Distinctions among Three Simarouba Species

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Distinctions among Three Simarouba Species Author(s): Edivani Villaron Franceschinelli, Kikyo Yamamoto and George J. Shepherd Source: Systematic Botany, Vol. 23, No. 4 (Oct. - Dec., 1998), pp. 479-488Published by: American Society of Plant TaxonomistsStable URL: http://www.jstor.org/stable/2419379Accessed: 28-04-2015 13:08 UTC

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Systematic Botany (1999), 23(4): pp. 479-488 (? Copyright 1999 by the American Society of Plant Taxonomists

Distinctions Among Three Simarouba Species

EDIVANI VILLARON FRANCESCHINELLI

Depto de Botanica, ICB, Universidade Federal de Minas Gerais Av. Antonio Carlos, 6627, Belo Horizonte MG, CEP: 31.270-901, Brazil

KIKYO YAMAMOTO and GEORGE J. SHEPHERD

Depto de Botanica, IB,Universidade Estadual de Campinas, Campinas SP, CEP:13.083-970, Brazil

Communicating Editor: Anita Cholewa

ABSTRACT. Simarouba amara is frequently confused with two other continental species of the neotropical genus, S. glauca and S. versicolor. Cluster and Principal Component Analyses were applied to verify the distribution and variation of the main diagnostic characters proposed in early revisions: flower and anther size, stamen appendage indument, leaflet surface, and venation features. Simarouba glatuca and S. versicolor were found to be morphologically closer to each other than to S. amara. Overlapping of characteristics in boundary populations of the three species was found. Geographical and morphological data other than leaf features also proved useful for species identification.

The neotropical genus Simarouba Aubl. (Simaroubaceae: Simarouboideae: Simaroubinae) comprises three predominantly continental species (S. amara Aubl., S. glauca DC., and S. versicolor A.St.- Hil.) and three species endemic to the Caribbean islands (S. berteroana Krug. & Urb. ex Urb., S. laevis Griseb., and S. tulae Urb.) [(Cronquist 1944; Franceschinelli and Yamamoto 1993) (Fig. 1)]. According to Engler (1874), Simarouba Aubl., Simaba Aubl. and Quassia L. comprise the subtribe Simaroubinae. Although Noteboom (1962) has transferred this subtribe to the rank of genus, we follow Engler's (1874) classification as has been followed in contemporary studies of the family Simaroubaceae (Thomas 1986; Pirani 1987; Franceschinelli and Yamamoto 1993).

Simarouba are trees and shrubs with alternate, pinnately compound (1-12 pairs of leaflets) leaves. The unisexual flowers are relatively small (up to 11.0 mm long) and arranged in large panicles (reduced in S. laevis). The calyx is connate along its basal half and has (4-) 5 (-6) sepals. The dialipetalous corolla also has (4-) 5 (-6) petals. The staminate flowers have (8-) 10 (-12) stamens with a scalelike appendage at the base of the filament. The pistillate flowers have a pseudo-apocarpous gynoe- cium comprised of a gynophore topped by (4-) 5 (- 6) individual, uniovulate carpels connate only along their ventral sutures and the single gynobasic style. The gynophore is present in staminate flowers, but the ovary is absent or vestigial. Stamens are absent or vesti-;ial in Distilate flowers. The fruit is a

carpophore with up to 5 drupaceous mericarps. Engler (1874) and Cronquist (1944) separate the species of this genus mainly by means of flower, petal and anther length, presence of indument on the stamen appendage, and leaflet surface and venation features.

Herbarium material confirms the diagnostic value of the characters used by Engler (1874) and Cronquist (1944) at distinguishing the insular species of Simarouba. We have observed, however, frequent confusion in the identification of the three continental species, S. amara, S. glauca, and S. versicolor. Field researchers have had problems separat- ing them, especially with plants from regions where their populations are parapatric such as in Costa Rica (S. amara and S. glauca), and in the States of Goias, Tocantins and Mato Grosso in Brazil (S. amara and S. versicolor). We previously found that leaf sclereid shape and their distribution pattern within the mesophyll provide a sharp distinction among the three continental species, and that S. glauca and S. versicolor could be more closely related to each other than to S. amnara (Franceschinelli and Yamamoto 1993).

The present study quantifies the variation of these diagnostic characters in S. amara, S. glauca and S. versicolor, in order to check their circumscription and the interspecific affinities suggested by that leaf anatomical study. Cluster analysis was used to define morphological groups and to visualize how these groups are related to each other. Ordination was used to verify how the various multistate variables differ among

479



480 SYSTEMATIC BOTANY [Volume 23

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30,

Adopted by E Z Bo.ghl --f trom H R Rypk*a \\ i X'o

110? tO0? 90? 80? 70? 60? 50? 40?

FIG. 1. Geographical distribution of the species of Simarouba Aubi. S. amara Aubi (A), S. berteroana Krug & Urb. ex Urb. (K), S. glauca DC (O), S. leavis Grieseb. (*), S. tullac Urb. (*), S. versicolor A. St. Hil.(O).

the species. Taxonomic interpretations based upon these analyses were supported by some other morphological and geographical information.

MATERIALS AND METHODS

In the present study, 123 specimens from 16 coun- tries were analyzed. The herbarium of the Missouri Botanical Garden (MO) provided the most important collection, which was complemented by specimens from Brazilian herbaria: Projeto RADAMBRASIL (HRB), Instituto Nacional de Pesquisas da Amaz6nia (INPA), Museu Nacional do Rio de Janeiro (R), Jardim Botanico do Rio de Janeiro (RB), Instituto de Botanica de Sao Paulo (SP), and Fundac,do Universi- dade de Brasflia (UB). Ninety-four different speci-

mens were used for numerical analyses (see Appen- dix 1). Additional morphological and geographical data were obtained from 32 specimens (Appendix 2), two of which had flowers and fruits and appear in both Appendix 1 and 2 (OTUs 62 and 86 of Appendix 1). The 30 remaining specimens of Appendix 2 were not included in Appendix 1 because they do not have flowers, from which many variables were obtained.

Data Analyses. The data matrix was obtained by considering each herbarium specimen as an OTU for which the diagnostic characters proposed by Engler (1874) and Cronquist (1944) in the latest revisions of the genus Simarouba (Table 1) were observed. Table 1 also shows the classes of qualitative characters adopted in the present study. Char- acters were standardized, so that each variable had



1999] FRANCESCHINELLI, ET AL.: SIMAROUBA 481

TABLE 1. Characters used for cluster and principal component analyses of the continental species of Simarouba Aubl. and the numerical values attributed to the phenotypic classes of these characters.

1. Flower length (mm) 2. Anther length (mm) 3. Stamen appendage indument

0 - Glabrous 1 - Glabrescent 2 - Pilose/villous

4. Leaflet adaxial epidermal cells (evident under low magnification 40x)

0 - not visible 1 - More or less conspicuous 2 - Very conspicuous

5. Indument of abaxial leaflet surface 0 - Glabrous 1 - Glabrescent/puberulous 2 - Pilose/tomentose

6. Leaf vein 0 - Immersed 1 - Prominulous 2 - Sharply prominent

a zero mean and a unit standard deviation. Ordinal values (0, 1, and 2) were assigned to the qualitative data (Table 1). Simple Euclidean distance was chosen as a similarity coefficient, because it is sensitive to additive, proportional, and minor image transla- tions. UPGMA (unweighted pair-group method using arithmetic averages), was chosen for this analysis because it minimally distorts the overall dissimilarities among groups.

In order to verify which of the variables account for most of the variation among groups and which are the most important in discriminating among species, Principal Component Analysis (PCA) was applied for a complete data set containing all three species and again for the S. glauca and S. versicolor data.

The computer program used to run Cluster and Principal Component Analyses was "FITOPAC 1.0" (Shepherd 1996). This program standardizes the data, provides the calculation of the distance matrix, and does the cluster and the ordination analyses.

RESULTS AND DISCUSSION

Cluster Analysis. The UPGMA clustering is presented in Fig. 2. Two large groups may be visual- ized in this dendrogram. The group on the left side (A) contains the whole sample of S. amara. The group on the right side is divided into two smaller clusters (B and C). Group B is composed almost entirely of S. glauca, including only four S. versicolor OTUs (numbers 82, 83, 84, and 94, which in fact cor-

respond to only three different specimens, since OTU 83 = OTU 84). Group C is basically composed of S. versicolor OTUs. Three OTUs of this species (numbers 95, 96, and 87) are sub-clustered on the right side of the dendrogram (probably because of their larger anthers) along with OTU 80 of S. glauca (probably due to its very large petals, pubescent leaflet, and obscured leaf veins).

The cluster analysis shows that the main characters used by Engler (1874) and Cronquist (1944) are useful in distinguishing S. amara from the other two species. However, S. glauca and S. versicolor are not as easily distinguished in this analysis. In order to check these results and determine which variables are the most important in discriminating among the species, PCA was applied to these data.

Principal Component Analysis (PCA). The variances accounted for the axes I to VI were respectively 55, 19, 10, 7, 6, and 3%. The first two principal axes (I and II) account for 74% of the variance. The diagram using the first two axes seems to reflect the taxonomic relationship among the species and groups of specimens.

The scatter of the specimens on axes I and II are shown in Fig. 3. Almost all of the characters used in this analysis made important contributions to axis I (Table 2). Flower and anther length and conspicu- ousness of leaf adaxial epidermal cells were the first three most important characters of this axis. Although the range of the two quantitative characters may overlap among the three species, S. amara is clearly distinguished from S. glauca and S. versicolor for a combination of these characters in axis I (Fig. 3). The sample of S. amara is concentrated on the left side of the diagram where OTUs with smaller flowers and anthers, leaf adaxial epidermal cells not visible under low magnification (40X), immersed leaf veins, and densely villous stamen appendages are located. Meanwhile, samples of S. glauica and S. versicolor are on the right side of the diagram where OTUs with larger flowers and anthers and leaf abaxial epidermal cells visible under low magnification (40X) are located. These OTUs have more prominent leaf veins and stamen appendages with sparser trichomes (especially S. glauca) than S. amara OTUs.

Axis II separates S. versicolor from S. glauca, although some OTUs belonging to one species are still mixed among those of the other. The main characters contributing to axis II are the density of trichomes on the abaxial leaf surface and stamen appendage (Table 2). Therefore, the predominant distribution of S. versicolor on the lower side of the diagram is due to the presence of trichomes on the




19 31 35 55 20 24 36 37 51 16 22

49 42 17 21 40 41 26 26 30 23 39 52 10 56 47 46 57 4

25 46 I5 8

1 1 34 33 50 54 7

1 2

27 36 63 73 65 65

643

6?6

62

72

75

76 77 79 61 64

67

62 64

60

66 76 65 86 92 70 53 67 92 694 90 96 67 60

SIMPLE EUCLIDEAN DISTANCE

FIG. 2. Dendrogram of the cluster analysis (UPGMA) applied to Simaroulba amara, S. glaulcaz and S. versicolor. In cluster A are S. azmara OTUs. In cluster B are mainly S. glaulca OTUs and in C are S. versicolor OTUs.

abaxial leaf surface and on the stamen appendage. The distribution of S. glauca OTUs on the upper side of the diagram is due to the glabrous or glabrescent leaflets and stamen appendages. These characteris-

tics are shared by three distinct S. versicolor specimens (or four OTUs: 82, 83, 84, and 94) which are still mixed with the S. glauca group. Although 83 and 84 OTUs belong the same specimen, they have




3.0-

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75

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1.04 ?. 223 @68 064,59 A58 @ 66

A1 A9 74

A29 AA6 45 94 *78 26 14*7 L4A10,56 A 3OAA A& !7A8 0177

0.0 A39* 8 -6?7* 0*72

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A33 ? 50 0 60

A43 *76 79 *80

-1.0 A34 *96

A38

095 *87

-2.0 *88 *90E89

*93 *91

85, 86

-3.0 - I97, 92

-3.0 -2.0 -1.0 0.0 1.0 2.0 3.0 4.0

FIG. 3. Ordination of Simarouba amara, S. glauca and S. versicolor on PCA axes I and II. A number along with the symbol * means that there are more than one OTU placed at the same point, as following: 7* = 7, 12,18, 32, and 53; 14* 14 and 28; 17* = 17, 21, 40, and 41; 19* = 19, 31, 35, and 55; 22* = 22, 16, 44, and 49; 24* = 24, 36, and 37; 39* = 39 and 23; 47* 47 and 48.

slight differences in flower length (1.2 mm in 83 and 1.3 mm in 84) and leaf epidermal cell evidence (more or less conspicuous in 83 and not visible in 84). This result reinforces the position of this S. versicolor specimen within the S. glauca group.

In summary, this PCA corroborates the cluster analysis, showing again that the diagnostic characters applied by Engler (1874) and Cronquist (1944) are useful to distinguish S. amara from S. glauca and S. versicolor, but not enough to separate these last two species. The geographical overlap of S. amara and S. glauca in Central America, and of S. amara and S. versicolor in South America have made the separation of these pairs of species difficult. If S. glauca and S. versicolor had overlapping ranges, the confusion between them would be much worse. Since the axes found in

the PCA with all three species do not necessarily cor- respond to the major axes of variation between S. glauca and S. versicolor, another PCA was carried out, including only the latter two species in order to check the pattern of character variation between them.

PCA Applied to S. glauca and S. versicolor. The variances accounted by axes I to VI were 41, 20, 16, 13, 5.2, and 4.8%, respectively. Axes I and H together account for 61% of the variance. The scatter of specimens between these two axes is shown in Fig. 4. The OTUs of S. glauca are somewhat clustered on the left side, while OTUs of S. versicolor are on the right side of the diagram and relatively more scattered than S. glauca. The contributions of each variable to axes I and II are presented in Table 3. Simarouba glauca is disfin- guished by the scarcity or absence of trichomes on its




TABLE 2. The contribution of each variable to axes I and II in the principal component analysis for Simarouba amara, S. glauca and S. versicolor.

AXES VARIABLES I II

Anther length 0.489(1) -0.246(5) Flower length 0.442(2) 0.130(6) Leaflet adaxial epidermal cells 0.423(3) -0.345(3) Leaflet vien 0.392(4) 0.331(4) Stamen appendage indument -0.386(5) -0.447(2) Indument of abaxial leaflet surface 0.289(6) -0.717(1)

leaves and stamen appendages and larger anthers, while Simarouba versicolor is mainly characterized by its densely tomentose leaves and villous stamen appendages and smaller anthers. Anther size differs between these two species, but their ranges overlap. For axis H, flower length is by far the most important

character followed by venation prominence. Simarouba versicolor has a greater variation in flower size than S. glauca, which may have caused the verti- cal dispersion of S. versicolor OTUs. The leaf veins of S. glauca are generally more evident than S. versicolor's. This probably contributed to the placement of the OTUs of S. glauca in the upper part of the diagram.

A sharp separation of S. glauca and S. versicolor was again not accomplished in this analysis. The two distinct specimens of S. versicolor (or three OTUs: 82, 83, and 84) which remain mixed within the S. glatnca group are specimens collected at the edge of the geo- graphic distribution of this species, in the State of Rond6nia-Brazil and in eastern Bolivia, where a dry forest type of vegetation is in contact with Amazon- ian rain forests. The location of these three OTUs in the diagram, separated from the other OTUs of S. versicolor, is due mainly to their larger anthers, sparsely pubescent stamen appendages, and glabrous leaflets.

2.5

@ 71

1.5 C 90 .70 *89

*81 * 64.72

630 073 @77 U 91

0.5 @ 61 08 062 @ 74 @79 *88 2

@65 .60

*82 85 * 82 * ~~~~~~~~93 86 *69 83 * 76 8

-0.5 - 068

E84 078 066

*96 * 87

-1.5 067

M*94 M*95

-2.5

80

-3.5 - I I I 1

-3.0 -2.0 -1.0 0.0 1.0 2.0 3.0

I FIG. 4. Ordination of S. glauca and S. versicolor on PCA axes I and II.




TABLE 3. The contribution of each variable to axes I and II in the principal component analysis for Simarouiba glauca and S. versicolor.

AXES VARIABLES I II

Indument of abaxial leaflet surface -0.524(1) 0.026(5) Anther length -0.520(2) -0.015(6) Stamen appendage indument -0.463(3) -0.307(3) Leaflet vein 0.362(4) -0.576(2) Leaflet adaxial epidermal cells -0.330(5) -0.246(4) Flower length 0.013(6) -0.715(1)

On the other hand, in a dry Costa Rican forest, Franceschinelli (pers. obs.) found a population of S. glauca with densely tomentose leaflets, as occurs in the OTUs 66 and 76 of this species from Florida and Jamaica, respectively. These OTUs are located close to some S. versicolor OTUs in the PCA diagram for the three species (Fig. 3). Therefore, common features of S. glauca may occasionally occur in S. versicolor and vice-versa.

The results obtained in this study confirmed the diagnostic value of the characters used by Engler (1874) and Cronquist (1944), but also that they are not always enough to separate the three continental species of the genus Simarouba. Petal form, after anthesis and fruit size and form, may provide other helpful morphological characters. Simarouba amara flowers generally have straight petals instead of being curled as found in S. glauca and S. versicolor. However, exceptions were found again, especially in plants of S. amara from the edges of its distribution area. For example, some OTUs of S. amara found in drier vegetation (e.g. OTU 32, from Humaita, Ama- zonas, Brazil) present curled petals. But fruit size in dry material differ clearly among the three species, at least for the 32 specimens where this character was analyzed (Appendix 2). Simarouba amara has smaller fruits (1.0-1.5 x 0.6-1.0 cm) than S. glauca (2.0-2.5- x 1.2-1.5 cm) and S. versicolor (2.0-2.5- x 1.5-2.0 cm). Leaf anatomy provides very constant and sharply distinctive characteristics for the three species (Franceschinelli and Yamamoto 1993). They represent the only exclusive characteristics for the three species, so they were used to check the identification of the OTUs with intermediary or mixed location in the cluster dendrogram and PCA diagrams.

Furthermore, from a geographical point of view, it is easy to separate S. glauca from S. versicolor. The for- mer has been collected only in dry forests of Florida, Central America, and few Caribbean islands. Its southern limit appears to be in Panama. In contrast, S. versicolor has been found only in the savanna and

dry forests of South America, mainly in Brazil, and its northern limit appears to be in xerophytic vegetation of N, NE, or NW-Brazil and E-Bolivia. There- fore, the rain forests of Panama and northern South America appear to be an ecological barrier that keeps these two species geographically separated. The allopatric distribution of S. glauca and S. versicolor, and the leaf anatomical data justify treating the three species as distinct taxa.

Results obtained in this study, as well as the anatomical data published by Franceschinelli and Yamamoto (1993), reinforce the hypothesis that S. glauca and S. versicolor may have evolved relatively little from a common ancestor or, as suggested by Cronquist (1944), that S. versicolor may have evolved from S. glauca or vice-versa. Sarmiento (1992) has suggested that the neotropical savannas have a common stock. Simaba blanchetii Turcz. (Simaroubacaeae) occurs in the savanna northern boundaries of Brazil, in the States of Mato Grosso and Piaui, and also in the savannas of Venezuela and Colombia. The distribution of this species is disrupted by the Amazonian forests. Other species show geographical distribu- tions disjunct between the savannas of South and Central America, such as Helicteres gttazttmeifolia Pilg. and H. baruensis DC (Franceschinelli, pers. obs.). Rynchospora consanguinea (Kunth) Boeckeler is disjunct between the Planalto of Brazil and southern Mexico (W. Thomas, pers. comm). There was probably a link between the savannas of Central and South America in a past geological age, and the fur- ther expansion of the lowland Amazonian rain forest may have eliminated or reduced the contact between these two areas (van der Hammen 1992).

The results from the numerical analyses with additional information as discussed above may be used to improve Cronquist's key (1944), as follows:

TAxONoMIC KEY

1. Anthers 0.4-1.0 (-1.2) mm long. Flowers 3-5 mm long, petals straight or occasionally curled after anthesis. Adaxial leaf epidermal cells not visible under low magnification (40X). Drupelets 1.0-1.5 x 0.6-1.0 cm. Honduras to Espirito Santo, Brazil, common in Amazonian rain forest riparian forests and the "cer- radao" vegetation of the Brazilian Central Plateau. . ............................ Simarouba amara

1. Anthers 1.0-2.0 mm long. Flowers 4-7.5 mm long, petals curled after anthesis. Adaxial leaf epidermal cells visible under low magnification (40X). Dru- pelets 2.0-2.5 x 1.3-2.0 cm ................. 2

2. Leaflets densely tomentose (seldom glabrescent or



https://www.researchgate.net/publication/261181070_Taxonomic_use_of_leaf_anatomical_characters_in_the_genus_Simarouba_Aublet_Simaroubaceae?el=1_x_8&enrichId=rgreq-33a37636-0b44-4d0f-9f5e-c695c38aad07&enrichSource=Y292ZXJQYWdlOzI2MTE3NzgyNTtBUzoyMjMyMTc5MzY1Mzk2NDhAMTQzMDIzMDcxMTIxMA==


glabrous) abaxially. Anthers 1.0-1.5 mm long. Sta- men appendage pilose/villous. Drupelets 2.0-2.5 x 1.5-2.0 cm. Savanna and dry forests of Brazil and Bolivia .. Simarouba versicolor

2'. Leaflets glabrous or glabrescent (rarely tomentose) abaxially. Anthers 1.3-2.0 mm long. Sta- men appendage glabrescent or glabrous. Dru- pelets 2.0-2.5 x 1.2-1.5 cm. Dry forests of Central and North America (Florida) and a few Caribbean Islands (Bahamas and Jamaica). . ......................... Simarouba glauca

ACKNOWLEDGMENTS. We thank the directors and cura- tors of the herbaria mentioned in the text from whom we have obtained material on loan. We are grateful to E. Gal- legher, W. Thomas, P. Wilson and D. Yanega for their valu- able comments and suggestions. This study was partly supported by a Scholarship from Fundacao de Amparo a Pesquisa do Estado de Sao Paulo (FAPESP-Bolsa de Aper- feiboamento, processo 83/2526-2) to E. V. Franceschinelli.

LITERATURED CITED CRONQUIST, A. 1944. Studies in the Simaroubaceae-II. the

genus Simaroiba. Bulletin of Torrey Botanical Club

71(3): 226-234. ENGLER, A. 1874. Simaroubaceae. Pages.197-246, ed. C.F.P.

Martius in Flora Brasiliensis 12(2), Munich. FRANCESCHINELLI, E.V. and K. YAMAMOTO. 1993. Taxonomic

use of leaf anatomical characters in the genus Simarouiba Aublet (Simaroubaceae). Flora 188(1): 117-121.

NOTEBOOM, H.P. 1962. Generic delimitation in Simaroubaceae tribus Simaroubeae and a conspectus of the genus Qucassia L.. Blumea 12(2): 509-527.

PIRANI, J.R. 1987. Flora da Serra do Cip6, Minas Gerais: Simaroubaceae. B.Botanica, Universidade de Sao Paulo 9: 219-226.

SARMIENTO, G. 1992. The savannas of tropical america. Pp: 245-285 in Ecosystems of the World (13): Tropical Savan- inas, ed. Bourliere, F.. Amsterdam: Elsevier.

SHEPHERD, G.J. 1996. FITOPAC 1.0. Manual do Usuario. Departamento de Botanica, Instituto de Biologia, UNICAMP. Campinas SP, Brazil.

SNEATH, P.A . and R.R. SOKAL 1973. Numerical Taxonomny. San Francisco: Freeman.

THOMAS, W.W. 1985: The Simaba gutianensis complex in northern South America.-Acta Amaz6nica, suppl. 15(1-2): 71-79.

VAN DER HAMMEN, T. 1992. Paleoecology and paleogeog- raphy of savannas. Pp: 19-35 in Ecosystems of the World (13): Tropical Savannas, ed. Bourli&re, F.. Amsterdam: Elsevier.

APPENDIX 1. Examined material of Sirnaroniba amara, S. glauca and S. versicolor for Cluster and Principal Component Analyses. The number of OTUs reaches 97 but this Appendix comprises only 94 different collections: two specimens (originally numbered as OTUs 41 and 48) were excluded and (*) OTUs 83 and 84 are duplicates from different herbaria of the same specimens.

OTU Collector Locality and Date Herbarium

S. amara 1 P.H. Gentle s.n. BELIZE, Stannbreek Distr., 22.1.1937 MO 1278787 2 PH. Gentle 3280 BELIZE, Stannbreek Distr., 22.1.1940 MO 1203056 3 Hartshorn 1372 COSTA RICA, Pr. Heredia, 18.XI.1979 MO 2884818 4 A.F. Sknctch s.n. COSTA RICA, Pr. S. Jose, 1.1939 MO 1103365 5 A.F. Sknctch s.n. COSTA RICA, Pr. S. Jose, 1.1939 MO 1152204 6 C.A. Shillingford s.n. DOMINICA, St. Paul, 21.1.1966 MO 2034177 7 Gentry & Dole 1946 PANAMA, Goofy Lake, 11.111.1977 MO 2605710 8 T.B. Croat 14026 PANAMA, B. Colorado, 22.111.1977 MO 2047187 9 E.L. Tyson s.n. PANAMA, Cerro Azul, 09.111.1969 MO 2217808

10 R.Foster 1666 PANAMA, B. Colorado, 30.111.1970 MO 2029377 11 TB. Croat 8368 PANAMA, B. Colorado, 03.111.1969 MO 1977534 12 Davidse & Gonzcclez 16580 VENEZUELA, D. Amacuro, 4-6.111.1979 MO 2886890 13 Davidse & Gonzdlez s.n. VENEZUELA, Dist. P. Camejo, 18.11.1978 MO 2706789 14 L. Marcano 283 VENEZUELA, 12.VII.1964 MO 2779881 15 GeWr,itr & Li,on 20239 COLOMBIA, Choco, 08.X.1977 MO 2717952 16 J.L). .SIhI;hcI1 s.n. COLOMBIA, Antioquia, 11.V.1977 MO 2661635 17 G. Klncg 3741 PERU, S. Martin, VII.1934 MO 1088718 18 J. Schnnike 9805 PERU, S. Martin, 12.VIII.1955 MO 2605877 19 A.A. Vargas s.n. PERU, Loreto, 13.XI.1962 MO 2935216 20 N. Begazo 198 PERU, Ucayali, 13.X.1980 MO 2924638 21 Meneces & Zabala s.n. BOLIVIA, P. Palomo-M. Berri, 02.IX.1979 MO 2424038 22 H.S. Irwin & al. 57530 SURINAME, Suild River, 24.IX.1963 MO 1799601 23 B. Magncire 24644 SURINAME, Tafelberg T. Mt., 06.IX.1944 MO 1570905 24 B. Magncire 24699 SURINAME, Tafelberg T. Mt., 06.IX.1944 MO 1570903 25 Duccke 60 BRAZIL, Manaus-AM, 01.XI.1935 MO 1159536 26 A. Janssen s.n. BRAZIL, Humaita-AM, 10.1.1980 MO 2185256 27 L. Coelho s.n. BRAZIL, Manaus-AM, 31.VIII.1955 INPA 1769 28 F. Mello & al s.n. BRAZIL, Manaus-AM, 12.VII.1955 INPA 1393










APPENDIX 1. Continued

OTU Collector Locality and Date Herbarium

S. amara 29 J. Chagas s.n. BRAZIL, Manaus-AM, O1.VIII.1956 INPA 4019 30 Rodrigues & Coelho 2595 BRAZIL, R. Negro-AM, 10.X.1961 INPA 9945 31 Luis s.n. BRAZIL, BR-17, km 4, AM, 28.VIII.1956 INPA 4132 32 A. Janssen s.n. BRAZIL, Humaita-AM, 10.1.1980 INPA 105602 33 R.L. Fr6es 25116 BRAZIL, R. Urubui-AM, 23.VIII.1949 SP 56810 34 D.F. Austin & al. 7103 BRAZIL, Porto Grande, 18.X.1979 INPA 105395 35 P. Cavalcante 3302 BRAZIL, Belem-PA, 16.VIII.1977 INPA 93416 36 Ducke s.n. BRAZIL, Baixo R. Negro-PA, 20.X.1920 INPA 12500 37 Anonymous BRAZIL, BR 22-PA, 27.X.1965 MO 1829723 38 M. Lobo & al. 185 BRAZIL, Santarem-PA, 06.XII.1978 HRB 4146 39 B. Ribeiro 1467 BRAZIL, Porto Platon-AP, 12.X.1976 MO 2775003 40 Krukoff 1966 BRAZIL, Maracume River-MA. 22.X.1932 MO 1042042 42 Malme s.n. BRAZIL, S. da Chapada-MT, 02.VII.1920 R 27979 43 C. Berg & al. s.n. BRAZIL, Humbold-MT, 16.X.1973 INPA 41891 44 E.P. Heringer & al. 26 BRAZIL, Brasilia-DF, 08.IX.1977 MO 2770394 45 Irwin & Soderstrom 5248 BRAZIL, Ch. Contagem-DF, 17.VIII.1964 SP 121825 46 E.P. Heringer & al. s.n. BRAZIL, Brasilia-DF, 1962 MO 2884865 47 J.A. Ratter & al. 3425 BRAZIL, Brasilia-DF, 09.VIII.1976 UB 44524 49 Anonymous BRAZIL, Ilh6us-BA, 03.IX.1944 R 41893 50 Blanchet 2727 BRAZIL, S. Jacobina-BA, 1837 MO 211473 51 Gomes & Miranda 183 BRAZIL, Aripuana-AM, 12.VIII.1976 INPA 63050 52 Ducke & A. Lima 64 BRAZIL, Gurjari-PE, 05.XII.1951 R 76234 53 F. Allemao 294 BRAZIL, State of Ceara-CE, no date R 71002 54 T.N. Guedes 641 BRAZIL, S. do Araripe-CE, 13.IX.1957 INPA 12501 55 I.A. Siqueira 20 BRAZIL, Linhares-ES, 08.IX.1978 INPA 105316 56 Anonymous BRAZIL, M. do Tabuleiro-ES, 02.X RB 114 57 Anonymous BRAZIL, M. do Tabuleiro-ES, 29.IX RB 104 58 Glaziou 11859 BRAZIL, Alcantara-RJ, 26.X.1880 R 7965

S. glauca 59 A.H. Curtiss 5625 USA, Key West-Florida, 18.IV.1896 MO 211495 60 H.N. Moldenke s.n. USA, Key Largo-Florida, 20.111.1930 MO 1003038 61 F Rugel 1846 USA, Florida Austral, "1842-1849" MO 211461 62 J. Farnum s.n. USA, SW end Plantation Key, II. 1930 MO 983783 63 A.P. Graber s.n. USA, S-Florida, III-VI/1877 MO 211460 64 A.H. Curtis s.n. USA, Elliott's Key, S-Florida, 111.1897 MO 211463 65 W.T. Gillis 7975 USA, S-Florida, 22.111.1969 MO 1974125 66 Correl & Correll 42011 BAHAMAS, 25.111.1974 MO 2624454 67 G.F. Gaumer s.n. MEXICO, Yucatan, 1917-21 MO 211466 68 G.F Gaumer s.n. MEXICO, Yucatan, 1917-21 MO 804634 69 G.F Gaumer s.n. MEXICO, Yucatan, 1917-21 MO 947991 70 W.E. Harmon s.n. GUATEMALA Crry, 26.XI.1970 MO 2187261 71 E. Contreras s.n. GUATEMALA, 22.111.1972 MO 2250830 72 E. Contreras 11066 GUATEMALA, Baja Verapaz, 27.11.1972 MO 2250844 73 R.T. Ortiz 1755 GUATEMALA, Sta. Elena, 13.V.1971 MO 2262863 74 E. Contreras s.n. GUATEMALA, Macanche, 22.111.1972 MO 2070570 75 I. Maxwell s.n. JAMAICA, 1927 MO 1611933 76 G.R. Proctor s.n. JAMAICA, Gouric Forest, 03.111.1971 MO 2041957 77 G. Yong s.n. HONDURAS, F. Morazan, 15.11.1977 MO 2640562 78 Nelson & Martinez 2014 HONDURAS, Yoro, 28.III-04.IV.1974 MO 2492646 79 Gillis & Gillis 10260 COSTA RICA, P. Guanacaste, 17.11.1971 MO 2412921 80 E.R. Heithaus 31 COSTA RICA, P. Guanacaste, 19.11.1971 MO 2276509 81 Escobar & Barrera 290 PANAMA, P. Veraguas, 22.XII.1973 MO 2225895

S. versicolor 82 J. Steinbach 7210 BOLIVIA, Lomas B. Vista, 01.IX.1095 MO 964449 83* M.G. Vieira & al. 1012 BRAZIL, Vilhena-RO, 07.XI.1979 MO 2888677 84* M.G. Vieira & al. 1012 BRAZIL, Vilhena-RO, 07.XI.1979 INPA 89333 85 Eiten & Eiten 5444 BRAZIL, I. Balsa-Loreto-MA. 01.IX.1963 SP 82307 86 Eiten & Eiten 5441 BRAZIL, I. Balsa-Loreto-MA. 01.IX.1963 SP 82311 87 C.C. Berg & al. s.n. BRAZIL, Humbold-MT, 16.X.1973 RB 152173 88 Anonymous BRAZIL, Cuiaba-MT, 22.VIII RB 1256 89 Andrade & Emmerich 461 BRAZIL, Sta. Isabel-TO, 12.IX.1960 R 111829 90 Anonymous BRAZIL, ca. Meia Ponta-GO, VIII.1872 R 70997 91 S. Barros da Silva 81 BRAZIL, Arraiais-GO, 30.VIII.1978 RB 202751 92 Martius 572 BRAZIL, State of Minas Gerais, no date MO 211474 93 Blanchet 3142 BRAZIL, State of Bahia, 1840 MO 1611960 94 Anonymous BRAZIL, Ilha Sta. Isabel-PI, no date RB 167039 95 G.M. Barroso 198 BRAZIL, Sete Cidades-PI, 14.IX.1977 RB 181236 96 Santino s.n. BRAZIL, Corrente-PI, 19.11.1982 HRB 00946 97 H.C. Cutler 8401 BRAZIL, Lavras-CE, 29.VIII.1945 MO 1627179




APPENDIX 2. Examined material of Simarouba amara, S. glauca and S. versicolor for fruit morphological analysis.

Collector Locality and Date Herbarium

S. amara D.F. Austin & al. 7028 BRAZIL, State of Amapa, 14.X.1979 INPA 97405 G. Vieira & al. 162 BRAZIL, State of Amazonas, Humaita, 25.IX.1979 INPA 88486 Prance & al. s.n. BRAZIL, State of Amazonas, HumaitA, 10.XI.1974 MO 2622328 A. Janssen s.n. BRAZIL, State of Amazonas, Humaita, 10.1.1980 INPA 95365 B. Albuquerque 1169 BRAZIL, State of Amazonas, Manaus, 07.X.1975 INPA 53279 Ducke 1178 BRAZIL, State of Amazonas, Manaus, 11.11.1943 MO 1264035 C. Manieri s.n. BRAZIL, State of Espirito Santo, Linhares, 1973 SP 127180 G.A. Black 47324 BRAZIL, State of Para, Bel6m, 13.XII.1947 INPA 2785 B. Maguire & al. 56636 BRAZIL, State of Rond6nia, Abuna, 14.IX.1963 SP 81240 Mota & Coelho 199 BRAZIL, State of Rondonia, Porto Velho, 22.IX.1975 INPA 52701 J. Murpa & al. 16949 BRAZIL, State of Roraima, Rio Uraricoera, 11.111.1979 INPA 85065 A.A. Beetle s.n. EL SALVADOR, 23.111.1939 MO 1240622 P Duss 2973 GUADELOUPE, 1892 MO 211468 A. Gentry 4937 PANAMA, Cerro Campana, 03.IV.1972 MO 2099468 R. Foster 831 PANAMA, Barro Colorado, 10.V.1969 MO 2042032 TB. Croat 8416 PANAMA, Barro Colorado, 05.111.1969 M01977496 T.B. Croat 8441 PANAMA, Barro Colorado, 07.111.1969 M01977517 A.A. Vargas s.n. PERU, Rio Mezan, 13.XI.1962 MO 2935216 L.M. Berti s.n. VENEZUELA, El Palmar-Delta Amacuro, 12.1.1965 MO 2142926

S. glauca Correll & Correll 42014 BAHAMAS ISLANDS, 25.111.1974 MO 2624453 R.R. Innes s.n. BELIZE, Aguacate, 11.IV.1979 MO 2690313 PH. Gentle s.n. BELIZE, 03.IV.1934 MO 1075876 J.D. Dwyer 10492 BELIZE, 27.111.1973 MO 2584693 G. W. Frankie s.n. COSTA RICA, Guanacaste, 14.IV.1969 MO 2121507 G.S. Hartshorn 1394 COSTA RICA, Bagaces, 07.111.1974 MO 2884870 R.T. Ortiz s.n. GUATEMALA, 13.V.1971 MO 2219256 M. Sierra 92 HoNDuRAs, Francisco Morazan, 07.V.1975 MO 2492704 J. Farnum s.n. (1) USA, Florida, SW end of Plantation Key, 11.1930 MO 983783 J. Farnum s.n. USA, Florida, SW end of Plantation Key, 11.1930 MO 983784

S. versicolor A.A. Dias 4 BRAZIL, State of Goias, Rio Araguaia, 06.X.1968 HRB 3027 Eiten & Eiten 5441 (2) BRAZIL, State of Maranhao, I. da Balsa, Loreto, 1.IX.1963 SP 82311 Prance & al. 18817 BRAZIL, State of Mato Grosso, Ch. Guimaraes, 11.X.1973 INPA 42296 L.A. Dambros 91 BRAZIL, State of Mato Grosso, S. F. Araguaia, 10.IX.1978 RB 205673

(1) This specimen = OTU 62 of Table 1. (2) This specimen = OTU 86 of Table 1.



Distinctions among Three Simarouba Species

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