution: Southeastern U.S. to eastern Texas. Seeds glossy black, broadly elliptic to nearly circular in outline (Figs. 1a, 1c), 1.0–1.5 mm long, 0.8–1.1 mm wide; the micropyle and rostrate hylum (funicular remains) subadjacent; the seed apices are obtuse to cuspidate at the micropyle end; cell orientation irregular but straight along the raphe; cells 4–6-sided polygonate in surface view, 25–50 mm wide; the cell face papillate but the cell surface is smooth (Figs. 1b, 1d), the cell edges distinct or indistinct; cuticle not evident. In some parts of samples (e.g., Morris 3365), the papillate projection of the cell surface is

collapsed or indented (Fig. 1b). This appears to be an artifact of drying and/or handling. Specimens examined: USA: Florida. Alachua Co., 6 Apr 1995, Carlsward & Abbott 105 (FLAS); Calhoun Co., 18 May 1965, McDaniel 6238 (FLAS); Columbia Co., 2 Jun 1988, Herndon 1975 (FTG); Gilchrist Co., 25 Oct 1985, Hansen et al. 10824 (FTG); Glades Co., 30 Jun 1967, Smith 1629 (FLAS); Hamilton Co., 29 Oct 1988, Morris 3365 (FLAS); Hillsborough Co, Meagher 7 (FTG); Jefferson Co., 11 Oct 1973, Kral 52379 (FLAS); Levy Co., 5 Jul 1979, Dunevitz 13 (FLAS); Martin Co., 21 Oct 1997, Gann & Bradley 1071 (FTG); St. John’s Co., 2 Nov 2001, Notis & Tilley 435 (FLAS). Louisiana. Washington Parish, 23 Jun 1973, Thomas et al. 35499 (FLAS). Hypoxis hirsuta (L.) Coville (Fig. 2). Distribution: Central and eastern Canada to central and eastern U.S. Seeds glossy black, broadly elliptic in outline (Figs. 2a, 2c), 0.8–1.5 mm long, 0.9– 1.1 mm wide; the micropyle and rostrate hylum (funicular remains) subadjacent to

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FIG. 2. Hypoxis hirsuta, seed (a, c) and papillate cells of the seed coat (b, d). a, b. Holland et al. 292. c, d. Watson s.n., August 1936.

adjacent; the seed apices are obtuse; cell orientation irregular but straight along the raphe; cells 4–8-sided polygonate to circular in surface view, 30–50 mm wide; the cell face papillate (Fig. 2b) but the cell surface is smooth (Fig. 2d), the cell edges distinct or indistinct; cuticle not evident. Specimens examined: USA. Georgia. Ft. Stewart, 4 Oct 1999, Holland et al. 292 (FTG). Louisiana. Allen Parish, 5 Apr 1980, Allen 10175 (FLAS). North Carolina. Watson s.n., August 1936 (FLAS). West Virginia. Barbour Co., 3 Jul 1960, Rossbach 2179 (FLAS). Hypoxis juncea Sm. (Fig. 3). Distribution: Southeastern U.S. Seeds glossy black, broadly elliptic to nearly circular in outline (Figs. 3a, 3b), 0.7–0.9 mm long, 0.6–0.8 mm wide; the micropyle and rostrate hylum (funicular remains) subadjacent; the seed apices are obtuse; cell orientation irregular but straight along the raphe; cells 5–7-sided rounded to irregular in surface view, 25–50 mm wide; the cell face strongly domed (Fig. 3b), the cell appearing inflated

(strongly colliculate) and the cell surface is smooth (Fig. 3d), wrinkled toward the edges, the cell edges indistinct (Fig. 3b); cuticle not evident. Specimens examined: USA. Florida. Highlands Co., 12 Apr 1964, Read 986 (FTG), 4 Apr 1981, Lindsey & Upchurch 306 (FTG); Indian River Co., 22 Aug 2001, Fisher & Scanion 208 (FLAS); Lake Co., 27 Mar 1910, Hood 21883 (FLAS); Lee Co., 10 Apr 1973, Brumbach 8313 (FLAS); Leon Co., 8 May 1966, McDaniel 7458 (FLAS); Levy Co., West s.n., 11 Apr 1934 (FLAS); Martin Co., Woodbury s.n., May 1988 (FTG); Nassau Co., 15 Apr 1959, Ward & Ward 1257 (FLAS); Palm Beach Co., 4 Mar 1963, Smith & Myint 903 (FLAS); Pasco Co., 24 Apr 1980, Baltzell 11054 (FLAS). Hypoxis rigida Chapm. (Fig. 4). Distribution: Southeastern U.S. to eastern Texas. Seeds glossy black, broadly elliptical to nearly circular in outline (Fig. 4a), 1.0 mm long, 0.9 mm wide; the micropyle and rostrate

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FIG. 3. Hypoxis juncea, seed (a, c) and colliculate cells of the seed coat (b, d). a, b. Read 986. c, d. Brumbach 8313.

hylum (funicular remains) adjacent to subadjacent; the seed apices are obtuse; cell orientation irregular but straight along the raphe; cells 5–7-sided rounded in surface view, 30–60 mm wide; the cell face strongly domed, the cell appearing inflated (strongly colliculate) and the cell surface is smooth, wrinkled toward the edges, the cell edges indistinct (Fig. 4b); cuticle not evident. Specimens examined: USA. Florida. Baker Co., West & Arnold s.n., 25 May 1940 (FLAS); Walton Co., 11 May 1967, Ward et al. 6405 (FLAS).

wide; the cell face low dome-shaped, the cell edges distinct (Fig. 5b); cuticle evident, detached and wrinkled, covering the cell edges and faces, elaborated into folds and crests across the cell face (Fig. 5d). Specimens examined: USA. Florida. MiamiDade Co., 15 Mar 1979, Avery 2085 (FTG), 26 Aug 1980, Avery 2259 (FTG), 11 May 1986, Herndon 1535 (FTG); Okaloosa Co., 16 May 1990, Herndon 2775 (FTG); Santa Rosa Co., Stanberry s.n., 5 May 1950 (FLAS). Louisiana. Winn Parish, 7 Sep 1978, Thomas 60442 (FLAS).

Hypoxis sessilis L. (Fig. 5). Distribution: Southeastern U.S. to eastern Texas. Seeds dark brown with shiny gold iridescence, broadly elliptical to nearly circular in outline (Figs. 5a, 5c), 1.0–1.6 mm long, 0.9– 1.3 mm wide; the micropyle and rostrate hylum (funicular remains) separated by ca. 90u; the seed apices are obtuse; cell orientation irregular but straight along the raphe; cells 4– 8-sided polygonate in surface view, 50–75 mm

Hypoxis wrightii (Baker) Brackett (Fig. 6). Distribution: Southeastern U.S. to eastern Texas, Mexico, Bahamas and Greater Antilles. Seeds dull dark brown, narrowly to broadly elliptical in outline (Figs. 6a, 6c), 0.8–1.2 mm long, 0.6–0.9 mm wide; the micropyle and rostrate hylum (funicular remains) subadjacent; the seed apices are obtuse; cell orientation irregular but straight along the raphe; cells 6- or 7-sided polygonate in surface view, 25–50 mm wide; the cells conical, the cell edges

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FIG. 4. Hypoxis rigida, seed (a) and colliculate cells of the seed coat (b). A. Ward et al. 6405. B. West & Arnold s.n., 25 May 1940.

distinct (Fig. 6d); cuticle evident, detached and wrinkled, light brown, visible at cell edges and covering the cell faces, elaborated into folds and crests across the cell face (Fig. 6b). Specimens examined: USA. Alabama. Mobile Co., 30 Apr 1967, Ward 6232 (FLAS). Florida. Collier Co., 21 Jan 1978, Popenoe & Smiley 1112 (FTG); Martin Co., 3 Nov 1979, Popenoe 1845 (FTG); Miami-Dade Co., 21 Aug 1995, Bradley 58 (FTG), 10 Jan 1992, Reimus 41 (FTG), 9 Dec 1979, Avery 2199 (FTG); Monroe Co., Aug 1999, Liu 270 (FTG), 6 May 1964, Avery s.n. (FLAS, FTG), 19 Nov 1964, Ward et al. 4293 (FLAS); Pasco Co., 17 Mar 1974, Baltzell 5908 (FLAS); Wakulla Co., 17 Aug 1991, Herndon 3082 (FTG). Georgia. Tift Co., 3 May 1974, Mullens et al. 74094 (FLAS). Discussion. This report shows the seeds of Hypoxis species in the eastern U.S. encompass a wide range of morphological diversity. They share the general elliptical to nearly circular outline and the black or brown color, attri-

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buted to the presence of phytomelan in the seed coat (Organezova 1995). Hypoxis seeds are noteworthy for the hardened funicular remnant, called the rostrate hilum by Brackett (1923) or the columnar projection by McVaugh (1989). The funicular remnant may be adjacent or subadjacent to the micropyle end of the seed, or it may be displaced toward the equator of the seed, as in H. sessilis. Despite the ample diversity found in the micromorphology of Hypoxis seeds, the species may be placed into three main groups. The first group, those with shiny black, papillate cells (Figs. 1b, 2b), includes H. curtissii and H. hirsuta. The second group, those with shiny black, rounded-inflated (colliculate) cells (Figs. 3b, 4b), comprises H. juncea and H. rigida. The third group of H. sessilis and H. wrightii is characterized by brown seeds with wrinkled, detached cuticles (Figs. 5b, 6d). The seeds of H. sessilis are unique among the eastern North American species in having iridescent seed coats. As noted by Nordal et al. (1985) and Wiland-Szyman´ska (2006) in their studies of East African Hypoxis, species with brown seed coats invariably possess an evident, detached cuticle, whereas as those with black seeds possess a cuticle that remains closely appressed or attached to the testa. Without a detailed phylogenetic study for Hypoxis, we are unable to determine whether the similarities noted here are indications of a shared recent ancestry (i.e., synapomorphies). We note, however, that most of the characteristics found in eastern North American Hypoxis can also be seen in other species from other parts of the world, so few of the morphological characteristics found in this study are unique features. The iridescent seed coat of H. sessilis is also found in H. decumbens L. of tropical America (Brackett 1923, as H. breviscapa Kunth) and H. angustifolia Lam. var. luzuloides (Robyns & Tournay) Wiland of Africa (Wiland-Szyman´ska and Adamski 2002). The shiny, black seed coats with colliculate cells of H. juncea and H. rigida are also seen in H. angolensis Baker and H. kilimanjarica Baker (WilandSzyman´ska 2001); while the black, papillate cells of H. curtissii and H. hirsuta are likewise found in H. angustifolia var. madagascariensis Wiland (Wiland-Szyman´ska and Adamski 2002). The brown, conical cells with elaborated, wrinkled cuticle of H. wrightii (Figs. 6b, 6d) do not resemble anything illustrated by

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FIG. 5. Hypoxis sessilis, seed (a, b) and wrinkled, detached cuticle of the seed coat (b, d). a, b. Stanberry s.n., 5 May 1950. c, d. Herndon 1535.

previous workers (Nordal et al. 1985, Henderson 1987, Wiland-Szyman´ska 2001, 2006, Wiland-Szyman´ska and Adamski 2002) and may represent a unique feature. The widespread occurrence of these seed coat characters among both American and African species suggests that phylogenetically informative characteristics of the seed coat of Hypoxis are affected by a high level of homoplasy, as has been noted in other genera of other families (e.g., Minuto et al. 2006, Abdel Khalik and Osman 2007). Conclusions. Seed characters are shown to have an critical role in Hypoxis taxonomy and great utility in indentifying species. Hypoxis curtissii and H. hirsute have seed coats with shiny black, papillate cells. The seed coats of Hypoxis juncea and H. rigida are shiny black, with colliculate cells. The seeds of H. sessilis and H. wrightii are brown and have wrinkled. detached cuticles. The seed coats of H. sessilis are iridescent.

Literature Cited ABDEL KHALIK, K. AND A. K. OSMAN. 2007. Seed morphology of some species of Convolvulaceae from Egypt (Identification of species and systematic significance). Feddes Repert. 118: 24–37. BEAUFORT-MURPHY, H. T. 1983. The seed surface morphology of the Gesneriaceae utilizing the scanning electron microscope and a new system for diagnosing seed morphology. Selbyana 6: 220–422. BRACKETT, A. 1923. Revision of the American species of Hypoxis. Rhodora 25: 120–147, 151–155. GOVAERTS, R. 2007. World Checklist of Hypoxidaceae. Retrieved 12 February 2008 from The Board of Trustees of the Royal Botanic Gardens, Kew, U.K. ,http://www.kew.org/wcsp/. HENDERSON, R. J. F. 1987. Hypoxis. Flora of Australia 45: 178–190, 220. HERNDON, A. 1992. The genus Hypoxis (Hypoxidaceae) in Florida. Florida Scientist 55: 45–55. HERNDON, A. 2002. Hypoxis, p. 201–204. In Flora of North America Editorial Committee (eds.). 2002. Flora of North America North of Mexico, vol. 26. Magnoliophyta: Lilidae: Liliales and Orchidales. Oxford University Press, New York, NY.

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FIG. 6. Hypoxis wrightii, seed (a, b) and wrinkled, detached cuticle of the seed coat (b, d). a, b. Liu 270. c, d. Bradley 58. MCVAUGH, R. 1989. Hypoxis L., p. 219–227. In W. R. Anderson [ed.], Flora Novo-Galiciana 15 Bromeliaceae to Dioscoreaceae. University of Michigan Herbarium, Ann Arbor, MI. MINUTO, L., S. FIOR, E. ROCCOTIELLO, AND G. CASAZZA. 2006. Seed morphology in Moehringia L. and its taxonomic significance in comparative studies within the Caryophyllaceae. Plant Syst. Evol. 262: 189–208. NORDAL, I., M. M. LAANE, E. HOLT, AND I. STAUBO. 1985. Taxonomic studies in the genus Hypoxis in East Africa. Nordic J. Bot. 5: 15–30. OGANEZOVA, G. G. 1995. [On the systematical position of the families Haemodoraceae, Hypox-

idaceae, and Taccaceae (the data on the seed structure)]. Bot. Zhurn. 80: 12–25. [in Russian with English abstract]. WILAND-SZYMAN´SKA, J. 2001. The genus Hypoxis (Hypoxidaceae) in Central Africa. Ann. Mo. Bot. Gard. 88: 302–350. WILAND-SZYMAN´SKA, J. 2006. Morphological variability of seeds in East African species of the genus Hypoxis L. (Hypoxidaceae). Biodiv. Res. Conserv. (Poznan´, Poland) 1–2: 31–33. WILAND-SZYMAN´SKA, J. AND Z. ADAMSKI. 2002. Taxonomic and morphological notes on Hypoxis angustifolia (Hypoxidaceae) from Africa, Madagascar, and Mauritius. Novon 12: 142–151.

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