Download Fuchsia pachyrrhiza (Onagraceae), a Tuberous

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
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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.)
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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.)
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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
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sYsThMATIc BOTANY
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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.