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Studies in A n n o n a c e a e X X X I I I . A revision o f Fusaea
(Baill.) Saff. 1
LARS W. CHATROU 2 AND PING H E 3
Chatrou, L. W. & P. He (Herbarium Division, Department of Plant Ecology and
Evolutionary Biology, Utrecht University, Heidelberglaan 2, 3584 CS Utrecht,
The Netherlands). A revision of Fusaea (Baill.) Saff. Brittonia 51: 181-203.
1999.--The neotropical genus Fusaea is revised on the basis of almost 400 herbarium collections. The number of species is reduced to two, as F. decurrens R.
E. Fr. is put into synonymy under F. longifolia (Aubl.) Saff. Three striking, newly
observed characters are reported. An unknown type of coherence of styles is
described. Wood anatomically, small rhombic crystals in the ray cells of the wood
provide a novelty for Annonaceae. The axes of the rhipidiate inflorescence are,
unlike other Annonaceae, not oriented in one plane by addorsement of the prophyll, but the angle of displacement is only 80-90 ~
Key words:
Annonaceae, Fusaea, revision.
Introduction and History
The genus Fusaea was founded by Safford in 1914. The type species F. longifolia
(Aubl.) Saff. was originally described by
Aublet (1775) as A n n o n a longifolia. Baillon
(1868a) placed this species in the genus Duguetia, separating it from the rest of the genus under the sectional name Fusaea. The
imbricate petals and sepals and the inflorescence structure strongly reminded Baillon of Duguetia. However, the fruit is not
c o m p o s e d of distinctly separate carpels, as
in Duguetia. Moreover, unknown for Duguetia are the outer stamens which are
modified into "lamelles p6talo~des, imbriqu6es, l o n g u e m e n t o b o v 6 e s " (Baillon,
1868a), i.e., staminodia. In the same year,
Baillon placed this species in Aberemoa
sect. F u s a e a as A. longifolia (Baillon,
1868b) without even referring to Duguetia
sect. Fusaea. Fries (1900), who followed
Baillon in regarding Fusaea as a distinctive
section of Aberemoa, stated that "this secThis paper is a revised version of chapter 4 in He,
1997.
2 Author to whom reprint requests should be sent.
3 C u r r e n t address: Department of Life Science,
Southwest China Normal University, Beibei, Chongqing 630715, R R. China.
tion differs in so many respects from the
remaining sections [of Aberemoa], that it
should perhaps be regarded as a separate
genus." The differences mentioned above,
and the presence of simple hairs instead o f
stellate hairs, led Safford (1914) to raise
Baillon's sect. Fusaea to generic rank. Although fully agreeing with Safford to give
Fusaea generic status, Fries (1930) had
doubts about the position of Fusaea within
the family.
In his series of generic revisions in Annonaceae, Fries (1934) added a second species to the genus: F. decurrens R. E. Fr. was
described on the basis o f only one flowering
specimen collected in the vicinity of Iquitos, Peru. In a later volume Fries (1937)
described the third species, F. peruviana R.
E. Fr., also citing only the (flowering) type
specimen. When treating Peruvian Annonaceae, Fries (1938) still was unfamiliar with
the fruits of F. decurrens and F. peruviana.
Also, Fries's (1959) treatment of Annonaceae in Engler and Prantl's Die natiirlichen
Pflanzenfamilien does not yield any novelties, and the generic description of the fruit
o f Fusaea still was given solely on the basis
of the fruit of F. longifolia.
To date, the position o f Fusaea within
Brittonia, 51(2), 1999, pp. 181 203.
9 1999, by The New York Botanical Garden Press, Bronx, NY 10458-5126 U.S.A.
ISSUED: 14 June 1999
182
BRITTONIA
the family is still open to discussion. More
specifically, its placement with regard to
other g e n e r a with ( p s e u d o - ) s y n c a r p o u s
fruits is debatable. Two views generally are
advocated. Either Fusaea is placed in one
group together with Duckeanthus, Duguetia, Letestudoxa, Pachypodanthium, and
Pseudartabotrys (Le Thomas et al., 1994;
Koek-Noorman et al., 1997), or Pachypodanthium/Duguetia and (among others) Fusaea/Duckeanthus are thought to represent
different evolutionary lineages (van Heusden, 1992; Schatz & Le Thomas, 1993).
Palynological and morphological data on
flowers and fruit fuel the main arguments
in this controversy. In this paper we do not
intend to solve this controversy. However,
in our treatment of the morphology of flowers and fruits we critically evaluate some
characters used by others while assessing
phylogenetic relationships within Annonaceae. The fruits of F. peruviana are described for the first time.
Morphology and Anatomy
LEAF ANATOMY
The specimens studied are indicated by
an asterisk in the List of Exsiccatae. From
these specimens transverse sections of the
central part o f the lamina including the primary vein, and of the petiole were made,
as well as cuticular preparations.
Abaxial side.--Indument: always present,
consisting o f trichomes of 1-7 cells, 2 0 0 900 txm long, appressed. Unspecialized epidermal cells: ( 1 5 - ) 2 0 - 4 0 ( - 4 5 ) x ( 1 0 - ) 1 5 2 5 ( - 4 0 ) ixm, anticlinal walls slightly
curved to (mostly) straight. Stomata: paracytic with 2 subsidiary cells on the level of
unspecialized epidermal cells, 12-24 per
mm. The length of the guard cells is 1 0 20(-30) t~m. Crystals present in both species as rhombic crystals and small crystal
sand.
Adaxial side.--Indument: absent, except
for scanty hairs on veins in F. peruviana.
Unspecialized epidermal cells: 15-35 (-40)
x ( 1 0 - ) 1 5 - 3 0 ( - 4 0 ) ~xm, anticlinal walls
straight, sometimes slightly curved. Crystals occur in every epidermis cell. They
adopt different shapes: needle-shaped crystals, druses, rhombic crystals and small grit-
[VOL. 51
like crystals of indefinite shape. By far most
abundant are rhombic crystals of small size,
4 - 8 X 3 - 6 izm.
In transverse section.--Lamina dorsiventral, 1 3 0 - 1 6 0 ( - 2 2 0 ) tzm thick. Epidermis
one-layered on both sides, ( 7 - ) 1 5 ( - 2 0 ) ixm
thick adaxially, 5 - 1 0 ( - 1 3 ) izm abaxially.
Mesophyll consists of 2 layers of palisade
parenchyma and 4 - 8 layers of loosely
packed spongy parenchyma. Primary vein
compound: a discontinuous layer o f phloem
accompanies a continuous ring of xylem at
the abaxial side. A zone of phloem tissue,
often in conjunction with sclerenchyma,
penetrates the xylem body. The intruding
phloem partially or fully dissects the xylem
body, thus creating an island of xylem tissue on the adaxial side. The vascular system is surrounded by a sheath of sclerenchyma. A narrow zone of flattened parenchymatic cells surrounds the vascular bundle abaxially. Sheath extensions: caps of
sclerenchymatic tissue abaxially reach into
the spongy parenchyma and adaxially into
the palisade parenchyma, but do not reach
the epidermis. Sclereids: stone cells occur
sparsely to abundantly in the parenchymatic
tissue situated in the centre of the xylem,
grouped into large clusters. Osteosclereids
extending from the adaxial epidermis to the
abaxial epidermis in the lamina were found
regularly. Crystals are absent in the mesophyll. Idioblasts occur in the spongy parenchyma of the lamina, and in the parenchymatic tissue of the midvein, both inside and
outside the vascular bundle. Petiole: vascular bundles occur disorderly. Idioblasts
usually occur eccentrically. Stone cells are
numerous, grouped into large clusters, and
sometimes can occur as a continuous layer
all around.
Discussion.--The leaf anatomical pattern
arising from the eight specimens studied is
constant. Variation is not apparent, and differences between the two species are lacking. The most salient features characterizing
Fusaea are the occurrence o f rhombic crystals in epidermal cells, sclereids o f the osteosclereid type, and the histology of the
primary vein. Neither character, however, is
exclusive to Fusaea. The latter two characters are exhibited only by a small group
of genera, namely the majority of the gen-
1999]
CHATROU & HE: ANNONACEAE
era of the Guatteria group and the Unonopsis-Onychopetalum alliance (van Setten
& Koek-Noorman, 1986). Strikingly, the
combination of these two characters is not
known to appear in any other genus with
(pseudo-)syncarpous fruits.
INFI.ORESCENCES
A c c o r d i n g to W e b e r l i n g and H o p p e
(1996), who largely follow Troll's (1964,
1969) typology of inflorescences, the basic
branching type of the inflorescences of Annonaceae is a determinate thyrse, i.e., a
multinodate main axis with a terminal flower. The partial inflorescences are rhipidiate
due to the addorsement of the prophyll (cf.
Fries, 1911, 1919). The description of inflorescences of Fusaea could then be derived from this basic type of general architectural pattern by introducing diverse variations (Weberling & Hoppe, 1996). In our
opinion, however, this rather static approach is not fully satisfactory regarding
the dynamics of inflorescence formation.
Here we prefer to describe the process of
development rather than create a sort of
classification. Starting with a basic unit, the
whole inflorescence can be understood as
the result of reiterative growth. Applying
this view permits a better perception of the
ontogeny of inflorescences, as well as a
much stronger basis for phylogenetic comparisons among genera o f Annonaceae.
Inflorescences of Fusaea are built up of
axes that have determinate meristematic activity, terminating in a flower (monotelic inflorescence). The basic unit is a terminal
flower with two subtending bracts. The
flower stalk has an articulation or abscission zone by which the unfertilized flower
or the ripened fruit is eventually shed. The
part of the flower stalk above this articulation is called the pedicel. The lower bract
(or prophyll in all cases, except for the first
lower bract on the inflorescence) is attached
just below the articulation, thus the pedicel
is seemingly borne in the axil of the lower
bract. The upper bract is attached to the
pedicel well above the articulation. The
lower bract is cucullate and caducous, and
in early stages completely encloses the axillary bud that is to produce the next-order
183
shoot (Figs. 1C, 2A). This bud includes the
pedicel with the terminal flower, both still
enclosed by the upper bract. The lower
bract encloses the next-order-lower bract as
well. Reiteratively, this lower bract includes
the bud of the next-higher-order shoot.
Thus, within a still closed lower bract, lateral shoots of two successive orders can
easily be observed (Figs. 1D, 2A). When
the axillary bud develops, it ruptures the
subtending lower bract along a suture (Fig.
1C). The upper bract is also cucullate, but
lacks an axillary bud, and in early stages
completely encloses the terminal bud. During flower development this bract ruptures
along the midrib into two, 3 - 5 m m long
parts, resembling two opposite bracts (Fig.
3A). This confusion has led to the erroneous description of two opposite bracteoles
by Berry (1995).
The reiterated development of axillary
shoots of still higher orders leads to an inflorescence which for m o s t Annonaceae has
been described as rhipidiate (Fries, 1919,
1959). By definition, the axes of a rhipidium are all oriented in one plane with the
prophylls opposite one another, the successive flowers alternating at angles of 180 ~
(Fig. 2B). Inflorescences of Fusaea, however, differ in this respect: instead of a true
addorsement of the lower bract, the angle
of its displacement is only ca. 8 0 - 9 0 ~ (Figs.
1A - B , 2C).
After the shedding o f several flowers, a
rachis is left, consisting o f successive flower stalk bases, up to the articulation, and
(scars of) the lower bracts. This part is
called a sympodial rachis by Maas and
Westra (1984) in their monograph of Anaxagorea. The longest sympodial rachis we
found (Krukoff8086) was 15 m m long (Fig.
IA, B). After having developed a sympodial rachis, an inflorescence often ramifies
into two. This is difficult to explain by the
regular axillary shoot formation just outlined. Probably the ramification is due to
auxiliary buds. A similar p h e n o m e n o n has
been described for Duguetia sessilis and D.
cadaverica (Maas et al.. 1993), and Mezzettia leptopoda ( W e b e r l i n g & H o p p e ,
1996). 11ae m a x i m u m number of flowers
developed in one rhipidium is 11. At any
one point in time a rhipidium may exhibit
184
BRITTONIA
[VOL.
51
FIG. 1. Inflorescences of Fusaea. A. Supra-axillary inflorescence, consisting of a peduncle, and a sympodial
rachis with a terminal bud on top. 1: are of coalescence of twig and petiole, 2: groove indicating coalescence
of peduncle and twig, 3: distal part of peduncle, 4: sympodial rachis. B. Schematic drawing of same inflorescence,
showing two rows of scars at the articulations. Circle indicates angle of displacement of succeeding flowers. C.
Terminal bud of inflorescence with ruptured lower bract. D. Terminal bud of inflorescence with lower bract
removed. The bud in the axil of the removed lower bract is indicated by a star, the next order lower bract
enclosing the next higher order shoot is indicated by a dot. (From Krukoff 8086.)
1999]
CHATROU & HE: ANNONACEAE
0
0
//,~,>--)~,
1111
v m
185
,
)~
11
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II
If
9
/1
II
11
I
Ii
II
"t~
i
\.?i
\
X
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/
I1
I/
I I II
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. ~, \\ ttb:~.. 11
',',\"-XI"
'B
\\ \~
fl 9
I:i /
tG4' ,'I
__ ~ ~ l
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[~t,
stillpresent
_-'_--~ lowerbract,droppedoff
~/7-/-777, upperbract, stillpresent
~u~/7/7
~ upperbract, droppedoff
::~;i~;~;7::;z; upperbract,juvenilestage
A lowerbractenclosingflower
of 2nd or 3rd order
9 same for Fusaea
r
upperbractenclosing
2nd order flowerbud
same for Fusaea
O lowerbractenclosingflowerbud
as wellas upperbract of 3rd order
shoot, both injuvenilestage
9 same for Fusaea
A
FIG. 2. Schematic drawings of an inflorescence of Fusaea, using an example from Listabarth & Vdsquez
11-1293. A. Supra-axillary inflorescence with flowers of three successive orders. B. Diagram of a rhipidium
with 3 flowers. C. Diagram of modified rhipidium of Fusaea conforming to A.
u p to five flowers i n v a r i o u s stages of development.
T h e i n f l o r e s c e n c e as d e s c r i b e d a b o v e
o r i g i n a t e s i n a t e r m i n a l position. T h e ter-
m i n a l flower soon shifts t o w a r d a supra-axi l l a r y p o s i t i o n (Figs. 1A, 2A). This is
c a u s e d by three processes, o c c u r r i n g sync h r o n o u s l y . First, the flower is o v e r t o p p e d
186
BRITTONIA
[ V O L . 51
F~6. 3. Fusaea longifolia. A. Leafy twig with a flower bud, showing the ruptured upper bract. B. Flower
with some sepals and petals removed, exhibiting carpels, stamens, and staminodes. C. Inflorescence. D. Fruit.
(A, de Granville 6445; B, C, Maas et al. 8066; D, Ribeiro et al. 1636.)
1999]
CHATROU & HE: ANNONACEAE
by the leafy twig originating from the vegetative bud in the axil of the subtending leaf
(i.e., of the leafy twig, not of the inflorescence): a normal case o f sympodial growth.
Second, this twig coalesces with the petiole
o f the subtending leaf (Fig. 1A). The synchrony of these two processes can be deduced from the absence o f leaf-opposed inflorescences in the studied material. These
would have occurred if the overtopping had
been completed betore the coalescence of
the twig and the petiole of the subtending
leaf. Finally a third f o r m of coalescence occurs. In most cases a groove between the
basal part of the inflorescence and the twig
can be observed (Fig. 1A). Coalescence between these two parts thus adds to the supra-axillary position of the inflorescence.
The peduncle is considered to be the noncoalesced, basal part of the inflorescence,
between the twig and the first lower bract.
FI.OWERS
The very young buds of Fusaea have
nearly free, valvate sepals. As the buds mature, the sepals enlarge through meristematic growth at the base. This meristematic
part is undivided and ring-like, thus finally
resulting in connation of the mature sepals.
The distal, free, valvate parts are visible as
three elevated ribs of 3 - 4 mm, meeting at
the apex of the bud. After opening of the
flower the connate, lower part of the calyx
ruptures into three, more or less equal sepals. These are saccate at the dorsal side,
although this feature is often obscured in
dried herbarium material. The sepals of F.
longifolia persist longer than those of F. peruviana, but for both species they rarely
persist on the fruits.
Although the fusion of petals in F. peruviana may give the impression of 6 petals
in one whorl (Fig. 4B), inner and outer petals are nevertheless discernible. Inner petals
are slightly larger and clearly wider than the
outer petals, and at anthesis the margins of
the inner petals fold against each other to
form a pollination c h a m b e r (Fig. 4B, C). In
F. longifolia the inner petals make a similar
pollination chamber.
As in most Annonaceae, the stamens of
Fusaea are spirally arranged. The outer one
187
or two cycles of stamens have been transformed into staminodes, which provide Fusaea with a character which, a m o n g neotropical Annonaceae, it shares only with
some species of Xylopia. The staminodes
have incorrectly been termed " p e t a l o i d "
(e.g., Baillon, 1868a; Berry, 1995). Their
origin can be understood by regarding the
m o r p h o l o g y of a sequence of stamens, f r o m
the center of the flower outward. The innermost stamens of Fusaea are 2 . 5 - 4 m m
long, the length of the thecae 2-2.5 m m .
The prolonged anther connective expands
into a s h i e l d - l i k e , m a s s i v e , 5 - 7 - a n g l e d ,
slightly convex structure on top of the stamen. Eight to eleven cycles from the center
(the fourth or fifth winding of stamens
counted from the periphery), the prolonged
connective changes a little toward tongueshaped, as if pushed up from the lower outer side. One or two cycles from the periphery the prolonged connective is clearly
tongue-shaped and equals the length of the
thecae. Thecae are still present, but shorter.
Only the outer one or two windings of stamens lack the thecae, while the thickened
prolonged connective m a y reach 6 m m in
length.
With regard to the functional aspects of
the staminodes, it is tempting to hypothesize that they are a modified floral feature
related to beetle pollination, i.e., that they
c o n s t i t u t e f e e d i n g tissue ( G o t t s b e r g e r ,
1988). So far no observations have been reported on the staminodes truly being an adaptation to beetle pollination. Flowers o f
the only collection with explicit mention o f
their mature state (Maas et al. 8066) show
clear gnawing scars on m a n y staminodes.
Whether pollinating beetles (or other insects) gnaw at staminodes remains to be
studied.
The ovaries of Fusaea are fused basally.
The extent of fusion slightly exceeds the
height of the ovule, and is 0.8-1 mm. As
the height of the o v a r y is ca. 3 mm, the
largest part of the o v a r y is free. Such is
already the case in a young developmental
stage: all ovaries o b s e r v e d in very young
buds are fused along their lateral walls to
just above the ovules. Light-microscopy
slides were made to study the morphological origin of this fusion. It was hypothe-
188
BRITTONIA
[VOL. 51
FIG. 4. Fusaea peruviana. A. Leafy twig with fruit. B-D. Flowers. (A, V6squez & Jaramillo 7184; B D,
Listabarth & Vasquez 11-1293.)
1999]
C H A T R O U & HE: A N N O N A C E A E
189
FIG. 5. Fusaea Iongifolia. A. Cross section through the basal part of the gynoecium. The central ovaries are
sectioned at the coherent part. The ovaries around are sectioned at the free part. B. Cross section through the
upper part of the g y n o e c i u m showing the arrangement of the hexangular styles. C. Same section at higher
magnification, showing interlocking papillae between the styles. (From Prance et al. 25410.)
sized either to be caused by the floral receptacle protruding between and coalescing
with the carpels, as described for Rollinia
exsucca (Deroin, 1988), or to be the result
o f fusion of the carpels themselves as in
A n n o n a sect. Oligantha (Fries, 1959). The
latter is the case in F u s a e a (Fig. 5A). M o r e
detailed studies are needed to reveal whether this fusion has a congenital origin or
whether postgenital fusion processes occur.
The free parts of the ovaries are covered
with hairs to 0.3 m m long. Toward the apex
o f the o v a r y these hairs b e c o m e progressively shorter to 0.02 m m or less and are
papilla-like. On top o f the ovary, Fusaea
has a distinctive style and stigma. In contrast to most A n n o n a c e a e that lack a style,
the transition f r o m o v a r y to style is delineated by a constriction. In addition, the ovary and the style have a different shape in
transverse section. Whereas the o v a r y is
m o r e or less regularly hexangular, the style
exhibits a clear ventral slit (Fig. 5B). Finally, there is a clear difference in the type
o f epidermal outgrowths. The style is covered by much smaller papillae ( 3 0 - 5 0 txm)
than the papilla-like outgrowths of the carpels ( 1 0 0 - 2 0 0 i~m). In contrast to the papilla-like outgrowths o f the carpels, the papillae of the styles interlock to f o r m one
column of coherent styles (Fig. 5C). The
stigma is discernible f r o m the style by a
darker color, black instead of brown, and an
indument of erect hairs to 1.1 m m long. In
immature flowers, the stigmas do not exceed the surrounding stamens, but in nearly
mature flowers they do, and often all stigmas are covered by a whitish, mucilaginous
substance. For primitive angiosperms, the
postgenitally fused apical zones of the gynoecium and the mucilaginous secretion
have been n a m e d intragynoecial and extragynoecial compita, respectively; these c o m pita o v e r c o m e the primitive condition o f
apocarpy (Endress, 1982). The term " c o m p i t u m " was introduced by Cart and Carr
(1961) and refers to the c o m m o n transmitting tissue in the styles of syncarpous gynoecia. In Annonaceae, the occurrence o f
styles interlocking by their papillae, to
which the term c o m p i t u m is not applicable
strictly speaking, has been primarily found
in genera whose carpels fuse after fertilization (Deroin, 1991). Briechle-M~ick (1994)
decribes coherent epidermis cells in the
basal part of the style in Annona and Rollinia. The coherence o f styles in Fusaea
complies with none of the three types mentioned for A n n o n a and Rollinia, as in Fusaea the epidermal cells interlock all along
the style. A partial compitum, i.e., fusion o f
only few, inner styles, as in Cananga odorata (Deroin, 1997), is absent in Fusaea. A
possible adaptive advantage of the coherent
190
BRITTONIA
styles o f Fusaea will have to be uncovered
by fluorescence microscopy, but it is doubtful whether the coherent styles can function
as a compitum.
The floral receptacle is discoidal and has
a central cavity 5 m m diam. and 1-2 m m
deep. The carpels are situated at the bottom
of this cavity, the bottom itself being slightly to distinctly convex. Because o f this depression o f the carpellate portion o f the receptacle, the carpels are concealed for about
half their length. A similar morphology in
Letestudoxa has been described as "included into the receptacle" (Le Thomas, 1969).
This description could easily be confused
with the above-mentioned case o f the floral
receptacle coalescing with the carpels (Deroin, 1988). We therefore prefer to describe
the p h e n o m e n o n as "carpels immersed into
concave part o f floral receptacle."
FRUIT
The fruit of Fusaea is a fleshy, subglobose syncarpium. The individual carpels of
which the fruit is composed, which are hexagonal in cross section, can still be recogn i z e d b y dark d e l i n e a t i o n s or shallow
grooves on the fruit surface. The carpels at
the base o f the fruit have developed to a
lesser degree. Instead of becoming regular
hexagonal areoles, they are more stretched
in shape and smaller in size. These basal
carpels do not develop seeds. The apical
parts of the ovaries may not fuse and remain recognizable as minute tubercles. In
F. longifolia, these tubercles are usually absent. Small, but distinct, pointed tubercles
with a m a x i m u m height of 2 m m occur
rarely. In F. peruviana 75% o f the fruits we
studied have clear, lamella-like tubercles
with the ventral suture of the carpel clearly
recognizable. These tubercles are up to 5
m m long.
In their work on fruit and seed anatomy,
van Setten and Koek-Noorman (1992) state
that Fusaea is one of the two genera in Annonaceae, together with Pseudartabotrys, in
which the basal part of the fruit is formed
by a collar consisting of the disc-shaped,
connate part of the calyx. This, unfortunately, is a misinterpretation. The part of
the flower which in fruit will form this col-
[VOL. 51
lar undoubtedly is the floral receptacle. This
receptacle is widened and disc-like. On the
outer side of flower buds it is already clearly distinguishable from the connate sepals
by a difference in color, and by a shallow,
ring-like furrow. After anthesis, when sepals, petals, and stamens abscise, this discshaped receptacle persists. During fruit development the syncarpium is formed, and
the pedicel thickens. The staminate portion
of the receptacle is pushed aside by the
elongating carpellate portion o f the receptacle and the developing carpels. At the
base of mature fruits the former attachments
of sepals, petals, and the staminate portion
of the receptacle often remain clearly visible (Fig. 3D). This part of the former flowering receptacle often has been called a collar, and has been used as an identification
character to distinguish fruits of Fusaea
from fruits ofAnnona (cf. Maas, 1995). For
two reasons this is somewhat problematic.
First, this collar is not always visible, as the
enlarging carpels might overgrow the staminate portion o f the receptacle, eventually
rendering it invisible. Second, at the base
of the fruit o f some species of Annona (e.g.,
A. trunciflora; Rainer, pers. comm.) parts of
the floral receptacle remain visible in a similar way, which consistently should be
called " c o l l a r " as well. Regarding this
problematic nature o f the term " c o l l a r " we
describe the phenomenon as "protruding
torus remnants."
In dried fruits of Fusaea, the elongated
fruiting receptacle can often be taken out of
the fruit without damaging the receptacle or
the carpels. Sometimes the fruiting receptacle even loosens spontaneously after drying. It indicates that syncarpy in Fusaea is
merely the result of the lateral fusion o f carpel walls, and that the fruiting receptacle
does not contribute to the fusion by protruding between the carpels, unlike Duguetin and Pachypodanthium.
The basal part of seeds of Fusaea is provided with a small aril, largely covering the
hilum. The aril is a ring of very densely
packed, fiber-like structures.
WOOD ANATOMY (by Ben J. H. ter Welle)
All wood specimens are deposited in the
wood collection of the Herbarium Division,
1999]
CHATROU & HE: ANNONACEAE
Utrecht University (Uw). Identification o f
the material was based on the herbarium
vouchers of these samples. The two samples of F. p e r u v i a n a available for this study
were taken f r o m the original herbarium
voucher. Consequently, these samples have
a limited diameter (1 cm).
Material studied. Fusaea longifolia. Guyana: Jansen-Jacobs et al. 2313 (Uw 33955). Suriname: Lindeman 3531 (Uw 2307), 5801 (Uw 3955), 6742 (Uw
4559), 6957 (Uw 4675); Lindeman et al. 533 (Uw
26487); Schulz 9315 (Uw 8874). French Guiana: de
Granville et al. 6601 (Uw 30033). Peru: Maas et al.
6320 (Uw 30329). Brazil: Krukoff 8086 (Uw 16133).
F. peruviana. Peru: Vdsquez & Jaramillo 8506 (Uw
35939); Berlin 637 (Uw 35940).
Description (see Fig. 6 ) . - - G r o w t h rings
absent or present, often faint. The end of a
growth ring border is m a r k e d by a reduction
in lumen diameter, sometimes combined
with an increase in fiber wall thickness, and
occasionally with a decrease in vessel diameter. Vessels diffuse, solitary (15-20%),
but mainly in radial multiples and (some)
irregular clusters of 2 - 4 ( - 6 ) , ( 8 - ) 1 0 - 2 9 ( 32) per mm:, round to slightly oval, but also
m o s t l y angular, ( 4 0 - ) 6 5 - 9 0 ( - 1 2 0 )
txm
diam., vessel m e m b e r length: ( 2 6 5 - ) 3 5 5 5 0 5 ( - 6 1 5 ) p~m. Perforations simple. Intervascular pits alternate, round, 2 - 3 txm diam.
Striation present to v e r y common. Vesselray and v e s s e l - p a r e n c h y m a pits as the intervascular pits, but half-bordered. Fibers
non-septate, lumen diameter to 7 - 1 3 txm,
walls to 5 - 9 p~m. Pits simple, equally present on the radial and the tangential walls,
3 - 4 txm diam., length: ( 9 4 0 - ) 1 1 0 5 - 1 3 5 0 ( 1615) ixm. F/V ratio: 2.63-3.09. R a y s heterogeneous, with few to v e r y few uniseriates, and mostly 3 - 6 ( - 8 ) - s e r i a t e , c o m p o s e d
mainly of (weakly) procumbent, and some
square and upright ray cells. Height of the
uniseriate rays to 9 - 1 5 cells ( = 1 8 5 - 4 6 0
ixm), and of the multiseriate rays to 6 4 125(-185) cells (= 1 2 9 0 - 4 5 0 0 p,m). Width
of the multiseriate rays to 100-230 p,m.
N u m b e r per mm: ( 2 - ) 3 - 4 ( - 5 ) . Rays often
dissected. Small rhombic crystals c o m m o n
in most ray cells. P a r e n c h y m a in apotracheal, c o n t i n u o u s , c o n c e n t r i c t a n g e n t i a l
bands, 1 cell wide, sometimes 2 cells wide
over a short distance (2-3 cells), with 3 4 ( - 5 ) fibers between two bands. N u m b e r of
191
bands 12-15, sometimes 18, usually varying from 10 to 15 per m m . Scanty paratracheal p a r e n c h y m a present, but scarce, as inc o m p l e t e v a s i c e n t r i c sheaths. L e n g t h :
( 3 0 0 ) - 3 9 5 - 5 4 0 ( - 6 0 0 ) p~m, and 2 - 4 cells.
D i s c u s s i o n . - - T h e general w o o d anatomical characters are in line with the very specific w o o d anatomy o f the family, characterized by the tangential, concentric parenc h y m a bands. The small rhombic crystals
in the ray cells, however, provide F u s a e a
with a very specific characteristic. These
crystals are described for the first time here.
Loureiro and da Silva (1968) and Loureiro
et al. (1979) provided only macroscopic
characteristics; Loureiro (1969) described
the microscopic w o o d anatomy of Fusaea.
N o n e of these authors mentioned rhombic
crystals in the rays. According to Metcalfe
and Chalk (1950), A n n o n a c e a e typically
lack crystals, although some species of P o lyceratocarpus, G o n i o t h a l a m u s , and H o r n s c h u c h i a have numerous, small crystals.
Our own results (ter Welle, unpubl, data)
show that the small crystals in Goniothala m u s and Trigynea c a u d a t a (syn. H o r n s c h u c h i a caudata) are v e r y similar to the
ones observed in F u s a e a . However, it is unclear as yet whether this characteristic will
be useful at the genus level for these taxa,
as it is in Fusaea. In A n a x a g o r e a (ter Welle
in Maas & Westra, 1984) small druses
turned out to be of generic value as well.
All other quantitative data for F u s a e a are
overlapping with those of other genera
studied in detail.
Species R e c o g n i t i o n
Based only on the type collection of F.
decurrens, Fries (1934, 1937) distinguished
that species f r o m F. longifolia by its long-
decurrent lamina base, flat secondary veins
on upper surface, and narrower as well as
more sharply pointed staminodes. Comparison of the numerous subsequent collections
reveals that F. longifolia, the most c o m m o n
and widespread species o f the genus, shows
marked morphological variation, also in the
characters used by Fries to distinguish F.
longifolia and F. decurrens. Based on measurements of these diagnostic features o f
158 specimens, three scatter diagrams (Fig.
192
BRITTONIA
[ V O L . 51
FIG. 6. Wood anatomical characters of Fusaea longifolia. A, B. Transverse sections. C. Tangential section.
D. Radial section, crystals. E. Tangential section, crystals. (A, Lindeman 6957 Uw 4675; B, Schulz 9315=Uw
8874; C, Lindernan 3531 Uw 2307; D, Lindernan 6742 Uw 4559; E, Lindeman et al. 533=Uw 26487.)
7 A - C ) s h o w the q u a n t i t a t i v e v a r i a t i o n o f
these d i s t i n g u i s h i n g c h a r a c t e r s a n d c o m p a r e
these f e a t u r e s f o r the t w o s p e c i e s . W e p l o t t e d 11 s p e c i m e n s i d e n t i f i e d as F. d e c u r r e n s
b y s e v e r a l b o t a n i s t s a n d 147 s p e c i m e n s
i d e n t i f i e d as F. l o n g i f o l i a . T h i s i d e n t i f i c a tion w a s i n c o r p o r a t e d into the g r a p h s as it
is i n f o r m a t i v e a b o u t the p a s t r e c o g n i t i o n o f
1999]
CHATROU & HE: ANNONACEAE
I
2.8
2.6
2.4
.'~ 2,2
~2.0
"~ 1.8
c 1.6
1.4
I
9
I
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.
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.8
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9
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193
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Q~
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00
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99 O O ~ O 9O.9 9
50
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f . .
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9
9 9 O~
80
90
100
9
110
120
Lamina base angle (o)
,
9
i
i
i
2.8~
1-~ ~z~t-
9
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~o~ 9
i
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9"9
" ~
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x~el~-e ~
~4'. o ~
~.o~. o ; .
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.%
-,:,
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50
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9
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9 ~,o+,o,+
t
i
90
100
110
!
120
S t a m i n o d e apex angle (~
FIG. 7. Scatter diagrams, showing the overlapping of the characters previously used to distinguish Fusaea
longifolia and F. decurrenx. (A. Lamina base angle vs. staminode width. B. Lamina base angle vs. staminode
apex angle. C. Staminode apex angle vs. staminode width.)
194
BRITTONIA
the two species. The morphological data
plotted in the scatter diagrams show no discontinuity, and therefore F. decurrens is put
into s y n o n y m y of F. longifolia.
Both the fusion and the indument of the
petals clearly distinguish F. longifolia and
F. peruviana. This sharply contrasts with
the ability to differentiate between the species on the basis of leaf and fruit characters.
Tertiary venation distinguishes F. peruviana from specimens of F. longifolia f r o m
the Guianas, f r o m the lower A m a z o n River,
and even f r o m southern Peru and Bolivia.
Those specimens of F. Iongifolia f r o m areas
where the two species are sympatric, however, show strong tendencies toward tertiary
venation patterns similar to F. peruviana.
The fruit does not provide strong differentiating characters either. Most fruits of F.
peruviana have longer tubercles, but a quarter of the fruits we studied lack clear tubercles like m o s t fruits of F. longifolia.
Position of the Genus
The reticulate nature of character expression impedes the establishment o f a phylogeny for the Annonaceae (Schatz & Le
Thomas, 1993). The simultaneous occurrence of plesiomorphic and apomorphic
characters also profoundly affects attempts
to pronounce upon the position o f Fusaea
within the family.
By having the outer stamens transformed
into staminodes, Fusaea exhibits a clear autapomorphic character within the Duguetia
group o f related genera (Fries, 1959; van
Setten & K o e k - N o o r m a n , 1992; K o e k N o o r m a n et al., 1997). The outer staminodes in Xylopia very probably reflect a
parallel origin. The odd architecture o f the
inflorescence, with the flowers not oriented
in one plane, and the rhombic crystals in
the rays might be other autapomorphies.
They are autapomorphies at least within the
Duguetia group. Outside this group, Monanthotaxis whytei might have a similar inflorescence architecture. This is suggested
by a drawing in Weberling & Hoppe, 1996,
but the a c c o m p a n y i n g text does not indicate
this. Besides Fusaea rhombic crystals are
found in uurelated Goniothalamus species
and Trigynaea caudata.
[VOL. 51
In the section on leaf anatomy, some
characters are mentioned which Fusaea
shares with genera f r o m the Guatteria-alliance and the Unonopsis-alliance. Data
are too scarce to pronounce upon the presence o f these characters within the Duguetia group, as leaf anatomical data are available only for Duguetia. This genus, however, differs in all three features which
characterize Fusaea: rhombic crystals, osteosclereids, and the histology of the prim a r y vein.
Fusaea s h a r e s s o m e s y n a p o m o r p h i e s
with Letestudoxa, Pseudartabotrys, and
Duckeanthus. With Duckeanthus it shares
the typical large, pouched sepals which are
very similar although the sepals of Duckeanthus are free, while those of Fusaea initiate largely connate. Another remarkable
s y n a p o m o r p h y is the occurrence o f curled
trichomes ("poils courts et f r i s r s " ) in Fusaea (on y o u n g twigs) and Letestudoxa bella (on y o u n g twigs, petioles and lower side
of the lamina; Le Thomas, 1969). A synap o m o r p h y shared by all four genera is the
depressed disc-shaped floral receptacle. At
the base of the fruit large parts o f the floral
receptacle remain visible, which is mostly
called "collar." Fruit characteristics, and
especially the occurrence of a "basal collar,'" have been one of the main reasons to
classify Fusaea, Letestudoxa, Pseudartabotrys, and Duckeanthus together in one
group of allied genera with Duguetia and
Pachypodanthium (van Setten & KoekN o o r m a n , 1992; K o e k - N o o r m a n et al.,
1997), The collar of the two latter genera,
however, is derived from incompletely developed carpels, which are h o m o l o g o u s
with the stretched, sterile carpels at the base
of the syncarpium of Fusaea. This "basal
collar" is a pragmatic concept, helpful for
identifying genera. By ignoring its ontogenetic origin, however, and including only
presence or absence of a basal collar in a
database for phylogenetic analyses, the resuits of two different ontogenetic processes
are scored as the same character.
Similar inclusion of probably homoplasious characters under one single pragmatic
concept also occurs in the description of the
fruit type o f Annonaceae. K o e k - N o o r m a n
et al. (1997) use apocarpous, pseudosyn-
1999]
CHATROU & HE: ANNONACEAE
carpous, and syncarpous fruits as different
characters in their cluster analysis of genera. Defining syncarpy as fruits with fully
c o n n a t e carpels and p s e u d o s y n c a r p y as
fruits with partially connate carpels, genera
with varying extents of fusion between species (Duguetia, Pachypodanthium, Rollinia,
and even Annona) are forced into one category. The fruiting receptacle either protruding between the carpels, or dissociated
from them, probably is an important feature
reflecting the ontogenetic nature of syncarpy. Anatomical studies on the origin of sync a r p y are in p r o g r e s s ( S v o m a , pers.
comnl.).
Cladistic a n a l y s e s by D o y l e and L e
Thomas (1994) and Le Thomas et al,
(1994) include Fusaea, Letestudoxa, Duguetia, and Pachypodanthium into one
pseudosyncarpous clade. This clade is supported by palynological data, and contradicts the independent origin of syncarpy for
Fusaea suggested by Schatz and Le Thomas (1993). P a l y n o l o g i c a l l y , Fusaea fits
within the pseudosyncarpous group by its
i n a p e r t u r a t e pollen, g r a n u l a r i n f r a t e c t a l
structure, and small number of nexine foliations (Le Thomas et al., 1994). Most genera within the p s e u d o s y n c a r p o u s g r o u p
show autapomorphies in pollen characters,
that of Fusaea being large, tetrad pollen. In
contrast to other pseudosyncarpous genera,
Fusaea retained the plesiomorphic imperforate tectum, with an unusual thickness o f
the tectum as an autapomorphy, however.
The inclusion into one clade seems to conflict with the view o f van Heusden (1992),
who, on the basis of floral morphology,
placed Fusaea, Duckeanthus, Letestudoxa,
and Pseudartabotrys in one group, and Duguetia and Pachypodanthium in another. Le
Thomas et al. (1994), however, alleviate
this conflict by pointing to the distinguishing features of Duguetia and Pachypodanthium in their analysis. As these features are
apomorphies, these two genera could as
well be considered as a clade within the
pseudosyncarpous group.
In view of the morphological data presented here--especially those concerning
the infloresence, the gynoecium, the fruiting
receptacle, the origin of syncarpy, and the
synapomorphies mentioned a b o v e - - w e hy-
195
pothesize that a cladistic analysis based on
these data will strengthen the split of the
p s e u d o s y n c a r p o u s g r o u p into Fusaea,
Duckeanthus, Letestudoxa, and Pseudartabotrys on the one hand, and Duguetia and
Pachypodanthium on the other. This cladistic analysis will be u n d e r t a k e n shortly
( C h a t r o u , K o e k - N o o r m a n & Maas, in
prep.).
Taxonomic Treatment
FUSAEA (Baill.) Saff., Contr. U.S. Natl.
Herb. 18: 64. 1914; R. E. Fr., Acta Horti
Berg. 10(1): 49. 1930; R. E. Fr. in Engler
& Prantl, Nat. Pflanzenfam., ed. 2, 17alI:
58. 1959. TYPE: F. longifolia (Aubl.)
Saff.
Duguetia A.St.-Hil. sect. Fusaea Baill., Adansonia 8:
326. 1868.
Aberemoa Aubl. sect. Fusaea Baill., Hist. pl. 1: 206,
f. 233-235. 1868.
Fusaea sect. Fusaea ("Eu-Fusaea") R. E. Fr., Acta
H o n i Berg. I2(2): 274. 1937.
Fusaea sect. Synpetalantha R. E. Fr., Acta Horti Berg.
12(2): 274. 1937.
Trees (rarely shrubs), to 25 m tall. Young
twigs, petioles, and lower side o f lamina
and primary vein covered with straight and
curly hairs. Petioles canaliculate. Lamina o f
leaves (elliptic-)oblong-obovate, narrowly
obovate to obovate, chartaceous to slightly
coriaceous, (greenish) brown above, brown
below, apex cuspidate to acuminate, base
attenuate (acute to nearly rounded), primary
vein impressed above, prominent below,
secondary veins regularly curved to almost
straight, 10-22 on either side o f primary
vein, impressed (rarely flat) above, raised
below, forming distinct loops at obtuse angles, tertiary venation reticulate to percurrent. Inflorescences in foliate zone (rarely
cauliflorous), s u p r a - a x i l l a r y , 1 - 5 ( - l l ) flowered. Flowering and fruiting peduncles
to 5 mm long. Flowering and fruiting pedicels slightly curved. L o w e r bract cucullate,
enclosing axillary bud, caducous. Upper
bract midway along the pedicel, initially cucullate and enclosing the flower bud, ultimately rupturing into two parts and their
resembling 2 opposing bracteoles, caducous. Flower buds compressed ovoid, ovoid
to broadly ovoid. Flowers pendent, creamy,
yellowish brown, or whitish yellow, some-
196
BRITTONIA
times tinged reddish-purplish on the inner
side. Sepals 3, valvate, initially connate except for apex, ultimately rupturing into 3
subequal, saccate parts. Petals 6, in 2
whorls of 3 each, imbricate, free or connate
for basal %, longitudinally veined, outer
side densely to totally covered with whitish
to (yellowish) brown, appressed hairs. Toms flat to convex, with concave centre.
Staminodes 3 0 - 6 0 , in 1-2 spiral cycles
around outermost stamens, (pale) yellow,
orange to salmon, densely to totally covered
with very short, whitish hairs. Stamens
200-300, pale yellow to yellowish brown,
orange to salmon, prolonged connective a
5-7-angled disc with convex apex, densely
covered with very short, whitish hairs. Carpels 3 0 - 1 0 0 , immersed into concave part of
floral receptacle, ovary with one, basal
ovule, style and stigma distinct, ovary and
style densely papillate, styles coherent, stigma dark brown to black, densely to totally
covered with hairs. Fruit syncarpous, yellowish green to dark purplish outside, yellowish, orange to salmon-pink inside (in
vivo), (broadly) ovoid to subglobose with a
truncate or cordate base, torus remnants
mostly protruding, fertile carpels 30-100,
areoles mostly delineated by dark lines or
shallow grooves, hexagonal, smooth or tuberculate. Seeds reddish brown to dark
brown, shiny, aril composed o f densely
packed, fiber-like structures, ruminations lamellate in four equal parts, raphe a flat to
slightly raised rib, shallowly canaliculate,
straight, indistinct.
Key to the species of F u s a e a
1. Number of percurrent tertiaries per intercosta
( 0 - ) 6 - 9 ( - 1 3 ) ; petals free, only the extreme base glabrous within; floral receptacle convex with concave centre; fruit
smooth or slightly tuberculate with short
tubercles not longer than 2 mm.
F. longifi)lia
1. Number of percurrent tertiaries per intercosta
(12-)14-16(-19); petals basally connate,
basal %- 89 glabrous within; floral receptacle slightly convex to flat with concave
centre; fruit often strongly tuberculate,
with tubercles 2-5 mm long ....
F. peruviana
[VOL. 51
FUSAEA LONGIFOLIA (Aubl.) Saff., Contr.
U.S. Natl. Herb. 18: 65, f. 73-74. 1914.
Annona longifolia Aubl., Hist. pl. Guiane
1: 615, pl. 248. 1775. Duguetia longifolia
(Aubl.) Baill., Adansonia 8: 327. 1868.
Aberemoa longifolia (Aubl.) Baill., Hist.
pl. Guiane 1: 206. f. 233-235. 1868.
TYPE: F R E N C H GUIANA. Banks of
C r i q u e des Galibis, w i t h o u t date,
J.B.C.F. Aublet s.n. (LECTOTYPE: B M
[photo!]). (Fig. 3)
Uvaria? spectabilis DC. in Dunal, Monogr. Anonac.
92. 1817. TYPE: FRENCH GUIANA: Without locality, without date (ill Martin s.n. (HOLOTYPE: B M n.y.; "kleptotype": G n.y.).
Annona rhombipetala Ruiz & Pay. ex G. Don, Gen.
hist. 1 : 87. 1831. Fusaea rhombipetala (Ruiz & Pay.
ex G. Don) J. E Macbr., Field Columbian Mus., Bot.
Set. 4(7): 172. 1929. TYPE: PERU. Hu~inuco: Chicoplaya and San Antonio de Playa Grande, 1797
(fl), H. Ruiz L. s.n. (HOLOTYPE: B [photo!]).
Fusaea decurrens R. E. Fr., Acta Horti Berg. 12(1):
207. 1934. TYPE: PERU. Loreto: Mishuyacu, near
Iquitos, 100 m, F e b - M a r 1930 (ill G. Klug 952 (HOL O T Y P E : US; [SOTYPES: F-n.y., NY; "kleptotype": S).
Trees (rarely shrubs), (1)3-15(25) m tall,
(1)5-25(30) cm diam. Young twigs, petiole,
and lower side of lamina and primary vein
densely to totally covered with yellowish
brown, appressed to erect hairs to 1.2 mm
long, the shorter ones curly. Petioles 3-10
m m long, 2-4.5 mm diam. Lamina of larger
leaves (elliptic-)oblong-obovate, narrowly
obovate to obovate, 10-35 • 3 - 1 2 cm,
length/width ratio 2.5-4, chartaceous to
slightly coriaceous, acumen 5 - 3 0 ( - 4 0 ) m m
long, 1 0 - 2 2 secondary veins on either side
of primary vein, angles with primary vein
6 0 - 8 5 ~ smallest distance between loops
and margin 2-5 mm, number of percurrent
tertiary veins ( 0 - ) 6 - 9 ( - 1 3 ) . Inflorescences
1 - 5 ( - 1 0 ) - f l o w e r e d . Indument: peduncles,
pedicels, bracts, and outer side of sepals
sparsely to totally covered with yellowish
brown, appressed to erect, sometimes curly
hairs to 1 m m long, inner side o f sepals
glabrous, outer side of petals totally covered with white to (yellowish) brown, appressed hairs to 1.4 m m long, inner side o f
petals, except for extreme base, totally covered with whitish silvery to (yellowish)
brown, appressed hairs to 1.4 m m long. Peduncles 1-3 m m long, 3 - 4 mm diam., fruiting peduncles 2 - 4 mm long, 3-5.5 m m
1999]
C H A T R O U & HE: A N N O N A C E A E
diam. Pedicels 1 5 - 2 0 m m long, 2.5-3.5
m m diam., fruiting pedicels 12-20 m m
long, 5 - 8 m m diam. Upper bract depressedovate, 3 - 5 m m long. Flower buds ovoid to
broadly ovoid, to 20 m m diam. Flowers
creamy to yellowish brown, tinged reddishpurplish on inner side (in vivo). Sepals (triangular-)ovate to broadly (triangular-)ovate,
1 0 - 2 2 x 1 0 - 2 2 mm, apex acute. Petals
free, outer petals oblong-obovate, rhombicobovate to obtrullate, 3 0 - 5 0 ( - 6 0 ) x 15-25
m m , apex acute, inner petals oblong-obovate, obtrullate to broadly obtrullate, 3 5 60 x 15-30 mm, apex acute. Torus c o n v e x
with concave center. Staminodes 3 0 - 6 0 ,
yellowish brown, orange to salmon (in
vivo), narrowly triangular-obovate to obtrullate, 3 - 8 x 0 . 8 - 3 mm, apex acute to
nearly rounded. Stamens ca. 300, yellowish,
orange to salmon (in vivo), 2 . 5 - 4 m m long,
prolonged connective 0 . 4 - 0 . 7 X 0 . 8 - 1 . 6
mm. Carpels 3 0 - 1 0 0 , ovary 2.5 m m long,
style 3 m m long, stigma densely covered
with whitish hairs to 1.1 m m long. Fruit
yellowish green to dark purplish outside,
yellowish, orange to pink inside (in viw)),
3 - 8 cm diam., fertile carpels 4 0 - 1 0 0 , areoles smooth, rarely slightly tuberculate, tubercles to 2 m m high, glabrous or sparsely
to densely covered with yellowish hairs to
0.2 m m long on tubercles. Seeds obovoid
to obtrulloid, 1 2 - 2 0 m m long, 7-11 m m
diam., reddish brown to dark brown, aril 2 5 m m high.
Distribution, habitat, and phenology.-Widely distributed in Colombia, Venezuela,
Guyana, Suriname, French Guiana, Ecuador, Peru, Brazil, and Bolivia. (Fig. 8). In
non-inundated and inundated (v4rzea, igap6) forest; on sandy or lateritic soil, from
sea level to 6 0 0 ( - 9 0 0 ) m. Flowering and
fruiting specimens have been collected all
the year round.
Representative s p e c i m e n s examined. C O I , O M B I A .
A m a z o n a s : Trapecio Anmz6nico, Rio Loreto-Yac4,
N o v 1945 (t'r). Schultes 6954 (F). Antioquia: Mun.
Mt, tat6, Urab4, Villa Arteaga, 16 20 Feb 1953 (fr),
Schultes & Cahrera 18684 (US): Mun. Caucasia, rd.
to Nechf. 14. I km from Ca, ucasia Planeta Rica rd., Hacienda l_,a Candelaria, 24 Nov 1986 (fl), "Zarucchi &
Cdrdenas 4250 (COl,, MO, NY, U). C h o c 6 : 2 - 4 km
N W of Teresita, 18 May 1967 (fr). Duke 11066 (MO,
NY): Mun. Riosucio. l:'arque Nacional Natt, ral Los Katfos, Quebrada La Virgen. 18 Jun 1976 (fr), Le6n 97
197
(MO). C 6 r d o b a : Paramillo National Park, jct. of Rio
Tigre and Rio Mango, 28 Jnl 1988 (st1, Gentry &
Cuadtv*s 63896 (U). S a n t a n d e r : Puerto P a r r a - C a m p o
Capote, 10 Dec 1979 (fl, fr), Rentert'a Arriaga et al.
2136 (COl,, HUA). Vaup~s: Carlo Cubiy6. C o m u n i dad Indfgena La Sabana, 28 Apr 1993 (ill, Madrifidn
et al. 1205 (U), vicinity of Mittl, 20 May 1976 (fr),
Zarucchi 1607 (COl,, GH, K).
V E N E Z U E L A . A m a z o n a s : Dept. Atures, 149 km
from jet. of Rio G u a y a p o and Rio Sipapo, May 1989
( i l l Foldats & Velacco 91,r (UI: Cerro Ncblina base
c a m p on Rio Mawarinuma, 22 Apt 1984 (st), Gentry
& Stein 46852 (U). Bolivar: Mun. Sucre, vic. of Santa
Maria de Erebato, Feb 1989 (yfl 1, Fernandez & Sanojtl
5071 (U. US).
G U Y A N A . Simuni Cr., Rupununi River, 14 A u g
1931 (fr), Forest Dep. Brit. Guiana 2132 (Kt; Rupt,nuni Distr., Kuyuwini landing, Kuyuwini River. 2 Feb
1991 (fl), Jansen-Jacobs et al. 2313 (UI; Potaro-Siparuni, lwokrama Reserve. Fssequibo River, Pisham
Falls, 15 Feb 1995 (fr), Mutctmick & Allicock 744 (t J):
basin of Essequibo Rivcr, near mouth o f Onoro Cr..
15-24 Dec 1937 (fl, fr), A. C. Smith 2779 (A, F G,
NY, S. U. US): Marudi Mts., along trail from NorMan
Mines camp to Aishalton, 12 Nov 1982 (yfr/, Stqff'er.s
et al. 315 (U).
S U R I N A M E . Sectie O. 22 Jan 1907 (fl, fr), ~'tltl Hall
9i (K. L, U); Mapane Cr., C o m m e w i j n e Distr., 14 Dec
1961 (ill tlekking 1198 (U): Natural Reserve Brownsberg. Brokopondo Distr., I 1 Jun 1979 (fr), Heyde 691
(U): Nassau Mms., Marowijne Distr.. 16 Feb 1949 (fl),
l x m j o u w & Lindeman 2119 (K. NY, U), JodensavanneMapane Cr. area, C o m m e w i j n e Distr., 17 Mar 1953
(fl), Lindeman 3531 (LI,, U).
F R E N C H G U I A N A . St. Laurent du Maroni, 15 Apr
1961 (fl), Aubr&'ille 266 (P): Crique Kapiri, basin of
Approuage River, 14 Jan 1991 (tt), Cremer.s 11592 (B,
MO, U): N of Mts. Galbao, 10 km W S W of Satil, 17
May 1973 (fr), de Granville 1667 (CAY, NY, E U):
Haute Camopi, 1 km N of Mr. Belv6dbre, 1 Dee 1984
(fr), de Granville 7090 (B, NY, U): I,es Eaux Claires,
near Crique Tortue, 10 Feb 1993 (fl), Maas et al. 8066
(U): Crique Passoura. 7 M a y 1991 (fr), Sahatier &
Pr&,ost 3979 (CAY, U); Karouany, 1854 (fl). Sagot 5
(BR. E G. K. S, U).
E C U A D O R . Napo: Reserva Etnica Huaorani, maxus road and oil pipeline, K m 108, 18 Jan 1995 ( i l l
Aulestia & Omehuat 3254 (QCNE). S u c u m b f o s : Cuyabeno Reserve, N of I,aguml Grande, A p r - D c c 1988
(st), Valencia et al. 67440 (QCA. U).
PERU. A m a z o n a s : Rio Santiago valley, 65 km N
o f Pinglo, Quebrada Caterpiza. 19 Nov 1979 (fr), Huashikat 1326 (MO); ibidem, 21 Mar 1980 (frL Huashikat 2317 (MOL H m l n u c o : Tingo Maria. 4 A u g
1940 (fl), A.wlund 12730 (G, S, US): Aucayacu. 10
Sep 1965 (l'r). Schunke V. 847 (COI,, F, NY, US). l , o f
eto: Jenaro Herrera, iiap. Arboretum, 25 Oct I994 (ft'),
Chatrou et al. 1 ( A M A Z , U. USM. WU): Yurimaguas,
lower Rio Huallaga. 23 A u g - 7 Sep 1929 (fr/. Killip &
Smith 28194 (US): La Victoria, Rio Amazonas. 9 May
1929 (fr). Williams 3076 IF). M a d r e de Dios: 10-15
km N N W of Shintuya, 8 Dec 1985 (fi'). P'oxter et al.
10662 (E U): Parque National del Man6. 14 Oct 1986
(ytl), Foster et al. 11824 (UI. Paseo: Iscozacin Distr.,
BRITTONIA
198
80
70
[VOL. 51
60
50
8
....
~3___~
"...o
~ o .
_~*_. . . . . . . . . . .
I
0
o
.5;."
"x.
o
.//
f
11 /
......JL_
11
l
1
Fusaea /on
70
80
FIG. 8.
Distribution
GO
of
50
Fusaea long(folia a n d F. peruviana.
.4D
1999]
C H A T R O U & HE: A N N O N A C E A E
22 Oct 1986 (fl). Pariona & Rut: 1037 (t" MO, U).
Ucayali: Bosque National Alexander ,,'on Humboldt,
13 Feb 1981 fir). Gent 0' et al. 31306 (MO).
BRAZ[I,. Acre: Mun. Cruzeiro do Std, branch of
A~ude. 5 km from Vila Rodrigues Alves, 12 Nov 1991
(fl) C i d e t al. 10719 {UL A m a p R : Rescrva incra, Rio
Falsino. 2 2 - 2 6 Aug 1983 ( i l l Campbell et al. 14575
~U); Mun. Oiapoque, 60 km SSE of Oiapoque. 1 Dec
1984 (fl), Mort et aL 17100 (NY, U). A m a z o n a s : K m
124 of M a n a u s - P o r t o Velho Hwy., 25 Mar 1974 (IlL
Campbell et al. P20923 NY, U, US): Rio Solim6es,
mouth of Rio Jutaf, 20 Nov 1927 (ill Ducke R B I 9 6 2 3
(RB, S): Mun. Fonte Boa, Paran,'i do M a m u p m a , Grecf,
1 Nov 1986 (fl), CM et al. &173 (U): I,ago do Jumt/,
Parintins region, 2 Feb 1957 ( i l l Frdes 33104 (S): km
155 of Manaus-Itacoatiara Rd.. 16 Dec 197,1 fir), Gentry & Ramos 13345 (MO, U): Mun. Sao Paulo de Olivenqa, basin of Rio Solim6es. near Palmares. 11 S e p 26 Oct 1936 (fl). K r u k o f f 8 0 8 6 (A, B, BR, E G, MICIt.
MO. NY. R S, U, US); basin of Rio Dement, vic. o f
Tototobf, 2 Mar 1969 (fr). Prance et al. 10394 ( A A U
GH, MO, NY, S, US); Mt, n. Barcelos, 10 Jul 1985 (ft.
fr), J.A, Sih,a 308 (MO. NY. SR U. US). M a r a n h f i o :
Mun. Monv,So. basin of Rio Turiaqu, Ka'apor Indian
Reserve, 31 Jan 1985 (fl), Bah;e & Ribeiro 155 (NY.
U): Rio Alto Turia~:u, Nova Esperan~:a. 29 Nov 1978
(fl). Jangoux & Bahia 46 (NY, U). M a t o Grosso: Rio
Aripuanfi, at base of Salto dos Dardanelos, 13 Oct
1973 (ill Berg et al. P I 8 4 7 9 (NY, U, /IS): Rio Aripuanfi, margin of new airstrip o f Humboldt Centre, 10
Oct 1973 (tt, fr), Prance et al. 18384 (NY. U. US).
ParR: Km 103 of Santardm Ruropolis Hwy.. 4 Feb
1976 (ill Bamps 5313 (BR, NY); Acarfi, Fazenda Borba Gato, near Rio Acarfi, 1980 (fr), Daly et al. 866
(U); Peixeboi, 22 Oct 1926 ( i l l Ducke RB19622 (K,
RB, S): Breu Branco, Rio "Ik~cantins, Sep 1948 (fr),
Fr6es 23567 (GH. NY); Mocambo, E M B R A P A Forest
Reserve. 10 km fi'om Beldm, 14 Nov 1984 (fl), Gento"
48971 (U); Rio .lari, Serra de Monte Dourado, 16 Nov
1967 (fr), E. Oliveira 3545 (NY)" Mun. Paragominas,
17 km S of Ligas~o do Par& 1 Mar 1980 (fl), Plowman
et al. 9426 (F GH. MICH. MO, NY, U). Rio de J a neiro: Without locality, without date, E. Pereira s.n.
(ECON, probably cultivated). R o n d 6 n i a : Angustura,
Rio Machado region. 5 Dec 1931 fir), Kruk{?/J" 1537
(A, G, MIClt, NY. MO. S, U): 16 km from Vilhena
on rd. to Colorado, 31 Oct 1979 (fl fr), Nelson 332
(MICH, MO. NY, U); basin of Rio Madeira, Serra dos
Tres lrrn~os, opposite M u t u m p a r a n & 29 Nov 1968 ( i l l
Prance et al. 8973 (NY. U, US). Roraima: Serra da
Lua, 21 Jan 1969 (ytl). Prance et al. 9367 (NY, U);
Indian trail from Surucucu, between Maitfi and Indian
village Paramiteri, 17 Feb 1971 (fl. fr), Prance et al.
10595 (NY); k m 329 of M a n a u s Caracarai Hwy., 17
Nov 1977 {ill & e w a r d et aL 47 (MO. NY, U).
BOLIVIA. Bent: Km 13 of Riberalta-Guayaramerin
rd., 19 Nov 1989 ( i l l Daly et al. 6260 (MO, U); Cachnela Esperanza. Rio Bent. Nov 1923 (ill Meyer 134
(U, Z). C o c h a b a m b a : Km 240 of Santa Cl~z-Villa
Tunari Hwy., 11 Jul 1989 (fl), Smith et al. 13683
(MO). P a n d o : S bank of Rio Abunfi, 5 km above
mouth, 14 Nov 1968 (fl), P r a n c e et al. 8441 {NY. U);
30 km S W of Cobija on the rd. to Naraueda, 14 A u g
1982 (ylt). Sperling & King 6613 (U).
199
Vernacular names.--Colombia: An6n
de monte, cargadero amargo, chirimoyo,
nagu'i cuerinegro, yaya; Venezuela: majagua; Suriname: bergipanta, boszuurzak,
jari-jari, langbladige jari-jari, panta (Sranang dialect), peperhout; French Guiana:
aza odou (Saramaka dialect), k ~ w ~ a l a
(Way~pi dialect), maichi (Paramaka dialect), mille mamanyaret, mamanyar6, maman-yaw6 (Cr6ole dialect), pinaioua (Carib
dialect), yawlyiki (Wayaipi dialect),
yanw'kala, yanwicara (Oyampi dialect);
Ecuador:
nanguehue,
moncapatahue
(Waorani dialect); Peru: anona masha, bara
caspi, chirimuya, espintana, tortuga caspi,
yeis (Huambisa dialect); Brazil: araticum,
ata, birib& envira, envira ata, envira-menjuba, envireira, espintana, kar~tt~'y, latoure
(Mucajaf-Uaicfi dialect), pimiyw-hu (big
fish hook tree).
Uses.--The bark is used for making
shoulder straps for porters (Colombia, Duke
11066), and for treating diarrhea (Brazil,
Balde & Ribeiro 2885). The wood is used
to make "takaris," poles for pushing canoes (French Guiana, de Granville 6445,
Oldeman & Sastre 107), is used as firewood
(Brazil, Balde & Ribeiro 2885), and for
construction purposes (Brazil, Balde & Ribeiro 1390, 1414) The fruit is edible (Brazil, a.o. BalYe & Ribeiro 1414), a use also
reported from French Guiana by Aublet
(1775).
FUSAEA PERUVIANA R. E. Fr., Acta Horti
Berg. 12(2): 273. 1937. TYPE: PERU.
Loreto: Yurimaguas, Rio Huallaga, 13
Feb 1924 (fl), J.G. Kuhlmann RB24362
(HOI.OTVPE: S; ~sorYPE: RB-n.v.). (Fig. 4)
Trees, 5-15 m tall, 2-15 cm diam. Young
twigs, petioles, and lower side of lamina
and primary vein sparsely to densely covered with yellowish, appressed to erect
hairs to 0.8 mm long, the shorter ones curly.
Petioles 3-8 mm long, 2-4.5 mm diam.
Lamina of larger leaves oblong-obovate,
narrowly obovate to obovate, 10-40 • 3 14 cm, length/width ratio 2.5-4, chartaceous, acumen 5-50 mm long, 10-20 secondary veins on either side of primary vein,
angles with primary vein 50-75 ~, smallest
distance between loops and margin I-3
200
BRITTONIA
mm, number of percurrent tertiary veins
(12-)14-16(-19), Inflorescences 1-3-flowered. I n d u m e n t : p e d u n c l e s , p e d i c e l s , b r a c t s ,
a n d o u t e r s i d e o f s e p a l s s p a r s e l y to d e n s e l y
c o v e r e d w i t h w h i t i s h to y e l l o w i s h , app r e s s e d to erect, s o m e t i m e s c u r l y h a i r s to
0.7 m m l o n g , i n n e r side o f s e p a l s g l a b r o u s ,
o u t e r side o f p e t a l s t o t a l l y c o v e r e d w i t h
w h i t i s h - s i l v e r y to y e l l o w i s h , a p p r e s s e d
hairs to 1.2 m m long, i n n e r side o f p e t a l s
t o t a l l y c o v e r e d w i t h w h i t i s h to y e l l o w i s h ,
a p p r e s s e d h a i r s to 0.5 m m long, b a s a l 88
glabrous. Peduncles 1-5 mm long, 3-4 mm
diam., fruiting peduncles 2-5 mm long, 36 mm diam. Pedicels 14-22 mm long, 2-3
mm diam., fruiting pedicels 18-22 mm
long, 5 - 7 m m d i a m . U p p e r b r a c t d e p r e s s e d
o v a t e , 3 - 4 m m long. F l o w e r b u d s c o m p r e s s e d o v o i d , to 18 m m d i a m . F l o w e r s
c r e a m y to y e l l o w i s h w h i t e (in v i v o ) . S e p a l s
o v a t e to b r o a d l y t r i a n g u l a r - o v a t e , 1 0 - 1 3 •
1 3 - 1 6 m m , a p e x acute to r i g h t - a n g l e d . P e t als c o n n a t e f o r b a s a l 1/~, o u t e r p e t a l s r h o m b i c - o b o v a t e to obtrullate, 2 4 - 3 5 • 8 - 1 3
m m , a p e x a c u t e to o b t u s e , i n n e r p e t a l s o b trullate to b r o a d l y obtrullate, 2 0 - 4 0 • 1 5 20 m m , a p e x a c u t e to obtuse. T o m s flat to
s l i g h t l y c o n v e x , w i t h c o n c a v e center. S t a m i n o d e s ca. 40, p a l e y e l l o w (in v i v o ) , o b long-obovate, narrowly triangular-obovate
to o b t r u l l a t e , 3 . 5 - 5 x 1 . 5 - 2 m m , a p e x a c u t e
to n e a r l y r o u n d e d . S t a m e n s 2 0 0 - 3 0 0 , p a l e
y e l l o w (in v i v o ) , 2 . 5 - 3 . 5 m m l o n g , p r o longed connective 0.4~0.6 • 0.8-1.4 mm.
Carpels 30-100, immersed into concave
part o f floral r e c e p t a c l e , o v a r y 2 - 2 . 5 m m
l o n g , s t y l e 2 - 2 . 5 m m long, s t i g m a d e n s e l y
to t o t a l l y c o v e r e d w i t h hairs to 0.4 m m
long. F r u i t g r e e n to w h i t i s h (in v i v o ) , 5 - 8
c m d i a m , , fertile c a r p e l s 3 0 - 6 0 , a r e o l e s
h e x a g o n a l , s t r o n g l y t u b e r c u l a t e to n e a r l y
s m o o t h , t u b e r c l e s 2 - 5 m m high, g l a b r o u s
or s p a r s e l y to d e n s e l y c o v e r e d w i t h w h i t i s h
to y e l l o w i s h h a i r s to 0.2 m m l o n g o n tubercles. S e e d s ( n a r r o w l y ) o b o v o i d , 1 4 - 2 2
mm long, 7-8 mm diam., reddish brown,
aril 2 - 3 . 5 m m high.
Distribution,
habitat,
and phenology.--
D i s t r i b u t e d in the n o r t h e r n a n d c e n t r a l p a r t
o f A m a z o n i a n Peru, a n d a d j a c e n t p a r t o f
E c u a d o r a n d B r a z i l i a n A m a z o n a s (Fig. 8).
G e n e r a l l y in n o n - i n u n d a t e d , s o m e t i m e s in
i n u n d a t e d ( i g a p 6 ) forest; on s a n d y o r lat-
[ V O L . 51
eritic soil, at a l t i t u d e s f r o m 100 to 300 m.
Flowering specimens have been collected
all the y e a r r o u n d , fruiting s p e c i m e n s m a i n l y f r o m O c t o b e r to A p r i l .
Representative specimens examined. ECUADOR.
Morona Santiago: Taisha, Rio Panguientza, 5 km NW
of military camp, 21 Jun 1980 (fl), Brandbyge & Asanza C. 32184 (AAU).
PERU. Amazonas: Quebrada Huampami, Tseasim,
3 Apr 1973 (fl, fr), Ancuash 152 (MO); Rio Cenepa,
E of Huampami community, 19 Dec 1972 (fl), Berlin
637 (U); Rio Santiago, 2 km from Caterpiza, l 1 Oct
1979 (fl), Huashikat 880 (MO, U); ibidem, without
date (fr), Huashikat 177lA (MO); ibidem, 19 Nov
1979 (fr), Huashikat 1326 (MO); Distr. Imaza, Yamayakat community, Rio Marafion, 16 Mar 1995 (fl, fr),
Jaramillo et al. 617 (U). Hu~inuco:W Sira Mtns., 26
km S of Puerto Inca, Panguana Biological Field Station, 1 Feb 1993 (fl), Listabarth & Vdsquez 11-1293
(U); ibidem, 20 Oct 1994 (yfr), Rainer 244 (U);
Bosque Nacional de Iparia, 19 Dec 1966 (fl, fr), Schunke V. 1362 (COL, E G, NY, S, US). Loreto: Rio Napo,
Sucusari, 3 Nov 1994 (fl, fr), Chatrou et al. 7 (AMAZ,
NY, U, USM, WU); Pevas-Pijuayal, 11 Mar 1986 (fr),
Dfaz et al. 50 (U); Andoas, Rio Pastaza near Ecuador
border, 15 Aug 1980 (fl, fr), Gentry, et al. 29779 (E
MO, U); San Antonio, Rio Itaya, 12 Dec 1982 (fl, fr),
Vdxquez & Jaramillo 3546 (AMAZ, MO, TEX, U,
USM); Miraflores, Quebrada Tamshiyacu, 21 Feb 1986
(fr), Vdsquez & Jaramillo 7184 (AMAZ, MO, U); Rio
Esperanza, 10 Mar 1986 (fr), Vdsquez & Jaramillo
7302 (AMAZ); Nauta, rd. to Iquitos, 9 Dec 1986 (fl),
V4squez & Jaramillo 8506 (MO); ibidem, 9 Dec 1986
(fr), Vdsquez & Jaramillo 8507 (MO); km 44 of Iquitos-Nauta Rd., 12 Dec 1988 (fl, fr), Vdsquez & Jaramillo 11378 (MO, U, USM). Ucayali: Bosque Nacional Alexander von Humboldt, 30 Jan 1980 (fl), Begazo 92 (MO, U); Atalaya, confluence of Rio Urubamba and Rio Tambo, 7 Mar 1981 (fl), Reynel 151 (E U);
Coronel Portillo, Bosque Nacional Alexander yon
Humboldt, 1 Mar 1983 (fl, fr), Vdsquez 3888 (MO, U,
USM).
BRAZIL. Amazonas: Vila Bittencourt, Rio Japur4,
19 Nov 1982 (fl), Amaral et aL 594 (NY).
Vernacular
names
and
uses.--eeru:
Achmina, icoja, yeis, yugkuanim, yumi
yafs. T h e w o o d is u s e d for h o u s e c o n s t r u c tion (Peru, H u a s h i k a t 1 7 7 1 a ) .
Acknowledgments
T h e a u t h o r s t h a n k the c u r a t o r s o f A ,
A A U , A M A Z , B, B R , C, CAY, C O A H ,
C O L , E, E C O N , E G, G H , H U A , K, L, L L ,
M I C H , M O , NY, P, R B , S, SP, S P E T E X ,
U, U C , U S , U S M , W I S , W U , a n d Z for
kindly providing herbarium specimens on
loan; H e i m o R a i n e r a n d L u b b e r t W e s t r a for
m a n y s u g g e s t i o n s a n d fruitful d i s c u s s i o n ;
1999]
C H A T R O U & HE: A N N O N A C E A E
Hendfik Rypkema for preparing the drawings; Iris van Woerden and Dewanand Makhan for technical assistance; Paul Maas and
Jifke Koek-Noorman for comments on the
manuscript; and Christian Listabarth, Heimo Rainer, and Paul Maas for providing
slides. Critical review by David M. Johnson, Nancy A. Murray, and George E.
Schatz is gratefully acknowledged. This
study was supported by the Netherlands Organization for Scientific Research (NWO;
grant no. 805-40.201), and by the Faculty
of Biology, Utrecht University.
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B. L u g a r d o n & J. A. Doyle9 1994. Pollen
ultrastructure and relationships of Fusaea (Baillon)
Safford and Duguetia A. Saint-Hilaire (Annonaceae). Rev. Palaeobot. Palynol, 83: 55-64.
L o u r e i r o , A. A. 1969. Contribui~fio ao estudo anat6mico da madeira de Anonficeas da Amaz6nia. Boletim do INPA, Boffmica 30: 1-10.
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M a a s , P. J. M. 1995. Pages 413-415.11,: J. A. Steyermark, P E. Berry & B. K. Holst, editors. Flora
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Dicotyledons. I. Clarendon Press, Oxford.
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known species. Contr. U.S. Natl. Herb. 18: 1-68.
S e h a t z , G. E. & A. Le T h o m a s . 1993. Annonaceae:
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Osterreichische Akademie der Wissenschaften, Vienna.
List of Exsiccatae
1 = Fusaea
longifolia (Aubl.) Saff.; 2 = Fusaea peruviana
R. E. Ft.; items
with an asterisk (*) indicate vouchers for leaf anatomical studies.
Albuquerque, B. W. P. de & L. E Co61ho, 379 (1).
Amaral, I. L. et al., 326 (1); 594 (2); 1244, 1336 (1).
Ancuash, E., 152 (2).
Anderson, W. R., 11885 (1).
Asplund, E., 12730 (1).
Assunq~o, P. A. C. L. & E. Pereira, 269 (1).
Aublet, J. B. C. E, s.n. (1).
Aubr6ville, A., 266 (1).
Aulestia, M. [et al.], 3000, 3004, 3099, 3254, 3498 (1).
Balge, W. L. & B. G. Ribeiro, 155, 329, 341,445,497,
683, 1390, 1414, 2885, 3012 (1).
Bamps, P., 5165, 5203, 5221, 5313, 5329, 5364 (1).
Barrier, S., 4016, 4037, 4046, 4355 (1).
Beck, H. T. et al., 502 (1).
Begazo, N., 92* (2).
Benoist, R., 650 (1).
Berg, C. C. et al., P18441, P18479, P18535 (1).
Berlin, B., 637 (2).
Black, G. A., 56-18883 (1).
Boom, B. M. & S. A. Mori, 1712 (1).
Brandbyge, B. & C. Asanza, 32184 (2).
BW ( = B o s c h w e z e n Suriname), 2478, 2626, 2727,
4532, 5593 ( 1).
Callejas, R. et al., 5415 (1).
Campbell, D. G. et al., 6449, 9883, 10212, 14439,
14486, 14575, 14633, 14669, 14738, 15134, P20923
(1).
Cfirdenas, D., 266, 690, 1003, 1954, 2038 (1).
Cavalcante, R B., 795 (1).
Chatrou, L. W. et al., 1, 2 (1); 7* (2).
Chota, M. [et al.], 4/93, 8/688 (1).
Cid E, C. A. [et al.], 1105, 1436, 1619, 1654, 1895,
2179, 2373, 6028, 6978, 8245, 8373, 9783, 9809,
10645, 10719 (1).
Co61ho, L. E, 79 (1).
Cordeiro, E. & J. E Silva, 206 (1).
Cremers, G., 11592, 11611 (l).
Daly, D. C. [et al.], 866, 1032, 3890, 3984, 5692, 6260
(l).
Diaz, M., 103 A (1).
Diaz, E et al., 50 (2).
Dionizia, E et al., 83 (1).
Donselaar, J. van, 1394 (1).
Duarte, A. E, 6974, 9817 (1).
marked
Ducke, A., MG7978, RB17867, RB19622, RB19623
(1).
Duke, J. A., 11066 (1).
Duque-Jaramillo, J. M., 2384, 2429 (p.p.), 2495 (1).
Evrard, C., 9631 (1).
Fernfindez, A. & E. Sanoja, 5071 (1).
Foldats, E. & J. Velazco, 9137 (1).
Fonnegra, R. & E. Renterfa A., 1096 (1).
Forest Dep. Brit. Guiana, 2132 (1).
Foster, R. B. et al., 8933, 10662", 10992, 11824 (1).
Freitas, C. A. A., 64 (1).
Fr6es, R. L., 20778, 23567, 28383, 32366, 33104,
34340 (1).
Gentry, A. H. [et al.], 13345, 20070, 26032 (1); 29779
(2); 31306, 46852, 48971, 56001, 56046, 61959,
62986, 63023, 63896, 65893 (1).
Granville, J. J. de [et al.], 312, 439, 475, 646, 1667,
2064, B.4268, B.4519, 6104, 6445, 6601, 7090 (1).
Grenand, P., 564, 2879 (1).
Gutti6rrez, V. & R. E. Schultes, 837 (1).
Hall, C. J. J. van, 9i (1).
Haught, O., 2043, 2184 (1).
Hekking, W. H. A., 1198" (1).
Henkel, T. W. et al., 4799, 5166 (1).
Heyde, N. M., 691 (1).
Huashikat, V. 880", 1326, 1771A (2); 2317 (1).
Idrobo, J. M., 8515, 8521 (1).
Jacquemin, H., 1833, 2036, 2354 (1).
Jangoux, J. & R. P. Bahia, 46, 87, 751 (1).
Jansen-Jacobs, M. J. et al., 2313, 2827 (1).
Jaramillo, J., 14822 (1).
Jaramillo, N. et al., 617 (2).
Killeen, T. et al., 3521 (1).
Killip, E. P. & A. C. Smith, 28194 (1).
Klug, G., 952 (1).
Krukoff, B. A., 1537, 8086 (1).
Kuhlmann, J. G., 389 ( RB 132083), 1975 (1); RB
24362 (2).
Kukle, P., 71 (1).
Lanjouw, J. & J. C. Lindeman, 2119 (1).
Lemge, A., s.n. (1).
Lemoult, E., s.n. (1).
Le6n, H., 97 (1).
Lepsch Cunha, N. M. et al., 905 (1).
Lescure, J. P., 150 (1).
1999]
C H A T R O U & HE: A N N O N A C E A E
Lindeman, J.C., 3531, 3632, 4738, 5026, 5801, 6742,
6957", 6983 (1).
Lindeman, J. C., A. R. A. G6rts-van Rijn et al., 533
(1).
Listabarth, C. & H. Vasquez, 11-1293 (2).
Loubry, D., 128 (1).
Maas, R J. M. et al., 6320, 7774, 7777, 8056, 8066
(1).
Maciel, U. N. et al., 386 (1).
Madrififin, S. et al., i205 (1).
Maguire, B., 40710 (l).
Martin, J., s . n . (1).
McDowell, T. D., 2106 (1).
M61inon, E. M., s . n . , 78, 86, 172, 270, 1862 (1).
Meyer, G., s . n . , 134 (1).
Mori, S. A. [et al.], 14758, 15401, 15558, 16309,
17100, 17566, 17674, 20761, 20987 (1).
Murillo, J. & O. Rom~in, 599, 610 (1).
Mutchnick, E & B. Allicock, 744 (1).
Nascimento, O. C., 350, 435* (1).
Nee, M., 42590 (1).
Nelson, B. W., 332, 938 (1).
Oldeman, R. A. A. [et al.], 51, 107, T.613, T.908,
B.830, 1205, 1923, 2385, 2987, B.3106 (I).
Oldenburger, E H. E et al., 1132 (1).
Oliveira, A. A. et al., 116 (1).
Oliveira, E., 3545, 4080 (1).
Pacheco, M. et al., 147 (1).
Pariona, W. & J. Ruiz, 1037 (l).
Pereira, E., s . n . (1).
Perrottet, G. S., s . n . (1).
Pipoly, J. J., 7487 (1).
Pires, J. M. [et al.], 3787, 4464, 4469, 51791 (1).
Plowman, T. et al., 9415, 9426, 9488, 12194 (1).
Poiteau, R A., s . n . (1).
Prance, G. T. et al., 866 (see Daly 866), 1480, 1538,
1827, 1852, 3788, 3851, 4594, 8441, 8973, 9022,
9367, 10394, 10595, 10823, 11002, 16469, 18384,
22793, 25392, 25410 (see Silva 25410), 25550 (see
Silva 25550), 25699 (see Silva 25699), 25874 (see
Silva 25874), 30253 (1).
Rabelo, B. V. [et al.], 2418, 2891, 3196 (1).
Rainer, H., 232, 244 (2).
Reeder, D. & L. Roberts, LBBI2305 (I).
Renterfa A., E. et al., 2136, 2316 (1).
Reynel R., C., 46 (1), 151 (2).
Ribeiro, J. E. L. S. et al., 1636 (1).
Ri6ra, B. 288, 977 (1).
Rimachi Y., M., 3392, 8281 (1).
203
Rivero,? , s . n . (1).
Rodrigues, W. A., 5525, 9002 (I),
Rodrigues, W. A. & D. E Co61ho, 4096, 5571 (1).
Rodrigues, W. A. & A. Loureiro, 5955 (1).
Rodrigues, W. A. & O. R Monteiro, 7373 (I).
Rodrigues, W. A. [et al.], 4096, 5525, 5571, 5955,
7373, 9002, 10573 (I).
Romero-Castafieda, R., 4119, 4933, 4935. 6252, 8403
(1).
Roosmalen, M. G. M. van, 112 (1).
Rosa, N. A. [et al.], 2704, 2720, 2723 (1).
Rudas, A. et al., 1559 (1).
Ruiz, H. & J. A. Pav6n, s . n . (1).
Sabatier, D. R. L. & M. E Prdvost, 3979 (1).
Sagot, R A., 5 (1).
Sanchez S., M. et al., 711 (1).
Sanoja, E., 2467 (1).
Santos, M. R., 36 (1).
Sastre, C. H. L. [et al.], 80, 4376, 4562 (1).
Schultes, R. E. let al.], 6954, 16039", 18684 (1).
Schulz, J. P., 7967, 9315 (1).
Schnnke V., J. M., 847 (1); 1362 (2); 6570, 10533 (1).
Service Forestier, 7125, 7137, 7216, 7251 (1).
Silva, A. S. et al., 25410 (see Prance 25410), 25550
(see Prance 25550), 25699 (see Prance 25699),
25874 (see Prance 25874).
Silva, J. A., 308 (1).
Silva, M. G. let al.], 2457, 3993 (1).
Silva, N. rE let al.], 82, 1771, 4622 (1).
Smith, A. C., 2779 (1).
Smith, D. N. et al., 13683 (1).
Solomon, J. C., 6173 (1).
Sothers, C. A. [et al.], 650, 740 (1).
Sperling, C. R. & S. King, 6613, 6648 (1).
Spichiger, R. et al., 1767, 1769 (1).
Steward, W. C. et al., 47, P20271, P20361 (1).
Stoffers, A. L. et al., 315 (1).
Tjon Lira Sang, R. J. M., LBB16270 (1).
Toledo, C. B. et al., 167 (1).
Trichon, V., 13 (1).
Valencia, R. et al., 67440, 68251 (1).
Vfisquez, R. [et al.], 1005, 2084 (1); 3546, 3888, 7184,
7302, 8506, 8507, 11378 (2).
Veyret, Y. 1508 (1).
Vicentini, A. [et al.], 396, 463A, 732 (I).
Villiers, J. E, 4357, 4358, 4370, 4464 (1)_
Wachenheim, G., s . n . , 129, 361, 371, 433 (1).
Williams, LI., 3076 (1).
Zarucchi, J. L. let al.], 1607, 4250 (1).
Zuluaga R., S., 983 (1).
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