Observations on the Phytogeography of the Lecythidaceae Clade (brazil Nut Family)

The Lecythidaceae clade of the order Ericales is distributed in Africa (including Madagascar), Asia in the broadest sense, and South and Central America. Distribution maps are included for the Lecythidaceae clade as follows: family maps for Napoleonaeaceae and Scytopetalaceae; subfamily maps for the Barringtonioideae, Foetidioideae, and Lecythidoideae, and maps for the subclades of Lecythidaceae subfam. Lecythidoideae. The following topics are discussed: (1) the difficulties using herbarium specimens for studies of phytogeography; (2) the worldwide distribution of the Lecythidaceae clade; (3) the migration of Lecythidaceae from the Old into the New World or vice versa; (4) the phytogeography of the New World subclades of Lecythidaceae; (5) the ability of some New World subclades of Lecythidaceae to occupy very large distributions; (6) the adaptations of New World Lecythidaceae to different habitats; (7) the Pleistocene refuge hypothesis; (8) the evolution of high species diversity of the family in eastern Central America/northwestern South America; (9) the possible migration of species from the Guayana lowlands and western Amazonia into Central Amazonia after large wetland areas drained after the Amazon River began to flow eastward; (10), the migration of Lecythidaceae into the Atlantic Forest of Brazil from both northeastern and southwestern Amazonia or vice versa; and (11) the worldwide distribution of floral symmetry of the Lecythidaceae clade. Mori et al.: Lecythidaceae phytogeography 2 The New World Lecythidaceae (Brazil nut family), related to members of the Old World Lecythidaceae (Figs. 1–2B), are best known for the edible seeds of the Brazil nut (Bertholletia excelsa Bonpl.) and the cultivation of the cannonball tree (Couroupita guianensis Aubl.) as an ornamental in tropical and subtropical botanical gardens. The Lecythidaceae lineage in the New World is recognized by its showy and morphologically diverse flowers with either actinomorphic or zygomorphic androecia (Figs. 3–7). In addition, the fruits are woody and dehiscent in most genera of the New World, (e.g., in the Lecythis pisonis clade, Figs. 8, 10J), indehiscent and berry-like (Gustavia clade, Fig. 8A), drupe-like (Grias clade), and some species are secondarily indehiscent (e.g., Bertholletia excelsa, Fig. 9, 10C). The spectacular flowers and fruits show adaptations for pollination and dispersal (Prance & Mori 1998) by biotic and abiotic agents. The family is ecologically dominant in lowland forests in many parts of the Amazon Basin (Steege et al. 2006) and present, but less frequent, in periodically flooded forests, cloud forests, and savannas. Species of the family, the Brazil nut tree in particular, are icons of Amazonian trees (Mori 2001). In general, if numerous species of Lecythidaceae are present in lowland forests it is likely that those forests have not been drastically disturbed by humans in the recent past (Mori et al. 2001). This family forms a clade in the Ericales (Schöenberger et al. 2005), referred to as the Lecythidaceae clade in this paper. The combined analysis of ndhF and trnL-F genes by Mori et al. (2007) and morphological data supports recognizing Napoleonaeaceae (Prance 2004) and Scytopetalaceae (Appel 1996, 2004) as related but separate families from Lecythidaceae. Authors in Kubitzki (2004) accept the division of Lecythidaceae into the subfamilies Foetidioideae, Barringtonioideae (not Planchonioideae fide Thorne 2000), and Lecythidoideae (Prance & Mori 2004). See Map 1 for the worldwide distribution of Lecythidaceae and Table I for the current family classification and number of species in each clade. Current phylogenies do not prohibit recognizing the three subfamilies as the families Foetidiaceae, Barringtoniaceae, and Lecythidaceae. An argument for this point of view is that there are no apparent anatomical, cytological, or morphological characters uniting them into a single family. In contrast, there are key characters that can be used to separate the three subfamilies as families (see key below). We have not made the change to recognize the three families because some characters need to be confirmed by more sampling (e.g., the orientation of the xylem and phloem in cortical bundles), and because of the lack of data for other characters (e.g., chromosome counts for Crateranthus, Foetidia and all Scytopetalaceae except Asteranthos brasiliensis and molecular sequences for more taxa, especially for Crateranthus, and Petersianthus). In this paper, Lecythidaceae, instead of Lecythidaceae subfam. Lecythidoideae, is used when the family is mentioned for taxa of the New World whereas the Lecythidaceae clade refers to the Napoleonaeaceae, Scytopetalaceae, and Lecythidaceae. In a large-scale ecological study of lowland Amazonian forests (Steege et al 2006), the Lecythidaceae ranked third in total number of trees. They are surpassed in number by Fabaceae (legumes) and Sapotaceae (chicle family), but Eschweilera coriacea (DC.) S.A Mori. is ranked as the most abundant of all tree species in the study. In another paper, Steege et al. (2013) concluded that there are 390 billion individual trees ≥10 cm DBH and 16,000 species of trees of that size in Amazonia. The study found that 227 species (including all families) accounted for nearly half of all of the trees sampled and demonstrated how important relatively few species of Lecythidaceae and other families are for maintaining ecosystem services of Amazonian forests. Other studies have documented large numbers of individuals as well as high species diversity of Lecythidaceae, especially in central Amazonia (Mori & Lepsch-Cunha 1995) and the Guianas (Mori & Boom 1987). A 100-hectare plot inventoried by Mori et al. (2001) in central Amazonia found that 10% of the individuals and 6% of the species belonged to Lecythidaceae. In higher-elevation cloud forests, periodically flooded forests and dry habitats, New World Lecythidaceae are present but at much lower densities and species richness than in lowland non-flooded forests. Mori et al.: Lecythidaceae phytogeography 3 Figure 1. The non-Bertholletia grade. This cladogram includes most Old Word lineages (all with actinomorphic flowers), the actinomorphic-flowered genera of the New World, the only tubular zygomorphicflowered genus in the clade, and two zygomorphic-flowered genera from the New World. The remaining zygomorphic-flowered genera in the New World belong to the Bertholletia clade (Figs. 2A–2B). The positions of the flower symmetry types are marked on the cladogram. This is a jackknife tree generated using Xac (Farris, 1997), which is based on a combination of ndhF and trnL-F sequences. From Mori et al. (2007) but modified by changing Cariniana decandra Ducke to Allantoma decandra (Huang et al. (2008). Mori et al.: Lecythidaceae phytogeography 4 Figure 2A. The Bertholletia clade and its outgroup as recovered by Huang et al. (2015) are represented in this and Figure 2B. Old World species of the Lecythidaceae clade are not included in this cladogram. The cladogram is based on a strict consensus of 66 most parsimonious (MP) trees based on total evidence. Boot strap values (>50%) are given above the branches. The positions of the flower symmetry types are marked on the cladogram. Eschweilera congestiflora and E. simiorum have been changed to Lecythis congestiflora and L. simiorum to reflect the transfer of these species to Lecythis. Mori et al.: Lecythidaceae phytogeography 5 Figure 2B. Continuation from 2A. Mori et al.: Lecythidaceae phytogeography 6 Figure 3. Flowers of the Lecythidaceae clade. A. Napoleonaeaceae. B. Foetidioideae. C. Scytopetalaceae. D. Barringtonioideae. E. Lecythidoideae. Drawings by B.Angell. Mori et al.: Lecythidaceae phytogeography 7 The distribution ranges of taxa of Lecythidaceae are driven by abiotic factors that isolate populations as well as create new habitats to which Lecythidaceae either adapt or become extinct. These factors include (1) formation of rivers, large lakes, or epicontinental seas and their changes over time; (2) uplift of mountains that create valleys and slopes, altitudinal differences, and different temperature regimes; and (3) soil moisture that ranges from always saturated (swamp forests), periodically saturated (along rivers), not saturated (non-flooded forests), and periodically dry areas (e.g., savannas and thorn scrub vegetation). Most species of New World Lecythidaceae grow in non-flooded forests but some have adapted to savanna, wet habitats, and cloud forests. Extreme rainfall, especially if a wet year is long and followed by consecutive wet years, can cause high mortality to species of Lecythidaceae adapted to lowland, non-flooded forests (Mori & Becker 1991). In contrast, we do not know of any species that grow in extremely dry areas such as the thorn-scrub vegetation (caatinga) in northeastern Brazil and the Chacó of Argentina or in cold areas such as the Araucaria Forests of Brazil and the páramos of the Andes. In a paper about the origins of the flora of southern Brazil, Lyman Smith (1962) wrote “Ever since the first land plants evolved, the face of the earth has been changing constantly, so that we may safely assume that the flora of any given region today has arrived from somewhere else. In the case of land recently risen out of the sea, it is relatively easy to see whence its flora came, but in the case of a great center of distribution like the Amazon Basin it is difficult if not impossible to reconstruct its past.” With the use of technologies not available to Lyman Smith, hypotheses about the geographical history of plants can now be addressed using up-to-date scientific tools. His paper represents the first step in understanding the historical biogeography of a region (eastern Brazil), whereas we present a review of the status of the phytogeography of the Lecythidaceae clade. Our goal is to make available what we have learned about this pantropical family of trees so that others can use our observations to develop and test hypotheses about the evolution and phytogeography of Lecythidaceae. METHODS Locality coordinates of Lecythidaceae were downloaded from The New York Botanical Garden’s Virtual Herbarium and other sources, such as the Global Biological Information Facility (GBIF 2016 accessed). The data were plotted using ArcGIS 10.4 (ESRI 2017). Cultivated specimens and specimens with incorrect coordinates (e.g., plotted in the incorrect hemisphere or in the ocean), were either corrected or filtered from the group. Metadata were taken from the collections and were assigned to the data points. The data were projected to the World Cylindrical Equal Area and were merged into one layer and saved in the project geodatabase. Using the ArcGIS geoprocessing tool Grid Index Features, a grid consisting of 10,000 km units was created and overlaid on the data points, joining by both one-to-one and one-to-many relationships to count all points within a grid square (join count produced in one-to-one join) and to count all distinct variables within each grid square (one-to-many join). The one-to-many join enables the counting of distinct species per grid square by exporting the information from ArcGIS to an Excel spreadsheet and using the Pivot Tables tool in Excel to expedite the counting of distinct variables. Collection density and species richness are visualized using the spatially joined collection point data to grid square, based on distinct grid ID number (auto-populated by ArcGIS). The families Napoleonaeaceae and Scytopetalaceae and the subfamilies Barringtonioideae, Foetidioideae, and Lecythidoideae are mapped to family and subfamily, respectively. In the maps of these lineages, a dot represents the presence of the family or subfamily at that locality. In contrast, the dots on the maps of the subclades of subfamily Lecythidoideae represent collections identified to species. In some maps (e.g., the maps of the Gustavia and the Eschweilera parvifolia clades) “heat maps” are used to indicate the number of species (number in grid) and number of collections (color of Mori et al.: Lecythidaceae phytogeography 8 grid). This type of map is used because maps of high diversity clades become crowded and are difficult to read. Maps for all species can be viewed individually on the Lecythidaceae Pages (Mori et al. 2010). The New World subclades mapped in this paper are those recognized by Huang et al. (2015) and Mori et al. (2015). In some maps, unrelated species grouped together illustrate congruent distributions. For example, different species with overlapping ranges in eastern Central America/northwestern South America suggest that geological events in this region caused similar distributions among numerous species (Map 23). The presence of errors in the identification of collections (Mori 1998) and errors in mapping specimens make it difficult for botanists to accept or reject hypotheses based on data from some herbarium specimens (Steege et al. 2016). For example, Meyer et al. (2016) removed 53% of the 119 million collections studied because the discarded specimens lacked coordinates, the coordinates were incorrect, or the determinations were incomplete or obviously wrong. In this study, we corrected incorrect coordinates of some specimens (e.g., coordinates mapped in the sea) and did not include specimens with doubtful determinations. There are two phylogenies referred to in this paper. Figure 1, based on Mori et al. (2007), represents the non-Bertholletia grade and its relationship with the Bertholletia clade. Thus, Figure 1 shows the relationships of Old and New World taxa and the placement of the Bertholletia clade. In the original publication by Mori et al. (2007) the non-Bertholletia grade was erroneously called a “clade” when it should have been called a “grade” because it is paraphyletic and the Bertholletia clade is derived from within it. The cladogram represented in Figures 2A–B includes only New World taxa (Huang et al. 2015). Interactive Google maps are available for the New World species of Lecythidaceae on the Lecythidaceae Pages (Mori et al. 2010). These maps provide links to the data associated with the collections when the dot representing a collection is clicked. RESULTS The results of this project are the maps and their interpretations (Maps 1–27). The maps include families (e.g., Scytopetalaceae, Map 3), subfamilies (e.g., Lecythidaceae subfam. Lecythidoideae, Map 6), clades (e.g., Lecythis pisonis clade, Map 13), genera (e.g., Gustavia, Map 8), or species (e.g., Allantoma, Map 10). Descriptions and illustrations of the morphology of the clades belonging to the Lecythidaceae subfam. Lecythidoideae clade can be found in Huang et al. (2015) and Mori et al. (2015). Key to the clades of Lecythidaceae sensu lato 1. Cortical bundles normally oriented (xylem inside phloem outside). Flowers with actinomorphic androecia and styles much shorter than stamens or flowers zygomorphic and styles shorter or only slightly projected beyond stamens; stigma small and not pentagonal; pollen tricolpate (Fig. 7A). Chomosome numbers x = 17. Native only to the Neotropics ............................................................................... Lecythidaceae subfam. Lecythidoideae 1. Cortical bundles normally or inversely oriented (xylem outside phloem inside). Flowers only with actinomorphic androecia and styles as long as or longer than the stamens, if shorter than stamens the stigma large and pentagonal; pollen tricolpate or syntricopate (Fig. 7B). Chromosome numbers x = 13, 16, 21, or unknown. All but one species (Asteranthos brasiliensis Desf. of the Scytopetalaceae) native to the Paleotropics. Mori et al.: Lecythidaceae phytogeography 9 2. Leaf blades with poorly defined secondary veins, the tertiary veins parallel to secondary veins. Calyx with 4, valvate, triangular lobes; petals absent; androecium with stamens free or nearly so. Fruits conical. Madagascar, surrounding islands, and nearby Africa .................................................................................. Lecythidaceae subfam. Foetidioideae 2. Leaf blades with well-defined secondary veins, the tertiary veins reticulate. Calyx with >4, valvate or imbricate, ovate lobes; petals present; androecium with stamens fused. Fruits globoid,