A morphological cladistic analysis of Lecythidoideae with emphasis on Bertholletia, Corythophora, , and

1 2 3 YA-YI HUANG ,SCOTT A. MORI , AND LAWRENCE M. KELLY

1 The New York Botanical Garden, 2900 Southern Blvd., Bronx, NY 10458-5126, U.S.A. Current address: Biodiversity Research Center, Academia Sinica, Taipei 11529, Taiwan; e-mail: lecy.yhuang@ gmail.com 2 Institute of Systematic Botany, The New YorkBotanical Garden, 2900 Southern Blvd., Bronx( NY 10458-5126, 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 Eschweilera and 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 in the genera. The data matrix included 49 parsimony-informative characters derived from vegetative, floral, , and seed morphology and anatomy. The results based on the consensus of all most parsimonious indicate that Bertholletia, Corythophora, Eschweilera,andLecythis form a clade supported by brachyparacytic stomata, the absence 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 inflores- cence scales and the absence of nectar. Eschweilera is monophyletic only if E. congestiflora and E. simiorum are excluded. The monophyly of Eschweilera is supported by the presence of a two-locular ovary. Lecythis is not monophyletic, but sections Corrugata, Pisonis,andPoiteaui are monophyletic. Three species of section Lecythis aremorecloselyrelatedtoEschweilera, 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 &Mori,1979; Mori & Prance, 1990b;Moriet grow in lowland rainforest (Mori & Prance, al., 2007; Huang et al., 2008). Species of 1990b). The family consists of three subfa- the Lecythidoideae are confined to tropical milies (Mori et al., 2007): Foetidioideae, America. The is monophyletic Planchonioideae, and Lecythidoideae. The and each of the subfamilies is monophyletic Foetidioideae consists of 17 species in one (Morton et al., 1998;Morietal.,2007; APG III, genus. These species are found in East Africa, 2009). The relationships within the subfamilies, Madagascar, and Mauritius (Mori et al., however, are not fully understood, especially 2007). The Planchonioideae consists of 59 within the Lecythidoideae. species in six genera. They are found in tropical Lecythidoideae includes both endemics with Asia, tropical Africa, Australia, and the Pacific narrow distributions and widespread taxa. They Islands (Mori et al., 2007). The Lecythidoideae occupy diverse habitats but are most abundant consists of ca. 210 species in 10 genera (Prance in non-flooded 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. 2011] HUANG ET AL.: MORPHOLOGICAL ANALYSIS OF LECYTHIDOIDEAE 397

1990b). Species of Lecythidoideae are charac- However, the type species of Eschweilera and terized by fibrous bark; simple, alternate ; Lecythis were not included and some critical actinomorphic or zygomorphic androecia; taxa were not sampled, e.g., Eschweilera numerous ; inferior or half-inferior section Te t r a p e t a l a S. A. Mori. In this analysis, ovaries; bitegmic ovules; and the presence of Bertholletia, Corythophora, Eschweilera,and cortical bundles (Prance & Mori, 1979). Lecythis together were monophyletic (the The of Lecythidoideae places great Bertholletia clade), but the phylogenetic rela- emphasis on floral features, especially on the tionships among them were not fully resolved structure of the androecium. The ten genera of (Fig. 1 in Mori et al., 2007). Within the Lecythidoideae can be divided into two groups Bertholletia clade, moreover, the results further based on androecial symmetry. Three genera indicated that Eschweilera and Lecythis may have actinomorphic androecia: Allantoma not be monophyletic. Miers (eight species; Huang et al., 2008), Of the four genera, Lecythis was described L. (nine species; Mori 1979b; Clark & Mori, first. In 1758, two years after Loefling died, 2000; Cornejo & Mori, 2010;Morietal.,2010), Linnaeus published Loefling’s description of and Gustavia L. (41 species in three sections; a new genus, Lecythis Loefl., but the first Mori, 1979a;Morietal.,2007). Seven genera species in the genus (Lecythis ollaria L.) was have zygomorphic androecia: Bertholletia not published until 1759 (Dorr & Wiersema, Bonpl. (one species; Prance, 1990b), Cariniana 2010). These were the first valid publica- Casar. (nine species; Huang et al., 2008), tions of Lecythidaceae, even before the Corythophora R. Knuth (four species; Mori & family status was established. Lecythis is Prance, 1990c), Couratari Aubl. (19 species in the third largest genus of Lecythidoideae; three sections; Prance, 1990c), however, it is the most diverse of all genera Aubl. (three species; Prance, 1990a), Eschwei- in terms of floral and fruit features (Mori, lera Mart. ex DC. (93 species in four sections; 1990c). Species of Lecythis are distributed Mori & Prance, 1990d;Mori,1992, 1995a, from Nicaragua to Rio de Janeiro, 2007), and Lecythis Loefl. (27 species in four (Fig. 27 in Mori & Prance, 1990b) sections; Mori, 1990c, 1995b). Based on Bertholletia was described by Humboldt and comparative morphology, Mori et al. (2007) Bonpland (1807). Bertholletia excelsa Bonpl. hypothesized that the actinomorphic androe- (the ) is the only species of the genus. cium is the plesiomorphic state in the Lecythi- It is also the best known species in the family doideae. Most actinomorphic-flowered genera because of its edible seeds (Prance, 1990b). have their greatest diversity west of the Andes Bertholletia excelsa can be easily distinguished or in western Amazonia, whereas the zygomor- from the other three genera by two instead of phic-flowered genera are most diverse in six calyx lobes, the operculum falling inside central Amazonia and the Guianas. instead of outside the fruit, and by the absence Morton et al. (1998) conducted a phyloge- instead of the presence of a fleshy aril. It is netic analysis to test the monophyly of Lecy- widespread throughout Amazonia and the thidaceae and the monophyly of each of the Guianas (Fig. 21 in Mori & Prance, 1990b). three subfamilies based on morphological, Knuth (1939) established Corythophora based anatomical, cytological, and plastid rbcL and on Corythophora alta R. Knuth. He separated trnL sequence data. This study included one Corythophora from Lecythis because all the species to represent each genus, and one hood appendages of C. alta possess anthers, individual was sampled for each species. The whereas most species of Lecythis do not have results indicated that Lecythidaceae are mono- hood anthers or only part of the hood appen- phyletic and each of the three subfamilies is monophyletic (Fig. 1 in Morton et al., 1998). dages have anthers (Mori & Prance, 1990c). He Mori et al. (2007) performed another analysis separated Corythophora from Couroupita by its to test the monophyly of genera of the dehiscent versus indehiscent (Mori & subfamily Lecythidoideae based on plastid Prance, 1990c). Species of Corythophora are ndhF and trnL-F sequence data. This study limited to Surinam, French Guiana, and Brazil- incorporated more species into the analysis. ian Amazonia from Manaus to Amapá, where 398 BRITTONIA [VOL 63 they are found mostly north of the Amazon The taxonomy follows Prance and Mori River (Fig. 23 in Mori & Prance, 1990b). (1979) and Mori and Prance (1990b). The Eschweilera was first described by De sampled taxa are listed in Table I. — Candolle (1828). Martius (1837) accepted Data collection. Morphological and ana- Eschweilera as a genus and listed several tomical characters were collected based on fi features of Eschweilera distinct from Lecy- original observations in the eld and the this (e.g., bilocular ovary). However, many images available on the Lecythidaceae Pages subsequent authors still considered (http://sweetgum.nybg.org/lp/index.html). Eschweilera as part of Lecythis (Endlicher, Some characters were derived from the 1840;Berg,1856, 1857, 1858). In 1874, literature, herbarium specimens at INB, INPA, Miers maintained the generic status of MO, NY, and US, or pickled collections at Eschweilera and provided a list of features NY. that distinguished Eschweilera from Lecy- fragments used for study of venation this. The generic status of Eschweilera has patterns and stomata were placed in vials not changed since then. Eschweilera is the with 50% alcohol and bathed in boiling largest and the most widely distributed water for ten minutes. This procedure was genus of Lecythidoideae. Species of repeated two or three times until no further Eschweilera range from Veracruz, Mexico, color leached into the solution. After cool- to Rio de Janeiro, Brazil (Fig. 25 in Mori & ing to room temperature, samples were Prance, 1990b). washed with water two or three times, and In the present study, a cladistic analysis then changed to a 2% NaOH solution. The based on morphological and anatomical NaOH solution was replaced every day characters was performed. The objectives until the mesophyll of the leaf became of this paper are to examine the mono- transparent. After clearing, the samples phyly of Eschweilera and Lecythis and to were washed with water to remove NaOH study the phylogenetic relationships residue. The specimens were then mounted within the Bertholletia clade. To carry in Hoyer’s mounting medium. Alternatively, out these objectives we reexamined and samples were put in a 5% bleach solution redefined the characters used in previous until the stomata were visible when viewed classifications (Prance & Mori, 1979; with a compound microscope. Anatomical Mori & Prance, 1990b). In addition, we and morphological leaf features followed included more parsimony-informative the terminology the Leaf Architecture characters than the non-molecular charac- Working Group (1999). ters used in Morton et al. (1998)and Pollen morphology was studied using more taxa of the Bertholletia clade than scanning electron microscopy (SEM). Pol- Mori et al. (2007). len samples were taken from herbarium specimens with mature flowers or flower buds at an advanced stage of development. Methods and materials were boiled until softened and, Sampling.—This study included 86 ingroup with aid of a dissecting microscope, anthers taxa, representing Bertholletia, Corytho- were removed from the staminal ring and phora, Eschweilera,andLecythis. Taxon the ligule for species that have ligular sampling covers the range of morphological anthers. The anthers were air-dried and variation in genera and sections recognized pollen was then shed and mounted directly by Mori and Prance (1990b). Fourteen onto a SEM stub and coated with gold. The species were included as outgroup taxa, coated pollen was observed with a Hitachi representing Gustavia, Grias, Allantoma, S2700-SEM. Cariniana, Couroupita,andCouratari.The Characters were divided into two or more selection of the outgroup taxa followed the discrete states. All multi-state characters were molecular analysis of plastid ndhF and coded as non-additive. The following 49 trnL-F sequence data, but with fewer characters were included in the analysis. The species for each genus (Mori et al., 2007). data matrix is shown in Table II. 2011] HUANG ET AL.: MORPHOLOGICAL ANALYSIS OF LECYTHIDOIDEAE 399

TABLE I TABLE I LIST OF SAMPLED TAXA (NO. OF SAMPLED/NO. OF TOTAL (CONTINUED). SPECIES). TAXAWITH * ARE TYPE SPECIES OF THE GENUS OR E. rimbachii Standl. SECTION; TAXAWITH ** ARE TYPE SPECIES OF BOTH SECTION E. sagotiana Miers AND GENUS. E. sessilis A. C. Sm. E. simiorum (Benoist) Eyma Bertholletia Bonpl. (1/1) E. subglandulosa (Steud. ex O. Berg) Miers B. excelsa Bonpl. E. tessmannii R. Knuth Corythophora R. Knuth (4/4) E. tresoriana sp. ined. C. alta R. Knuth* E. truncata A. C. Sm. C. amapaensis Pires ex S. A. Mori & Prance E. wachenheimii (Benoist) Sandwith C. labriculata (Eyma) S. A. Mori & Prance Lecythis Loefling (25/27) C. rimosa W. Rodrigues subsp. rimosa Section Corrugata S. A. Mori (5/5) C. rimosa W. Rodrigues subsp. rubra S. A. Mori L. confertiflora (A. C. Sm.) S. A. Mori Eschweilera Mart. ex DC (55/93) L. corrugata Poit.* Section Tetrapetala S. A. Mori (3/3) L. idatimon Aubl. E. alvimii S. A. Mori L. persistens Sagot subsp. aurantiaca S. A. Mori E. tetrapetala S. A. Mori* L. persistens Sagot subsp. persistens E. compressa (Vellozo) Miers L. pneumatophora S. A. Mori Section Bracteosa S. A. Mori (2/4) Section Pisonis S. A. Mori (4/4) E. bracteosa (Poeppig ex O. Berg) Miers* L. ampla Miers E. cyathiformis S. A. Mori L. lanceolata Poiret Section Jugastrum Prance & S. A. Mori (1/1) L. pisonis Cambess.* E. tenuifolia (O. Berg) Miers* L. zabucajo Aubl. Section Eschweilera S. A. Mori & Prance (49/85) Section Poiteaui S. A. Mori (3/3) E. aguilarii S. A. Mori L. barnebyi S. A. Mori E. alata A. C. Sm. L. brancoensis (R. Knuth) S. A. Mori E. albiflora (DC.) Miers L. poiteaui O. Berg* E. amazonica R. Knuth Section Lecythis S. A. Mori (13/15) E. amazoniciformis S. A. Mori L. alutacea (R. Knuth) S. A. Mori E. amaplexifolia S. A. Mori L. chartacea O. Berg E. andina (Rusby) J. F. Macbr. L. gracieana S. A. Mori E. antioquensis Dugand & Daniel L. holcogyne (Sandwith) S. A. Mori E. apiculata (Miers) A. C. Sm. L. lurida (Miers) S. A. Mori E. atropetiolata S. A. Mori L. mesophylla S. A. Mori E. biflava S. A. Mori L. minor Jacq. E. calyculata Pittier L. ollaria Loefling** E. caudiculata R. Knuth L. parvifructa S. A. Mori E. chartaceifolia S. A. Mori L. prancei S. A. Mori E. collina Eyma L. retusa Spruce ex O. Berg E. congestiflora (Benoist) Eyma L. schomburgkii O. Berg E. coriacea ( DC) S. A. Mori L. tuyrana Pittier E. correae sp. ined. Outgroup taxa E. decolorans Sandwith Gustavia speciosa (Kunth) DC. E. grandiflora (Aubl.) Sandwith Grias peruviana Miers E. hondurensis Standley Allantoma decandra (Ducke) S. A. Mori, Y.-Y. Huang E. integrifolia (Ruiz & Pav. ex Miers) R. Knuth & Prance E. jacquelyniae S. A. Mori Allantoma integrifolia (Ducke) S. A. Mori, Y.-Y. Huang E. juruensis R. Knuth & Prance E. laevicarpa S. A. Mori Allantoma lineata (Mart. ex O. Berg) Miers E. longirachis S. A. Mori Cariniana estrellensis (Raddi) Kuntez E. mexicana T. Wendt, Mori & Prance Cariniana pyriformis Miers E. micrantha (O. Berg) Miers Couratari guianensis Aubl. E. nana (O. Berg) Miers Couratari macrosperma A. C. Sm. E. neei S. A. Mori Couratari multiflora (Sm.) Eyma E. ovalifolia (DC) Nied. Couratari stellata A. C. Sm. E. ovata (Cambess.) Mart. ex Miers Couroupita guianensis Aubl. E. panamensis Pittier Couroupita nicaraguianensis DC. E. parviflora (Aubl.) Miers Couroupita subsessilis Pilg. 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 400 TABLE II DATA MATRIX FOR PHYLOGENETIC ANALYSIS .INAPPLICABLE CHARACTERS ARE INDICATED WITH DASHES “-” UNKNOWN CHARACTER STATES ARE INDICATED WITH QUESTION MARKS “?”, ALL STATES ARE SHOWN FOR POLYMORPHISMS .

Taxon 1 5 10 15 20 25 30 35 40 45

Bertholletia excelsa 1000101111 00010 1 02 11 01110 0- 000 10110 0112 1 10000 00- 0 Corythophora alta 1000001111 01010 4 02 11 01110 0- 010 01110 1010 1 10000 0100 Cory. amapaensis 1000001111 01010 4 02 11 01110 0- 010 00110 1010 1 10000 0100 Cory. labriculata 1000001111 01010 4 02 11 01110 0- 010 00110 1012 1 10000 0100 Cory. rimosa 1000001111 01010 4 02 11 01110 0- 010 01110 1010 1 10000 0100 Cory. rimosa rubra 1000001111 01010 4 02 11 01110 0- 010 01110 1010 1 10000 0100 Eschweilera aguilarii 1001001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0120 E. alata 1000001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 E. albi flora 1001001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 E. alvimii 1000001111 01010 4 00 11 01110 10001 00110 0110 1 10000 0100 E. amazonica 1000001111 00010 4 02 11 01110 11010 00110 0110 1 10000 0110 E. amazoniciformis 1000001111 00010 2 00 11 01110 11010 00110 0110 1 10000 0100 E. amplexifolia 1001001111 00010 4 02 11 01110 11010 00110 0110 1 10000 0120 E. andina 1001001111 00010 4 02 11 01110 11010 00110 0110 1 10000 0120 E. antioquensis 1001001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 E. apiculata 1000001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 E. atropetiolata 1000001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 fl E. bi ava 1000001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 BRITTONIA E. bracteosa 1000001111 00111 4 02 11 01110 11010 00110 0110 1 10000 0110 E. calyculata 1001001111 00010 4 02 11 01110 11010 00110 0110 1 10000 0120 E. caudiculata 1001001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 E. chartaceifolia 1000001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 E. collina 1001001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 E. compressa 1000001111 00110 4 00 11 01110 10001 00110 0110 1 10000 0100 E. correae sp.ined 1001001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 E. coriacea 1001001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 E. cyathiformis 1000001111 00111 4 02 11 01110 11010 00110 0110 1 10000 0110 E. decolorans 1100001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 E. grandi flora 1101001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 E. hondurensis 1000001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 E. integrifolia 1001001111 00010 4 02 11 01110 11010 00110 0110 1 10000 0120 E. jacquelyniae 1001001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 E. juruensis 1000001111 00010 4 02 11 01110 11010 00110 0110 1 10000 0110 E. laevicarpa 1100001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 E. longirachis 1001001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0120 E. mexicana 1001001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 E. micrantha 1000001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 E. nana 1000001111 01010 4 02 11 01110 10001 00110 0110 1 10000 0100 E. neei 1001001111 ?0110 4 02 11 01110 11010 00110 0110 1 10000 0110 E. ovalifolia 1000001111 00010 4 02 11 01110 11010 00110 0110 1 10000 0120 E. ovata 1000001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 E. panamensis 1001001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0120 E. parvifolia 1000001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 E. parvi flora 1001001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 E. pedicellata 1000001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 E. pittieri 1001001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 63 [VOL E. pseudodecolorans 1000001111 00110 4 02 11 01110 11010 00110 0112 1 10000 0110 E. rankiniae 1000001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 E. rimbachii 1001001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 E. sagotiana 1000001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 E. sessilis 1001001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0120 2011] TABLE II (CONTINUED ). Continued Taxon 1 5 10 15 20 25 30 35 40 45 E. subglandulosa 1000001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 E. tenuifolia 1000001111 00010 4 02 11 01110 11010 00110 0110 1 10000 00- 0

E. tessmannii 1000001111 00010 4 02 11 01110 11010 00110 0110 1 10000 0110 AL ET HUANG E. tetrapetala 1000001111 01110 4 00 11 01110 10001 00110 0110 1 10000 0100 E. tresoriana 1001001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 E. truncata 1000001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 E. wachenheimii 1001001111 00110 4 02 11 01110 11010 00110 0110 1 10000 0110 Lecythis alutacea 1000001111 00010 4 12 11 01110 0- 000 10110 0112 1 10000 0100 L. ampla 1100001111 00010 4 02 11 01110 0- 010 01010 0002 1 10100 0100 L. barnebyi 1000101111 00010 4 02 11 01110 0- 010 01010 0112 1 10000 0100 L. brancoensis 1000101111 00010 4 02 11 01110 0- 010 01010 0112 1 10000 0100 L. chartacea 1000001111 00110 4 02 11 01110 0- 000 10110 0112 1 10000 0100 L. conferti flora 1000001111 00100 4 02 11 01110 0- 110 00010 1112 1 10000 0100 .:

L. corrugata 1000001111 00100 4 02 11 01110 0- 010 00110 1112 1 10000 0100 LECYTHIDOIDEAE OF ANALYSIS MORPHOLOGICAL L. gracieana 1000001111 00010 4 02 11 01110 0- 000 10110 0112 1 00000 00- 0 L. holcogyne 1000001111 00010 4 12 11 01110 0- 000 10110 0112 1 10000 0100 L. idatimon 1000001111 00100 4 02 11 01110 0- 110 00010 1112 1 10000 0100 L. lanceolata 1100001111 00110 4 02 11 01110 0- 010 01010 0002 1 10100 0100 L. mesophylla 1000001111 00010 4 02 11 01110 0- 000 10110 0112 1 10000 0100 L. minor 1000001111 00010 4 02 11 01110 10010 00110 0112 1 10000 0100 L. ollaria 1000001111 00010 4 02 11 01110 10010 00110 0112 1 10000 0100 L. parvifructa 1000001111 00010 4 ?2 11 01110 0- 000 10110 0112 1 00000 0100 L. persistens 1000001111 00100 4 02 11 01110 0- 110 01010 1112 1 10000 0100 L. persistens aurantiaca 1000001111 00100 4 02 11 01110 0- 110 01010 1112 1 10000 0100 L. pisonis 1100001111 00110 4 02 11 01110 0- 010 01010 0002 1 10100 0100 L. pneumatophora 1000001111 00100 4 02 11 01110 0- 110 00010 1112 1 10000 0100 L. poiteaui 1000101111 00010 4 02 11 01110 0- 010 01010 0112 1 10000 0100 L. prancei 1000001111 00010 4 12 11 01110 0- 010 00110 0112 1 00000 00- 0 L. retusa 1000101111 00010 4 02 11 01110 0- 000 10110 0112 ? 10000 0??0 L. rorida 1000001111 00010 4 02 11 01110 0- 000 10110 0112 ? 10000 0??0 L. schomburgkii 1000001111 00110 4 12 11 01110 0- 000 10110 0112 1 10000 0100 L. tuyrana 1000001111 00010 4 02 11 01110 10010 00110 0112 1 10000 0100 L. zabucajo 1100001111 00010 4 02 11 01110 0- 010 01010 0002 1 10100 0100 Gustavia speciosa 0000001011 10110 0,202,310 1- 00------010 0014 0 - 0000 0??2 Grias peruviana 0000001011 10110 0,1,2 0 0 0 0 1 - 0 0 ------0 1 0 0 0 1 2 0 - 0 0 0 0 0 0 - 0 A. decandra 1000000000 00010 3 01 00 1- 00------000 0011 1 10001 00- 1 A. integrifolia 1000000000 00010 3 01 00 1- 00------000 0011 1 10001 00- 1 A. lineata 1000000000 00010 3 01 00 1- 00------000 0012,31 10000 00- 0 Cariniana estrellensis 1000011111 10110 4 02 11 1000------000 0011 1 10001 00- 1 Cariniana pyriformis 1000011111 10110 4 02 11 1000------000 0011 1 10001 00- 1 Couratari guianensis 0010001111 10110 4 02 11 01111 - - 010 00100 0101 1 10000 10- 1 Couratari macrosperma 0010001111 ?0110 4 02 11 01111 - - 010 00100 0101 1 10000 10- 1 Couratari multi flora 0000001111 10110 4 02 11 01111 - - 010 00100 0101 1 10000 10- 1 Couratari stellata 0010001111 00110 4 02 11 01111 - - 010 00100 0101 1 10000 10- 1 Couroupita guianensis 0100001011 10110 4 02 11 01110 0- 010 01011 0014 0 - 1010 00- 1 Couroupita 0100001111 10110 4 02 11 01110 0- 010 01011 0014 0 - 1010 00- 1 nicaraguarensis Couroupita subsessilis 0100001011 10010 4 02 11 01110 0- 010 0101? 0014 0 - 1010 00- 1 401 402 BRITTONIA [VOL 63

1. Wood color. 0= sapwood not distinct from heartwood, 9. Quaternary venation. 0= dichotomizing, 1= regular 1= sapwood distinct from heartwood. Wood color is polygonal reticulate. In the dichotomizing type the pale-yellow to tan without distinction between sap- fourth-order veins branch freely, i.e., they do not wood and heartwood in Gustavia, Grias, Couroupita, unite with other veins and are the finest order of and Couratari. In contrast, the heartwood varies from venation that the leaf exhibits (Fig. 39.4 in Leaf reddish to chocolate brown and the sapwood is pale in Architecture Working Group, 1999). In the regular Allantoma, Cariniana, Corythophora, Bertholletia, polygonal reticulate type, the fourth-order veins Eschweilera, and Lecythis (Zeeuw, 1990). join to form polygons of similar size and shape 2. Oxidation of wounded tissues. 0= absent, 1= present. (Fig. 39.3 in Leaf Architecture Working Group, Wounded tissues oxidize and turn blue in species of 1999). Fifth order veins are the finest venation in Couroupita, some species of Lecythis (e.g., Lecythis this type. The fourth-order venation of Allantoma is pisonis Cambess. and its relatives), and a few species of dichotomizing. The fourth-order venation of all other Eschweilera (e.g., Eschweilera decolorans Sandwith). species of the Lecythidoideae is regular polygonal The color change is most distinct in wounded flowers and reticulate. fruits. 10. Areolation. 0= not well developed, 1= well devel- 3. Leaf pubescence, abaxial surface. 0= glabrous, 1= oped. Areoles are the smallest areas of leaf tissue pubescent. Some species of Couratari section Echi- surrounded by veins of any order (Leaf Architecture nata Prance and Couratari section Couratari Prance Working Group, 1999). The areoles are defined as have stellate hairs on the abaxial leaf surface. The poorly developed if they are highly irregular in size abaxial leaf surface is glabrous in all other species of and shape (Fig. 41.2 in Leaf Architecture Working the Lecythidoideae, including species of Couratari Group, 1999). Poorly developed areoles are only section Microcarpa Prance. found in species of Allantoma. In all other species of 4. Leaf punctations, abaxial surface. 0= absent, 1= present. Lecythidoideae the areoles are well developed with Many species of Eschweilera have black, brown, or four or five sides. reddish-brown dots on the abaxial leaf surface. These 11. Stomatal type. 0= brachyparacytic, 1= anomocytic. dots sometimes are referred to as cork warts (Roth, 1984; In brachyparacytic stomata, two cells are parallel to Fig. VII-4 in Mori & Black, 1987). the long axis of the guard cells but not completely 5. Leaf papillae, abaxial surface. 0= absent, 1= present. enclosing them (Fig. 55.12 in Leaf Architecture Papillae are outgrowths of the cuticle. This character is Working Group, 1999). In anomocytic stomata, five found in Bertholletia, some species of Lecythis (e.g., or more cells surround the guard cells and the cells Lecythis poiteaui O. Berg), and some species of Eschwei- adjacent to the guard cells are not differentiated in lera (e.g., Eschweilera congestiflora (Benoist) Eyma). any way from other epidermal cells (Fig. 55.2 in Mori and Black (1987) hypothesized that papillae may Leaf Architecture Working Group, 1999). Brachy- have adaptive value in reducing water loss through the paracytic stomata are found in Allantoma, Corytho- stomata. phora, Bertholletia, Eschweilera, Lecythis, and some 6. Domatia. 0= absent, 1= present. Domatia are small species of Couratari. Anomocytic stomata are found cavities at the junction of the secondary vein with the in Gustavia, Grias, Cariniana, Couroupita,and primary vein. These cavities are often lined with hairs and some species of Couratari. inhabited by mites (Huang, pers. obs.). Domatia are only 12. Inflorescence scales. 0= absent, 1= present. The rachis of found in some species of Cariniana (e.g., Cariniana the inflorescence is squamate in Eschweilera alvimii S. A. estrellensis (Raddi) Kuntze). Mori, Eschweilera nana (O. Berg) Miers, Eschweilera 7. Venation type. 0= eucamptodromous, 1= brochidodr- tetrapetala S. A. Mori and species of Corythophora. omous. In eucamptodromous venation, the secondary 13. Pedicel. 0= absent, 1= present. In Lecythidoideae, veins curve upward and gradually diminish apically pedicels are absent in species with spike or spike-like inside the margin without forming prominent arches inflorescences; pedicels are present in species with (Fig. 29.3 in Leaf Architecture Working Group, 1999). racemose or fasciculate inflorescences; and pedicels In brochidodromous venation, the secondary veins may or may not be present in species that have join together in a series of prominent arches (Fig. 29.1 paniculate inflorescences. in Leaf Architecture Working Group, 1999). The 14. Pedicel/ surface. 0= rugose/tuberculate, eucamptodromous venation pattern is found in species 1= not rugose/tuberculate. Species of Lecythis of Allantoma. All other genera have brochidodromous section Corrugata S. A. Mori have rugose/tuber- venation pattern. culate pedicels and hypanthia. This character is not 8. Tertiary venation. 0= percurrent, 1= reticulate. In found in any other species of Lecythidoideae. percurrent tertiary venation, the tertiary veins cross 15. Bract and bracteole persistence. 0= caducous, 1= between adjacent secondary veins in parallel paths persistent. The Lecythidoideae have one bract and without branching (Fig. 35.1 in Leaf Architecture two smaller bracteoles that enclose young flower Working Group, 1999). In reticulate tertiary venation, buds. The bract is located at the base of the pedicel the tertiary veins join with other tertiary or secondary while bracteoles usually are on the pedicel between veins at random angles (Fig. 35.4 in Leaf Architecture the base and the articulation of the pedicel or are Wo r k i n g G r o u p , 1999). The tertiary venation of located at the base of the pedicel just above the species of Allantoma and some species of Gustavia, bract. The bract and bracteoles are caducous in most Grias, Couroupita and Couratari are percurrent. The species, but in a few species they are persistent at tertiary venation of other species of the Lecythidoi- anthesis (e.g., Eschweilera bracteosa (Poepp. ex O. deae is reticulate. Berg) Miers). 2011] HUANG ET AL.: MORPHOLOGICAL ANALYSIS OF LECYTHIDOIDEAE 403

16. Calyx lobe number. 0= entire, 1= two, 2= four, 3= five, 21. tube. 0= absent, 1= present. In Gustavia, 4= six. Bertholletia excelsa has two calyx lobes. Grias Grias, and Allantoma, the basal portions of the neuberthii J. F. Macbr. and Eschweilera amazonicifor- filaments fuse and elongate to form a tube (Fig. 1A). mis S. A. Mori have four calyx lobes; species of The stamens arise directly from the rim of the tube in Allantoma have five calyx lobes; and species of Gustavia; from the rim and the upper inner surface Cariniana, Couroupita, Couratari, Lecythis, and most of the tube in Grias; and from the rim and the entire species of Eschweilera have six calyx lobes. Most inner surface of the tube in Allantoma. A staminal species of Grias have calyces that completely enclose tube is also found in species of Cariniana; however, the bud and open circumscissilely or irregularly one side of the tube elongates more than the other (Prance & Mori, 1979). For example, the calyces of and makes the androecium slightly zygomorphic Grias peruviana are entire or are split into two or four (Fig. 1B). The stamens of Cariniana also arise from irregular lobes (Mori, 1979b). The calyces of species of the rim or the entire inner surface of the tube. Gustavia are entire or four or six lobed (Mori, 1979a). Species of other zygomorphic-flowered genera do 17. Mucilage ducts in sepals. 0= absent, 1= present. Several not have a staminal tube. species of Lecythis section Lecythis S. A. Mori have 22. Type of zygomorphy. 0= oblique zygomorphy, 1= mucilage-bearing ducts in the sepals (e.g., Lecythis zygomorphy. An obliquely zygomorphic androecium alutacea (A.C.Sm.)S.A.Mori).Thecompositionand is characterized by the presence of a staminal tube, function of the mucilage is unknown. which is formed by uneven elongation of the fused 18. Petal number. 0= four, 1= five, 2= six, 3= eight. Species basal portions of the filaments. Obliquely zygomor- of Grias and some species of Eschweilera (e.g., E. phic androecia are found only in Cariniana tetrapetala) have four petals; species of Allantoma (Fig. 1B). On the other hand, a zygomorphic have five petals; species of Cariniana, Corythophora, androecium consists of a flat, donut-shaped cushion Couratari, Couroupita, Lecythis, and most species of and a strap-like structure, which is expanded from Eschweilera have six petals; and species of Gustavia one side of the cushion. The strap-like structure have six, eight, or twelve petals. Gustavia speciosa in curves over the staminal ring and the summit of the the present study has six or eight petals. ovary and is called the ligule. Zygomorphic androecia 19. Petal texture. 0= fleshy, 1= not fleshy.When the flowers are found in Bertholletia, Corythophora, Couratari, are fresh, the veins are invisible in fleshy petals when Couroupita, Eschweilera, and Lecythis (Fig. 1C). viewed with transmitted light. In contrast, the veins are Terminals with actinomorphic androecia were coded visible in non-fleshy petals. The fleshy petals are found as inapplicable. in Allantoma and Grias. The remaining genera of 23. Staminal ring. 0= absent, 1= present. In zygomor- Lecythidoideae, with a few exceptions, have non- phic-flowered genera, the stamens arise from a flat, fleshy petals. donut-shape cushion and surround the style to form a 20. Androecial symmetry. 0= actinomorphic, 1= zygomor- staminal ring (Fig. 2). Staminal rings are found in phic. In Lecythidoideae three genera (Gustavia, Grias, zygomorphic-flowered genera and are absent in and Allantoma) have radially symmetrical androecia Gustavia, Grias, Allantoma, and Cariniana. (actinomorphy) while seven genera (Bertholletia, Car- 24. Ligule. 0= absent, 1= present. A ligule is a strap-like iniana, Corythophora, Couratari, Couroupita, structure expanding from one side of the staminal Eschweilera,andLecythis) have bilaterally symmetrical ring (Fig. 2). The ligule is only found in zygomor- androecia (zygomorphy). phic-flowered genera. In most species the distal part

FIG.1. Structures of different androecial types. A. Actinomorphy, Gustavia hexapetala. Drawings are modified from Fig. 164 in Mori et al. (1997) and Fig. 2 in Mori et al. (2007). B. Oblique zygomorphy, Cariniana penduliflora. Drawings are modified from Fig. 70 in Prance and Mori (1979). C. Zygomorphy, Eschweilera pedicellata. Drawings are modified from Fig. 85 in Mori and Prance (1990b). 404 BRITTONIA [VOL 63

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

of the ligule bears appendages, which are separated Therefore the ligule of Couratari is coded as a from the staminal ring by a stamen/appendage-free separate character from the one of other zygomor- area (Fig. 2A). The only known exception is found phic-flowered genera. in Couroupita nicaraguarensis DC., which possesses 26. Coiled ligule. 0= absent, 1= present. In Bertholletia, a ligule without a stamen/appendage-free area Couroupita, Corythophora, and most species of (Fig. 2B). The appendage-bearing area of the ligule Lecythis, the ligule curves over the staminal ring is defined as the hood in Mori and Prance (1990b). and the summit of the ovary, but does not form a coil These appendages may or may not bear anthers. (Fig. 2). The appendage-bearing area of the ligule 25. External flap. 0= absent, 1= present. In Couratari, (the hood) is on top of the staminal ring and ovary in the appendage-free area of the ligule curves these species. On the other hand, in a few species of inward while the appendage-bearing area of the Lecythis and all species of Eschweilera, the ligule ligule (the hood) curves outward to form an further curves inward to form a single, a double, or a external flap (Fig. 3). This type of androecium is triple coil (Fig. 4). The hood is defined as that part of not found in any other zygomorphic-flowered the ligule extending beyond the distal end of the genera, in which the ligule only curves inward. appendage-free ligule.

FIG.3. External flap of Couratari. Couratari stellata. Drawing is modified from Fig. 51 in Mori and Prance (1990b). 2011] HUANG ET AL.: MORPHOLOGICAL ANALYSIS OF LECYTHIDOIDEAE 405

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

27. Ligular coil. 0= single, 1= double or triple. In a few Eschweilera (E. congestiflora and E. simiorum species of Eschweilera (e.g., E. alvimii) and Lecythis (Benoist) Eyma) and most species of Lecythis (e.g., Lecythis minor Jacq.), the ligule curves over section Lecythis. the summit of the staminal ring/ovary and bends 32. Anthers in the ligule. 0= absent, 1= present. inward once from the beginning of the appendage- Bertholletia excelsa, Corythophora amapaensis bearing area (the hood). The hood does not curve Pires ex S. A. Mori & Prance, Corythophora and lays straight between the appendage-free area of labriculata (Eyma) S. A. Mori & Prance, Lecythis the ligule and the staminal ring/ovary (Fig. 4A). In corrugata Poit., Lecythis confertiflora (A. C. Sm.) S. contrast, the hood further curves inward to form a A. Mori, and Lecythis pneumatophora S. A. Mori, double or a triple coil in most species of Eschweilera and species of Couratari, Eschweilera, and Lecythis (Fig. 4B). section Lecythis lack anthers in the ligule while 28. Ligular flanges. 0= absent, 1= present. In species of Corythophora alta, Corythophora rimosa W. A . Lecythis section Corrugata (excluding L. corru- Rodrigues, Lecythis persistens Sagot, and species gata), there is a well-developed flange that extends of Couroupita, Lecythis section Pisonis S. A. Mori from each side of the appendage-free area of the and Lecythis section Poiteaui S. A. Mori have ligule. This character is not found in any other anthers in the ligule. Morphologically, pollen of the zygomorphic-flowered species. ligular anthers may or may not differ from pollen of 29. Ligular appendages, on one side of the ligule. 0= absent, the anthers in the staminal ring. In Couroupita 1= present. Ligular appendages are located only on one guianensis Aubl. and C. nicaraguarensis, pollen of side of the ligule in some species of Lecythis,most the ligular anthers has a rugose surface and remains species of Eschweilera, and all species of Couroupita, in tetrads whereas pollen of the staminal ring has a Corythophora,andCouratari. smooth surface and is released in monads (Mori et 30. Ligular appendages. 0= absent, 1= present on both sides al., 1980; Tsou, pers. comm.). In of the ligule. In Eschweilera nana and species of and Aubl., ligular pollen does not Eschweilera section Te t r a p e t a l a , both the inner and the differ from pollen of the staminal ring in morphol- outer surfaces of the ligule bear appendages. This ogy. However, ligular pollen turns black later in character is not found in any other zygomorphic- anthesis, whereas pollen of the staminal ring does flowered species. not change color (Mori et al., 1980; Huang, pers. 31. Apical ligular appendages. 0= absent, 1= present. obs.). Ligular pollen in species of Corythophora and The appendages located at the apex of the ligule are Lecythis section Poiteaui (pers. obs.) is not in tetrads only found in Bertholletia excelsa, two species of and does not change color during anthesis. In vitro 406 BRITTONIA [VOL 63

experiments indicate that ligular pollen of Courou- species of Lecythis,e.g.,L. confertiflora.InCouratari pita guianensis and Lecythis pisonis does not and Eschweilera, nectar is produced from modified germinate while 21% of the pollen of the staminal appendages located at the apex of the ligular coil ring in the former species and 48% in the latter (Prance, 1990c;Mori&Prance,1990d); in Bertholletia species germinate (Mori et al., 1980). It is not excelsa, nectar is produced from the base of ligular known if the ligular pollen of other species is sterile. appendages (pers. obs.); in species of Lecythis,nectaris 33. Closed androecium. 0= absent, 1= present. Species produced from the base of ligular appendages (e.g., L. of Gustavia, Grias, Allantoma, Cariniana, Courou- confertiflora) or from the base of the stamens of the pita, and some species of Lecythis (e.g., Lecythis staminal ring (Lecythis persistens Sagot subsp. auran- idatimon Aubl.) have open androecia that allow tiaca S.A.Mori;Mori&Boeke,1987). potential pollinators and predators to easily reach the 38. Style apex. 0= with annular expansion, 1= without pollinator rewards. In contrast, species of Bertholle- annular expansion. An annular expansion right below tia, Corythophora, Couratari, and Eschweilera, and the apex of the style is only found in species of Lecythis some species of Lecythis (e.g., L. ollaria) have section Pisonis and some species of Couratari (e.g., closed androecia. The hood of these species presses Couratari stellata A. C. Sm.). against the staminal ring and limits the entry to 39. Ovary locules. 0= two, 1= three, 2= four, 3= five or pollinators with enough strength to open the hood. six. Most species of Corythophora and most species The degree of limitation depends on the tightness of of Eschweilera are two-locular; species of Coura- the hood against the staminal ring. Only pollinators tari, Cariniana, and most species of Allantoma are of the right body size have enough strength to push three-locular; species of Grias, Corythophora labri- their way into the flowers. An example was given in culata, Lecythis, and some species of Eschweilera a pollination study of Corythophora amapaensis and and Gustavia are four-locular. Allantoma lineata is C. rimosa (Mori & Boeke, 1987). Flowers of the four or five-locular; and Couroupita and some former species are larger and effective pollinators species of Gustavia are six-locular. tend to be larger bees than those that pollinate the 40. Operculum. 0= absent, 1= present. The operculum is latter species. Mori and Boeke (1987) observed that absent in species of Gustavia, Grias, and Courou- smaller trigonid bees similar to the pollinators of C. pita; the operculum is present in species of Allan- rimosa were not able to enter the flowers of C. toma, Cariniana, Couratari, Corythophora, amapaensis. Bertholletia, Eschweilera, and Lecythis. 34. Fertile stamens. 0= fewer than 50, 1= more than 100. 41. Operculum dehiscence. 0= indehiscent, 1= dehis- Fertile stamens are fewer than 50 in Allantoma and cent. In species of Allantoma, Cariniana, Couratari, most species of Cariniana, except Cariniana ianeir- Corythophora, Eschweilera, and most species of ensis R. Knuth, which has about 150 fertile stamens. Lecythis, the operculum falls spontaneously from the There are fewer than 100 fertile stamens in Coura- fruit and releases the seeds. In Bertholletia excelsa, tari. All other genera of Lecythidoideae have more the operculum is also dehiscent; however, it falls than 100 fertile stamens. Species of Cariniana and inside the fruit and the opening is smaller than the Couratari included in this study have fewer than 50 seeds. Thus, the seeds remain inside the fruit at fertile stamens. Therefore this character is divided maturity. The operculum is indehiscent in Lecythis into two states: fewer than 50 and more than one gracieana S. A. Mori, Lecythis parvifructa S. A. 100. Mori, and Lecythis prancei S. A. Mori. 35. Pollen aggregation. 0= monads, 1= tetrads. Most 42. Seeds embedded in pulp. 0= absent, 1= present. This species of Lecythidoideae have pollen in monads. character is only found in species of Couroupita.The Pollen in tetrads is only found in the ligule of seeds of Couroupita cannot be easily separated from the Couroupita guianensis and C. nicaraguarensis (Mori surrounding pulp, which is derived from the prolifer- et al., 1980; Tsou, pers. comm.). In vitro experiments ation of the septa and the placentae (Schoenberg, 1983). demonstrated that pollen in tetrads does not germinate Although the seeds of Gustavia and Grias are (Morietal.,1980). surrounded by pericarp, it is not juicy and pulpy and 36. Anther dimorphism. 0= absent, 1= present. When the the seeds can be easily removed from the fruit. flowers are fresh, all of the anthers in the same 43. Seeds sulcate. 0= absent, 1= present. The seeds of flower have the same color in most species of species of the Lecythis section Pisonis have longi- Lecythidoideae. The only known exceptions are tudinal grooves or furrows. This character is not found in species of Corythophora and Lecythis found in any other species of the Lecythidoideae. section Corrugata. Corythophora alta, C. rimosa, 44. Seed trichomes. 0= absent, 1= present. Seed and Lecythis persistens have anthers in the ligule. trichomes are an outgrowth of the exotesta (Tsou & The ligular anthers of these species are yellow or Mori, 2002). This character is only found in species orange while their anthers in the staminal ring are of Couroupita. white. Corythophora amapaensis, C. labriculata, 45. Unilateral seed wing. 0= absent, 1= present. Allan- Lecythis corrugata, L. confertiflora, L. idatimon,and toma (except A. lineata), Cariniana, and Couratari L. pneumatophora do not have ligular anthers. In the are the only genera of Lecythidoideae that have seed staminal ring, anthers of the innermost few rows (near wings. Tsou and Mori (2002) demonstrated that ligule) of these species are orange or dark yellow while unilateral seed wings in Allantoma/Cariniana and the remaining anthers are white or light yellow. circumferential seed wings in Couratari are differ- 37. Nectar. 0= absent, 1= present. Nectar is found in ent, both in origins and structures. Thus, seed wings Bertholletia excelsa, Couratari, Eschweilera,andsome are coded as two different characters. The unilateral 2011] HUANG ET AL.: MORPHOLOGICAL ANALYSIS OF LECYTHIDOIDEAE 407

seed wing originates from the mesophyll of the outer different from the androecium; some have integument of the ovule, there is no exotesta in the seed different colors at different parts of the petals wing, and the seed coat has branched vascular bundles but no fibers (Tsou & Mori, 2002). This character is (e.g., white petals with pink margins/apex); found in species of Cariniana and Allantoma,withthe and some have different colors at different exception of A. lineata. Seeds of A. lineata have no stages of anthesis, e.g., flowers of Lecythis unilateral wings but have rich oil content, which allows pisonis are purple at early stage and become them to float for at least six months (Ducke, 1948). fl Species of Cariniana and Allantoma that have seed completely white when owers are older. wings are wind dispersed, whereas A. lineata is water Characters of seed veins are very distinct in dispersed. A cladistic study of Cariniana and Allan- some species of Lecythis; however, variation toma indicated that the seed wings have been lost in A. of those characters is not fully understood and lineata (Huang et al., 2008). However, vestigial wings many taxa do not have any information for are found in seeds of A. lineata (pers. obs.). This suggests that the loss of seed wing is probably because character coding. Another excluded character is of adaptation for water dispersal. resin residue on the surface of the flowers or 46. Circumferential seed wing. 0= absent, 1= present. The immature fruits. The presence of resin was not circumferential seed wing originates from both the formally recorded in Lecythidoideae but was exotesta and the outer layers of mesotesta of the seed body, the seed wing has an exotesta, and the seed coat only mentioned occasionally on the labels of a has unbranched vascular bundles and fibers (Tsou & few herbarium specimens. It was first found in Mori, 2002). This character is only found in species of dry fruits of species of the Lecythis section Couratari. Corrugata, but more was discovered in species 47. Aril. 0= absent, 1= present. In most species of of Eschweilera. More study is needed before this Lecythidoideae, the seeds are attached to the ovary wall through a well-developed funicle that may or character can be used for phylogenetic analysis. may not be surrounded by a fleshy aril. Arils are not Phylogenetic analysis.—WinClada (Nixon, developed in species of Grias, Allantoma, Courou- 1999) was used to create the data matrix. pita, Cariniana, Bertholletia excelsa, Couratari, Characters were equally weighted and all Eschweilera tenuifolia (O. Berg) Miers, most species of Gustavia, and a few species of Lecythis (Prance & multi-state characters were coded as non- Mori, 1979; Mori & Prance, 1990b). additive. The parsimony-based program “ 48. Aril type. 0= basal, 1= lateral, 2= spreading. For analysis using New Technology” (TNT) was species that have a well-developed aril, the position used to generate phylogenetic trees (Goloboff of the aril is of taxonomic importance. Most species et al., 2008). A Maximum of 1000 trees was of Eschweilera have an aril running along the side of the seed (lateral), and some species of Eschweilera held and the combination of the following have an aril spreading around the seeds (spreading). algorithms was applied for tree search: The spreading aril may cover only the bottom part of Ratchet (RAT), Tree-Drifting (DFT), Secto- the seed or it may cover the whole seed. Some rial-Searches (SS), and Tree-Fusing (TF). The species of Gustavia, all species of Corythophora,a few species of Eschweilera, and most species of search strategy included two stages. The pur- Lecythis have an aril at the base of the seed (basal). pose of the first stage was to find the shortest 49. Cotyledons. 0= absent, 1= leaf-like, 2= fleshy. Cotyle- tree with the optimal score by performing 1000 dons are absent in Allantoma lineata, Bertholletia iterations of RATand 1000 cycles of DFT with excelsa, and all species of Corythophora, Eschweilera, random SS. The resulting trees were then and Lecythis. Species of Allantoma (except A. lineata), fi Cariniana, Couroupita and Couratari have leaf-like submitted to perform ve runs of TF. The cotyledons; and species of Gustavia have fleshy purpose of the second stage was to test the cotyledons. correctness of the consensus by finding the optimal score ten times independently. A strict Excluded characters.—Several characters consensus tree was calculated in Winclada. were explored for possible use but were Characters were optimized using the fast option excluded from the analysis. Characters of of Winclada. Branch support was constructed calyx imbrication and orientation and fruit by Bootstrap analysis with 1000 replications, shape and size are too variable and the 10 random taxon entry sequences per replica- variation is continuous and inconsistent. It is tion, and one tree saved per replication. difficult to divide the variation into discrete states and code each taxon accurately. color is useful on many occasions but is Results difficult to code. For example, many zygo- In total 49 informative characters were morphic-flowered species have a petal color included in the morphological data matrix. 408 BRITTONIA [VOL 63

Cladistic analysis generated 70 equally parsi- of inflorescence scales (Fig. 5; character 12) monious trees of 107 steps with a consistency and the absence of nectar (37). The mono- index (CI) of 0.52 and a retention index (RI) phyly of Corythophora is congruent with of 0.88. One of the trees is shown in Fig. 5, Mori and Prance (1990c) and Mori et al. and the strict consensus of all 70 trees is (2007). shown in Fig. 6. The topology of the strict Section Tetrapetala.—This clade contains consensus indicates that Bertholletia, Cory- all three species of Eschweilera section thophora, Eschweilera, and Lecythis together Tetrapetala (E. alvimii, Eschweilera com- (the Bertholletia clade) are monophyletic pressa (Vell.) Miers, and E. tetrapetala) (Fig. 6), albeit with <50% bootstrap support. recognized by Mori (1990a) and Eschweilera Within the Bertholletia clade, the resolution nana, which was included in Eschweilera further supports the monophyly of Corytho- section Eschweilera by Mori and Prance phora (Fig. 6) and a large clade that (1990e). The presence of appendages on both includes three species of Lecythis (L. minor, the inner and the outer surface of the ligule L. ollaria,andL. tuyrana) and all species (30) is a synapomorphy unique to section of Eschweilera except E. congestiflora and Tetrapetala clade (Fig. 5). Other synapomor- E. simiorum (Fig. 6). Lecythis is not phies include the presence of inflorescence resolved as monophyletic in the analysis, scales (12) and the absence of appendages on but Lecythis sections Corrugata, Pisonis only one side of the ligule (29). Within the and Poiteaui are monophyletic; Bertholletia clade, E. nana is sister to the other three excelsa, Eschweilera congestiflora, E. sim- species. A character that distinguishes E. iorum and species of Lecythis section nana from the other three species is the petal Lecythis A (excluding L. minor, L. ollaria, number (18). Eschweilera nana has six petals and L. tuyrana) remained as unresolved while the other three species have four petals. (Fig. 6). The sister relationship of E. nana and species of section Tetrapetala is a new finding of the present study. Discussion Mori (1990a) established section Tetrape- The Bertholletia clade and the phyloge- tala to accommodate three species that differ netic relationships within the clade.—The from all other species of Eschweilera in monophyly of the Bertholletia clade is having four instead of six petals (18), a non- supported in the present study. This result coiled instead of a double or triple-coiled is congruent with the previous molecular ligule (26, 27), and seeds with a basal instead analysis based on plastid ndhF and trnL-F of a lateral or spreading aril (48). It is sequence data (Mori et al., 2007). Synapo- confirmed that three species of section Tetra- morphies of the clade may be different in petala have a single instead of a non-coiled different most parsimonious (MP) trees ligule in the present study. A single-coiled because of different tree topology. None- ligule is only shared by E. nana and a few theless, many of the MP trees show that species of section Lecythis while seeds with a the monophyly of the Bertholletia clade is basal aril are shared by E. amazoniciformis, supported by the following characters: brachy- E. nana, all species of Corythophora, and paracytic stomata (Fig. 5,character11),ped- most species of Lecythis. Species of section icels absent (13), 4-locular ovaries (39), arils Tetrapetala and E. nana were placed in present (47), and cotyledons absent (49). Eschweilera because they have a two-locular Within the Bertholletia clade, four clades are ovary (39), which is an important feature for recognized, but the relationships among these most species of Eschweilera. Eschweilera clades are not resolved (Fig. 6). Clades and amazoniciformis and E. nana form a clade their synapomorphies are discussed in the in Mori et al. (2007). However, this sister following paragraphs. group relationship is not supported in the Corythophora.—This clade includes all present study (Fig. 6). four species of Corythophora recognized by Section Eschweilera B.—This clade Mori and Prance (1990c). Synapomorphies includes two species of Eschweilera section of the Corythophora clade are the presence Bracteosa S. A. Mori (E. bracteosa and 2011] HUANG ET AL.: MORPHOLOGICAL ANALYSIS OF LECYTHIDOIDEAE 409

Eschweilera cyathiformis S. A. Mori), the four species that have a bract and two only species of the monotypic Eschweilera smaller bracteoles persistent at anthesis (15; section Jugastrum Prance & Mori (E. tenui- Mori, 1990b). Section Jugastrum includes folia), and 45 species of Eschweilera section only one species, E. tenuifolia,which Eschweilera. Section Eschweilera B is sup- differs from other species of Eschweilera ported by the presence of a double or a triple- in having seed without an aril (47) and the coiled ligule (Fig. 5; character 27), which is seed germinates from the side instead of unique to this clade. The results of this study from the end (Prance & Mori, 1990). The indicate that the segregation of sections latter character is not included in the Bracteosa and Jugastrum from section present study because it is not parsimony Eschweilera is not supported because both informative. Section Eschweilera includes sections are nested within section Eschwei- most species of the genus (ca. 85 spp.). lera B(Fig.5). No further taxonomic Mori and Prance (1990e)defined that species in conclusions can be made because of the lack this section possess all of the following of resolution within the clade. features: six petals, a fully coiled androecial In Mori and Prance’s treatment (1990d), hood (referred as a coiled ligule (26) and a Eschweilera includes four sections. Section double or a triple coil (27) in the present study), Tetrapetala is discussed in the previous caducous bracts and bracteoles, and apical seed paragraph. Section Bracteosa consists of germination.

19 39 49 Gustavia speciosa 18 39 Grias peruviana 3949 A. lineata 7 9 10111318 45 A. integrifolia A. decandra

6 45 Cariniana pyriformis 116 3440 49 Cariniana estrellensis Couroupita nicaraguarensis Outgroup 2 35 39 404244 13 8 Couroupita subsessilis 8 161920 1 Couroupita guianensis

Couratari multiflora 25323334373846 Couratari guianensis 3 2122232434 Couratari macrosperma 11 Couratari stellata

1113 39 4749 Bertholletia clade A

FIG.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 indicate nodes collapsed in the strict consensus. Black circles show unique origins of states, and white circles are non-unique origins. A. Outgroup taxa and the Bertholletia clade. B. Lecythis, Corythophora, and Bertholletia. C. Eschweilera s.l./ Section Lecythis B clade. 410 BRITTONIA [VOL 63

B

FIG.5. (continued). 2011] HUANG ET AL.: MORPHOLOGICAL ANALYSIS OF LECYTHIDOIDEAE 411

C FIG.5. (continued). 412 BRITTONIA [VOL 63

In general, species of Eschweilera are pointed out the androecial resemblance characterized by a double or a triple coiled between L. corrugata and species of Cory- androecial hood (27), antherless hood appen- thophora and hypothesized the close relation- dages (32), a bilocular ovary (39), and seeds ships of section Corrugata through the link of with a lateral aril (48; Mori & Prance, 1990d). L. corrugata. This relationship is supported in Except for a double or a triple coiled ligule, the present study. other features are homoplasious in the present Section Pisonis.—This clade includes all study (Fig. 5). Mori et al. (2007) did not four species of Lecythis section Pisonis include section Tetrapetala in their study; recognized by Mori (1990c). Synapomor- section Eschweilera was divided into three phies of this clade include the presence of clades; and sections Bracteosa and Jugastrum oxidation of wounded tissues (Fig. 5; charac- were nested in the largest clade of section ter 2), an annular expansion below the apex Eschweilera (Fig. 1 in Mori et al., 2007). of the style (38), and sulcate seeds (43). The However, whether the three clades of monophyly of section Pisonis in the present Eschweilera are monophyletic is not resolved study is congruent with Mori (1990c) and in Mori et al. (2007). In contrast, the present Mori et al. (2007). study supports the monophyly of Eschweilera Section Poiteaui.—This clade includes all if E. congestiflora and E. simiorum are three species of Lecythis section Poiteaui excluded (Fig. 6). Nonetheless, both studies recognized by Mori (1990c). There is one demonstrate that the segregation of sections synapomorphy supporting this clade (Fig. 5): Bracteosa and Jugastrum from section the presence of leaf papillae on the abaxial Eschweilera is not necessary. surface (5). Mori et al. (2007) included only Section Corrugata.—This clade includes one species of section Poiteaui (L. poiteaui) all five species of Lecythis section Corrugata in their analysis. Their results showed that L. recognized by Mori (1990c). Synapomorphies poiteaui is nested in a clade that consists of of this clade are the presence of pedicels three species (L. prancei, L. minor and L. (Fig. 5; character 13) and rugose/tuberculate tuyrana) of section Lecythis (Fig. 1 in Mori et pedicels and hypanthia (14). The monophyly al., 2007). In the present study, however, L. of section Corrugata in the present study is minor, L. tuyrana, and L. ollaria are included congruent with Mori (1990c) and Mori et al. in a clade that contains all species of (2007). In addition, the present study also Eschweilera, except E. congestiflora and E. supports the sister relationship of Corytho- simiorum (Fig. 6). Lecythis ollaria is the type phora and section Corrugata (Fig. 5), which is species of Lecythis and section Lecythis not shown in Mori et al. (2007). The only (Mori, 1990c). This species is not included synapomorphy supporting this relationship is in Mori et al. (2007). Lecythis prancei along the presence of anther dimorphism (36), which with the remaining species of section Lecythis is also unique to Corythophora and section A, Bertholletia excelsa, E. congestiflora, and Corrugata. E. simiorum are unresolved in the consensus In addition to the presence of anther tree (Fig. 6). dimorphism, both species of Corythophora In Mori’s treatment (1990c), Lecythis is and section Corrugata have a non-coiled divided into four sections. Section Corrugata ligule (26), appendages present only on one includes five species that have rugose/tuber- side of the ligule (29), and seeds with a basal culate pedicels and hypanthia (14). Section aril (48). In general, species of section Pisonis consists of four species that are Corrugata can be distinguished from species characterized by the presence of wounded of Corythophora by an open instead of a tissues turning bluish (2), an annular expan- closed androecium (33) and a four instead of sion below the apex of the style (38), sulcate a two-locular ovary (39). However, one seeds (43), and pollen of the ligular anthers species of section Corrugata (L. corrugata) turning from yellow to black 24 hours after also has a closed androecium that resembles the flowers open. The last feature is not the one of Corythophora, and a four-locular included in the analysis but is described in ovary is also found in one species of the character of anthers in the ligule (32). Corythophora (C. labriculata). Mori (1990c) Section Poiteaui includes three species that 2011] HUANG ET AL.: MORPHOLOGICAL ANALYSIS OF LECYTHIDOIDEAE 413

Gustavia speciosa Grias peruviana 77 Cariniana pyriformis Cariniana estrellensis Couroupita subsessilis 89 Couroupita guianensis Couroupita nicaraguarensis A. lineata 92 Outgroup A. integrifolia A. decandra Couratari multiflora 93 Couratari guianensis Couratari macrosperma Couratari stellata E. simiorum E. congestiflora Section Eschweilera A Bertholletia excelsa Bertholletia L. chartacea L. rorida L. parvifructa L. alutacea L. retusa L. prancei Section Lecythis A L. schomburgkii L. gracieana L. mesophylla L. holcogyne L. brancoensis 55 L. poiteaui Section Poiteaui L. barnebyi L. zabucajo 78 L. lanceolata Section Pisonis L. pisonis L. ampla Corythophora labriculata 52 Corythophora amapaensis Corythophora alta Corythophora Corythophora rimosa Corythophora rimosa rubra L. corrugata 52 L. idatimon L. pneumatophora L. confertiflora Section Corrugata L. persistens L. persistens aurantiaca A Eschweilera s.l./Section Lecythis B

FIG.6. Strict consensus of 70 most parsimonious (MP) trees. Bootstrap values (>50%) are given above the branches. A. Outgroup taxa, Corythophora, Bertholletia,andLecythis. B. Eschweilera s.l./Section Lecythis B clade. have a terminal inflorescence, a flat androe- antheriferous appendages (32), and densely cial hood (referred as the absence of a packed stamens (up to 1000) on the coiled ligule (26) in the present study) with staminal ring (34). The first feature is not 414 BRITTONIA [VOL 63

L. minor Section E. amplexifolia L. ollaria Lecythis B E. apiculata L. tuyrana E. integrifolia E. nana 54 Section E. micrantha E. alvimii E. parviflora E. tetrapetala Tetrapetala E. pseudodecolorans E. compressa E. panamensis E. tessmannii E. laevicarpa E. atropetiolata E. decolorans E. amazonica E. rankiniae Section E. parvifolia E. truncata Eschweilera E. sp. ined. E. amazoniciformis E. tresoriana E. coriacea B E. jacquelyniae E. alata E. grandiflora E. pittieri E. sessilis Section E. antioquensis E. wachenheimii Eschweilera E. caudiculata E. ovata E. neei E. chartaceifolia B E. pedicellata E. mexicana E. collina E. albiflora E. andina E. sagotiana E. ovalifolia E. rimbachii E. subglandulosa E. aguilarii E. calyculata E. biflava E. juruensis E. hondurensis E. tenuifolia Section Jugastrum E. longirachis 61 E. bracteosa B E. cyathiformis Section Bracteosa FIG.6. (continued).

included in the analysis because of contin- hand, although the relationships are not com- uous and inconsistent variation. Section pletely resolved, the results of the present Lecythis has about 15 species that are study clearly indicate that Lecythis is not characterized by ligular appendages that monophyletic because section Corrugata is lack anthers and sweep inward without sister to Corythophora (Fig. 6) and three forming a complete coil. species of section Lecythis B(L. minor, L. Nonetheless, species of four sections all tuyrana,andL. ollaria) are more closely have a four-locular ovary (39), a well-defined related to Eschweilera than they are to other style, and ovules that are attached toward the species of Lecythis (Fig. 6). base of the septum (Mori, 1990c). The The position of Bertholletia excelsa in both character of ovary locule is homoplasious in the present study and Mori et al. (2007)is the present study. The last two features are not undetermined. Mori and Prance (1990a) included in the analysis because the variation suggested that the closest relatives of B. of the style is continuous and inconsistent and excelsa are some species of section Lecythis the attachment of the ovules is not parsimony based on morphological similarity. For exam- informative. Both Mori et al. (2007) and the ple, B. excelsa has a non-coiled ligule (26) present study support the monophyly of and the presence of appendages at the apex of sections Corrugata and Pisonis. However, the ligule (31), which is also found only in whether or not Lecythis is monophyletic is some species of section Lecythis. In addition, not resolved in Mori et al. (2007). On the other the presence of leaf papillae (5) on the abaxial 2011] HUANG ET AL.: MORPHOLOGICAL ANALYSIS OF LECYTHIDOIDEAE 415 surface is only found in B. excelsa, three Acknowledgments species of section Poiteaui, and a few species We thank Maristerra R. Lemes for her of section Lecythis. However, whether or not assistance in applying for collecting permits, B. excelsa and section Lecythis are mono- organizing field trips, and providing supplies phyletic is not resolved in the present study or for our field work in Amazonian Brazil. We Mori et al. (2007). are grateful to staff of the cited herbaria for Eschweilera congestiflora and E. simiorum their help with specimen study, Reinaldo were placed in section Eschweilera (Mori & Aguilar, Catherine Bainbridge, E. da Costa Prance, 1990d). However, both species have a Pereira, and C. A. Cid Ferreira for their help non-coiled ligule (26), the presence of the in the field. We also thank Robbin Moran for appendages at the apex of the ligule (31), a acting as editor-in-chief and two anonymous four-locular ovary (39), and seeds with a basal reviewers for reviewing our manuscript. The aril (48). These states are found in species of first author would also like to thank the section Lecythis A. Although the monophyly of Graduate Fellowship of The New York E. congestiflora, E. simiorum and species of Botanical Garden, Chancellor’s Fellowship section Lecythis A is undetermined in the of The Graduate Center of the City University present study, both species were included in a of New York, The Cuatrecasas Fellowship of clade that consisted of four species of section The Smithsonian Institution, The Travel Lecythis in Mori et al. (2007). It is likely that Award of Taipei Economic and Cultural both E. congestiflora and E. simiorum were Office in New York (TECO), The Willi placed in the wrong genus, but additional data Henning Society, and The National Tropical are needed in order to determine the genus to Botanical Garden for financial support of this which these two species belong. study.

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