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Taxonomic Revision of the Opuntia Humifusa Complex (Opuntieae: Cactaceae) of the Eastern United States

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Taxonomic Revision of the Opuntia Humifusa Complex (Opuntieae: Cactaceae) of the Eastern United States Phytotaxa 290 (1): 001–065 ISSN 1179-3155 (print edition) http://www.mapress.com/j/pt/ PHYTOTAXA Copyright © 2017 Magnolia Press Monograph ISSN 1179-3163 (online edition) https://doi.org/10.11646/phytotaxa.290.1.1 PHYTOTAXA 290 Taxonomic revision of the Opuntia humifusa complex (Opuntieae: Cactaceae) of the eastern United States LUCAS C. MAJURE1,2,*, WALTER S. JUDD2,3, PAMELA S. SOLTIS2 & DOUGLAS E. SOLTIS2,3 1Desert Botanical Garden, Department of Research, Conservation and Collections, 1201 N. Galvin Parkway, Phoenix, AZ 85008; [email protected] 2University of Florida, Florida Museum of Natural History, Dickinson Hall, Gainesville, Florida 32611; [email protected], [email protected], [email protected] 3University of Florida, Department of Biology, 220 Bartram Hall, P.O. Box 118525, Gainesville, Florida 32611 * Author for correspondence Magnolia Press Auckland, New Zealand Accepted by Duilio Iamonico: 3 Dec. 2016; published: 4 Jan. 2017 1 LUCAS C. MAJURE, WALTER S. JUDD, PAMELA S. SOLTIS & DOUGLAS E. SOLTIS Taxonomic revision of the Opuntia humifusa complex (Opuntieae: Cactaceae) of the eastern United States (Phytotaxa 290) 65 pp.; 30 cm. 4 January 2017 ISBN 978-1-77670-064-6 (paperback) ISBN 978-1-77670-065-3 (Online edition) FIRST PUBLISHED IN 2017 BY Magnolia Press P.O. Box 41-383 Auckland 1346 New Zealand e-mail: [email protected] http://www.mapress.com/j/pt/ © 2017 Magnolia Press All rights reserved. No part of this publication may be reproduced, stored, transmitted or disseminated, in any form, or by any means, without prior written permission from the publisher, to whom all requests to reproduce copyright material should be directed in writing. This authorization does not extend to any other kind of copying, by any means, in any form, and for any purpose other than private research use. ISSN 1179-3155 (Print edition) ISSN 1179-3163 (Online edition) 2 • Phytotaxa 290 (1) © 2017 Magnolia Press MAJURE ET AL. Abstract The Humifusa clade represents a recent radiation that originated in the late Pliocene or early Pleistocene and consists of about 10 species widely distributed in North America from northern Mexico north to Ontario, Canada, and south to the Florida Keys. This clade likely originated in the edaphically subxeric regions of northern Mexico and the southwestern United States, and from there it later spread to the southeastern United States and ultimately produced a small radiation in the eastern United States. Hybridization among evolutionarily divergent diploid species of the southeastern (SE) and southwestern (SW) United States subclades led to the origin of many polyploid taxa, which today occupy about 75% of the distribution of the clade. Here we present a taxonomic revision of the SE subclade of the Humifusa clade and polyploid derivatives that commonly occur in the eastern United States (i.e., the O. humifusa complex). We recognize eight taxa: Opuntia abjecta, O. austrina, O. cespitosa, O. drummondii, O. humifusa, O. mesacantha subsp. mesacantha, O. mesacantha subsp. lata, and O. nemoralis, as well as the interclade allopolyploid, Opuntia ochrocentra, derived, in part, from a member of the O. humifusa complex. Diagnostic keys, descriptions, original photos, and distribution maps are provided for each taxon. Neotypes are designated for the names O. austrina (NY) and O. youngii (USF), and O. drummondii and O. tracyi are lectotypified from an illustration in Maund & Henslow and a specimen at NY, respectively. Key words: cacti, hybridization, morphology, polyploidy, prickly pears, taxonomy Introduction Opuntia Miller (1754) (tribe Opuntieae DC.) is a genus native to the Americas and it is distributed from southern Argentina to Canada (Anderson 2001). Members of the clade occupy many habitats, from seasonally dry tropical and subtropical deciduous forests and scrub, to moderate desert environments, temperate prairies, coastlines, and forest openings (Britton & Rose 1919, Benson 1982, Anderson 2001, Pinkava 2003). Opuntia diplays a peculiar set of morphological characters including longitudinally flattened, determinate stem segments, or cladodes, that take over the photosynthetic function of the small and ephemeral long shoot leaves, which are produced as the cladode develops. Cladodes may be glabrous or pubescent (see Majure & Puente 2014), ranging in color from dark-green to purple. All species of Opuntia (and subfamily Opuntioideae K.Schum., tribes Cylindropuntieae Doweld, Opuntieae and Tephrocacteae Doweld) have glochids (Fig. 1A), or retrorsely barbed [with the exception of Micropuntia Daston (1946: 661) that has antrorsely-barbed glochids] and deciduous hair- like spines that are produced from specialized short shoots (areoles), which are mostly included within the stem tissue (see Mauseth 2006). These spines often become exserted and conspicuous as the cladode develops and form an impressive armament against herbivores. Glochids have also been shown to aid in water uptake in O. microdasys (Lehmann 1827: 16) Lehmann ex Pfeiffer (1837: 154); the retrorse barbs force water droplets from the apex to the base of the glochid where they are absorbed by the trichomes of the areole and then presumably by the apical meristem within each areole (Ju et al. 2012), aiding in water uptake in arid environments. Long spines are also produced in most species and can be strongly retrorsely barbed or smooth to the touch (although all spines produce overlapping cells that develop a small degree of "barbedness"; see Fig. 1B-C). Some species form only one type of spine, whereas others may develop both central (those produced from the center of the areole) and radial spines (those produced from the periphery of the areole; see Parfitt 1991, Pinkava 2003). The spine development pattern from the areole can be a useful taxonomic character. Spine color changes through time but can also be diagnostic at the species level. Opuntia species produce high quantities of betalain pigments (see Brockington et al. 2011, 2015) under stressful conditions, and water- or cold-stressed plants often become reddish, pinkish, or purplish, especially around the areoles, and certain members of specific clades always are purplish (i.e., the Macrocentra clade; Majure & Puente 2014). Species of Opuntia can form spreading to erect shrubs or even trees. Most tree-like taxa are found in tropical or subtropical areas (e.g., certain members of the Nopalea clade and species in the Galapagos Islands; see Britton & Rose 1919, Anderson 2001, Majure et al. 2012a). In temperate areas, smaller shrubby taxa, which commonly sprawl or trail along the ground, are more frequently found, such as O. macrorhiza Engelmann (1850: 206) and O. humifusa (Rafinesque 1820: 15) Rafinesque (1830: 247). TAXONOMIC REVISION OF THE OPUNTIA HUMIFUSA COMPLEX Phytotaxa 290 (1) © 2017 Magnolia Press • 3 FIGURE 1. SEM micrographs of characters of Opuntia from the O. humifusa complex. A) close-up of glochids of O. cespitosa at 106x (Majure 736), B-C) close-up of spine surfaces showing overlapping cells creating retrorse barbs in O. drummondii (Majure 843), B) spine tip at 200x, C) mid-section of spine at 289x, D) pollen grain of O. cespitosa (Majure 736) at 850x, E) pollen grain of O. mesacantha subsp. lata at 900x (Ervin s.n.), F) seed of O. cespitosa at 16x (Majure 736), G) seed of O. drummondii at 20x (Majure 843). All photos taken by L.C. Majure. 4 • Phytotaxa 290 (1) © 2017 Magnolia Press MAJURE ET AL. Most of the species exhibit open, insect-pollinated flowers with thigmonastic stamens (not to be confused with thigmotropic stamens that move in the direction of a stimulus), which move toward the stigma upon stimulation suggesting a bias towards oligolectic pollinators (see Schlindwein & Whittman 1997, Díaz & Cocucci 2003). However, bird pollination and the loss of stamen movement have evolved numerous times in the group (Majure & Puente 2014). Most species of “strictly” insect-pollinated Opuntia have pollen with a reticulate exine (see Majure & Puente 2014), and Majure and Ervin (2007) noted an increase in pore number in certain individuals—from 12–14 (Fig. 1D‒E)—and those species were subsequently discovered to be tetraploid [see O. cespitosa Rafinesque (1830: 216); Majure et al. 2012b]. The same increase in pore number can be seen in the hexaploid O. megarrhiza Rose (1906: 126) versus the diploid relative O. pachyrrhiza Hernández, Gómez-Honostrosa, Bárcenas (2001: 309) (see Fig. 3 K-L in Majure & Puente 2014). Although not a synapomorphy of Opuntia (but rather Opuntioideae), the seeds are characteristic in having a bony funicular girdle that surrounds a bony funicular envelope (Fig. 1F-G), which covers the embryo (Stuppy 2002). The latter may be glabrous or pubescent (Stuppy 2002, Majure & Puente 2014), and the surface features of the funicular envelope may be taxonomically useful in species delimitation. Putative synapomorphies of Opuntia s.str. are pollen with a reticulate exine, although this character was equivocal in some analyses (Majure & Puente unpubl. data), and has mostly been lost in certain bird-pollinated members of the clade (see Majure & Puente 2014), and spirally enrolled embryos [as shown in Stuppy (2002) and Majure et al. (2013)]. However, morphological synapomorphies are still being investigated in the group (Majure unpubl. data). The Opuntia clade likely originated in the late Miocene (Arakaki et al. 2011, Majure et al. 2012a) in southern South America and from there it dispersed north into the North American desert region [modern-day central and northern Mexico and southwestern United States (US)], where the clade diversified and expanded through to the Caribbean Islands and throughout the rest of the continental US. A small group, the Humifusa clade, eventually migrated to the eastern US (Majure et al. 2012a), where it experienced an additional, small radiation. The Humifusa clade consists of two subclades (Fig. 2), a southwestern subclade (SW) including the widespread and morphologically highly variable taxon, O. macrorhiza s.lat. (Fig. 3) and close relatives, e.g., O. pottsii Salm-Dyck (1849: 236.), and the southeastern subclade (SE), which includes O. austrina and several other species (Majure et al.
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