nueces del brasil

8/12/2019 Nueces Del Brasil

1/22

A morphological cladistic analysis of Lecythidoideaewith emphasis on Bertholletia , Corythophora , Eschweilera ,and Lecythis

YA-YI HUANG1 , SCOTTA. MORI2 , AND LAWRENCE M. K ELLY3

1 The New York Botanical Garden, 2900 Southern Blvd., Bronx, NY 10458-5126, U.S.A. Current address: Biodiversity Research Center, Academia Sinica, Taipei11529, Taiwan; e-mail: [email protected]

2 Institute of Systematic Botany, The New York Botanical Garden, 2900 Southern Blvd., Bronx( NY10458-5126, U.S.A.; e-mail: [email protected]

3 The New York Botanical Garden, 2900 Southern Blvd., Bronx( NY 10458-5126, U.S.A.;e-mail: [email protected]

Abstract . A cladistic analysis was conducted to test the monophyly of Eschweileraand Lecythis as well as to examine the relationships of these two genera and their close relatives Bertholletia and Corythophora . The study included 86 species, represent-ing all four genera and covering the range of taxonomic and morphological variation inthe genera. The data matrix included 49 parsimony-informative characters derived fromvegetative, oral, fruit, and seed morphology and anatomy. The results based on theconsensus of all most parsimonious trees indicate that Bertholletia , Corythophora , Eschweilera , and Lecythis form a clade supported by brachyparacytic stomata, theabsence of pedicels (with subsequent reversals in several clades), a two or four-locular ovary, the presence of an aril, and the absence of cotyledons. Within the

clade, the monophyly of Corythophora is supported by the presence of inores-cence scales and the absence of nectar. Eschweilera is monophyletic only if E .congesti ora and E . simiorum are excluded. The monophyly of Eschweilera issupported by the presence of a two-locular ovary. Lecythis is not monophyletic, but sections Corrugata , Pisonis , and Poiteaui are monophyletic. Three species of section Lecythis are more closely related to Eschweilera, and other species of section Lecythis along with Bertholletia excelsa remain as unresolved.

Key Words: Bertholletia , Corythophora , Eschweilera , Lecythis , Lecythidoideae,zygomorphy.

Lecythidaceae are small to large trees that grow in lowland rainforest (Mori & Prance,1990 b). The family consists of three subfa-milies (Mori et al., 2007): Foetidioideae,Planchonioideae, and Lecythidoideae. TheFoetidioideae consists of 17 species in onegenus. These species are found in East Africa,Madagascar, and Mauritius (Mori et al.,2007). The Planchonioideae consists of 59species in six genera. They are found in tropicalAsia, tropical Africa, Australia, and the PacicIslands (Mori et al., 2007). The Lecythidoideaeconsists of ca. 210 species in 10 genera (Prance

& Mor i, 1979; Mori & Prance, 1990 b; Mori et al., 2007; Huang et al., 2008). Species of the Lecythidoideae are conned to tropicalAmerica. The Lecythidaceae is monophyleticand each of the subfamilies is monophyletic(Morton et al., 1998;Morietal.,2007; APG III,2009). The relationships within the subfamilies,however, are not fully understood, especiallywithin the Lecythidoideae.

Lecythidoideae includes both endemics withnarrow distributions and widespread taxa. Theyoccupy diverse habitats but are most abundant in non- ooded primary forests (Mori & Prance,

Brittonia , 63(3), 2011, pp. 396 417 ISSUED: 1 September 2011 2011, by The New York Botanical Garden Press, Bronx, NY 10458-5126 U.S.A.


2/22


3/22

they are found mostly north of the AmazonRiver (Fig. 23 in Mori & Prance, 1990 b).

Eschweilera was rst described by DeCandolle (1828). Martius (1837) accepted Eschweilera as a genus and listed severalfeatures of Eschweilera distinct from Lecy-this (e.g., bilocular ovary). However, manysubsequent au thors s t il l cons idered Eschweilera as part of Lecythis (Endlicher,1840; Berg, 1856, 1857, 1858). In 1874,Miers maintained the generic status of Eschweilera and provided a list of featuresthat distinguished Eschweilera from Lecy-this . The generic status of Eschweilera hasnot changed since then. Eschweilera is thelargest and the most widely distributedgenus of Lecythidoideae. Species of Eschweilera range from Veracruz, Mexico,to Rio de Janeiro, Brazil (Fig. 25 in Mori &Prance, 1990 b).

In the present study, a cladistic analysis based on morphological and anatomicalcharacters was performed. The objectivesof this paper are to examine the monophyly of Eschweilera and Lecythis and tostudy the phylogenetic relat ionshipswithin the Bertholletia clade. To carry

out these objectives we reexamined andrede ned the characters used in previousclassi cations (Prance & Mori, 1979;Mori & Prance, 1990 b). In addition, weincluded more parsimony-informativecharacters than the non-molecular charac-ters used in Morton et al. (1998) andmore taxa of the Bertholletia clade thanMori et al. (2007).

Methods and materials

Sampling. This study included 86 ingrouptaxa, representing Bertholletia , Corytho- phora , Eschweilera , and Lecythis . Taxonsampling covers the range of morphologicalvariation in genera and sections recognized by Mori and Prance (1990 b). Fourteenspecies were included as outgroup taxa,representing Gustavia , Grias , Allantoma ,Cariniana , Couroupita , and Couratari . Theselection of the outgroup taxa followed themolecular analysis of plastid ndhF andtrnL-F sequence data, but with fewer species for each genus (Mori et al., 2007).

The taxonomy follows Prance and Mori(1979) and Mori and Prance (1990 b). Thesampled taxa are listed in Table I.

Data collection. Morphological and ana-tomical characters were collected based onoriginal observations in the eld and theimages available on the Lecythidaceae Pages(http://sweetgum.nybg.org/lp/index.html).Some characters were derived from theliterature, herbarium specimens at INB, INPA,MO, NY, and US, or pickled collections at NY.

Leaf fragments used for study of venation patterns and stomata were placed in vialswith 50% alcohol and bathed in boilingwater for ten minutes. This procedure wasrepeated two or three times until no further color leached into the solution. After cool-ing to room temperature, samples werewashed with water two or three times, andthen changed to a 2% NaOH solution. The NaOH solution was replaced every dayuntil the mesophyll of the leaf becametransparent. After clearing, the sampleswere washed with water to remove NaOHresidue. The specimens were then mountedin Hoyer s mounting medium. Alternatively,

samples were put in a 5% bleach solutionuntil the stomata were visible when viewedwith a compound microscope. Anatomicaland morphological leaf features followedthe terminology the Leaf ArchitectureWorking Group (1999).

Pollen morphology was studied usingscanning electron microscopy (SEM). Pol-len samples were taken from herbariumspecimens with mature owers or ower buds at an advanced stage of development.Flowers were boiled until softened and,with aid of a dissecting microscope, antherswere removed from the staminal ring andthe ligule for species that have ligular anthers. The anthers were air-dried and pollen was then shed and mounted directlyonto a SEM stub and coated with gold. Thecoated pollen was observed with a HitachiS2700-SEM.

Characters were divided into two or morediscrete states. All multi-state characters werecoded as non-additive. The following 49characters were included in the analysis. Thedata matrix is shown in Table II.

398 BRITTONIA [VOL 63
http://sweetgum.nybg.org/lp/index.htmlhttp://sweetgum.nybg.org/lp/index.htmlhttp://sweetgum.nybg.org/lp/index.html


4/22

TABLE ILIST OF SAMPLED TAXA (NO. OF SAMPLED/NO. OF TOTAL

SPECIES). TAXA WITH * ARE TYPE SPECIES OF THE GENUS OR SECTION; TAXA WITH ** ARE TYPE SPECIES OF BOTH SECTION

AND GENUS.

Bertholletia Bonpl. (1/1) B. excelsa Bonpl.

Corythophora R. Knuth (4/4)C. alta R. Knuth*C. amapaensis Pires ex S. A. Mori & PranceC. labriculata (Eyma) S. A. Mori & PranceC. rimosa W. Rodrigues subsp. rimosaC. rimosa W. Rodrigues subsp. rubra S. A. Mori

Eschweilera Mart. ex DC (55/93)Section Tetrapetala S. A. Mori (3/3) E. alvimii S. A. Mori E. tetrapetala S. A. Mori* E. compressa (Vellozo) Miers

Section Bracteosa S. A. Mori (2/4) E . bracteosa (Poeppig ex O. Berg) Miers* E . cyathiformis S. A. Mori

Section Jugastrum Prance & S. A. Mori (1/1) E . tenuifolia (O. Berg) Miers*

Section Eschweilera S. A. Mori & Prance (49/85) E. aguilarii S. A. Mori E . alata A. C. Sm. E . albi ora (DC.) Miers E . amazonica R. Knuth E . amazoniciformis S. A. Mori E . amaplexifolia S. A. Mori E . andina (Rusby) J. F. Macbr. E . antioquensis Dugand & Daniel E . apiculata (Miers) A. C. Sm. E . atropetiolata S. A. Mori E . bi ava S. A. Mori E . calyculata Pittier E . caudiculata R. Knuth E . chartaceifolia S. A. Mori E . collina Eyma E . congesti ora (Benoist) Eyma E . coriacea ( DC) S. A. Mori E . correae sp. ined. E . decolorans Sandwith E . grandi ora (Aubl.) Sandwith E . hondurensis Standley E . integrifolia (Ruiz & Pav. ex Miers) R. Knuth E . jacquelyniae S. A. Mori E . juruensis R. Knuth E . laevicarpa S. A. Mori E . longirachis S. A. Mori E . mexicana T. Wendt, Mori & Prance E . micrantha (O. Berg) Miers E . nana (O. Berg) Miers E . neei S. A. Mori E . ovalifolia (DC) Nied. E . ovata (Cambess.) Mart. ex Miers E . panamensis Pittier E . parvi ora (Aubl.) Miers E . parvifolia Mart. ex DC.** E . pedicellata (Richard) S. A. Mori E . pittieri R. Knuth E . pseudodecolorans S. A. Mori E . rankiniae S. A. Mori

TABLE I(CONTINUED).

E . rimbachii Standl. E . sagotiana Miers E . sessilis A. C. Sm. E . simiorum (Benoist) Eyma E . subglandulosa (Steud. ex O. Berg) Miers E . tessmannii R. Knuth E . tresoriana sp. ined. E . truncata A. C. Sm. E . wachenheimii (Benoist) Sandwith

Lecythis Loe ing (25/27)Section Corrugata S. A. Mori (5/5) L. conferti ora (A. C. Sm.) S. A. Mori L. corrugata Poit.* L. idatimon Aubl. L. persistens Sagot subsp. aurantiaca S. A. Mori L. persistens Sagot subsp. persistens L. pneumatophora S. A. Mori

Section Pisonis S. A. Mori (4/4) L. ampla Miers L. lanceolata Poiret L. pisonis Cambess.* L. zabucajo Aubl.

Section Poiteaui S. A. Mori (3/3) L. barnebyi S. A. Mori L. brancoensis (R. Knuth) S. A. Mori L. poiteaui O. Berg*

Section Lecythis S. A. Mori (13/15) L. alutacea (R. Knuth) S. A. Mori L. chartacea O. Berg L. gracieana S. A. Mori L. holcogyne (Sandwith) S. A. Mori L. lurida (Miers) S. A. Mori L. mesophylla S. A. Mori L. minor Jacq. L. ollaria Loe ing** L. parvifructa S. A. Mori L. prancei S. A. Mori L. retusa Spruce ex O. Berg L. schomburgkii O. Berg L. tuyrana Pittier

Outgroup taxaGustavia speciosa (Kunth) DC.Grias peruviana Miers Allantoma decandra (Ducke) S. A. Mori, Y.-Y. Huang

& Prance Allantoma integrifolia (Ducke) S. A. Mori, Y.-Y. Huang& Prance Allantoma lineata (Mart. ex O. Berg) MiersCariniana estrellensis (Raddi) KuntezCariniana pyriformis MiersCouratari guianensis Aubl.Couratari macrosperma A. C. Sm.Couratari multi ora (Sm.) EymaCouratari stellata A. C. Sm.Couroupita guianensis Aubl.Couroupita nicaraguianensis DC.Couroupita subsessilis Pilg.

399HUANG ET AL.: MORPHOLOGICAL ANALYSIS OF LECYTHIDOIDEAE2011]


5/22


6/22


7/22

1. Wood color. 0= sapwood not distinct from heartwood,1= sapwood distinct from heartwood. Wood color is pale-yellow to tan without distinction between sap-wood and heartwood in Gustavia , Grias , Couroupita ,and Couratari . In contrast, the heartwood varies fromreddish to chocolate brown and the sapwood is pale in Allantoma , Cariniana , Corythophora , Bertholletia , Eschweilera , and Lecythis (Zeeuw, 1990).

2. Oxidation of wounded tissues. 0= absent, 1= present.Wounded tissues oxidize and turn blue in species of Couroupita , some species of Lecythis (e.g., Lecythis pisonis Cambess. and its relatives), and a few species of Eschweilera (e.g., Eschweilera decolorans Sandwith).Thecolor change is most distinct in woundedowers andfruits.

3. Leaf pubescence, abaxial surface. 0= glabrous, 1= pubescent. Some species of Couratari section Echi-nata Prance and Couratari section Couratari Prancehave stellate hairs on the abaxial leaf surface. Theabaxial leaf surface is glabrous in all other species of the Lecythidoideae, including species of Couratarisection Microcarpa Prance.

4. Leaf punctations, abaxial surface. 0= absent, 1= present.Many species of Eschweilera have black, brown, or reddish-brown dots on the abaxial leaf surface. Thesedots sometimes are referred to as cork warts (Roth, 1984;Fig. VII-4 in Mori & Black, 1987).

5. Leaf papillae, abaxial surface. 0= absent, 1= present.Papillae are outgrowths of the cuticle. This character isfound in Bertholletia , some species of Lecythis (e.g., Lecythis poiteaui O. Berg), and some species of Eschwei-lera (e.g., Eschweilera congesti ora (Benoist) Eyma).Mori and Black (1987) hypothesized that papillae may

have adaptive value in reducing water loss through thestomata.6. Domatia. 0= absent, 1= present. Domatia are small

cavities at the junction of the secondary vein with the primaryvein. These cavitiesareoften lined withhairs andinhabited by mites (Huang, pers. obs.). Domatia are onlyfound in some species of Cariniana (e.g., Carinianaestrellensis (Raddi) Kuntze).

7. Venation type. 0= eucamptodromous, 1= brochidodr-omous. In eucamptodromous venation, the secondaryveins curve upward and gradually diminish apicallyinside the margin without forming prominent arches(Fig. 29.3 in Leaf Architecture Working Grou p, 1999).In brochidodromous venation, the secondary veins join together in a series of prominent arches (Fig. 29.1in Leaf Architecture Working Group, 1999). Theeucamptodromous venation pattern is found in speciesof Allantoma . All other genera have brochidodromousvenation pattern.

8. Tertiary venation. 0= percurrent, 1= reticulate. In percurrent tertiary venation, the tertiary veins cross between adjacent secondary veins in parallel pathswithout branching (Fig. 35.1 in Leaf ArchitectureWorking Grou p, 1999). In reticulate tertiary venation,the tertiary veins join with other tertiary or secondaryveins at random angles (Fig. 35.4 in Leaf ArchitectureWorking Group, 1999). The tertiary venation of species of Allantoma and some species of Gustavia ,Grias , Couroupita and Couratari are percurrent. Thetertiary venation of other species of the Lecythidoi-deae is reticulate.

9. Quaternary venation. 0= dichotomizing, 1= regular polygonal reticulate. In the dichotomizing type thefourth-order veins branch freely, i.e., they do not unite with other veins and are the nest order of venation that the leaf exhibits (Fig. 39.4 in Leaf Architecture Working Group, 1999). In the regular polygonal reticulate type, the fourth-order veins join to form polygons of similar size and shape(Fig. 39.3 in Leaf Architecture Working Group,1999). Fifth order veins are the nest venation inthis type. The fourth-order venation of Allantoma isdichotomizing. The fourth-order venation of all other species of the Lecythidoideae is regular polygonalreticulate.

10. Areolation. 0= not well developed, 1= well devel-oped. Areoles are the smallest areas of leaf tissuesurrounded by veins of any order (Leaf ArchitectureWorking Group, 1999). The areoles are dened as poorly developed if they are highly irregular in sizeand shape (Fig. 41.2 in Leaf Architecture WorkingGroup, 1999). Poorly developed areoles are onlyfound in species of Allantoma . In all other species of Lecythidoideae the areoles are well developed withfour or ve sides.

11. Stomatal type. 0= brachyparacytic, 1= anomocytic.In brachyparacytic stomata, two cells are parallel tothe long axis of the guard cells but not completelyenclosing them (Fig. 55.12 in Leaf ArchitectureWorking Grou p, 1999). In anomocytic stomata, veor more cells surround the guard cells and the cellsadjacent to the guard cells are not differentiated inany way from other epidermal cells (Fig. 55.2 inLeaf Architecture Working Grou p, 1999). Brachy- paracytic stomata are found in Allantoma , Corytho- phora , Bertholletia , Eschweilera , Lecythis , and somespecies of Couratari . Anomocytic stomata are foundin Gustavia , Grias , Cariniana , Couroupita , andsome species of Couratari .

12. In orescence scales. 0= absent, 1= present. The rachis of the in orescence is squamate in Eschweilera alvimii S.A.Mori, Eschweilera nana (O. Berg) Miers, Eschweileratetrapetala S. A. Mori and species of Corythophora .

13. Pedicel. 0= absent, 1= present. In Lecythidoideae, pedicels are absent in species with spike or spike-likein orescences; pedicels are present in species withracemose or fasciculate inorescences; and pedicelsmay or may not be present in species that have

paniculate in orescences.14. Pedicel/hypanthium surface. 0= rugose/tuberculate,1= not rugose/tuberculate. Species of Lecythissection Corrugata S. A. Mori have rugose/tuber-culate pedicels and hypanthia. This character is not found in any other species of Lecythidoideae.

15. Bract and bracteole persistence. 0= caducous, 1= persistent. The Lecythidoideae have one bract andtwo smaller bracteoles that enclose young ower buds. The bract is located at the base of the pedicelwhile bracteoles usually are on the pedicel betweenthe base and the articulation of the pedicel or arelocated at the base of the pedicel just above the bract. The bract and bracteoles are caducous in most species, but in a few species they are persistent at anthesis (e.g., Eschweilera bracteosa (Poepp. ex O.Berg) Miers).



8/22

16. Calyx lobe number. 0= entire, 1= two, 2= four, 3=ve,4= six. Bertholletia excelsa has two calyx lobes. Griasneuberthii J. F. Macbr. and Eschweilera amazonicifor-mis S. A. Mori have four calyx lobes; species of Allantoma have ve calyx lobes; and species of Cariniana , Couroupita , Couratari , Lecythis , and most species of Eschweilera have six calyx lobes. Most species of Grias have calyces that completely enclosethe bud and open circumscissilely or irregularly(Prance & Mori, 1979). For example, the calyces of Grias peruviana are entire or are split into two or four irregular lobes (Mori,1979b).Thecalyces of species of Gustavia are entire or four or six lobed (Mori, 1979a).

17. Mucilage ducts in sepals. 0= absent, 1= present. Severalspecies of Lecythis section Lecythis S. A. Mori havemucilage-bearing ducts in the sepals (e.g., Lecythisalutacea (A. C. Sm.) S. A. Mori). The composition andfunction of the mucilage is unknown.

18. Petal number. 0= four, 1=ve, 2= six, 3= eight. Speciesof Grias and some species of Eschweilera (e.g., E .tetrapetala ) have four petals; species of Allantomahave ve petals; species of Cariniana , Corythophora ,Couratari , Couroupita , Lecythis , and most species of Eschweilera have six petals; and species of Gustaviahave six, eight, or twelve petals. Gustavia speciosa inthe present study has six or eight petals.

19. Petal texture. 0= eshy, 1= not eshy. When the owersare fresh, the veins are invisible in eshy petals whenviewed with transmitted light. In contrast, the veins arevisible in non- eshy petals. The eshy petals are foundin Allantoma and Grias . The remaining genera of Lecythidoideae, with a few exceptions, have non-

eshy petals.

20. Androecial symmetry. 0= actinomorphic, 1= zygomorphic. In Lecythidoideae three genera (Gustavia , Grias ,and Allantoma ) have radially symmetrical androecia(actinomorphy) while seven genera ( Bertholletia , Car-iniana , Corythophora , Couratari , Couroupita , Eschweilera , and Lecythis ) havebilaterally symmetricalandroecia (zygomorphy).

21. Stamen tube. 0= absent, 1= present. In Gustavia ,Grias , and Allantoma , the basal portions of the

laments fuse and elongate to form a tube (Fig. 1A).The stamens arise directly from the rim of the tube inGustavia ; from the rim and the upper inner surfaceof the tube in Grias ; and from the rim and the entireinner surface of the tube in Allantoma . A staminaltube is also found in species of Cariniana ; however,one side of the tube elongates more than the other and makes the androecium slightly zygomorphic(Fig. 1B). The stamens of Cariniana also arise fromthe rim or the entire inner surface of the tube.Species of other zygomorphic-owered genera donot have a staminal tube.

22. Type of zygomorphy. 0= oblique zygomorphy, 1=zygomorphy. An obliquely zygomorphic androeciumis characterized by the presence of a staminal tube,which is formed by uneven elongation of the fused basal portions of the laments. Obliquely zygomorphic androecia are found only in Cariniana(Fig. 1B). On the other hand, a zygomorphicandroecium consists of a at, donut-shaped cushionand a strap-like structure, which is expanded fromone side of the cushion. The strap-like structurecurves over the staminal ring and the summit of theovary and is called the ligule. Zygomorphic androeciaare found in Bertholletia , Corythophora , Couratari ,Couroupita , Eschweilera , and Lecythis (Fig. 1C).Terminals with actinomorphic androecia were codedas inapplicable.

23. Staminal ring. 0= absent, 1= present. In zygomorphic- owered genera, the stamens arise from a at,donut-shape cushion and surround the style to form astaminal ring (Fig. 2). Staminal rings are found inzygomorphic- owered genera and are absent inGustavia , Grias , Allantoma , and Cariniana .

24. Ligule. 0= absent, 1= present. A ligule is a strap-likestructure expanding from one side of the staminalring (Fig. 2). The ligule is only found in zygomorphic- owered genera. In most species the distal part

FIG

. 1. Structures of different androecial types. A. Actinomorphy, Gustavia hexapetala . Drawings are modiedfrom Fig. 164 in Mori et al. (1997) and Fig. 2 in Mori et al. (2007). B. Oblique zygomorphy, Cariniana penduli ora .Drawings are modied from Fig. 70 in Prance and Mori (1979). C. Zygomorphy, Eschweilera pedicellata . Drawingsare modi ed from Fig. 85 in Mori and Prance (1990b).



9/22

of the ligule bears appendages, which are separatedfrom the staminal ring by a stamen/appendage-freearea (Fig. 2A). The only known exception is foundin Couroupita nicaraguarensis DC., which possessesa ligule without a stamen/appendage-free area(Fig. 2B). The appendage-bearing area of the liguleis de ned as the hood in Mori and Prance (1990 b).These appendages may or may not bear anthers.

25. External

ap. 0= absent, 1= present. In Couratari ,the appendage-free area of the ligule curvesinward while the appendage-bearing area of theligule (the hood) curves outward to form anexternal ap (Fig. 3). This type of androecium isnot found in any other zygomorphic-oweredgenera, in which the ligule only curves inward.

Therefore the ligule of Couratari is coded as aseparate character from the one of other zygomorphic- owered genera.

26. Coiled ligule. 0= absent, 1= present. In Bertholletia ,Couroupita , Corythophora , and most species of Lecythis , the ligule curves over the staminal ringand the summit of the ovary, but does not form a coil(Fig. 2). The appendage-bearing area of the ligule

(the hood) is on top of the staminal ring and ovary inthese species. On the other hand, in a few species of Lecythis and all species of Eschweilera , the ligulefurther curves inward to form a single, a double, or atriple coil (Fig. 4). The hood is dened as that part of the ligule extending beyond the distal end of theappendage-free ligule.

F IG . 2. Structure of zygomorphic androecium. A. Androecium of most zygomorphic-owered species (Fig. 30C inMori & Prance, 1990 b). B. Androecium of Couroupita nicaraguarensis . Note that there is no appendage-free area(Fig. 34C in Mori & Prance, 1990b).

F IG . 3. External ap of Couratari . Couratari stellata . Drawing is modied from Fig. 51 in Mori and Prance (1990b).



10/22

27. Ligular coil. 0= single, 1= double or triple. In a fewspecies of Eschweilera (e.g., E . alvimii ) and Lecythis(e.g., Lecythis minor Jacq.), the ligule curves over the summit of the staminal ring/ovary and bendsinward once from the beginning of the appendage- bearing area (the hood). The hood does not curveand lays straight between the appendage-free area of the ligule and the staminal ring/ovary (Fig. 4A). Incontrast, the hood further curves inward to form adouble or a triple coil in most species of Eschweilera(Fig. 4B).

28. Ligular anges. 0= absent, 1= present. In species of Lecythis section Corrugata (excluding L. corrugata ), there is a well-developed ange that extendsfrom each side of the appendage-free area of theligule. This character is not found in any other zygomorphic- owered species.

29. Ligular appendages, on oneside of the ligule.0= absent,1= present. Ligular appendages are located only on oneside of the ligule in some species of Lecythis , most species of Eschweilera , and all species of Couroupita ,Corythophora , and Couratari .

30. Ligular appendages. 0= absent, 1= present on both sidesof the ligule. In Eschweilera nana and species of Eschweilera section Tetrapetala , both the inner and theouter surfaces of the ligule bear appendages. Thischaracter is not found in any other zygomorphic-

owered species.31. Apical ligular appendages. 0= absent, 1= present.

The appendages located at the apex of the ligule areonly found in Bertholletia excelsa , two species of

Eschweilera ( E . congesti ora and E . simiorum(Benoist) Eyma) and most species of Lecythissection Lecythis .

32. Anthers in the ligule. 0= absent, 1= present. Berthol letia excelsa , Corythophora amapaensisPires ex S. A. Mori & Prance, Corythophoralabriculata (Eyma) S. A. Mori & Prance, Lecythiscorrugata Poit., Lecythis conferti ora (A. C. Sm.) S.A. Mori, and Lecythis pneumatophora S. A. Mori,and species of Couratari , Eschweilera , and Lecythissection Lecythis lack anthers in the ligule whileCorythophora alta , Corythophora rimosa W. A.Rodrigues, Lecythis persistens Sagot, and speciesof Couroupita , Lecythis section Pisonis S. A. Moriand Lecythis section Poiteaui S. A. Mori haveanthers in the ligule. Morphologically, pollen of theligular anthers may or may not differ from pollen of the anthers in the staminal ring. In Couroupita guianensis Aubl. and C . nicaraguarensis , pollen of the ligular anthers has a rugose surface and remainsin tetrads whereas pollen of the staminal ring has asmooth surface and is released in monads (Mori et al., 1980; Tsou, pers. comm.). In Lecythis pisonisand Lecythis zabucajo Aubl., ligular pollen does not differ from pollen of the staminal ring in morphol-ogy. However, ligular pollen turns black later inanthesis, whereas pollen of the staminal ring doesnot change color (Mori et al., 1980; Huang, pers.obs.). Ligular pollen in species of Corythophora and Lecythis section Poiteaui (pers. obs.) is not in tetradsand does not change color during anthesis. In vitro

F IG . 4. The structure of coiled ligules. A. Single-coiled ligule, Eschweilera alvimii . Drawing is modied from Fig.65 in Mori and Prance (1990b). B. Double-coiled ligule, Eschweilera ovata . Drawing is modied from Fig. 87 in Moriand Prance (1990b).



11/22

experiments indicate that ligular pollen of Courou- pita guianensis and Lecythis pisonis does not germinate while 21% of the pollen of the staminalring in the former species and 48% in the latter species germinate (Mori et al., 1980). It is not known if the ligular pollen of other species is sterile.

33. Closed androecium. 0= absent, 1= present. Speciesof Gustavia , Grias , Allantoma , Cariniana , Courou- pita , and some species of Lecythis (e.g., Lecythisidatimon Aubl.) have open androecia that allow potential pollinators and predators to easily reach the pollinator rewards. In contrast, species of Bertholle-tia , Corythophora , Couratari , and Eschweilera , andsome species of Lecythis (e.g., L. ollaria ) haveclosed androecia. The hood of these species pressesagainst the staminal ring and limits the entry to pollinators with enough strength to open the hood.The degree of limitation depends on the tightness of the hood against the staminal ring. Only pollinatorsof the right body size have enough strength to pushtheir way into the owers. An example was given ina pollination study of Corythophora amapaensis andC . rimosa (Mori & Boek e, 1987). Flowers of theformer species are larger and effective pollinatorstend to be larger bees than those that pollinate thelatter species. Mori and Boeke (1987) observed that smaller trigonid bees similar to the pollinators of C .rimosa were not able to enter the owers of C .amapaensis .

34. Fertile stamens. 0= fewer than 50, 1= more than 100.Fertile stamens are fewer than 50 in Allantoma andmost species of Cariniana , except Cariniana ianeir-ensis R. Knuth, which has about 150 fertile stamens.There are fewer than 100 fertile stamens in Coura-tari . All other genera of Lecythidoideae have morethan 100 fertile stamens. Species of Cariniana andCouratari included in this study have fewer than 50fertile stamens. Therefore this character is dividedinto two states: fewer than 50 and more than one100.

35. Pollen aggregation. 0= monads, 1= tetrads. Most species of Lecythidoideae have pollen in monads.Pollen in tetrads is only found in the ligule of Couroupita guianensis and C . nicaraguarensis (Moriet al., 1980; Tsou, pers. comm.). In vitro experimentsdemonstrated that pollen in tetrads does not germinate(Mori et al., 1980).

36. Anther dimorphism. 0= absent, 1= present. When theowers are fresh, all of the anthers in the sameower have the same color in most species of

Lecythidoideae. The only known exceptions arefound in species of Corythophora and Lecythissection Corrugata . Corythophora alta , C . rimosa ,and Lecythis persistens have anthers in the ligule.The ligular anthers of these species are yellow or orange while their anthers in the staminal ring arewhite. Corythophora amapaensis , C . labriculata , Lecythis corrugata , L. conferti ora , L. idatimon , and L. pneumatophora do not have ligular anthers. In thestaminal ring, anthers of the innermost few rows (near ligule) of these species are orange or dark yellow whilethe remaining anthers are white or light yellow.

37. Nectar. 0= absent, 1= present. Nectar is found in Bertholletia excelsa , Couratari , Eschweilera , and some

species of Lecythis , e.g., L. conferti ora . In Couratariand Eschweilera , nectar is produced from modiedappendages located at the apex of the ligular coil(Prance, 1990c; Mori & Prance, 1990d); in Bertholletiaexcelsa , nectar is produced from the base of ligular appendages (pers. obs.); in species of Lecythis , nectar is produced from the base of ligular appendages (e.g., L.conferti ora ) or from the base of the stamens of thestaminal ring ( Lecythis persistens Sagot subsp. auran-tiaca S. A. Mori; Mori & Boek e, 1987).

38. Style apex. 0= with annular expansion, 1= without annular expansion. An annular expansion right belowthe apex of the style is only found in species of Lecythissection Pisonis and some species of Couratari (e.g.,Couratari stellata A. C. Sm.).

39. Ovary locules. 0= two, 1= three, 2= four, 3= ve or six. Most species of Corythophora and most speciesof Eschweilera are two-locular; species of Coura-tari , Cariniana , and most species of Allantoma arethree-locular; species of Grias , Corythophora labri-culata , Lecythis , and some species of Eschweileraand Gustavia are four-locular. Allantoma lineata isfour or ve-locular; and Couroupita and somespecies of Gustavia are six-locular.

40. Operculum. 0= absent, 1= present. The operculum isabsent in species of Gustavia , Grias , and Courou- pita ; the operculum is present in species of Allan-toma , Cariniana , Couratari , Corythophora , Bertholletia , Eschweilera , and Lecythis .

41. Operculum dehiscence. 0= indehiscent, 1= dehis-cent. In species of Allantoma , Cariniana , Couratari ,Corythophora , Eschweilera , and most species of Lecythis , the operculum falls spontaneously from the

fruit and releases the seeds. In Bertholletia excelsa ,the operculum is also dehiscent; however, it fallsinside the fruit and the opening is smaller than theseeds. Thus, the seeds remain inside the fruit at maturity. The operculum is indehiscent in Lecythis gracieana S. A. Mori, Lecythis parvifructa S. A.Mori, and Lecythis prancei S. A. Mori.

42. Seeds embedded in pulp. 0= absent, 1= present. Thischaracter is only found in species of Couroupita . Theseeds of Couroupita cannot be easily separated from thesurrounding pulp, which is derived from the prolifer-ation of the septa and the placentae (Schoenber g, 1983).Although the seeds of Gustavia and Grias aresurrounded by pericarp, it is not juicy and pulpy andthe seeds can be easily removed from the fruit.43. Seeds sulcate. 0= absent, 1= present. The seeds of species of the Lecythis section Pisonis have longi-tudinal grooves or furrows. This character is not found in any other species of the Lecythidoideae.

44. Seed trichomes. 0= absent, 1= present. Seedtrichomes are an outgrowth of the exotesta (Tsou &Mori, 2002). This character is only found in speciesof Couroupita .

45. Unilateral seed wing. 0= absent, 1= present. Allan-toma (except A. lineata ), Cariniana , and Couratariare the only genera of Lecythidoideae that have seedwings. Tsou and Mori (2002) demonstrated that unilateral seed wings in Allantoma / Cariniana andcircumferential seed wings in Couratari are differ-ent, both in origins and structures. Thus, seed wingsare coded as two different characters. The unilateral



12/22

Excluded characters. Several characterswere explored for possible use but wereexcluded from the analysis. Characters of calyx imbrication and orientation and fruit shape and size are too variable and thevariation is continuous and inconsistent. It isdif cult to divide the variation into discretestates and code each taxon accurately. Flower color is useful on many occasions but isdif cult to code. For example, many zygo-morphic- owered species have a petal color

different from the androecium; some havedifferent colors at different parts of the petals(e.g., white petals with pink margins/apex);and some have different colors at different stages of anthesis, e.g., owers of Lecythis pisonis are purple at early stage and becomecompletely white when owers are older.Characters of seed veins are very distinct insome species of Lecythis ; however, variationof those characters is not fully understood andmany taxa do not have any information for character coding. Another excluded character isresin residue on the surface of the owers or immature fruits. The presence of resin was not formally recorded in Lecythidoideae but wasonly mentioned occasionally on the labels of afew herbarium specimens. It was rst found indry fruits of species of the Lecythis sectionCorrugata , but more was discovered in speciesof Eschweilera . More study isneededbefore thischaracter can be used for phylogenetic analysis.

Phylogenetic analysis. WinClada (Nixon,1999) was used to create the data matrix.Characters were equally weighted and allmulti-state characters were coded as non-additive. The parsimony-based program Treeanalysis using New Technology (TNT) was

used to generate phylogenetic trees (Goloboff et al., 2008). A Maximum of 1000 trees washeld and the combination of the followingalgorithms was applied for tree search:Ratchet (RAT), Tree-Drifting (DFT), Secto-rial-Searches (SS), and Tree-Fusing (TF). Thesearch strategy included two stages. The purpose of the rst stage was to nd the shortest tree with the optimal score by performing 1000iterations of RAT and 1000 cycles of DFTwithrandom SS. The resulting trees were thensubmitted to perform ve runs of TF. The purpose of the second stage was to test thecorrectness of the consensus by nding theoptimal score ten times independently. A strict consensus tree was calculated in Winclada.Characters were optimized using the fast optionof Winclada. Branch support was constructed by Bootstrap analysis with 1000 replications,10 random taxon entry sequences per replica-tion, and one tree saved per replication.

ResultsIn total 49 informative characters were

included in the morphological data matrix.

seed wing originates from the mesophyll of the outer integument of the ovule, there is no exotesta in the seedwing, and the seed coat has branched vascular bundles but no bers (Tsou & Mori, 2002). This character isfound in species of Cariniana and Allantoma , with theexception of A. lineata . Seeds of A. lineata have nounilateralwingsbut have rich oil content, which allowsthem to oat for at least six months (Ducke, 1948).Species of Cariniana and Allantoma that have seedwings are wind dispersed, whereas A. lineata is water dispersed. A cladistic study of Cariniana and Allan-toma indicated that the seed wings have been lost in A.lineata (Huang et al., 2008). However, vestigial wingsare found in seeds of A. lineata (pers. obs.). Thissuggests that the loss of seed wing is probably becauseof adaptation for water dispersal.

46. Circumferential seed wing. 0= absent, 1= present. Thecircumferential seed wing originates from both theexotesta and the outer layers of mesotesta of the seed body, the seed wing has an exotesta, and the seed coat has unbranched vascular bundles and bers (Tsou &Mori, 2002). This character is only found in species of Couratari .

47. Aril. 0= absent, 1= present. In most species of Lecythidoideae, the seeds are attached to the ovarywall through a well-developed funicle that may or may not be surrounded by a eshy aril. Arils are not developed in species of Grias , Allantoma , Courou- pita , Cariniana , Bertholletia excelsa , Couratari , Eschweilera tenuifolia (O. Berg) Miers, most speciesof Gustavia , and a few species of Lecythis (Prance &Mori, 1979; Mori & Prance, 1990b).

48. Aril type. 0= basal, 1= lateral, 2= spreading. For species that have a well-developed aril, the positionof the aril is of taxonomic importance. Most speciesof Eschweilera have an aril running along the side of the seed (lateral), and some species of Eschweilerahave an aril spreading around the seeds (spreading).The spreading aril may cover only the bottom part of the seed or it may cover the whole seed. Somespecies of Gustavia , all species of Corythophora , afew species of Eschweilera , and most species of Lecythis have an aril at the base of the seed (basal).

49. Cotyledons. 0= absent, 1= leaf-like, 2= eshy. Cotyle-dons are absent in Allantoma lineata , Bertholletiaexcelsa , and all species of Corythophora , Eschweilera ,and Lecythis . Species of Allantoma (except A. lineata ),

Cariniana , Couroupita and Couratari have leaf-likecotyledons; and species of Gustavia have eshycotyledons.



13/22

Discussion

The Bertholletia clade and the phyloge-netic relationships within the clade. Themonophyly of the Bertholletia clade issupported in the present study. This result is congruent with the previous molecular analysis based on plastid ndhF and trnL-F sequence data (Mori et al., 2007). Synapo-morphies of the clade may be different indifferent most parsimonious (MP) trees because of different tree topology. None-theless, many of the MP trees show that the monophyly of the Bertholletia clade issupported by the following characters: brachyparacytic stomata (Fig. 5, character 11), ped-icels absent (13), 4-locular ovaries (39), arils present (47), and cotyledons absent (49).Within the Bertholletia clade, four clades arerecognized, but the relationships among theseclades are not resolved (Fig. 6). Clades andtheir synapomorphies are discussed in thefollowing paragraphs.

Corythophora. This clade includes allfour species of Corythophora recognized byMori and Prance (1990c). Synapomorphiesof the Corythophora clade are the presence

of in orescence scales (Fig. 5; character 12)and the absence of nectar (37). The monophyly of Corythophora is congruent withMori and Prance (1990c) and Mori et al.(2007).

Section Tetrapetala. This clade containsall three species of Eschweilera sectionTetrapetala ( E . alvimii , Eschweilera compressa (Vell.) Miers, and E . tetrapetala )recognized by Mori (1990a) and Eschweileranana , which was included in Eschweilerasection Eschweilera by Mori and Prance(1990e). The presence of appendages on boththe inner and the outer surface of the ligule(30) is a synapomorphy unique to sectionTetrapetala clade (Fig. 5). Other synapomorphies include the presence of inorescencescales (12) and the absence of appendages ononly one side of the ligule (29). Within theclade, E . nana is sister to the other threespecies. A character that distinguishes E .nana from the other three species is the petalnumber (18). Eschweilera nana has six petalswhile the other three species have four petals.The sister relationship of E . nana and speciesof section Tetrapetala is a new nding of the present study.

Mori (1990a) established section Tetrape-tala to accommodate three species that differ from all other species of Eschweilera inhaving four instead of six petals (18), a non-coiled instead of a double or triple-coiledligule (26, 27), and seeds with a basal insteadof a lateral or spreading aril (48). It iscon rmed that three species of section Tetra- petala have a single instead of a non-coiledligule in the present study. A single-coiledligule is only shared by E . nana and a fewspecies of section Lecythis while seeds with a basal aril are shared by E . amazoniciformis , E . nana , all species of Corythophora , andmost species of Lecythis . Species of sectionTetrapetala and E . nana were placed in Eschweilera because they have a two-locular ovary (39), which is an important feature for most species of Eschweilera . Eschweileraamazoniciformis and E . nana form a cladein Mori et al. (2007). However, this sister group relationship is not supported in the present study (Fig. 6).

Section Eschweilera B. This cladeincludes two species of Eschweilera section Bracteosa S. A. Mori ( E . bracteosa and


Cladistic analysis generated 70 equally parsi-monious trees of 107 steps with a consistencyindex (CI) of 0.52 and a retention index (RI)of 0.88. One of the trees is shown in Fig. 5,and the strict consensus of all 70 trees isshown in Fig. 6. The topology of the strict consensus indicates that Bertholletia , Cory-thophora , Eschweilera , and Lecythis together (the Bertholletia clade) are monophyletic(Fig. 6), albeit with


14/22

Eschweilera cyathiformis S. A. Mori), theonly species of the monotypic Eschweilerasection Jugastrum Prance & Mori ( E . tenuifolia ), and 45 species of Eschweilera section Eschweilera . Section Eschweilera B is supported by the presence of a double or a triple-coiled ligule (Fig. 5; character 27), which isunique to this clade. The results of this studyindicate that the segregation of sections Bracteosa and Jugastrum from section Eschweilera is not supported because bothsections are nested within section Eschwei-lera B (Fig. 5). No further taxonomicconclusions can be made because of the lack of resolution within the clade.

In Mori and Prances treatment (1990d), Eschweilera includes four sections. SectionTetrapetala is discussed in the previous paragraph. Section Bracteosa consists of

four species that have a bract and twosmaller bracteoles persistent at anthesis (15;Mori, 1990b). Section Jugastrum includesonly one species, E . tenuifolia , whichdiffers from other species of Eschweilerain having seed without an aril (47) and theseed germinates from the side instead of from the end (Prance & Mori, 1990). Thelatter character is not included in the present study because it is not parsimonyinformative. Section Eschweilera includesmost species of the genus (ca. 85 spp.).Mori and Prance (1990e) de ned that species inthis section possess all of the followingfeatures: six petals, a fully coiled androecialhood (referred as a coiled ligule (26) and adouble or a triple coil (27) in the present study),caducous bracts and bracteoles, and apical seedgermination.

Gustavia speciosa

Grias peruviana

A. lineata

A. integrifolia

A. decandra

Cariniana pyriformis

Cariniana estrellensis

Couratari guianensis

Couratari multiflora

Couratari macrosperma

Couratari stellata

Couroupita subsessilis

Couroupita guianensis

Couroupita nicaraguarensis

493919

3918

4939

11

13

45

1813111097

456

8

44424039352

3

46383734333225

1

3424232221

2019168

494034161

Outgroup

Bertholletia clade4947391311

AF IG . 5. One of 70 most parsimonious (MP) trees. The tree length is 107 steps, the consistency (CI) index is 0.53,

and the retention index (RI) is 0.88. Characters are optimized onto the tree using fast option of Winclada with

supporting characters shown on branches. Branches without supporting characters are collapsed. Arrows indicatenodes collapsed in the strict consensus. Black circles show unique origins of states, and white circles are non-uniqueorigins. A. Outgroup taxa and the Bertholletia clade. B. Lecythis , Corythophora , and Bertholletia . C. Eschweilera s.l./ Section Lecythis B clade.



15/22


F IG . 5. (continued).

B


16/22

CF IG . 5. (continued).



17/22

In general, species of Eschweilera arecharacterized by a double or a triple coiledandroecial hood (27), antherless hood appen-dages (32), a bilocular ovary (39), and seedswith a lateral aril (48; Mori & Prance, 1990d).Except for a double or a triple coiled ligule,other features are homoplasious in the present study (Fig. 5). Mori et al. (2007) did not include section Tetrapetala in their study;section Eschweilera was divided into threeclades; and sections Bracteosa and Jugastrumwere nested in the largest clade of section Eschweilera (Fig. 1 in Mori et al., 2007).However, whether the three clades of Eschweilera are monophyletic is not resolvedin Mori et al. (2007). In contrast, the present study supports the monophyly of Eschweileraif E . congesti ora and E . simiorum areexcluded (Fig. 6). Nonetheless, both studiesdemonstrate that the segregation of sections Bracteosa and Jugastrum from section Eschweilera is not necessary.

Section Corrugata . This clade includesall ve species of Lecythis section Corrugatarecognized by Mori (1990c). Synapomorphiesof this clade are the presence of pedicels(Fig. 5; character 13) and rugose/tuberculate

pedicels and hypanthia (14). The monophylyof section Corrugata in the present study iscongruent with Mori (1990c) and Mori et al.(2007). In addition, the present study alsosupports the sister relationship of Corytho- phora and section Corrugata (Fig. 5), which isnot shown in Mori et al. (2007). The onlysynapomorphy supporting this relationship isthe presence of anther dimorphism (36), whichis also unique to Corythophora and sectionCorrugata .

In addition to the presence of anther dimorphism, both species of Corythophoraand section Corrugata have a non-coiledligule (26), appendages present only on oneside of the ligule (29), and seeds with a basalaril (48). In general, species of sectionCorrugata can be distinguished from speciesof Corythophora by an open instead of aclosed androecium (33) and a four instead of a two-locular ovary (39). However, onespecies of section Corrugata ( L. corrugata )also has a closed androecium that resemblesthe one of Corythophora , and a four-locular ovary is also found in one species of Corythophora (C . labriculata ). Mor i (1990c)

pointed out the androecial resemblance between L. corrugata and species of Cory-thophora and hypothesized the close relation-ships of section Corrugata through the link of L. corrugata . This relationship is supported inthe present study.

Section Pisonis . This clade includes allfour species of Lecythis section Pisonisrecognized by Mori (1990c). Synapomor- phies of this clade include the presence of oxidation of wounded tissues (Fig. 5; charac-ter 2), an annular expansion below the apexof the style (38), and sulcate seeds (43). Themonophyly of section Pisonis in the present study is congruent with Mori (1990c) andMori et al. (2007).

Section Poiteaui. This clade includes allthree species of Lecythis section Poiteauirecognized by Mori (1990c). There is onesynapomorphy supporting this clade (Fig. 5):the presence of leaf papillae on the abaxialsurface (5). Mori et al. (2007) included onlyone species of section Poiteaui ( L. poiteaui )in their analysis. Their results showed that L. poiteaui is nested in a clade that consists of three species ( L. prancei , L. minor and L.tuyrana ) of section Lecythis (Fig. 1 in Mori et

al., 2007). In the present study, however, L.minor , L. tuyrana , and L. ollaria are includedin a clade that contains all species of Eschweilera , except E . congesti ora and E . simiorum (Fig. 6). Lecythis ollaria is the typespecies of Lecythis and section Lecythis(Mori, 1990c). This species is not includedin Mori et al. (2007). Lecythis prancei alongwith the remaining species of section LecythisA, Bertholletia excelsa , E . congesti ora , and E . simiorum are unresolved in the consensustree (Fig. 6).

In Moris treatment (1990c), Lecythis isdivided into four sections. Section Corrugataincludes ve species that have rugose/tuber-culate pedicels and hypanthia (14). Section Pisonis consists of four species that arecharacterized by the presence of woundedtissues turning bluish (2), an annular expan-sion below the apex of the style (38), sulcateseeds (43), and pollen of the ligular anthersturning from yellow to black 24 hours after the owers open. The last feature is not included in the analysis but is described inthe character of anthers in the ligule (32).Section Poiteaui includes three species that



18/22

have a terminal inorescence, a at androe-cial hood (referred as the absence of acoiled ligule (26) in the present study) with

antheriferous appendages (32), and densely packed stamens (up to 1000) on thestaminal ring (34). The rst feature is not

Gustavia speciosa Grias peruviana

Corythophora altaCorythophora amapaensisCorythophora labriculata

Corythophora rimosaCorythophora rimosa rubra

L. chartaceaL. rorida

Bertholletia excelsa

E. simiorumE. congestiflora

L. parvifructaL. alutaceaL. retusaL. pranceiL. schomburgkiiL. gracieanaL. mesophylla

L. brancoensis L. poiteauiL. barnebyiL. zabucajoL. lanceolataL. pisonisL. ampla

L. corrugata

L. persistens L. persistens aurantiaca

L. idatimonL. pneumatophoraL. confertiflora

A. lineataA. integrifolia A. decandra

Cariniana pyriformisCariniana estrellensis

Couratari guianensis Couratari multiflora

Couratari macrospermaCouratari stellata

Couroupita subsessilisCouroupita guianensisCouroupita nicaraguarensis

Outgroup

Bertholletia

Section Eschweilera A

Section Corrugata

Section Pisonis

Section Poiteaui

Section Lecythis A

Corythophora

Eschweilera s.l./Section Lecythis B

77

89

92

93

52

78

52

55

L. holcogyne

AF IG . 6. Strictconsensusof 70 mostparsimonious (MP) trees.Bootstrapvalues(>50%) aregiven above thebranches.A.

Outgroup taxa, Corythophora , Bertholletia , and Lecythis . B. Eschweilera s.l./Section Lecythis B clade.



19/22

included in the analysis because of contin-uous and inconsistent variation. Section Lecythis has about 15 species that arecharacterized by ligular appendages that lack anthers and sweep inward without forming a complete coil.

Nonetheless, species of four sections allhave a four-locular ovary (39), a well-denedstyle, and ovules that are attached toward the base of the septum (Mori, 1990c). Thecharacter of ovary locule is homoplasious inthe present study. The last two features are not included in the analysis because the variationof the style is continuous and inconsistent andthe attachment of the ovules is not parsimonyinformative. Both Mori et al. (2007) and the present study support the monophyly of sections Corrugata and Pisonis . However,whether or not Lecythis is monophyletic isnot resolved in Mori et al. (2007). On the other

hand, although the relationships are not completely resolved, the results of the present study clearly indicate that Lecythis is not monophyletic because section Corrugata issister to Corythophora (Fig. 6) and threespecies of section Lecythis B ( L. minor , L.tuyrana , and L. ollaria ) are more closelyrelated to Eschweilera than they are to other species of Lecythis (Fig. 6).

The position of Bertholletia excelsa in boththe present study and Mori et al. (2007) isundetermined. Mori and Prance (1990a)suggested that the closest relatives of B.excelsa are some species of section Lecythis based on morphological similarity. For example, B. excelsa has a non-coiled ligule (26)and the presence of appendages at the apex of the ligule (31), which is also found only insome species of section Lecythis . In addition,the presence of leaf papillae (5) on the abaxial

E. bracteosaE. cyathiformis

E. tessmanniiE. atropetiolataE. amazonicaE. parvifoliaE. sp. ined. E. tresorianaE. jacquelyniaeE. grandifloraE. sessilisE. wachenheimiiE. ovataE. chartaceifoliaE. mexicana E. albifloraE. sagotianaE. rimbachiiE. aguilariiE. biflavaE. hondurensisE. longirachis

E. amplexifolia E. apiculataE. integrifoliaE. micrantha

E. parvifloraE. pseudodecolorans

E. panamensisE. laevicarpaE. decoloransE. rankiniaeE. truncata

E. amazoniciformisE. coriaceaE. alataE. pittieri

E. antioquensis E. caudiculataE. neeiE. pedicellataE. collinaE. andinaE. ovalifoliaE. subglandulosa

E. tenuifoliaE. juruensisE. calyculata

E. nana

E. tetrapetalaE. alvimii

E. compressa

L. minorL. ollariaL. tuyrana

SectionEschweilera B

Section Jugastrum

Section Bracteosa

SectionLecythis B

SectionTetrapetala

SectionEschweilera B

61

54

BF IG . 6. (continued).



20/22

surface is only found in B. excelsa , threespecies of section Poiteaui , and a few speciesof section Lecythis . However, whether or not B. excelsa and section Lecythis are monophyletic is not resolved in the present study or Mori et al. (2007).

Eschweilera congesti ora and E . simiorumwere placed in section Eschweilera (Mori &Prance, 1990d). However, both species have anon-coiled ligule (26), the presence of theappendages at the apex of the ligule (31), afour-locular ovary (39), and seeds with a basalaril (48). These states are found in species of section Lecythis A. Although the monophyly of E . congesti ora , E . simiorum and species of section Lecythis A is undetermined in the present study, both species were included in aclade that consisted of four species of section Lecythis in Mori et al. (2007). It is likely that both E . congesti ora and E . simiorum were placed in the wrong genus, but additional dataare needed in order to determine the genus towhich these two species belong.

Taxonomic conclusions

Our study supports the monophyly of

Eschweilera sensu lato if E . congesti oraand E . simiorum are excluded (includingsections Jugastrum and Bracteosa ). However,instead of dividing Eschweilera s.l. into four sections as suggested by Mori and Prance(1990d), our results support only the segre-gation of the section Tetrapetala (including E .nana ) from section Eschweilera .

The taxonomy of Lecythis , on the other hand, is complicated. Based on our results, Lecythis is paraphyletic and all of thegenera in the Bertholletia clade are poten-tially derived from within Lecythis . Limitedresolution within the Bertholletia clademakes it dif cult to recognize a monophyletic Lecythis that does not contain at minimum almost all of Eschweilera . Only Lecythis sections Corrugata , Pisonis , Poi-teaui are supported as monophyletic, but it is not clear how these groups should betreated taxonomically. Further study will benecessary in order to gain a better understand-ing of relationships in the Bertholletia clade andarrive at a sensible arrangement of monophyletic genera and infrageneric taxa withinthe group.

Acknowledgments

We thank Maristerra R. Lemes for her assistance in applying for collecting permits,organizing eld trips, and providing supplies

for our

eld work in Amazonian Brazil. Weare grateful to staff of the cited herbaria for their help with specimen study, ReinaldoAguilar, Catherine Bainbridge, E. da CostaPereira, and C. A. Cid Ferreira for their helpin the eld. We also thank Robbin Moran for acting as editor-in-chief and two anonymousreviewers for reviewing our manuscript. The

rst author would also like to thank theGraduate Fellowship of The New York Botanical Garden, Chancellor s Fellowshipof The Graduate Center of the City Universityof New York, The Cuatrecasas Fellowship of The Smithsonian Institution, The TravelAward of Taipei Economic and CulturalOf ce in New York (TECO), The WilliHenning Society, and The National TropicalBotanical Garden for nancial support of thisstudy.

Literature cited

Angiosperm Phylogeny Group [APG]. 2009. Anupdate of the Angiosperm Phylogeny Group classi-

cation for the orders and families of owering plants: APG III. Botanical Journal of the LinneanSociety 161: 105 121.

Berg , O . 1856. Barringtonieae and Lecythideae. RevisioMyrtacearum Americae. Linnaea 27: 441 461.

. 1857. Mantissa I ad Revisionem MyrtacearumAmericae. Trib. II Barringtonieae and Trib III.Lecythideae. Linnaea 29: 258 264.

.1858. Myrtaceae, tribus II. Barringtonieae, tribusIII. Lecythideae. In: C. F. P. von Martius (ed.). FloraBrasiliensis 14: 469 526.

Candolle, A. P. de . 1828. Myrtaceae tribes Barringto-nieae and Lecythideae. Prodromus systematis natu-ralis regni vegetabilis 3: 288 296.

Clark, J. L. & S. A. Mori. 2000. Grias longirachis(Lecythidaceae), a new species from northwesternEcuador. Brittonia 52: 145 148.

Cornejo, X. & S. A. Mori . 2010. Grias theobromicarpa(Lecythidaceae), a new species from northwesternEcuador. Brittonia 62: 99 104.

Dorr , L. J. & J. H. Wiersema . 2010. Typi cation of names of American species of vascular plants proposed by Linnaeus and based on Loeing's Iter Hispanicum (1758). Taxon 59: 1571 1577.

Ducke , A . 1948. rvores Amaznicas e sua propagao.

Boletim do Museu Goeldi de Historia Natural eEthnographia. Belm 10: 81 92.Endlicher , S. L. 1840. Genera plantarum. Fr. Beck,

Wein.



21/22

Goloboff , P., J. S. Farris & K. C. Nixon . 2008. TNT, a free program for phylogenetic analysis. Cladistics 24: 1 13.

Huang, Y.-Y, S. A. Mori & G. T. Prance. 2008. A phylogeny of Cariniana (Lecythidaceae) based onmorphological and anatomical data. Brittonia 60: 69 81.

Humboldt , A. von & A. Bonpland . 1807. PlantaeAequinoctiales 1: 122 127.

Knuth, R. 1939. Lecythidaceae. In: Engler, P anzen-reich VI. 219a: 1 146.

Leaf Architecture Working Group . 1999. Manual of leaf architecture morphological description andcategorization of dicotyledonous and net-veinedmonocotyledonous angiosperms. Smithsonian Insti-tution. Washington, DC., USA.

Martius , C. F. P. 1937. Flora Brasiliensis 14: 469 526.Miers , J . 1874. On the Lecythidaceae. Transactions of

the Linnean Society of London 30: 157 318.Mori , S. A. 1979a. Gustavia . In: G. T. Prance & S. A.

Mori (eds.). Lecythidaceae-Part I. The actino-morphic- owered New World Lecythidaceae( Asteranthos , Gustavia , Grias , Allantoma , andCariniana ). Flora Neotropica Monograph 21:128 197.

. 1979b. Grias . In: G. T. Prance & S. A. Mori(eds.). Lecythidaceae- Part I. The actinomorphic-

owered New World Lecythidaceae ( Asteranthos ,Gustavia , Grias , Allantoma , and Cariniana ). Flora Neotropica Monograph 21: 197 209.

. 1990a. Eschweilera section Tetrapetala . In: S.A. Mori & G. T. Prance (eds.). Lecythidaceae Part II. The zygomorphic-owered New World genera(Couroupita , Corythophora , Bertholletia , Couratari , Eschweilera , and Lecythis ). Flora Neotropica Mono-

graph 21: 169

172. . 1990b. Eschweilera section Bracteosa . In: S. A.Mori & G. T. Prance (eds.). Lecythidaceae Part II.The zygomorphic-owered New World genera (Cour-oupita , Corythophora , Bertholletia , Couratari , Eschweilera , and Lecythis ). Flora Neotropica Mono-graph 21: 172 177.

. 1990c. Lecythis . In: S. A. Mori & G. T. Prance(eds.). Lecythidaceae Part II. The zygomorphic-

owered New World genera (Couroupita , Corytho- phora , Bertholletia , Couratari , Eschweilera , & Lecy-this ). Flora Neotropica Monograph 21: 267 326.

. 1992. Eschweilera pseudodecolorans (Lecythi-daceae), a new species from central Amazonian.Brittonia 44: 244 246. . 1995a. Observaes sobre as espcies de Lecy-thidaceae do leste do Brasil. Boletim de Botnica,Departamento de Botnica, Instituto de Biocincias,Universidade de So Paulo. So Paulo 14: 1 31.

. 1995b. In: S. A. Mori & N. Lepsch-Cunha(eds.). The Lecythidaceae of a Central Amazonianmoist forest. Memoirs of the New York BotanicalGarden 75: 47 49.

. 2007. Lecythidaceae. In: B. E. Hammel, M. H.Grayum & N. Zamora (eds.). Manual de Plantas deCosta Rica. Volume VI. Dicotiledneas (Haloragaceae-Phytolaccaceae). Monographs in Systematic Botanyfrom the Missouri Botanical Garden: 111: 903.

, J. E. Orchard & G. T. Prance . 1980. Intra oral pollen differentiation in the New World Lecythidaceae,subfamily Lecythidoideae. Science 209: 400 403.

& D. Black . 1987. Chapter VII. Stem and Leaf.Memoirs of the New York Botanical Garden 44: 72 85.

& J. D. Boeke . 1987. Chapter XII. Pollination.Memoirs of the New York Botanical Garden 44: 137 155.

. & G. T. Prance . 1990a. Taxonomy, ecology, andeconomic botany of the Brazil nut ( Bertholletiaexcelsa Humb. & Bonpl.: Lecythidaceae). Advancesin Economic Botany 8: 130 150.

& . 1990b. Lecythidaceae Part II. Thezygomorphic- owered New World genera (Courou- pi ta , Corythophora , Bertholletia , Couratari , Eschweilera , and Lecythis ). Flora Neotropica Mono-graph 21: 1 376.

& . 1990c. Corythophora . In: S. A. Mori& G. T. Prance (eds.). 1990. Lecythidaceae Part II.The zygomorphic-owered New World genera (Cour-oupita , Corythophora , Bertholletia , Couratari , Eschweilera , and Lecythis ). Flora Neotropica Mono-graph 21: 158 267.

& . 1990d. Eschweilera . In: S. A. Mori& G. T. Prance (eds.). 1990. Lecythidaceae Part II.The zygomorphic-owered New World genera (Cour-oupita , Corythophora , Bertholletia , Couratari , Eschweilera , and Lecythis ). Flora Neotropica Mono-graph 21: 158 267.

& . 1990e. Eschweilera section Eschwei-lera . In: S. A. Mori & G. T. Prance (eds.). 1990.Lecythidaceae Part II. The zygomorphic-owered New World genera (Couroupita , Corythophora , Ber-tholletia , Couratari , Eschweilera , and Lecythis ).Flora Neotropica Monograph 21: 158 267.

, C.-C. Tsou, C. C. Wu, B. Cronholm & A.

Anderberg . 2007. Evolution of Lecythidaceae withan emphasis on the circumscription of Neotropicalgenera: information from combined ndhF and trnL-F sequence data. AmericanJournalof Botany 94:289 301.

, G. Cremers, C. Gracie, J.-J. de Granville, S.V. Heald, M. Hoff & J. Mitchell . 1997. Guide to theVascular plants of Central French Guiana: Part 2.Dicotyledons. Memoirs of the New York BotanicalGarden 76: 395.

, J. D. Garca-Gonzalez, S. P. Angel & C.Alvarado . 2010. Grias purpuripetala (Lecythida-ceae), a new purple-owered species from southernColombia. Brittonia 62: 105 109.

Morton, C. M., G. T. Prance, S. A. Mori & L. G.Thorburn . 1998. Recircumscription of Lecythida-ceae. Taxon 47: 817 827.

Nixon, K. C. 1999. The parsimony Ratchet, a newmethod for rapid parsimony analysis. Cladistics 15:407 414.

Prance, G. T. 1990a. Couroupita . In: S. A. Mori, & G. T.Prance (eds.). Lecythidaceae Part II. The zygomorphic- owered New World genera (Couroupita , Cor- ythophora , Bertholletia , Couratari , Eschweilera , and Lecythis ). Flora Neotropica Monograph 21: 88 103.

. 1990b. Bertholletia . In Mori,S.A.& G.T. Prance.1990. Lecythidaceae Part II. The zygomorphic-

oweredNewWorld genera(Couroupita , Corythophora ,

Bertholletia , Couratari , Eschweilera , and Lecythis ).Flora Neotropica Monograph 21: 114 118. . 1990c. Couratari . In: S. A. Mori, & G. T.

Prance (eds.). Lecythidaceae Part II. The zygomor-



22/22

phic- owered New World genera (Couroupita , Cor- ythophora , Bertholletia , Couratari , Eschweilera , & Lecythis ). Flora Neotropica Monograph 21: 118 158.

& S. A. Mori . 1979. Lecythidaceae- Part I. Theactinomorphic- owered New World Lecythidaceae( Asteranthos , Gustavia , Grias , Allantoma & Carini-ana ). Flora Neotropica Monograph 21: 1 270. & . 1990. Eschweilera section Jugastrum . In: Mori and Prance (eds.). Lecythidaceae Part II. Thezygomorphic- owered New World genera (Couroupita ,Corythophora , Bertholletia , Couratari , Eschweilera , and Lecythis ). Flora Neotropica Monograph 21: 177 181.

Roth, I . 1984. Strati cation of tropical forests as seen inleaf structure. Tasks for vegetation science 6: 1 518.Dr. W. Junk Publishers. The Hague. Netherlands.

Schoenberg , M. M. 1983. Carpologia de Couroupita guianensis Aublet (Lecythidaceae) I-Morfologia eclassi cao. Acta Biologica Paranaense , Curitiba12: 43 47.

Tsou, C.-H. & S. A. Mori. 2002. Seed coat anatomy andits relationship to seed dispersal in subfamily Lecy-thidoideae of the Lecythidaceae (The Brazil Nut Family). Botanical Bulletin of Academia Sinica 43:37 56.

Zeeuw, C. H. 1990. Secondary xylem of NeotropicalLecythidaceae. In: S. A. Mori & G. T. Prance (eds.).Lecythidaceae Part II. The zygomorphic-owered New World genera (Couroupita , Corythophora , Ber-tholletia , Couratari , Eschweilera , and Lecythis ).Flora Neotropica Monograph 21: 4 59.


nueces del brasil

Documents