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Systematic Botany (1988), 13(4): pp. 483-492 © Copyright 1988 by the American Society of Plant Taxonomists Fuchsia pachyrrhiza (Onagraceae), a Tuberous New Species and Section of Fuchsia from Western Peru PAUL E. BERRY Departamento de BiologIa de Organismos, Universidad Simon BolIvar, Apartado 80659, Caracas 1080, Venezuela BRUCE A. STEIN Missouri Botanical Garden, St. Louis, Missouri 63166-0299 Present address: International Program, The Nature Conservancy, 1815 N. Lynn Street, Arlington, Virginia 22209 SHERWIN CARLQuIsT Rancho Santa Ana Botanic Garden and Department of Biology, Pomona College, Claremont, California 91711 JOAN N0wICKE Department of Botany, National Museum of Natural History, Smithsonian Institution, Washington, District of Columbia 20560 ABsrRAcT. Fuchsia pachyrrhiza is described and is the type of the new section Pachyrrhiza. The species is known from only two localities along the western slope of the Peruvian Andes. Distinguishing sectional characters are the presence of a whorl of reflexed stamens, tuberous roots, alternate leaves, pollen with smooth viscin threads, and small flowers with a distinctively ridged nectary. The tuberous roots appear to be adapted for water as well as starch storage, and are most likely related to the strongly seasonal habitat and deciduous habit of the species. Chromosome number is n = 11, the normal diploid condition for the genus, and only bivalents are present at meiosis. No clear affinities with other sections of Fuchsia can be discerned based on the characters examined. A very distinctive Fuchsia was collected along the Pacific slope of the northern Peruvian An des by the second author during the rainy sea son of 1985. Upon examination, this plant proved to be an undescribed species that pos sesses a suite of characters not found in any currently recognized section of the genus (Ber ry 1982). The area was revisited in 1987 to make more detailed field observations on the species, and to obtain additional material for cytologi cal, anatomical, and morphological analysis, as well as live material for cultivation and for mac romolecular analysis (Sytsma, in prep.). In this paper we formally describe the new species and section, and present information on its mor phology, palynology, and cytology. Because of the unusual tuberous roots and deciduous habit, a detailed investigation of the root and wood anatomy was also undertaken. 483 TAxoNoMIc TREATMENT Fuchsia Section Pachyrrhiza P. Berry & B. A. Stein, sect. nov—TYPE: Fuchsia pachyr rhiza P. Berry & B. A. Stein. Frutex radicibus valde tuberosis. Folia ple rumque alterna. Flores axillares, bisexuales, se palis petalis duplo longioribus, parum basi con natis, nectario disco annulari styli basin cingenti atque 4-porcato inter tubum stylumque, petalis subconvolutis; staminibus filamentis antisepa us erectis, antipetalis in tubum reflexis inclu sisque; bacca seminibus multis, 120—150. Shrubs with thick, tuberous roots. Leaves mostly alternate, deciduous. Flowers hermaph roditic, solitary, axillary, and pendant. Floral tube suburceolate, 4-lobed, the nectary forming a ring around the base of the style, with 4 con spicuous ridges extending out to the floral tube 484 [Volume 13 SYSTEMATIC BOTANY and tapering upwards towards the rim. Sepals longer than the floral tube, shortly connate at base. Petals erect and subconvolute, ca. ½ the length of the sepals. Stamens in two series, fil aments of the antisepalous stamens erect, those of the antipetalous stamens reflexed and in cluded within the floral tube. Pollen mostly 2-, rarely 3-aperturate, with smooth viscin threads and elongate sculpture elements in the ektex me. Stigma capitate, slightly 4-lobed. Berries oblong with 120—150 seeds per fruit, n = 11. Fuchsia pachyrrhiza P. Berry & B. A. Stein, sp. nov. (fig. 1).—TYpE: Peru, Cajamarca, 11-15 km from Contumazá on road to Cascas, 94101 km above Casa Grande (Panamerican Hwy.), 7°25’S, 78°50’W, 2450—2550 m, 8 Feb 1987, Stein et al. 4066 (holotype: MO; isotypes: AAU, B, CAS, F, HUT, K, NY, U, US, USM). Frutex 1—2 metralis, radicibus tuberosis. Folia anguste elliptica, plerumque alterna, decidua. Flores pendentes, secundi, tubo florali subur ceolato, 6.5—7.5 mm longo, rubro-auriantiaco, parum ovario longiore, petalis suborbiculari bus, erectis subconvolutisque, marroninis; staminibus filamentis 1—1.5 mm longis, anti petalis in tubum reflexis. Numerus chromoso micus n = 11. Erect to scandent shrubs 1-2 m high. Branch es arching to divergent with reddish-brown, exfoliating bark; young stems pilose with hairs 0.3-0.5 mm long. Roots tuberous with large clusters present at base of the stem, individual segments irregularly ovoid to clavate, to 16 cm long and 5.5 cm in diam. Leaves deciduous in the dry season, mostly alternate, occasionally opposite or ternate, membranaceous, narrowly elliptic, 5—13cm long, 1.5—2.5cm wide, glabrous above with impressed veins, subglabrous to pi lose below, margins serrulate; secondary veins 9—15 on either side of the midvein. Petioles pi lose, 5-21 mm long, often leaving a subspinose protrusion on the stem after leaf abscission. Stipules dark, triangular with subulate tips, 0.8— 1.1 mm long, persistent. Flowers solitary in up per leaf axils, pendant and secund. Pedicels 19— 44 mm long. Ovary oblong, pilose, light red, 57 mm long, 1.5-3 mm in diam. Floral tube sub urceolate, 6.5-7.5 mm long from top of ovary to point of petal and stamen insertion, 4-5 mm in diam. and 4-lobed at the base, narrowed to 3.5 mm in diam. in the middle, ca. 4.5 mm in diam. at the rim, sparsely pilose outside, gla brous within; nectary a ring ca. 1 mm high, surrounding and tightly appressed to the base of the style, with 4 stout ridges extending up along the floral tube and tapering towards the rim. Sepals triangular, spreading at anthesis, 9— 11 mm long, connate at base for 2-3 mm, 3 mm wide at the base of the lobes. Tube and sepals red to orange-red. Petals maroon, suborbicular, erect, slightly convolute, 5—6.5 mm long, 4.5— 5.5 mm wide. Stamens in two series, the anti sepalous stamens erect and exserted above the floral tube, with filaments 1-1.5 mm long, the antipetalous stamens reflexed and included within the tube, with filaments 1 mm long; an thers oblong, 2-3.5 mm long, 1-2 mm wide, with a small, mucronate tip, dorsifixed, the exserted anthers slightly larger; pollen 2- (rare ly 3-) aperturate, longest dimensions 84-96 em (based on 10 grains), the ektexine with elongate sculpture elements and smooth viscin threads attached near the proximal pole. Style glabrous, 12—14 mm long, pink; stigma capitate, shortly 4-lobed, 2 mm long, 1.5-2 mm in diam., pink. Berry oblong, 15-20 mm long, 10-12 mm in diam., deep maroon; seeds laterally com pressed, 1.2—1.6 mm long, ca. 1 mm wide, 120— 150 per fruit. n = 11. Distribution (fig. 2). Known only from two localities on the western slopes of the Peruvian Andes, near Contumazá in Cajamarca Depart ment and near Cochabamba in Ancash Depart ment, at elevations of 2450—2900 m. Additional specimens examined. PERU. Cajamarca: 12 km S of Contumazá on road to Cascas, 2530 m, fi. & fr., 2 Feb 1985, Stein & Todzia 2047 (K, MO, US, USM). Ancash: Prov. Huaraz, 10 km by road from Cochabamba, 9°27’S, 77°51’W, 2870 m, fr., 6—8 Jun 1985, Smith & Buddensiek 10912 (MO). ECOLOGY Fuchsia pachyrrhiza grows on the Pacific slope of the Andes in an area characterized by a long dry season. The short rainy season generally occurs between December and April. Individ uals of this species are apparently deciduous during the dry season, producing flushes of leaves and flowering shoots after the onset of the rains. The vegetation at the type locality is a mixture of xeric elements characteristic of the 1988] BERRY E AL.: FUCHSIA 485 FiG. 1. Fuchsia pachyrrhiza P. Berry & B. A. Stein, a. Flowering branch. b. Underground tuber cluster. c. Detail of single flower. d. Longitudinal section of young flower with style removed—note the lower, reflexed set of stamens. e. Detail of petal shape, flattened from normal position with incurved sides. f. Detail of stigma. g. Detail of a basal stem leaf. (From Stein et al. 4066.) 486 [Volume 13 SYSTEMATIC BOTANY using a Reichert temperature-compensated op tical refractometer. MORPHOLOGY \ TrujiII4 \. im 200km FIG. 2. Distribution of Fuchsia pachyrrhiza in Peru. lower elevation dry forest (such as columnar cacti and terrestrial bromeliads) and mesic ele ments (such as Siparuna, Hedyosmum, Salpichroa, and Brachyotum), which are often confined to relictual scrub forest patches. The Ancash pop ulation was collected in an open dwarf forest dominated by Escallonia and Myrsianthes. Fuchsia pachyrrhiza is an infrequent shrub that grows in shallow, rocky soil, mostly in the shade of small trees, but occasionally in full sun along roadbanks or on mossy cliff faces. The speckled hummingbird (Adelomyia me lanogenys), a short-billed species, was observed visiting flowers of F. pachyrrhiza at the type lo cality, and is likely one of its pollinators. Nectar from several non-bagged flowers was measured at a concentration of 21% sucrose-equivalents, This distinctive new species possesses a type of nectary unique within the genus, as de scribed above (fig. id). Furthermore, Fuchsia pachyrrhiza contains a series of features unusual for the genus, suggesting an isolated phyloge netic position for this new section. These char acters include alternate leaves, tuberous roots, a whorl of reflexed stamens, and small flowers with partially connate sepals. Individually, these features are found in other sections, but never in this combination. Alternate leaves are found in three other sections (sects. Skinnera, Hemsley ella, and Kierschlegeria), which on other grounds are not closely related to each other. Since al ternate leaves in Fuchsia seem to be associated with species exhibiting a deciduous habit, the possibility that this phyllotaxy is a develop mental outcome of rapid stem elongation and leaf flushes is worth investigating. Tuberous roots are also found in some members of sects. Ellobium and Hemsleyella, and most likely have evolved independently in each group in re sponse to seasonally dry habitats. Reflexed an tipetalous stamens characterize the Central American sects. Jimenezia and Encliandra, but sect. Encliandra differs greatly from sect. Pachyrrhiza in its dioecious to gynodioecious flowers and few-seeded fruits, while sect. Jimenezia has en tirely opposite leaves and flowers grouped into tight racemes. Partially connate sepals other wise occur only in sects. Quelusia and Hemsley ella (in all the component species). The reticu late distribution of these characters throughout the genus therefore appears to offer little help in establishing the relationships of sect. Pachyrrhiza. PALYN0L0GY Pollen from two collections of Fuchsia pachyrrhiza was examined with EM and SEM (figs. 3—7). In Stein et at. 4066, pollen from the exserted stamens was processed separately from that of the included stamens, but there were no readily discernable differences in the pollen of the two stamen types. In Stein & Todzia 2047, about 3% of the pollen was 3-aperturate, where as in Stein et at. 4066 3-aperturate grains were very rare in both stamen types. In all three poi 1988] BERRY ET AL.: FUCHSIA 487 FiGs. 3—7. SEM of pollen from Fuchsia pachyrrhiza. 3. Grain on left is slightly oblique, mesocolpus-centered equatorial view; grain on right is a polar view of proximal face with viscin threads. (From exserted stamens of Stein et al. 4066, x 800.) 4. Group of grains held together by viscin threads, arrows mark incipient third apertures on two grains; two other grains at top are 3-aperturate. (From Stein & Todzia 2047, x 500.) 5. Grain third from the top has incipient third aperture (arrow). (From included stamens of Stein et al. 4066, x 500.) 6. Proximal pole showing attachment of smooth viscin threads, note elongate sculpture elements. (From Stein & Todzia 2047, x 7500.) 7. Proximal pole showing attachment of smooth viscin threads, note very elongate sculpture elements. (From included stamens of Stein et al. 4066, x 7500.) 488 [Volume 13 SYSTEMATIC BOTANY refrigerated until study. Meiotic chromosome preparations were made by T. Hoshino of Oka yama University of Science, Japan, using 1% aceto-orcein stain. At meiotic metaphase there were eleven bivalents(n = 11; fig. 8), the normal diploid condition within the genus (Berry 1982). 1 ANATosny * FIG. 8. (n = •%_ Photomicrograph of meiotic metaphase 1111). (From Stein et al. 4066, x300.) len samples, however, some 2-aperturate grains had a distinct protrusion usually located mid way between the two apertures (arrows in figs. 4,5), producing a very asymmetrical grain. With LM these protrusions could be seen to have a definite thickening of endexine, suggesting an incipient third aperture. At 83—96 m long, the pollen is relatively large for the genus. The viscin threads are smooth and the ektexine has elongated sculp ture elements (figs. 6, 7). Smooth threads are unusual in the genus and are thought to be a derived condition (Nowicke et al. 1984; Skvarla et al. 1978); they occur in only nine other species of Fuchsia representing four different sections (sects. Schufia, Encliandra, Jimenezia, and Kier schiegeria). Most of these species have globular sculpture elements in the ektexine, however, and only sects. Kierschlegeria and Encliandra combine the elongated elements with smooth threads as is found in sect. Pachyrrhiza. Fuchsia pachyrrhiza has the most elongate sculpture ele ments (fig. 7) yet seen in the genus (see No wicke et al. 1984). CYTOLoGY Young flower buds of the type collection were fixed in the field in Farmer’s solution (3:1 ab solute ethanol to glacial acetic acid) and kept Fresh tuberous roots, stems with little sec ondary growth, and stems with cylinders of wood to 3 mm in thickness were fixed in for maim-acetic-alcohol. Young stems and tuber ous roots were infiltrated in a tertiary butyl al cohol series, embedded in paraffin, and sectioned on a rotary microtome. Older stems were transferred to water and sectioned on a sliding microtome. Both rotary and sliding mi crotome sections were stained in a safranin-fast green combination. Macerations were prepared by means of Jeffrey’s Fluid and stained in saf ranin. Primary Stem. Two to three layers of col lenchyma are present beneath the epidermis. Internal to the collenchyma are about three lay ers of thin-walled cortical parenchyma. One or two cell layers of fibers surround the secondary phloem, forming a mostly uninterrupted cyl inder. Pith consists of spherical thin-walled parenchyma cells. Idiobiasts containing raph ides are present in the parenchyma near the intraxylary phloem, as well as in the cortical parenchyma. Tuberous Root (figs. 9-13). Tuberous roots lack both fibers and a central pith region (fig. 9). Instead, vessels or vessel groups are sepa rated from each other by starch-bearing paren chyma cells that enlarge greatly during growth of the root, producing patterns in which the parenchyma cell walls tend to radiate away from the vessels or vessel groups (fig. 9). The outside of the tuberous root (fig. 10) bears a thin-walled periderm inside of which are found numerous layers of thin-walled parenchyma. These cells are often tangentially elongate, in accordance with an increase in root circumference, and are subdivided into strands of two to four cells (fig. 10, near top). Idioblastic cells containing raph ides are scattered in the cortex; the irregular gray patches visible in the cortex (fig. 10) result from spreading of the gelatinous sheath that accompanies raphides. Secondary phloem (fig. 10, center; fig. 11, top) consists of occasional Fics. 9—13. Sections of tuber roots of Fuchsia pachyrrhiza. (All from Stein et at. 4066.) 9. Transection of center of root; vessels widely separated by parenchyma cells. 10. Transection of outer portion of tuberous root; secondary xylem and secondary phloem contain mostly parenchyma. 11. Portion of secondary phloem (above) and secondary xylem from root periphery transection. 12. Tangential section from root periphery, showing vessels of secondary xylem. 13. Vessel elements from tangential section of root periphery; lateral wall pitting is scalariform and pseudoscalariform. Magnification scale above figure 9 for figures 9, 10, 12 (divisions = 10 11m). Scale above figure 11 (divisions = 10 Scale above figure 13 (divisions = 10 lLm). Ii 490 sYsThMATIc BOTANY [Volume 13 FiGs. 14—19. Sections of secondary xylem of woody stems of Fuchsia pachyrrhiza. (All from Stein et al. 4066.) 14. Transection, showing divergent pattern of inner and outer portions. 15. Tangential section of outer portion; ray cells simulate fibers in width and length. 16. Vessels, rays, and parenchyma-like septate fibers from tangential section of outer wood. 17. Tangential section of inner portion of wood; rays are all 19881 491 BERRY ET AL.: FUCHSIA sieve tube elements accompanied by compan ion cells. Most of the secondary phloem is phloem ray parenchyma, but parenchyma pre dominates in fascicular regions as well. Simi larly, secondary xylem consists of thin-walled ray parenchyma separating fascicular areas con taining angular, often squarish vessels that are widely separated from each other radially (figs. 10, 11). Axial parenchyma is visible in tangen tial section as strands of two to four cells ad jacent to vessels (fig. 12). Vessel elements pos sess lateral wall pitting that is scalariform or pseudoscalariform; the latter consists of a ba sically alternate pitting pattern in which pits are markedly elongate laterally. Pit borders are narrow, with correspondingly wide apertures (fig. 13). Idioblasts containing raphides are scat tered in the parenchyma of secondary phloem and secondary xylem (figs. 10, 12). Secondary Xylem of Stem (figs. 14-19, table 1). The wood examined tends to have a dis tinctive outer region (fig. 14, top) with denser vessels and wider and thinner-walled libriform fibers (compare figs. 15, 16 with figs. 17, 18). Accordingly, inner and outer wood features are presented separately in table 1. The darker patches of libriform fibers in figure 14 represent gelatinous fibers, probably a manifestation of tension wood. Growth rings are absent or in distinct (fig. 14). Vessels are solitary or grouped, usually in radial multiples, and perforation plates are all simple. Pits are vestured (fig. 19). Lateral wall pitting of the inner wood consists of alternate, oval pits Ca. 5 sm in diameter on vessel-vessel contacts; pitting is opposite to sca lariform with wider apertures on vessel-paren chyma contacts. In outer wood, the lateral wall pitting consists of slightly larger pits with re duced borders and with correspondingly larger apertures. All imperforate tracheary elements are septate libriform fibers, with slitlike pits ca. 2 m long (figs. 16, 18). Axial parenchyma is scanty and vasicentric in strands of four to six cells (visible near vessels, right portion of fig. 16). Rays are exclusively uniseriate, and are composed wholly of erect cells; they therefore TABLE 1. Anatomical measurements of stem xylem (all figures represent means; n.d. no difference). = Inner wood Outer wood Vessels Number/group Diameter 2 Number/mm Element length Wall thickness 1.88 0.41 m 88 332 rm 1—2 m n.d. n.d. 200 nd. 0.5—1.2 m Libriform fibers Diameter Length 20 m 514 m 23 rm n.d. Rays Height 127 rm n.d. resemble septate fibers and axial parenchyma strands in tangential sections (figs. 15—18). Crys tals are absent in secondary xylem, but raphides occur in idioblasts in the secondary phloem. Starch grains are present in moderate quantity in septate fibers, xylem axial parenchyma, and xylem rays. Discussion of Anatomy. Tuberous roots in Onagraceae have been described anatomically for Fuchsia decidua (sect. Ellobium) and Xylonagra arborea (Carlquist 1982), and differ from those examined in F. pachyrrhiza in having pith re gions. The secondary xylem and phloem in the tuberous roots of F. pachyrrhiza is more sparsely scattered in a parenchymatous background than in the above two species. Otherwise, the tubers of F. pachyrrhiza and F. decidua are notably sim ilar. The large cell size and proportionately low starch content of the tuberous roots in F. pachyrrhiza suggest a water storage function for this organ, a conclusion also reached by Carl quist (1982) for F. decidua and Xylonagra arborea. These findings are consistent with the season ally dry habitats in which all three species oc cur. The wood of F. pachyrrhiza agrees qualita tively and quantitatively with other species of 4— uniseriate. 18. Tangential section of inner portion, showing septate fibers and rays composed of upright cells. 19. SEM photomicrograph of vestured pits from vessel wall of tangential section of inner xylem. Magnification scale above figure 9 for figures 9, 14, 15, 17. Scale above figure 11 for figures 11, 16, 18. Scale shown for figure 19. 492 [Volume 13 SYSTEMATIC BOTANY Fuchsia examined by Carlquist (1975, 1977, 1982), except for the development of an outer zone with more numerous vessels per mm 2 in a back ground of wider, thinner-walled fibers. It is not clear why wood patterns shift from the inside to the outside of the stem in F. pachyrrhiza, al though it may be related to climatic changes that occurred during the growth period. The rays of F. pachyrrhiza are distinctive in being exclusively uniseriate with erect cells, a juve nile condition previously reported only in F. splendens (Carlquist 1962, 1975). This may be due to the relatively small diameter of the stem sample of F. pachyrrhiza examined, since rays become wider and the proportion of erect to procumbent cells decreases with prolonged cambial activity (Barghoorn 1941). AcKNowI.eocMENTs. We wish to express our thanks to Peter H. Raven, who helped pursue the study of this new species. Takuji Hoshino kindly furnished the meiotic chromosome count and figure 8, and Abundio Sagástegui A., Jacquelyn Kallunki, and Car ol Todzia provided valuable field assistance in Peru. Collection of this new species was made possible by fieldwork supported under National Science Foun dation doctoral dissertation improvement grant BSR 84-13912 to BAS, and NSF grant BSR 85-18906 to Peter H. Raven. LITERATuRE CITED BARGH00RN, E. S. 1941. The ontogenetic develop ment and phylogenetic specialization of rays in the xylem of dicotyledons. II. Modification of the multiseriate and uniseriate rays. Amer. J. Bot. 28: 273-282. BERRY, P. E. 1982. The systematics and evolution of Fuchsia sect. Fuchsia (Onagraceae). Ann. Missouri Bot. Gard. 69:1—198. CAKLQuIsT, S. 1962. A theory of paedomorphosis in dicotyledonous woods. Phytomorphology 12:3045. 1975. Wood anatomy of Onagraceae, with notes on alternative modes of photosynthate movement in dicotyledon woods. Ann. Missouri Bot. Gard. 62:386-424. 1977. Wood anatomy of Onagraceae: Addi tional species and concepts. Ann. Missouri Bot. Gard. 64:627—637. 1982. Wood anatomy of Onagraceae: Further species; root anatomy; significance of vestured pits and allied structures in dicotyledons. Ann. Missouri Bot. Gard. 69:755—769. N0wICKE, J. W., J. J. SKvARLA, P. H. RAvEN, AND P. E. BERRY. 1984. A palynological study of the genus Fuchsia (Onagraceae). Ann. Missouri Bot. Gard. 71:35—71. SEvARLA, J. J., P. H. RAvEN, W. F. CrnssoE, AND M. SHARP. 1978. An ultrastructural survey of viscin threads in Onagraceae pollen. Pollen et Spores 20:5—143.