Phylogenetic Relationships, Seed Characters, and Dispersal System Evolution in Amaryllideae (Amaryllidaceae)

25 Pages·1996·21.2 MB·English

by  D A Snijman

PHYLOGENETIC
and
Snijman^
D, A,
H. Linder^
SEED
RELATIONSHIPS, P.
AND
CHARACTERS,
DISPERSAL SYSTEM
EVOLUTION
IN
AMARYLLIDEAE
(AMARYLLIDACEAE)'
Abstract
The
phylogetiy of the mostly Afriean tril)e Amaryllideae is presented as a l)asis for classification and an enquiry into
the evohitionary interrelationship between seed and fruit characters and seed dispersal modes. The cladistic analysis
is based on morphological, seed anatomical, and cytological data, of which seed and fruit specializations are ilhistrated.
Three dispersal modes, anemochor>; atcleclujr>/rain wash, and autochory, are optimized onto the selected cladogram
and the pattern is considered in terms of functional fruit and seed morphology. The new classification recognizes two
monophyletic subtribes: Crininae [Boophone sensu Crinum, Ammocharis, and and
stricto, Cybistetes) Amar\^llidinae
{Amaryllis, Nerine. Brumiigia, Crossyne, Hessea, Strumaria. and Carpolyza). The phylogeny suggests Amarylli-
that in
dinae the ability of the green, stomatose seeds to mature after they are released favored the development of rapidly
shed, wind-tumbled infructescences in three clades especially in semiarid, southwestern Africa. In Crininae the seeds
are large, cork-covered, endosperm-rich, and relatively slow developing. The limited seed dispersal mode Crinum
in
and Ammocharis a[)pears to be a consecjuence of the derived indehiscent fruit, which is basal in Crininae, and the
anchoring function of their persistent, lax scape.
Amaryllideae, a monophyletic group consisting nomic uses. The charred and crushed bulb scales
of 11 currently reeognizc^d genera and approxi- of Ammocharis coranica (Ker Gawl.) Herb, have
mately 155 species, is one of nine tribes (sensu been used as an adhesive (Phillips, 1917, 1938),
Dahlgrcn et ah, 1985) in the nionueotyledouous and a decoction of the bulbs of Boophone Herb.,
The members
family Amaryllidaceae. are bnl- Brumvigia Crinum, and Nerine Herb, have
all Heist.,
bous herbs with distichous or rarely rosulate leaves provided medicine and poison many African peo-
to
&
and a lateral, solid, naked scape which ternu- pie (Phillips, 1917; Watt Breyer-Brandwijk,
is
nated by an umbel-like cluster of flowers. Their 1962). The use of the highly toxic bulbs of Boo-
seeds are characteristically large and nondormant. phone disticha Herb, for arrow poison by early
(L.f.)
Although remarkably uniform in floral and vegeta- hunter-gatherers has been particularly well docu-
&
much
morphology,
tive diversity exists in the tribe nu^ited (Bradlow, 1994; Forbes, 1986; Forbes
s
fruiting structures, some of which function as spe- Rourke, 1980). Numerous forms and hybrids of
Mem-
wind
cialized units of dispersal in or water. Nerine, Amaryllis L., and Crinum are cultivated for
bers of the tribe inhabit grassland, savanna, and their elegant flowers, and the s[)herical fruiting
tropical forests in sub-Saharan Africa, but are most heads oi Boophone and Brunsiigia are locally gath-
speciose in southern Africa, where habitats include ed for dried floral arrangements.
semiarid, dwarf shrublands in a winttM-rainfall di- Amaryllideae were delimited as monophy-
first
mate. The tribes only pantropical representative letic by Traub (1965, 1970), who recognized the
is
Crinum L., which extends from Africa to Matlagas- presence of threadlike "fibres" in toni-off leaves
Mascarene and and and
car, the Pacific Islands, the bulb scales as diagnostic for the tribe (char-
America, and
tropics of Asia, Australia. acter This feature has since been corroborated
1).
Several Amaiyllideae have traditional and eco- by four non-homoplasious synapomorphies: uniteg-
This study is a modification of part of a Ph.D. thesis presented to the Department of Botany, University of Cape
'
Town, South Africa. The first author thanks S. E. Foster, J. C. Manning, J. C. Palerson-Jones, P. L. Perr)', A. J.
Romanowski. and S. E. Wand for help (hiring this slndy. A. W. Meerow thanked for valuable comments on the
J. is
manuscript.
Compton Herbarium, Bag
^ National Botanical Institute. X7, Claremont 77ii5, South Africa.
P.
"* Bolus Herbarium, University of Caj)e Town, liondebosch 7700, South
Africa.
Ann. Missouri Bot. Card. 83: 362-386. 1996.
Volume Number 3 Snijman & Under 363
83,
1996 Phylogenetic Relationships Amaryllideae
in
Table Major recent classifications of Amarj'llideae.
1.
Crinum, Aninio- Amaryllis,
Hesse
charis, Cyhis- Nerinef a,
Boophone Brunsvigia Carpolyza, Strumaria Crossyne
tetes,
Traub Crininae Crininiae Stru mariniae
(1957)
H
Traub Crineae Crineae esseae
(1962)
Traub Crineae Crineae Strumarieae
(1963)
Traub (1965, 1970) Crineae Crineae Crineae
Dahlgren Amar}'llideae Amaryllideae Amaryllideae
et al. (1985)
&
D. U. Muller-Doblies (1985) Crininae Crininae Strumariinae
&
Snijman Linder Crininae Amar>'llidinae Amaryllidinae Amarj'llidinae
mic ovules (Huber, 1969) and bisulculate pollen wind or water. To analyze the evolution of these
mechanisms, changes seed and
grains (Schulze, 1984) with spinulose exine sculp- dispersal in fruit
(Meerow, which we add green em- characters are traced on the phylogenetic tree to
turing 1995), to
modes may
bryos in nondormant, water-rich seeds (character assess whether the different dispersal
have been by these functionally related
facilitated
33).
Various subtribal classifications of Amar)llideae characters. Lastly, in an attempt to establish evo-
have been proposed (Table most of which reflect lutionary patterns in the ecology of Amaryllideae,
1),
the nomenclatural confusion introduced by Traub's we use the phylogeny to analyze the interrelation-
(1957, 1962, 1963, 1965, 1970) continuous mis- ships between seed and fruit characters, dispersal
application of the name Amaryllis to the unrelated traits, phenology, and phytogeography.
These
genus Hippeastrum Herb. (Biaimmit, 1987).
MATERIALS AND METHODS
systems differ only in the rank attributed to the two
groups recognized Amaryllideae
subtribal in (Cri-
CHARACTER
ANALYSIS
Thus
neae sensu Traub, 1965, 1970). the rela-
far,
Ammocharis
groups have Morphological data on Herb.,
tionships of the genera within these
never been disputed. Brunsvigia, Crinum, and Nerine were obtained from
Kirstenbosch
Amaryllidinae (Pax, 1887) or Crininae (Traub, the literature, living collections at
1957, 1963), the larger of the two subtribes, are National Botanical Garden, and dried material at
characterized by the presence of minute "fibres" NBG. Crinum variabile (Jacq.) Herb, and all spe-
between the broken parts of leaves and bulb scales, cies of Amaryllis, Boophone, Crossyne Salisb., Car-
&
Milne-Redh. Schweick.,
a solid scape, and regular to zygonioii)hic flowers polyza Salisb., Cybisietes
(Traub, 1963). St * • which are defined by Hessea Herb., and Strumaria Jacq. were studied in
no single character but by a combination of char- the field, and the South African summer-rainfall
Crinum and Ammocharis were
comprise small plants with mostly two representatives of
acters,
leaves surrounded by an amplexicaul cataphyll; studied in cultivation.
regular flowers with a reduced perigonc tube; Leaves, flowers, and seeds for anatomical study
fila-
FAA 70%
ments inserted into a sheath formed by the anther were fixed in (90 ml ethanol; 5 ml glacial
connective; and style variously connate to the fila- acetic acid; 5 ml formaldehyde), subsequently de-
embedded
ments (Muller-Doblies, 1985). hydrated in an ethanol-tolucne series, in
10—15
Essentially these interf)retalions were limited to wax. and cut with a rotarv microtome at ixm.
and morphological data and Sections were stained with safranin and alcian
basic vegetative
floral
they were phenetically based; therefore the mono- blue, and photographed with a Zeiss Axioskop.
phyly of the subtribal groups was never explicitly Seeds examined by scanning electron microscopy
questioned. were fixed in FAA, dehydrated in ethanol, and crit-
The primary aim of this study was to use new ical point dried before sputter-coating with Au/Pd.
Cambridge S200
morphological data from the infructescences, cap- Photographs were taken with a
SEM
sules, and seeds of Amaryllideae in a phylogenetic at 10 kV. Documentation for the taxa studied
Appendix The
analysis to establish monophyletic groups of gen- micromorphologically is given in I,
and monophyly micromorphological characters reported here for C,
era, to assess the of the traditionally
recognized subtribes Amaryllidinae and StiTimari- variabile conform to published results of other Af-
inae. Of special interest in Amaryllideae are the rican, Asian, and Australian species of the genus
&
unique and complex seed dispersal mechanisms by (Dutt, 1962, 1970; Howell Prakash, 1990; Merry,
1
364
Annals
the
of
Garden
Missouri Botanical
Table 2. Distribution of character stales among the genera of AniaryUiJeae and subgenera of Hessea and St rumaria.
Indeterminate coded "it?'j""
states are as
* •
Haemantlieae 00000 00000 00000
OOOiM) (KMM)0 O(XMM) (KMM)
Crinum 10100 00100 ?0000 11 KM) 10011 10(MM) 1110
Ammocharis 11100 00100 00000 11000 10011 10000 1110
11100 00100
Cybistetes 0(X)00 11100 12011 10000 1110
Boophone
10000 (K)(K)0 0(K)00 IKKK) 10111 00000 1110
Amaryllis 10000 0(KMM) 11000 IIKK) KKMM)
0<MMM) (M)10
Neririe 10000 OOO(X) 2000 11100 11000 001
M)
1
1 (
1 1
Brunsvigia 11000 01010 12000 11100 00111
2(MM) (M)10
1
Crossyne 11001 01210 ?2000 11100 12000 00111 0010
Hessea suhg. Hessea 10010 (K)Oil 02002 IKXX) 12000 00111 00
1
Namaquanala
Hessea 10010 00011 01101 11000 12000 00
siil)g. (M)10
1 1 I
Hessea subg. Kamiesbergia 10010 00011 0201 12000 0010
? 1 (KM) fM)lll
1
Slrumaria subg. Struinuria 10000 00000 00000 11011 10000 00111 0011
Strumaria subg. Tedingea 100?0 000 00000 11011 11000 00111 001?
1
Strumaria subg. Gemmaria 10010 looyo
(XKX)1 11011 12000 00111 00
1
Carpolyza KMKM) 00010
(KX)Ol 1I(M)I 11000 00111 0011
&
1937; Toilliez-Genoud, 1965; Venkateswarlu tree as a phylogenetie hypothesis. To choose among
New
Lakshmi,
1978). seed data are provided for the set of most parsimonious trees, we use logic
tlie
Boophune, AmnwcharLs,
Brunsvigia, Crossyne, adding homoplasy
lies- that to the potential of a char-
dSt rum
an ana.
sea, which
aeter already highly homoplasious should
is
Of
the 34 morphological characters
identified for not he as significant as adding to the potential ho-
the phylogenetic analysis, 5 have overlap-
slightly moplasy of an otherwise non-homoplasious char-
ping number,
states: leaf pedicel length, anther at- acter. Consequently, we select those topologies from
ta(;hment, staminal tube length, and sc-ape habit
af- the set of most parsimonious trees that minimize
The
seed
ter set. sets of different states recognized
the possible homoplasy of the least homoplasious
in these characters nevertheless proved be
to in-
characters. There are several approaches by which
formative, since the topology was considerably
less
this logic can be implemented. Goloboff (1993) de-
when
resolved they were excluded from the phy-
veloped a method simultaneously downweight-
for
logenetit: analyses. Only one of the four multistate
i„g homoplasious characters and locating parsi-
was
characters treated as unordered. Autapomor-
monious
trees, but this has been criticized by
phies were excluded from the cladistic analyses but
Meacham
burner (199S). proposed method
(1994) a
were mserted
later onto the cladograms. Character
fo^ calculating the character com,,atibilit,es in a
state distribution provided Table
is in 2.
and
data set, weighting those characters that are
We
maximally compatibh^ used
the successive ap-
CLADISTIC ANALYSIS
proximations weighting scheme implemented
in
Hennig86
using the rescaled consistency index: the
Cladistic analyses were carried out using the im-
produ(;t of the character consistency index and the
enumeration Hennig86
plicit (ie*) option of (Farris,
and t'haracler retention index (Farris, 1969; Carpenter,
1988), tree bisection reconncction (TBR)
tlu^
PAUP Maximally homoplasious
branch swapping 1988). characters, they
of (Swofford, 1993), Trees if
were rooted by designating an outgroup (Nixon & o^'cur in only two taxa, would have a consistency
Carpenter, 1993). Anderberg and Tehler '^nde\ (CI) of 0.5, a rescaled consistency index of
(1990)
and
suggested that for taxonomic studies only con- t), a weight of 0. Minimally homoplasious char-
strict
=
-
sensus trees, containing only components retrieved acters, with CI 1 and retention index (RI)
1,
by each of the complete of most parsimonious would have a rescaled consistency index of and
set 1
trees, should be used. This a very consen^ative a weight of 10, In extreme cases Goloboff (1991a,
is
approat'h, as these consensus trees are substantial- l^us questioned the validity of using the rescaled
1>)
ly less informative than the most parsimonious consistency index as a measure deciding which
trees for
on which they are based (Farris, 1983), and they most parsimonious cladogram be preferred.
is to
reveal little about process, as in character state Despite these reservations, successive approxima-
&
change
(West Faith, 1990). Carpenter (1988) tions weighting analysis considered have value
is to
&
therefore argues that one of the most parsimonious when used with caution (Crisp Weston,
1995).
cladograms should b<^ preferred over a consensus Our preferred most parsimonious was com-
tree
Volume Number & Under 365
3 Snijman
83,
1996 Phylogenetic Relationships Amaryllideae
in
e-
pared with the majority rule tree and the strict con- shown to he correct. Before elongation the Iracheids
sensus tree, and decay analysis (Bremer, 1988; are ca. 325 jJim long and at all stages the wall
Donoghue ah, 1992) was conducted provide thickenings are charac^teristically lightly stained hy
et to
When
measures of strength for the phylogenetic hypoth- safranin. artificially stretched the cottony ap-
esis represented by the most parsimonious tree to- pearance of these elements is reliably diagnostic for
pology. To investigate alternative hypotheses of the tribe.
Ama-
monophyly, the additional cost of grouping
2. Outermost bulb scales: fleshy to parchment-
(3)
within the Boophone clade was determined
ryllis
hard and
like 0, brittle 1.
&
MacClade (Maddison Maddison,
using 1987).
Character distributions on cladograms were exam- In the outgroup and most representatives of
CLADOS
ined, and figures were generated using Amaryllideae, the outer tunics fonn brown, softly
(Nixon, 1992). fibrous coverings. Bulbs with extremely thick cov-
To analyze the number of times a particular dis- erings, which become hard and brittle, are found
Ammochar
persal mode evolved and to determine its interre- in is, Cybistetes, Crossyne, and the Bran^-
lationship with seed, and phenology states in vigia species with prostrate leaves. Although the
fruit,
the lineage, the dispersal modes and phenological chemical substances in these thick, dark brown or
slates were plotted on the tenninal taxa of the tan-colored tunics are unknown, these secondarily
coded
cladogram and the most parsimonious interpreta- thickened bulb tunics are as a single state.
tion of the character states at each inner node was
—
3. (10) Leaf habit: annual 0, lasting longer than
obtained using Farris optimization (Farris, 1970;
a year
1.
Mickevich, The coded seed
1982). states for dis-
A
persal are taken from Van der (1982): anemo- strictly annual growth pattern, in which just
Pijl
chory (wind dispersal), which is divided into ane- one set of foliage leaves is produced and shed each
members
mogeochory (tumbling) and anemoballists (wind year, found in most of Amaryllideae
is
may
and and Crinum species
atelcchory (limited dispersal); the outgroup. In contrast,
ballists);
autochory (dispersal by the plant which either be evergreen as in Ammocharis and Cy-
itself), is or,
may
used here in the passive sense. For the analysis of bistetes, they have mature foliage leaves that
were coded back during seasonal drought then regrow
plant phenology, the foliage leaves as die at
As
end dormant
synanthous (the leafing period coincides with the the of the period. Troll (1954)
flowering period) or hysteranthous (the leafing pe- showed in Ammocharis coranica (Ker Gawl.) Herb.,
riod separated from the flowering period). regrowth of the mature leaves is due to a well-de-
is
All known seed and fruit characteristics were in- veloped intercalary meristem, which results in the
eluded in the data matrix for phylogeny construe- truncate leaf apices that characterize most species
mode
lion, but for the analysis of dispersal only the in these genera. This growth pattern is particularly
abscission of the infructescence (character 22) was remarkable in plants of Cybistetes longifolia from
used. Following Deleporte (1993), the primary cod- the arid Richtersveld, southwestern Africa, in
ing of such a i-haracter may not necessarily intro- which the leaf blades elongate and die back up to
duce circularity into our interpretation of dispersal three times during a single year in response to al-
&
system evolution. temating wet and i\ry sequences (Snijman Wil-
liamson, 1994).
CHARACTER CODING —
4. Leaf number: at least four 0, two 1.
(3)
The weightings determined by the successive ap- A reduced number of foliage leaves found in
is
proximations character weighting routine are given species of Hessea and Strumaria subg. Gem-
all
parentheses and autapomorphies are marked
in maria. Most individuals these taxa have two
in
an
with asterisk. have been
leaves per year, but, rarely, three leaves
recorded (Snijman, 1994). Four or usually more fo-
Bulb without extensible elements
1. (10) scales:
Amanlli-
^ liaee leaves per shoot occur in all other
when = . numerous . •! 1 ° ^
pulled wit,h extensible /
0,
, , ^ ,,
deae and i. n most genera of Haemanlh, eae and t,he
—
when
elements pulled
1.
family.
Although Traub (1965, 1970) stated that "fibres"
=
unmarked
pigmentation: speckled
Leaf
5. 0,
"^
appear when the bulb scales and leaves of Amar-
with red abaxially
1.
an unpublished
yllideae are torn apart, report
(P.
Goldblatt, pers. comm.) that these highly extensible Only in Crossyne are the leaves abaxially speck-
elements are long, spirally thickened tracheids is led with red, an autapomoq^hy for the genus.
366
Annals
of the
Garden
Missouri Botanical
=
pubescent Stamen
6. "^Leaf surface: glal)rous 11. position: spreading declinate
0, (at (2) 0,
-
least in juveniles)
1. 1.
Leaves with soft, simple, uniseriate hairs (0.2-
Declinate stamens, absent from the outgroup, are
6.0 nun lung) are uni(jue Strumaria suhg. Gem-
to consistently found in Amaryllis, Nerine, and Bruns-
maria. Pubesc(»nce diminishes in souk^ species of Both Crinum and
vigia. states o("cur in Crossyne,
group
this maturity {Strumaria Bohkeveldia)
at sect. which
are treated as indeterminate.
but is always present in juv<Miiles, This specializa-
=
tion treated as an autapomurphy. 12. (4) Staminal tube: absent 0, rudimentary
is
conspicuous
2.
1,
=
Leaf margin: unthickened
7. (10) 0, ht^avily
Stamens Amaryllideae
thick enec in either separate
1.
1
{Ammocharis, Boophone, Crinum, and
Cyhistetes) or
The h^f
margins of Brunsvigia and Crossyne are
The
proximally connate varying degrees. con-
to
raised with
thic^k-walled cells, oft<Mi giving the
nation in Amaryllis, coded as ru(Hmentary, ex-
iss
leaves a slightly crisped, reddened outline.
mm)
tremely short and extends above
(ca. 1 the
=
8. (10) Leaf margin: untoolhed 0, with thin- eonfluence of only the outer tepal whorl before b<^-
=
walled branching teeth with thick-walled coming free. In Nerine, Brunsvigia, Crossyne, and
1,
bratiching bristles 2. Hessea, the staminal tube extends shortly to well
abov(^ the confluence of l>oth inner and outer tepal
Multiseriate, branching, cartilagenous cuia
are
cili
If
whorls, and thus coded as conspicuous. Renre-
is
r /A &o
A' r>
present on margins Lrinum
leal of (AiToyo Cut- „
„
r,
. may
II sentatives ol Hessea subi g. Hessea h, ave t,he l, on-
l^o/1^
i^
1 1984), A\mmocha1ris', and1 / . . and
ler, Cyhistetes, lh<*se 7
mm
- i i . ., ^
gest staminal tubes in the tribe, up to 4 long.
are thin-walled in comparison to the long, bristly
1- A in contrast to those ot Hessea sub^. Namaquanula,
cilia on the }lealc margi'ns V C/^rossyne. rTrh, i.s mult, i.- i-ii i_-i -i
ol
.
in which the tube is almost abi sent, })utatively a
state character treated as unordered.
is
secondaiy
reduction (Snijman,
1994).
9. (4) Pedicel length at anthesis: equaling or less The interpretation of the stamens in Strumaria
=
than perigone length 0, at least twice the subg. Strumaria more complex. Although sepa-
is
=
perigone length
1. rate in hidentata Schinz, the stamens in th e re-
.S.
maining
four taxa are connate. Serial sections in S,
Two
variables determine inflorescence form
at
'"""«'«' liovvever, indicate that the outer stamens
A
anthesis: pedirol length and flower clus-
size.
^""^ P'oximally adnate to the style (Siiijinan. 1994).
tered inflorescence in which pe.Hcel length less
is
^trumana
staminal eonnalu.n
'T''"" suhg.
than perigone length predominates Amaryl- ^'^^^ .11
tlie in
'5'"""«"« autapomorphic and
regard(>d as
treat-
'^
lidaceae, but widely spreading
inflorescences, with
I'xlependendy from staminal other
'^^ th.- tul.e in
pedicels at least twice as long as the perig<.ne, are
Amaryllideae.
^^'"^'"^ "*"
characteristic of Brunsvigia, Crossyne, Hessea, and
Strumaria The
subg. Tedingea. states slightly over-
13. *Filament triclwmes: trichomes absent
0,
lap in Nerine and Carpolyza, but when partitioned
trichomes present
1.
according to the method of Almeida and Bisl
^y
Tlu^ filaments are smooth Amar) and
(1984), the data for tliese taxa couhl be reliably in all llideae
lIa<Mnantbeae, except Hessea subg. Namaquanula,
scored (Snijman,
1992).
whi're they are proximally covennl with
short
tri-
^
10. (10) Floiver color during senescence: piemen- innA\
^ /a
^ / D^''^*' cihomes on ,tihe adiaxi•ali surface (Snijman, 1994).
*
=
—
tation accentuated pigmentation
lost
0, 1.
14. ^Filanwnt morphology: whorls uniform
botli
Verdoorn drew
(1973) attention color
first to
and
outer inner whorls dimorphic
0,
1.
when
changt^s in llowers of Amaryllideae she
tht;
noted tliat floral pigmentation in most southern Af- Unknown elsewhere in Amarj^llidaceae are the
Crinum
rican species is accentuated with age, specialized, dimorphic filaments of Hessea stenosi-
&
whereas
in a few species it is lost. Enhanc<Hl col- phon (Snijman) D. U. Mull.-Doblies. The short
common
oring is in tlie senescent flowers of all gen- outer filaments occlude the perigone throat, where-
a of Amaryllideae and Haemantlu^ae, except in as the inner filaments of this species are erect and
where
Hessea, pigmentation
is consistently lost in club-shaped, with a structural composition highly
all species. Crossyne, whose two species have con- representative of osmophores as described by Vogel
Irasting states, was tn^ated as indeterminate, and (1990). The epidermal cells are densely eytoplas-
Crinum was
s(n)red as plesiomorphic until addi- mie and the inner parenc^liyma contains strikingly
tional data clarify the interpretation :^onspicuous masses of starch (Snijman, 1994). Fra-
Volume Number 3 Snijman & Under 367
83,
1996
Phylogenetic Relationships Amaryllideae
in
grance emission from these structures to be Crossyne, and Cybistctes the stamens remain evenly
is still
sprea
tested. d.
± =
15. (4) Anther attachment: dorsifixed =^ 0, in a 19. (10) Style form: slender 0, proximally en-
short connective sheath (subcenlrifixed) larged
1, 1.
a long connective sheath
in (centrifixed) 2.
With
the exception of Strumaria, the style in
Previously described as "basifixed" (Baker, Amaryllideae and the outgroup typically slender.
is
1888, 1896; Dyer, 1976; Phillips, 1951; Traub, Goldblatt (1976) recognized proximally en-
first tlie
1963), the anthers of Hessea and Carpolyza were larged style in Strumaria as a derived, unique char-
recently redefined in terms of the degree to which acter. The slylar swellings are variable but take
the filament tip is inserted into a tube formed by three basic forms: increasingly thickened upward
The nanowed
the anther coimective. relative lengths of the then abruptly above {Strumaria subg.
dorsal and ventral walls of the tubular connective Tedingea); more or less equally thickened in the
enabled D. and U. Mtiller-Doblies (1985) to rcc- lower half (subg. Strumaria)-, or distinctly broadest
ognize three states of anther attachment: dorsifixed at the base and gradually tapering upward (subg.
anthers (relative lengths less than 50%), subcen- Gemmaria) (Snijman, 1994).
50—75%), and
anthers lengths cen-
trifixed (relative
20. (10) Nectar collection site: pooled around the style
more
trifixed anthers (relative lengths than 75%).
=
=
base 0, in three discrete sites in the axils he-
Despite apparent
their arbitraiy subdivision, cur-
tween the inner filaments and style 1.
rent data indicate that the states only sllghlly
overlapping. Anthers are dorsifixed in the outgroup Nectar collects in a central well around the base
and in most genera of Amaiyllideae; subcentrifixed of the style in the outgroup and in most genera of
Namaquanula,
in Hessea subg. Strumaria subg. Amaryllideae. This contrasts with Carpolyza and
Gemmaria, and Carpolyza; and centrifixed in lies- Strumaria, where nectar collects in three discrete
The
sea subg. Hessea. interpretation of the anther sites, in the axils Ix^tween the inner filaments and
attachment in Hessea subg. Kamiesbergia not yet the style base. These separate nectar collection
is
resolved (Muller-Doblies, 1992; Snijman, 1994). To sites vary in depth and diameter. In most species
reflect the hypothesized morphocline in anther at- {Carpolyza, Strumaria subg. Tedingea and subg.
tachmcnt, the character states are treated as ad(h- Gemmaria)^ the site shallow, hohhng nectar in a
is
Through and
tive single large droplet. lengthwise radial
extension of the confluence formed by the outer
= fil-
16. (10) Pollen morphology monosulcate bis-
0,
:
ament whorl and Strumaria Strumar-
style in subg.
ulculate
1.
the volume of the cavities between the inner
ia,
Relative to the large, boat-shaped-elliptic, mon- filaments and style has been increased, and deep
osulcate pollen grains in other genera of Amaryl- nectar wells have developed. Preliminary studies
lidaceae (Meerow, 1995), pollen grains of Amaryl- have shown that within Strumaria, nectar\^ anatomy
lideae are consistently bisulculate and normally quite diverse. Without exreption the nectaries
is
dispersed at the two-celled stage (Dutt, 1962; Erdt- are septal, but considerable variation found in
is
&
man, 1966; Howell Prakash, 1990; Sehulze, the position of the nectaries relative to the locules.
1984). in their size, and their degree of convolution. Al-
though the extent of septal nectary diversity in
=
17. (10) Pollen exine: reticulate 0, spinulose 1.
Amaryllideae does not approach that reported in
Unlike reticulate exine elsewhere in Amarylli- llaemodoraceae (Simpson, 1993), a detailed study
daceae, surface ornamentation of pollen is uniform of floral anatomy may give further insight into the
gemmate
in Amaryllideae; with scattered large spi- tribe's functional flond morphology.
nulae (Meerow,
1995).
=
21. Ovule: bitegmic unitegmic
(10) 0, 1.
symmetrically placed
18. Style position:
(1) 0,
In contrast the bitegmic ovules of most Amar-
to
displaced
laterally
1.
yllidaceae, the ovules in Amaryllideae are unileg-
The
style is uniformly symmetrically placed in mic. Representatives reporttnl to have a solitaiy in-
the outgroup, Boophone, Ammocharis, Hessea, Stru- tegument are Amaryllis (Markotter, 1936;
maria, and Carpolyza, All remaining Amaryllideae Oganezova, 1990; Schlimbacli, Boophone
1924);
have a laterally displaced style. Lateral displace- disticha (Schlimbach, 1924); Brunsvigia minor
ment of the style usually associated with decli- Lindl. and several Crinum species (Hofmeister,
is
nate stamens but in certain species of Crinum, 186\); Cybistetes {Markoncr, 19^6); an(] Nerine sar-
368 Annals the
of
Garden
Missouri Botanical
nicnsis (L.) Ih'rh. capsul<»s in one representative, as well as at a level
if<
(
Amaryllidaceae, fonnod
1932). immt^dialt^ly l)asal to the
Furthermore, several speeies of Criniim liave basis for selecting capsule deliiscenee as {}w
th<*
been described as having ateguiic ovules (Toilliez- outgroup character state. This coding parallels
C<'noud, 196S; Tomita, However, the defin- Dahlgren and Rasrnussi^n's (1983) hypothesis that
lO.'U).
from eap-
enibr)'ological studies of Dult (1957a, b, 1959, baccate fruits are secondarily (h^rivtvl
ilive
1962) and Vt^nkaleswarlu and Laksluni (1978), on sules In Amaryllidaceae.
Crmum
a ranfre of species, present strong evidence ^r /mw n n =
r
iJ^veilopi• n^ Jniil: never rost. tMJat. e 0, ros-
^''- (''')
/
„
. , . 1 r - 1
for the (^xisl<;nce of an integumt*nt before its loss
tellate 1.
transformation of the ovule into the seed.
durinij; lh<^
The present study also (H>nhnns the presence of Ammovharis, Boophone, Crinum, and Cyhistrtes
unitegmic ovul(\s in Brunsvigia and Nerine (sen; Ap- have fruits which, while developing, are beak(Ml
The
pendix and reports th(Mr pn^senee in Crossyne, with (he persistent base of the jx^igone tube.
1)
Ilessea, and Strumarla, This current data giv<^ fur- beak [xTsists on the mature fiuits only in Crinum,
iher support to Huber's (1969) hypotlu^sis that uni- and its final length has proved to be diagnoslically
&
valuable many species (Nordal Wahlstr0m,
legmic ovules are synaponior[)hic for the tribe. in
None memluas
1980; Verdoorn, 1973). of the otluT
22. Snipe habit during seal dispersal: withering
(1)
beaked
of Amaryllideae or the outgroup has fruits.
back seed detaching
after releaj 0, at
Mature
ground h^vel after seed rtdease from the cap- 26. (10) fruit: regular 0, irrcirular
=
=
ground 27. Mature not large conspicu-
sules d<'taching h^vt^l lu^fore 1. fruit: 0,
1, at
"^
=
seed r<d(*ase from the capsule 2. 23. *//a/;;7 ously enlarged 1.
of fruiting eliusler during seed dispersal: re-
more symmetrical
Th<^ form of or less
th(* fruit is
maining attached o scape detaching from
0,
I
Amaryllideae Amniocharis, Crinum,
in exc<'pt in
scape
1.
and where mold(Ml by the enelostul
CyhisteteSy is
it
At maturity the scapi^ in Amarjllideae varies in devt^loping seeds. As the shape of the seeds is often
&
duration and place of abscission. The scape per- extremely variable (Manasse, 1990; Snijman
its
sists above ground until long after seed release, Williamson, 1994; Toilli(^z-Genoud, 1965), the fruit
then slowly widiers away the outgroup, Amaryl- also assumes an irn^gular form. Conspicuously
in
Ammoeharis, Boophone, Crinum, and Strumaria larg(% obconical to randy spindh-shaped capsules
lis,
mm
subg. Strumaria. Elsewhen^ in the tribe, the scape (reaching up to 60 nun long and 25 across in
many
detaches from the bulb ground level soon after species), with visible transverse v<Mning, are
at
seed release (Carpolyza, Nerine, and Strumaria auta[)omor()liic for Brunsvigia.
from
subg. Tedingea) or befon* the release of see<l
=
28. (10) Testa: without stomata 0, stomatosc 1.
the ca[)sules {Cyhistetes, Brunsvigia, Crossyne, Hes-
common
Thus outgroup Hae^man-
sea, and Strumaria subg. Gi'mnuiria). through AIllu>ugh not in the
phylnmclan, occur
early abscission of the scape in the latter laxa, tht^ae, ihy seeds, cruste<l with in
fiv»^
the entin^ infructcscence becomes the main unit of one representative, Cyrtanthus; widely in oth(*r
dispersal. Dispersal similar Boophone, but die Amaiyllidaceae; and consistently in Aliiaccae, the
is in
structural unit uniquely derived by the abscis- family basal to Amaryllidaceae (Fay cl al., 1994).
is
AmarjUideae
sion of entire fruiting cluster from the top of In contrast, the mature seeds of are
th<"
the scape. Multistate character 22 treated as or- water-rich and lack phytomelan in the coat. Schlim-
is
dered, and until abscission tissues of the scape bach (1924) was the first to report stomata on tin;
tlie
and
are studied anatomically, the stales are considered setnl coat oi Nerine sarniensis (= A^. eurvifoUa),
Boyd them Carpolyza
be homologous. (1932) later rec^orded in spir-
to
A
alis (LTlerit.) Salisb. survey of the testa in this
=
24. (10) Fruit: dehiscent 0, indehisc(^nt 1.
shown on
study has that stomata an; also present
In the outgroup indchisccnt fruits occur in four le se Is of additional repres(^ntatives of Nerine, in
tl
and Strumaria (Ap-
capsule found only Brunsvigia, Crossyne,
genera, wluM'eas a dehisct^nt Ilessea,
is
Cyrtanthus Dehisct^nt capsules also occur pendix The stomata are anomocylic (Fig. 5B-E),
in L.f. 1).
&
uniformly closely similar Hippeastreae^ and as typical for Amai7llidacca(^ (Arroyo Cutler,
in tlu* is
&
Lycorideae (Dahlgren et 1985) and in Alli- 1984; Dahlgnui Clifford, 1982), and die sur-
al.,
ac(^ae, which nu)lecular data identified as basal to rounding (*ells are covered by a sculptured cuticle
Amaryllidaceae (Fay 1994). Although not (Fig. 5D, E), in which the central slriations become^
al.,
(;t
common and sinuous
the outgroup, the existence of dehiscent increasingly thick witli age.
in
Volume Number &
3 Snijman 369
83, Linder
1996
Phylogenetic Relationships Amaryllideae
in
29. (10) Integument in developing seed: disinte- Chromosome numbers in Amaryllideae are well
&
grating largin 30. Integw known (Goldblatt, 1972; Gouws, 1949; Nordal
0, g 1. (10)
=
and
merit in developing mature seed: without Wahlstr0ni, 1980) and a karyotype of x 11
is
=
chlorophyll 0, chlorophyllous 1. considered basic in Amarjllideae (Goldblatt, 1976)
and
the family (Inariyama, 1937; Meerow, 1984;
In Brunsvigia, Crossyne, Nerine, Hessea, Stru-
Sato, 1938). Species of Carpolyza and Strumaria
maria, and Carpolyza Integument expands
the into
=
have a reduced base number x 10
of (Goldblatt,
a water-rich, chlorophyllous tissue with vascular
1976; Snijman, 1994), the only exception being
S.
As {=
strands. reported in N. saniiensis N. curvi-
=
pygmaea
Snijman, which has x Although
11.
folia) this achieved by increasing the number
is
=
most taxa in Haemantheae have x 9 and 8 (In-
and
the size of the cells after fertilization (Schlim-
&
ariyama, 1937; Ising, 1970; Vosa Marchi, 1980)
bach, and when integument
1924), finally ripe, the
some species of Clivia have the base number of x
amounts and
contains rich of starch chlorophyll
=
11 (Gouws,
1949).
4B-D).
(Goebel, 1932) (Fig. In the otlicr represen-
tatives of Amaryllideae the integument remains un-
OUTGROUP
SELECTION
and
differentiated finally disintegrates (Dutt, 1970;
&
Venkateswarlu Lakshmi, whereas
1978), in th Traub's (1962, 1963) tribal classification of
outgroup, the integuments of seeds shed in a dry, Amaryllidaceae provides a valuable framework for
dormant stale are crushed maturity. selecting an outgroup has synapomorphies
at that
&
shared with the ingroup (see Nixon Carpenter,
Endosperm mature
31. (10) in seed: undifferentiat-
1993). Traub's system divides the currently recog-
—
ed extemally fonned
0, into cork externally
= nized tribes (Dahlgren et al., 1985) into two infra-
Mature
32. seed: without chlorophyll
1. (10)
family groups, the Amarylloidinae and the Pancra-
=
endosperm endosperm
in with chlorophyll
0,
tioidinae. Within the Amarylloidinae, the apparent
=
1.
between Amar-
close similarity representatives of
A
novel feature in Ammocharis, Boophone, Cri- yllideae and Hippeastreae (Brummit, 1987)
is
num, and
Cybistetes the development of a few based essentially on highly homoplasious
is floral
layers of cork tissue from the peripheral cells of the characters, but the pollen, and seed charac-
fruit,
endosperm (Fig. 4E, F). Although well known in ters are discontinuous (see Meerow, 1995). Other
Crinum
(Merry, 1937; Schlimbach, 1924; Venka- differences between the two tribes are root and
&
teswarlu Lakshmi, 1978) and Cybistetes {= Am- scape structure, and spathe valve arrangement, and
mocharis falcata sensu Markotter, 1936), a cork- in these ch ters Haemantheae intermediate
is
&
covered endosperm is reported here in two (Arroyo Cutler, 1984). The close relationship
additional genera: Boophone and Ammocharis postulated between Haemantheae and
(Fig. to exist
Another
5F, H). novel feature in these genera Amaryllideae, for which equitant spathe valves (Ar-
is
that chloroplasts occur in the peripheral cell layers royo, 1984) a possible synapomorphy, thus ac-
is
beneath the phellogen, even wlien the seed is cov- counts for our choice of Haemantheae as outgroup
ered by the pericarp (Dutt, 1957a, 1962; Schlim- to root the cladogram. All the characters defined
bach, 1924). Amaryllis is the only laxon of Amar- for the analysis of the Amaryllideae apply also to
yllideae in which the extensively developed the outgroup Haemantheae.
endosperm
does not have corky or chlorophyllous
outer layers (Schlimbach, 1924) (Fig. 4A). In all DELIMITATION OF GENERA IN AMARYLLIDEAE
other Amaryllideae the endosperm remains undif-
All the currently recognized genera of Amaryl-
and
ferentiated comparatively poorly developed.
lideae were examined to ensure that their delimi-
=
33. (10) Embryo: without green pigment green tation could reasonably be considered monophylet-
0,
=
1. This accomplished by identifying hypothetical
ic. is
synapomorphies of the ingroups relative to other
Dahlgren and Clifford (1982) suggested that the
&
taxa (Nixon Carpt^nter, 1993). Amaryllis, Carpo-
embryo of Crinum could be chlorophyllous. Since
^
lyzay and Cybistetes were accepted as monophyletic
then Howell and Prakash (1990) recorded this fea-
by virtue of their being monotypic.
Crinum
ture in Jlaccidum Herbert, while our study
Boophone commonly
sensu lato (five species) has
confirms the presence of green-pigmented embryos
been distinguished from other genera of Amarylli-
in every genus in Amaryllideae. The chh)rophyll
deae by large bulbs, inflorescences of more than
content, however, is yet to be investigated.
100
flowers, a perigone with tube shorter than the
34. (10) Basic chromosome number: 11 0, 10 1. tepals, long pedicels in fruit, and triquetrous dry
370 Annals
the
of
Garden
Missouri Botanical
fruits with solitaiy or few seeds per locule (Dyer, bell-shaped, with spreading or declinate stamens;
1976; Nordal, 1982). Milne-Redhead and the leaves, which sometimes form a false-stem, are
Sehweickerdt (1939) questioned the inclusion chaimeled or ribbed, thin-textured or fleshy, with
first
The
of species with both dehiscent and indehiscent intact or truncate tips (Nordal, 1977). truncate
fruits in Boophone and recommended that the gc- leaf apices, which also occur in Ammocharis and
neric limits be rc(»xaniined. In agreement with Cyhisletes^ result from a well-d(weloped and puta-
Muller-Doblies three groupings have been tivcly derived intercalar) meristem (Troll, 1954),
(1994),
back and regrow
proposed for the five species. whicii enables tlie leaves to <lie
Boophone disticha and Boophone hneman- over several seasons. Evident synapomoq^hies do
(1)
beaked Crinum from Ammocharis;
thoides M. Leight. share indehiscent, not exist to separate
F.
fruits, which are also found in Crinum, Amniochdr- therefore, Crinum is probably paraphyletic with
embedded How-
Ammocharis and
and However, the species are ujiique- Cybisictes in
Cybistetes,
it.
is,
and
ly characterized by the abscission of the fniiting ever, for the analysis /lmmor/rari.s Cy/>/.s/eff.s are
by Snijman and
head from the of the scape. ConsenjutMitly, this provisionally retained, as suggested
to()
species pair, whicli includes the type species of Williamson (1994), and following the reconunen-
Verdoom
Boophone, considered be monophyletic. dalions of Nordal (1977) and (1973) ex-
to
is (2)
Crinum
Boophone guttata Herb, dud Boophone Jiava W. isting subgeneric divisions of are avoided
(L.)
Barker ex Snijman have leaves abaxially speck- because they are so weakly supported.
F.
led with red, and fringed with long, rigid, branching Nerine, with ca. 23 species, is possibly the sec-
hairs. These tw^o unique features are taken as evi- ond llaarrigreesstt genus of Amaryllideae. Geiu^ra of
1
dence of the monopbyly of the species pair, and Aniai7llideae are distinguished by subtle floral
are assigned the genus Crossyne, which was characters, and the extremely similar floral mor-
th(*y to
recently resurrected by D. and U. Miillcr-Doblies phology shared by species of Nerine provides good
monopbyly
Boophone pulchra W. Barker shares evidence the proposed of the genus,
(1994). for
(3) F.
The more
none of the putative synapomorphies recognized for characteristic attenuate, or less crisped,
synapo-
the ru^wly defined Boophone and Crossyne. Possible tepal outlin<* of Nerine species is a likely
derived characters in Boophone pulchra, relative to mor|)hy for the genus.
the tribe as a whole, include the presence of ma- Brunsiigia (19 species) is uniquely macropai)il-
many
cropapillae on the adaxial leaf epidermis and en- late on the adaxial leaf epidermis in species
&
larged. usually triciuctrous capsules, features that (Arroyo Cutler, 1984), and large, inflated cap-
mm
occur in species of Brunsrigia. For the phyloge- sules (sometimes up to 70 long) with visible
netic analysis of Amai7llideae, Boophone pulchra transversal veins occur in all the species. Both fea-
therefore, treated as belonging to Brunsvigia in lures provide good evidence for the inclusion of
is,
accordance with D. and U. Muller-Doblies (1994). Boophone pulchra in Brunsrigia. Although not in-
somewhat
The only feature in which Brunsrigia pulchra (W. flated, similarly shaped, triquetrous or
&
Barker) D. U. MuU.-Doblies differs from other elongat<Ml diy fruits also exist in Boophone sensu
F.
mode
Brunsvigia species the elongation of the pedicels stricto and Cybistetes. Tlie difft^n^nt of dehis-
is
opposed
after anthesis rather than prior to anlhesis. Al- cence in the latter genera (indehiscent as
however,
though typical oi Boophone sensu stricto, this char- to dehiscent: character 24) suggests, that
acter state occurs in several other nuMiibers of die tlie fruits have been separaltdy derived. The en-
tribe {Amaryllis and Cybistetes) and cannot be rec- larged capsule is regarded here as evidence for the
ognized a> autapomor[)hii- [ox Boophone sensu stric- monopbyly of Brunsvigicu
Ilessea (13 species) and Strumaria (23 species),
to.
commonly
Crinum cun'cntly regarded as the largest genus distinguished by their consistently acti-
is
&
in the tribe with ca. 65 species (Fangan Nordal. nomorphic flowers, are the only genera of Amar>'l-
1993). Species concepts of these ornamental plants lideae currently classified to reflect explicitly es-
&
hav(» traditionally bt;en too narrow (Fangan Nor- tal)lishcd phylogenetic relationships. Hessea, with
dal, 1993; Hannibal, 1985), and thus far rcvisional three subgenera, is defined by one unique syna-
pomorphy: pigmentation
work for the African floras has resulted in a re- the total loss of floral at
duced number of taxa being upheld (Nordal, 1977), senescence (Snijman, 1994). The synapomorphy for
&
The genus cytologically variable (Nordal Strumaria, also with three subgenera, is the
is
Wahlstr0m, 1980), but vegetative and floral diver- uniquely swollen or winged style base (Snijman,
maximum
Amar-
sity is comparable to that of other genera of 1994). In order to provide structure for
mono-
yllideae (Brunsvigia, Hessea, and Strumaria). Flow- the phylogeny of Amarj'llidcae, the reliably
ers vary from hypocrateriform to funnel-shaped or phyletic subgenera of Hessea and Strumaria were
Volume Number Snijman & Under 371
3
83,
Amaryllideae
1996 Phylogenetic Relationships
in
Haemantheae
18 23
Boophone
2425 3132
Crinum
Ammocharis
1
2 22
HHh
1617182133 Cybistetes
1
2
1
1 1 1 1 I 1
Amaryllis
Nerine
Brunsvigia
Crossyne
Hessea subgen Hessea
-0+
Namaquanula
Hessea subgen
1 1
14
Hessea subgen Kamiesbergia
1110
10
2
4 1922
6
Gemmaria
iHhHhf" Strumaria subgen
1112
1012202234
4
Carpolyza
-IHHhH-H
111
9 22
ninr Strumaria subgen Strumaria
1519
Strumaria subgen Tedingea
Figure Strict consensus tree of Amar}llideae. Solid bars Indicate non-homoplasious synapomorphies; gray bars
1.
indicate parallelisms and open bars indicate reversals.
we
also Included in the analyses. All taxa included in that have chosen for interpreting character evo-
the phylogenetic analyses are listed in Table 2. lution (Fig. 2) differs from the strict consensus tree
The Crinum-Ammocharis-
(Fig. as follows.
1) (1)
Results
more
Cybistetes clade fully resolved. Bruris-
is (2)
and Strumaria
Crossyne, Hessea, Carpolyza,
'''Si^'
The analyses with equal character
cladistic
minimal
a clade that resolved in 14 of the 16
fo^m
weighting (excluding autaponiorphies) gave 16 niln-
^ clade of Hessea suhge which
^^^^^-
imal length cladograms of 54 steps, a consistency ^^"S^^^ (3) ,
^^« retrieved in 10 of the 16 minimal length trees,
index (CI) of 0.68, and a retention Index (RI) of
present. The subgenera of Siramana are pres-
is
The consensus generated (4)
0.80. tree (Fig.
strict
1)
component more
Support
PAUP i" ^ ^lade. for this
by and Hennig86 shows that all 16 clado- ^'^^ is
Gemmaria
complex. Strumaria subg. basal
is to
grams agree In the following respects. Boophone,
(1)
Carpolyza and Strumaria subg. Tedingea and sub-
Crinum, Ammocharis, and Cybistetes appear as a
genus Strumaria in 10 of the minimal length trees,
monophyletic group. Amaryllis resolves as basal
(2)
but component supported only by the hom-
this is
to Nerine, Brunsvigia, Crossyne, Hessea, Carpolyza,
RI
and Strumaria. Brunsvigia and Crossyne resolve oplasious character 22(1) (CI 0.28, 0.54). In
(3)
and contrast, Carpolyza resolves as basal to the clade
in a monophyletic clade. Hessea, Carpolyza,
(4)
Strumaria form monophyletic group. of Strumaria subgenera In 6 of the trees retrieved.
a
Successive weighting retrieved 2 of the 16 most However, character 19 (style proximally enlarged,
parsimonious trees. These differ only in the degree CI 1.00 and RI 1.00), which supports the Strumaria
shown The unique Amaryllidaceae (Snijman,
of resolution In the Hessea clade. tree clade, is in