Review of Vegetative Branching in the Palms (Arecaceae).
Abstract Vegetative branching is common in the palms (Arecaceae). However, current terms to describe vegetative branching diversity are not consistent and do not cover the full range of branching types. In this study vegetative branching types in the palms were reviewed and defined, and the phylogenetic distribution of palm branching types was described. Branching types were described from a literature review and field observations; 1903 species representing all 181 genera were included. Five branching types were found: lateral axillary branching, shoot apical division, false vivipary, abaxial branching, and leaf-opposed branching. Most species (55%) exhibited no vegetative branching. Lateral axillary was the most common branching type. Lateral axillary branching and shoot apical division were predicted to be the earliest-evolved branching types. The present study suggests that branching types have different evolutionary histories, and it is likely that the solitary habit is more common now than when palms initially diverged from commelinid relatives.Keywords Arecaceae * Branching * Commelinid monocots * Monocotyledons * Palmae * Palm phylogeny * Vegetative anatomy * Vegetative propagation
Vegetative Branching in the Palms and the Need for a New Classification System
Branching is the outgrowth or division of a meristem and results in a new axis. Plants can branch sexually, producing an axis used for sexual reproduction, or vegetatively, producing a separate and genetically identical vegetative axis (Doust & Doust, 1988). The vast majority of plants display some form of vegetative branching, which results in a great diversity in plant form and architecture (Bell & Tomlinson, 1980). Plants branch vegetatively in three ways: axillary (occurring in the leaf axils), apically (at the apex of the shoot), or adventitiously (in neither of the previous two locations) (Halle et al., 1978). Axillary branching, the most common type of branching in plants, has two forms that account for much of the architectural diversity displayed in plants: long and short shoots. Short shoots are specialized units, usually producing photosynthetic or reproductive structures or spines that bear no indeterminate lateral branches (Halle et al., 1978). Long shoots grow, add height, and can proliferate to produce additional lateral axillary branches that become either long or short shoots.
Vegetative branching is common in the monocots, where it is used as a mechanism to increase in size, since most monocots lack secondary growth (Halle et al., 1978). The three main terms used to describe branching in the monocots are (1) axillary, (2) dichotomous, and (3) adventitious branching (Tomlinson, 1973). However, these terms are not consistently used in descriptions of monocot branching diversity.
While similar vegetative branching types exist in the palms (Arecaceae Bercht. & J.Presl) and their monocot relatives, the terminology to describe these types is not uniform and many terms have been applied to the same branching type (Tomlinson, 1961; Tomlinson, 1971; Fisher, 1973; Fisher & Tomlinson, 1973; Fisher, 1974; Fisher et al., 1989; Mendoza & Franco, 1998; Fisher & Zona, 2006). Detailed descriptions are often greatly simplified in the popular palm literature (Tomlinson, 1973; Dransfield et al., 2008a, b). Consequently, the current branching vocabulary for palms does not consistently and accurately describe the diversity of vegetative branching in the family.
The three vegetative branching types commonly described in palms are similar to the branching types used for the monocots (Tomlinson, 1990): axillary branching, apical dichotomous branching, and non-axillary branching. However, branching terms have also been classified depending on variation in outgrowth. Axillary branching, the most commonly described, is used to describe the formation of a primordial bud in the leaf axil at the base of orthotropic (vertical) shoots. If axillary branches grow erect immediately, they create branch types called basal suckers. If the basal sucker grows horizontally before turning to grow erect, it forms a rhizome (Tomlinson, 1990). Rhizomatous branching is occasionally classified as its own, unique branching type. Apical dichotomous branching occurs when the apical meristem of the stem bifurcates, creating two apical meristems. In palms, species differ in whether the meristem splits into two even (isotomous) or uneven (anisotomous) parts (Tomlinson & Moore, 1966; Gola, 2014). In palm literature, the term dichotomy has been used incorrectly to imply equality of outgrowth (Tomlinson. 1990). Non-axillary branching describes a branch that does not arise in the leaf axil (Tomlinson, 1973). The term, however, does not further differentiate among locations of the branch (non-apical portions of the stem, lamina or inflorescence), which can differ among taxa.
Classifying branching based on location of meristem for some types (non-axillary, dichotomy) vs. variation in outgrowth for others (basal suckers, rhizomatous) means that branching terms are defined at different points during development. Since vegetative branching terms are currently classified at different developmental levels, the phylogenetic distribution of branching in the palms cannot be appropriately described. A new, internally-consistent classification of branching is needed to understand branching type phylogeny in the palms.
Understanding the relationship between phylogeny and branching type will increase our understanding of the evolution and ecology of vegetative branching in the palms and will provide a framework for understanding branching in all monocots. The purpose of this study was to (1) identify, define and classify the types of vegetative branching in the palm family Arecaceae and (2) describe the phylogenetic distribution of these branching types in palms.
A New Vegetative Branching Classification System in the Palms
Determining Vegetative Branching Types in the Palms
The classification system used was based on vegetative branching meristem location. Each branching type was defined by (1) branching meristem (axillary, apical, nonaxillary); and, if non-axillary, (2) location of branch (inflorescence, leaf base or stem). Branching type(s) of species were identified from literature reviews of journal articles and books describing branching patterns and from analysis of living specimens in the palm collections at Fairchild Tropical Botanic Garden and Montgomery Botanical Center (Coral Gables, FL, USA) (Table 2). Branching types proposed in this study, with terms found in the literature, are presented in Table 1.
The five branching types were lateral axillary branching, shoot apical division, false vivipary, abaxial branching and leaf-opposed branching. A dichotomous key was created to facilitate understanding and recognition of each branching type (Table 3). Lateral axillary branching was defined as vegetative outgrowth of an axillary meristem on the vegetative shoot (stem) (Fig. lb). Many species display lateral axillary branching but can also not branch, presenting a solitary stem; these species were classified as having lateral axillary branching. Shoot apical division was defined as the division of the apical meristem into two equal or unequal meristems (Fig. 1c). False vivipary was defined as adventitious vegetative outgrowth of buds in the apical bracts of an inflorescence that eventually rooted in the soil and produced vegetative shoots (Fig. 1d). Abaxial branching was defined as the vegetative outgrowth of an adventitious meristem located on the abaxial surface of the leaf at the base of the leaf sheath (Fig. le). Leaf- opposed branching was defined as the vegetative outgrowth of an adventitious meristem borne on the stem, opposite the lamina and petiole and enclosed within the edges of the leaf sheath (Fig. 1f) Branching type combinations can also occur; two branching combinations were found in the palms: shoot apical dichotomy + lateral axillary branching; and false vivipary + lateral axillary branching.
The above branching type names were assigned using the uniqueness and priority principles of botanical nomenclature (Greuter et al., 1999). The term dichotomy was not used because it has been defined multiple ways and the evidence for whether shoot apical division results from an equal apical division was often lacking. Most commonly, dichotomy implies equal division of the shoot apical meristem (Tomlinson, 1990), but the term has also been defined as two independently functioning axes (Gola, 2014) or as two more or less equal axes. Thus, the term has been used to describe both a developmental process (equal division of the shoot apex) and the result of branch outgrowth. Since there was discrepancy among definitions and usage of dichotomy, the term apical division was used to describe any division of the apical meristem (uniqueness principle). The terms shoot apical division and false vivipary needed additional clarification because these terms were not clearly defined in previous literature. The term false vivipary was selected because it was first published in the grass literature to describe a phenomenon similar to what was found in the palms (priority principle) (Van der Pijl, 1982; Bell & Bryan, 2008).
Descriptions of Vegetative Branching Types in the Palms
The classification system described above was used to describe branching in palm species, genera and subfamilies. Species were recognized following the accepted species in the Kew World Checklist of Palms on February 5, 2016 (Goverts et al., 2011). The numbers of species, genera and subfamilies with each branching type were counted to determine the most abundant branching type and combination found at each taxonomic level.
In total, 181 genera (out of 181 genera in the family, 100% genus coverage), comprising 1903 species (out of 2501 species in the family, 76% species coverage), were sampled (Table 2). The five branching types described above were identified in the species considered; these were distinguished from the solitary phenotype, which had no vegetative branching. Some species displayed more than one branching type, referred to as branching combinations. Two branching combinations were observed: shoot apical division + lateral axillary; and false vivipary + lateral axillary. Most commonly, species exhibited no vegetative branching; four of the five subfamilies, 147 genera (81% of genera), and 1043 species (55% of observed species) were solitary (Table 2, Fig. la). Some species were found with a branching type or as a solitary individual (175 species, 9% of observed species).
1) Lateral axillary branching was the most widely distributed vegetative branching type in the palms; it was described in four of five subfamilies, 61 genera (34% of genera), and 646 species (34% of observed species) (Table 2, Fig. 2). Four forms of lateral axillary branching were identified: basal suckering, rhizomatous branching, aerial suckering and displaced axillary branching. Basal suckering was defined as lateral axillary branching where the branches grew orthotropically (vertically) immediately and were restricted to the base of the parent shoot. Basal suckering was the most common form of lateral axillary branching, found in at least 600 palm species. Basal suckers may be produced throughout the life of an individual or basal suckers may be produced only during certain times. For example, Plectocomia Mart. & Blume species (15 species) and two Licuala Thunb. species (L. celebica Miq. and L. gracilis Blume) produced basal suckers after a period of dormancy, usually after the death of the parent shoot (Tomlinson. 1990). Phoenix L. species produced basal suckers until they were sexually reproductive and then stopped producing basal suckers (Tisserat & DeMason, 1985).
Rhizomatous branching was defined as lateral axillary branching where branches were restricted to the base of the stem but grew plagiotropically (horizontally) for some time before growing orthotropically (vertically). At least 33 species exhibited rhizomatous branching. Rhizomatous branching was found in combination with basal suckering in two species (Acoelorrhaphe wrightii H.Wendl. ex Becc. and Cyrtostachys renda Blume).
Aerial suckering was defined as basal suckering that was not restricted to the base of the stem but also occurred on aerial portions of the stem. Wendlandiella gracilis sub. Polyclada Dammer, Linospadix apetiolatus Dowe & A.K. Irvine, Hyospathe elegans hort ex Hook. F., and Geonoma baculifera Kunth exhibited aerial suckering (Tomlinson, 1990; Chazdon, 1991). In this study, aerial suekering was placed within lateral axillary branching because the branching mechanism for aerial suekering was developmentally the same as the branching mechanism for lateral axillary branching, and species with aerial lateral axillary branching had basal suekering as well.
Displaced lateral axillary branching, found in Korthalsia Blume, was defined as vegetative axillary meristems that were initiated in the axil of the first or second leaf primordium and then were displaced during development on to the internode above or onto the base of the leaf above. The displaced lateral axillary branching type was placed within lateral axillary branching because the branching mechanism was lateral axillary and the transition out of the axil occurred after initiation of the meristem (Fisher & Drans field, 1979).
2) Shoot apical division was distributed throughout the palms, having been described in four subfamilies, seven genera (3% of genera), and 21 species (1% of observed species) (Table 2, Fig. 2). Three forms of shoot apical division were identified: isotomy, anisotomy and Nannorrhops branching.
Isotomy, which is equal apical division followed by equal growth, has been studied anatomically in three palm genera and eight species: Hyphaene Gaertn. (H. compressa H. Wendl, H. coriacea Gaertn., H. dichotoma (J.White Dubl. Ex Nimmo) Furtado, H. reptans Becc., and II. thebaica Mart.), Nypa fruticans Wurmb. and Matricaria saccifera Gaertn. (Gola, 2014). Leaf arrangement and equal forking in divided crowns of mature plants suggest isotomy, but anatomical study of shoot apical development is needed for confirmation of other species (Fisher, personal correspondence).
Anisotomy, which is unequal division followed by differential growth, was exhibited by Eugeissona Griff (E. ambigua Becc., E. brachystachys Ridl., E. insignis Becc., E. minor Becc., E. triste Griff., and E. utilis Becc.). Anisotomous division was so unequal in Eugeissona species that the division appeared to be lateral axillary branching on non-basal portions of the stem (Fisher et al., 1989). Apical division in palms has been reported to range from equal (isotomous) to unequal (aniosotomous) division. In Chamaedorea cataractarum Mart., the anisotomous division of the apical meristem occurred very early in development, and as the stems matured, the division appeared to be equal (Fisher, 1973). Only developmental studies showed that the division did not initiate equally.
Nannorrhops branching, which has not previously been recognized as a distinct branching type, was defined as equal apical division with branch-pair differentiation. For example, in Nannorrhops ritchiana H. Wendl., the apical meristem divides into one fertile and one vegetative branch (Tomlinson & Moore, 1968).
3) False vivipary has been described in two subfamilies, three genera (1% of genera), and ten species (0.5% of observed species) (Table 2, Fig. 2): Calamus Auct. ex. L. (C. castaeneus Griff, C. dianbaiensis C.F.Wei, C. gamblei Becc., C. ingens (J.Dransf.) W.J.Baker, C. kampucheaensis A.J.Hend. & Hourt, C. nematospadix Becc., and C. pygmaeus Becc.), Salacca Reinw. (S. flabellata Furtado, and S. wallichiana Mart.), and Socratea salazarii H.E.Moore (Fisher & Mogea, 1980; Baker et al., 2000; Pintaud & Millan, 2004; Rupert et al., 2012). In each account of false vivipary, different terms were used to describe the phenomenon (Fisher & Mogea, 1980; Baker et al., 2000; Pintaud & Millan, 2004; Rupert et al., 2012). The architectures of the palms with false vivipary were different, yet the branching of the inflorescence was the same-vegetative shoots formed at the apex of the inflorescence. If the shoot reached the ground, it rooted and a shoot grew upward. Calamus gamblei, C. pygmaeus and C. nematospadix are all climbing rattans (Dransfield, 1992), Socratea salazarii is an erect and usually solitary palm (Pintaud & Millan, 2004), while Salacca flabellata is an acaulesent palm (Furtado, 1949).
4) Abaxial branching was described in one subfamily (Arecoideae), two genera (2% of genera), and seven species (0.3% of observed species) (Table 2, Fig. 2). In abaxial branching, a vegetative branch originating on the abaxial surface of the leaf sheath occurred on the basal and intermediate internodes of orthotropic stems in Oncosperma Blume species and Dypsis lutescens (H. Wendl.) Beentje & J. Dransf. Species with abaxial branching usually do not display lateral axillary branching.
5) Leaf-opposed branching was described in one subfamily (Calamoideae), two genera (1% of genera), and seven species (0.3% of observed species). Leaf-opposed branching occurred on basal internodes and on aerial internodes of the stem, as in the liana Myrialepis paradoxa (Kurz.) J. Dransf. Axillary branching, leaf-opposed branching and abaxial branching are distinct types of stem nodal meristems based on location and position of the branching meristem (Fig. 2). In axillary branching, the meristem is located in the axil of the leaf. In abaxial branching, the vegetative branching meristem is located on the abaxial surface of the leaf sheath. In leaf-opposed branching, the branching meristem is borne on the stem, enclosed by the edges of the leaf sheath and opposite to the lamina and petiole.
Individuals within a species sometimes displayed more than one branching type at a time, here called branching combinations. The two branching combinations found were shoot apical division + lateral axillary and false vivipary + lateral axillary branching. Shoot apical division + lateral axillary branching was exhibited by one species of Basselinia Vieill. (Arecoideae), all 27 species of Korthalsia Blume (Calamoideae), two species of Hyphaene (Coryphoideae) and monospecific Nannorrhops ritchiana (Coryphoideae). False vivipary + lateral axillary branching was exhibited by five species of Calamus (Calamoideae), and Socratea salazarii (Arecoideae) (Table 2).
Phylogenetic Distribution of Vegetative Branching Types in the Palms
Subfamily-level and genus-level phylogenies were used to examine the phylogenetic distribution of branching types. The phylogeny from Baker et al. (2009) was selected for character mapping because it had the most recent genus-level phylogeny. Adjustments were made for new and deleted taxa (Dransfield et al., 2008a, b; Baker & Bacon, 2011; Bernal & Galeano, 2013; Baker, 2015; Noblick & Meerow, 2015). Branching types were used for character mapping, since the specific branching type was the character that was retained or lost. The Mesquite software (Maddison & Maddison, 2011), a software package used by evolutionary biologists to analyze comparative data, was used to map vegetative branching onto the published cladograms. Ancestral branching types were determined using the most parsimonious tree in Mesquite. A subfamily level cladogram was analyzed to predict the ancestral branching type for the family. Cladograms for Arecoideae, Calamoideae and Coryphoideae were analyzed to predict the ancestral branching type for each of these three subfamilies. A cladogram for Ceroxlyloideae was not included because this subfamily had no vegetative branching except for a single species, Ravenea deliculata Rakotoarin. A cladogram for Nypoideae was not included because it is monospecific (Nypa fruticans Wurmb).
At the subfamily level, lateral axillary branching and shoot apical division were predicted as the ancestral vegetative branching types (Fig. 3). The solitary state (no vegetative branching) was also an ancestral state. False vivipary evolved a minimum of two times: once in the Calamoideae and once in the Arecoideae (Fig. 3). Abaxial branching evolved a minimum of two times in the Arecoideae (Oncosperma and Dypsis). Leaf-opposed branching evolved two times in the Calamoideae, in Myrialepis Becc. and in Calamus.
The Calamoideae, the most basal and second largest subfamily (659 species), was the most diverse in vegetative branching types (Table 2); it exhibited four branching types and both branching combinations. On average, one branching type was exhibited in a genus. With three branching types, Calamus exhibited the most branching types in Calamoideae. The ancestral branching type of Calamoideae was predicted to be lateral axillary branching (Fig. 4). In the Calamoideae, more species had vegetative branching (341 species, 86% of observed Calamoideae species) than the solitary habit (58 species, 14% of observed species). Lateral axillary branching evolved a minimum of one time in the Calamoideae. In five genera, all species had lateral axillary branching; these genera were Laccosperma G. Mann & H.Wendl. (six species), Eremospatha Mann & H. Wendl. (11 species), Oncocalamus Mann & H. Wendl. (five species), Mauritiella Burret (four species), Plectocomia Mart. & Blume (15 species), and Plectocomiopsis Becc. (six species). Ten species in two genera in the Calamoideae displayed false vivipary: Calamus (eight) and Salacca (two). Shoot apical division evolved at least two separate times in the Calamoideae; species of Eugeissona and Korthalsia exhibited shoot apical anisotomy. Leaf-opposed branching, described only in the Calamoideae, was the least common branching type in the Calamoideae; Myrialepis (one species) and Calamus (seven species) were the only two genera with leaf-opposed branching. In Calamoideae, 15% of observed species did not display any branching, and two genera, Mauritia L.f. (two species) and Pigafetta (Blume) Becc. (two species) exhibited no branching.
The majority of the Coryphoideae, the third largest subfamily (492 species), were solitary, exhibiting no vegetative branching (39 genera/283 species, 74% of observed Coryphoideae species). Some members of Coryphoideae displayed lateral axillary branching (16 genera /79 species, 20% of observed Coryphoideae species) or shoot apical division (three species of Hyphaene, 0.7% of observed Coryphoideae species). One branching combination, shoot apical division + lateral axillary, was found (two species of Hyphaene and Nannorrhops ritchiana) (Table 2). The ancestral branching type of the Coryphoideae was lateral axillary branching (Fig. 5). The genus Hyphaene (eight species) exhibited the most branching types and combinations in the Coryphoideae (two types-lateral axillary and shoot apical division and one branching combination (shoot apical division + lateral axillary)). All species in subtribe Rhapidinae, except for Trachycarpus H.Wendl., exhibited lateral axillary branching: Chamaerops L. (one species), Rhapidophyllum H. Wendl. & Drude (one species), Maxburretia Furtado (three species), Rhapis L.f. (ten species) and Guihaia J. Dransf., S.K. Lee & F.N. Wei (two species). The subtribe Rhapidinae was the only Coryphoideae clade higher than genus-level where lateral axillary branching was retained throughout all species of the clade. Lateral axillary branching evolved at least 12 times, and shoot apical division evolved at least two times in Coryphoideae. There were no species in the Coryphoideae that displayed false vivipary, abaxial branching or leaf-opposed branching.
The Arecoideae, the largest subfamily (1376 species), exhibited four branching types and two branching combinations (Table 2). The majority of the Arecoideae exhibited no branching (59%, 657 observed species). Dypsis Noronha ex Mart, exhibited three branching types, which was the most genus-level branching types for the Arecoideae. The ancestral branching type of the Arecoideae palms was lateral axillary (Fig. 6). Five genera in Arecoideae had no solitary species (i.e., all species exhibited vegetative branching): Iriartella H.Wendl. (two species), Wettinia Poepp. ex Endl. (21 species), Jubaeopsis Becc. (one species), Podococcus Mann & H.Wendl. (two species) and Sclerosperma G. Mann & H. Wendl. (three species). Shoot apical division evolved at least four times, occurring in Allagoptera, Basselinia, Dypsis, and Matricaria. However, shoot apical division was not easily observed in these genera. In Basselinia, Dypsis and Matricaria, shoot apical division occurs early in development of the stem (Moore & Uhl, 1982; Fisher & Zona, 2006). Allagoptera Nees is a creeping palm and apical division occurs low to the ground. While shoot apical division was not as obvious as in Hyphaene (Coryphoideae), morphological signs of apical division (forking) are still present and observable in Allagoptera. False vivipary evolved once in Socratea salazarii. Abaxial branching evolved twice, occurring in Dypsis lutescens and Oncosperma. (Tables 4, 5, 6 and 7).
The Ceroxyloideae, the fourth largest subfamily (47 species), had one species that branched vegetatively. The ancestral state of Ceroxyloideae was no branching; 99% of species exhibited no vegetative branching. Ravenea deliculata, from the largest genus in Ceroxyloideae (Ravenea, 21 species), displayed lateral axillary branching both basally and aerially (Rakotoarinivo, 2008). On the basis of number of species, the Ceroxyloid palms exhibited fewer branching types and combinations than expected.
Nypoideae, the smallest subfamily (one species, Nypa fruticans), exhibited one branching type (shoot apical division), and the ancestral branching type was shoot apical division.
Evolutionary History of Vegetative Branching in the Palms
The phylogenetic distribution of vegetative branching types suggests that lateral axillary branching is the ancestral branching type and that branching evolved before palm divergence from immediate ancestors. Monocots evolved in the mid/late Jurassic period, about 160 million years ago. (Wikstrom et al, 2001). Recent evidence suggests palms diverged in the Turanian, about 90 million years ago (Harley, 2006). Newer findings demonstrate that palms diverged much earlier than commelinid relatives (Barrett et al., 2016). At some point between monocot evolution and evolution of the current palm species, a diversity of branching types evolved in the palms.
While fossilized remains of palms are distributed throughout the fossil record, stems are less commonly found as fossils, and multiple-stemmed fossils are missing from the literature entirely (Erwin & Stockeny, 1994; Harley, 2006). There is a form genus for palms with rhizomatous stems, Rhizopalmoxylon (Palmoxylon is the form genus for petrified wood) and there is apparently no literature on its architecture, specifically, whether there are multiple stems per individual (Harley, 2006). Nypa fruticans, a multi-stemmed palm once widespread on many continents, has fossilized pollen, fruit, and leaves but no stem fossils (Gee, 2001; Mehrotra et al., 2003). It is difficult to determine when branching evolved in Nypa, and in palms in general, without any branching or architectural information from fossils.
While the fossil record does not distinguish the ancestral branching type, it is possible to predict evolutionary trajectories for each branching type. Because of the prevalence of lateral axillary branching in commelinid relatives, as well as in the palm family, lateral axillary branching may have been present before the divergence of palms. Lateral axillary branching is a common branching type, and more common than the solitary habit, in Poaceae Barnhart (Holtuum, 1955; Ward & Leyser, 2004; McSteen & Leyser, 2005; Doust, 2007), Cyperaceae Juss. (Rodigues & Maranho-Estelita, 2009), Zingiberaceae Martinov (Bell, 1979) and Dasypogonaceae Dum. (Clifford et al., 1998); Dasypogonaceae, sister to the palms, is entirely rhizomatous. Therefore, lateral axillary branching may share a common evolutionary history throughout the commelinid relatives.
While analysis from the present review suggest that shoot apical division is an ancestral branching type, shoot apical division in the commelinids is described only in Strelitzia Banks (Strelitziaceae) (Fisher, 1976). Also, shoot apical division is not nearly as widespread through the palm family as lateral axillary branching. It is likely that shoot apical division evolved after the divergence of palms.
This review suggests that the remaining branching types-false vivipary, abaxial branching, and leaf-opposed branching-probably evolved after the divergence of palms. False vivipary and leaf-opposed branching are found in commelinid relatives. False vivipary is common in the Poaceae (Chlorophytum comosum (Thunb.) Jacques, Deschampsia alpina (L.) Roem. & Schult., Festuca ovina var. vivipara L., Dactylis glomerata L., Poa x jemtlandica K.Richt.), as well as the Zingiberales (Costaceae Nakai and Marantaceae R.Br.). In Costaceae (Zingiberales) and Marantaceae (Zingiberales), bulbils are produced in the axils of inflorescence bracts (Jenik, 1994), a branching type closely related to false vivipary. Leaf-opposed branching is found in Musa L. (Fisher, 1973). However, the presence of these branching types in commelinid relatives does not mean that the ancestral palm displayed these branching types. Results from this study suggest that false vivipary and leaf-opposed branching evolved later in palm evolutionary history. False vivipary and leaf-opposed branching displayed by the palms and their commelinid relatives are most likely an example of homoplasy, and distinct evolutionary histories led to similar branching types. Abaxial branching, however, has been described only in the palms and may be a branching type unique to the family.
The evolutionary history of branching types may not be easily determined because the evolution (and loss) of branching types in the palms is continuous and occurred at different speeds among subfamilies (Faurby et al., 2016). The different evolutionary trajectories of vegetative branching in subfamilies Calmoideae and Arecoideae exemplify that evolution (and loss) of branching types is continuous and occurred at different speeds. In Calamoideae, most commonly an entire genus shares a branching type. Branching types in Calamoideae do not appear to be changing at the species level. Alternatively, in Arecoideae, species within a genus may not share a common branching type. In the Arecoideae, the genera are mostly solitary but have a few branching species. There are two distinct trajectories that could lead to a primarily solitary genus with a few branching species in Arecoideae. Either the ancestor to the genus did not branch and the ability to branch has re-evolved in a few species, or the ancestor did branch and the extant species have lost the ability to branch. Evolution of branching in palms may be influenced by differences in the ecology of different taxa.
Ecology of Vegetative Branching in the Palms
Regardless of evolutionary history, vegetative branching is less common in palms than in their commelinid relatives (Tomlinson, 1973). Like most monocots, including their commelinid relatives, palms do not produce secondary xylem (wood) from a vascular cambium, which limits their ability to make large trees. One of the main differences between palms and their close relatives, however, is their large, strong, woody trunks. Palms form a woody trunk through cell thickening and lignification on the surface layers of the cells in the outer cortex. It is possible that the lignification of the surface of the palm stem prevents activation and growth of dormant axillary buds. The lignified stem may have imprisoned the buds, and the ability to branch via axillary buds was lost over evolutionary time. Lignified stems (woody trunks) presumably have been selected because they increase fitness and the chance of survival (Schluter, 2001). Vegetative branching may be less common in the palms because there was selection for palms with thicker, taller trunks rather than thinner trunks that can branch (Henderson, 2002a).
It is important to note that all palms, even solitary palms, branch sexually. All palms have meristems that produce inflorescences. Similar branching types exist in vegetative and sexual branching in the palms. The most common type of sexual branching is axillary, exhibited by the vast majority of palms, where an inflorescence is produced from a bud in the leaf axil (Dransfield et al., 2008a, 2008b). In sexual branches, there is variation in types of displaced axillary branching that results in different branching patterns (Fisher & Maidman, 1999). In Salacca and Kerriodoxa J. Dransf., the sexual bud is borne in the leaf axil but may be captured by the subtending developing leaf, and the bud emerges through a slit on the abaxial side of the leaf sheath (Fisher & Mogea, 1980). In a few genera in the Calamoideae (Korthalsia, Calamus, Myrialepis, Plectocomia and Plectocomiopsis) the bud is displaced longitudinally and is adnate to the internode and leaf sheath above the node of origin (Fisher & Dransfield, 1977; Fisher & Mogea, 1980). In sexual apical branching, the apical meristem produces a large determinate inflorescence (i.e., Corypha L. and Tahina J. Dransf. & Rakotoarin.) (Dransfield et al., 2008a, 2008b). False vivipary is a combination of asexual and sexual branching, where the sexual branching reverts to vegetative branching in the inflorescence, using the same stem system. Abaxial and leaf-opposed sexual branching types have not been recorded in the palms.
While sexual branching is more common in the palms than vegetative branching, there are ecological benefits of vegetative branching. First, branching increases net primary productivity for the individual genet. When the palm branches vegetatively, it produces more crowns with more leaves, and the increase in leaves could increase photosynthetic potential (Duncan, 1971). In palms like Serenoa Hook.f., Allagoptera and Nypa, a creeping habit allows the stem to produce more roots (Tomlison, 1990; Fisher & Jayachandran, 1999). The creeping habit can support a greater photosynthetic potential. However, if the branching type is shoot apical division and the habit is erect (as in Hyphaene dichotoma), the trunk may be unable to support more crowns physically and physiologically.
Another ecological consequence of branching is that having multiple stems increases chances of an individual's survival in disturbance-prone environments, such as under-stories of rainforests and coastal strands (Tomlinson, 1990). Certain species of Chamaedorea Willd. and Geonoma Willd. live in disturbance-prone environments in the understory of rainforests, where falling debris poses a threat to their survival (Bullock, 1980; Clark & Clark, 1989; Chazdon, 1992; James, 2013;). A solitary palm only has one apical meristem and damage to that apical meristem results in death of the plant. In a multiple-stemmed palm, a genet can survive after damage to a single apical meristem. Thus, having multiple stems increases their chance of surviving a fallen branch or trunk of a large canopy tree. The understory palms Geonoma baculifera and Hyospathe spp., which have vegetative branching, exemplify this habit. These species are clumping palms that grow in the understory of rainforests. If damage occurs to a terminal apical meristem of these species, aerial axillary buds grow to produce plantlets. The stem eventually falls and the plantlets root, producing new ramets.
Nypa and Allagoptera also colonize environments where water level and substrate are unstable. Nypa fruticans colonizes coastal strands where water level is in constant flux and muddy banks are unstable (Tomlinson, 1990). Allogoptera colonizes sandy beaches and dunes, where water level changes daily and the dunes are likely to change shape (Dransfield et al., 2008a, 2008b). For Nypa and Allogoptera, branching is by shoot apical division on horizontally-growing stems, which allows them to form large monotypic stands. If damage occurs to a stem, such as meristem or stem rot from prolonged flooding, many other apical meristems exist that will survive and continue branching. Nypa and Allagoptera may also help stabilize these unstable environments.
While vegetative branching is a survival mechanism, as in Chamaedorea, Geonoma, Hyospathe, Nypa and Allagoptera, it is also a mechanism for clonal reproduction (Mogie, 1992). In unstable environments, such as flood plains, coastal strands and habitats with frequent fire or droughts, seed germination and establishment can be difficult. The ability of an individual to branch vegetatively and reproduce asexually ensures continued reproduction of the species into the next generation.
The Calamoideae epitomize the ecological benefit gained from vegetative branching. They are an interesting group because most species exhibit vegetative branching and climb prolifically. A major innovation in the Calamoideae was their liana habit (Gianoli, 2004; Couvreur et al., 2014). These palms climb, branch and dominate the canopy of Asian rainforests (Dransfield, 1992; Dransfield, 1997; Dransfield et al., 2008a, 2008b). Vegetative branching, therefore, allows the Calamoideae to climb through and explore the canopy prolifically. These palms colonize the canopy more efficiently than unbranched palms could. Vegetative branching allows the Calamoideae to exploit the canopy habitat; at the same time, the liana habit means that the plants do not invest in large woody trunks.
The Calamoideae also contain the greatest number of species that branch through false vivipary. False vivipary is interesting ecologically because it is only successful if the inflorescence is able to root in the forest floor, presumably when the crown is close to the ground (Bell & Tomlinson, 1980). In grasses displaying false vivipary, the inflorescence is never more than a few centimeters from the ground and the plantlet can easily reach the soil to root. In palms, false vivipary occurs on both erect (Socratea), climbing (Calamus) and acaulescent (Salacca) stems and is successful in all of these habits (Fisher & Mogea, 1980; Dransfield, 1992; Dransfield, 1997; Baker et al., 2000; Pintaud & Millan, 2004; Rupert et al., 2012). For all species that exhibit false vivpary, successful rooting of the false viviparous shoot has been described for sterns near the soil, but the exact heights have not been recorded. There are at least four possible relationships between stem height and successful false vivipary. First, there could be no relationship; false viviparous shoots could form at any height in the canopy and successfully root in the soil. No relationship between height of the shoot and successful rooting is the least likely of the scenarios, since the viviparous shoot may have a very long distance to reach the soil. Second, the false viviarpous shoots could form at any height in the canopy but not root successfully above a certain stem height (critical height). Alternatively, false vivipary may only occur on stems below a critical height, and stems of Calamus and Socratea may stop producing false viviparous inflorescences once they reach a certain height. The fourth possibility is that the viviparous shoot could abscise and fall to the forest floor. More studies on the morphology and ecology of false vivipary in the palms are needed in order to determine which mechanism occurs in which species.
Summary
This review of vegetative branching in palms reclassified vegetative branching types in the palms based on location of the branching meristem and then described variation within those types. This review demonstrated that diverse branching types exist in the Arecaceae. The phylogenetic distribution of shoot apical division, false vivipary, abaxial branching and leaf-opposed branching within the palm family and subfamilies gives insights into palm evolutionary history and ecological constraints. This review highlights how the lack of an overview of vegetative branching in the palm literature and the use of multiple, often poorly-defined terms for similar branching types has inhibited our understanding of basic palm evolution and ecology.
https://doi.org/10.1007/s 12229-018-9200-2
Acknowledgements We would like to thank Dr. Scott Zona for his extensive guidance and help editing. Dr. Jack Fisher for his help with the anatomical analysis and Dr. P. Barry Tomlinson for his help with the literature review and for anatomical insights. SME gratefully acknowledges the support of the Florida International University Dissertation Year Fellowship and the FIU International Center for Tropical Botany, both of which provided time for completing her dissertation; this research was completed in partial fulfillmet of her dissertation requirements. She also acknowledges the support of a Fairchild Tropical Botanic Garden Graduate Fellowship, which supported her during her dissertation research.
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Appendix
Table 4 Genera, species counts and references for the five
branching types and their combinations for subfamily Calamoideae.
Number under species counts give specics reviewed or
examined/number of species in genus
A. Species Number of specics that exhibit...
count
Genus No Lateral
branching axillary
Calamus 263/521 40 210
Eleiodoxa 1/1 1
Eremospatha 11/11 11
Eugeissona 6/6
Korthalsia 28/28
Laccosperma 6/6 6
Lepidocaryum 1/1 1
Mauritia 2/2 2
Mauritiella 4/4 4
Metroxylon 7/7 6 1
Myrialepis 1/1
Oncocalamus 5/5 5
Pigafetta 2/2 2
Plectocomia 15/15 15
Plectocomiopsis 6/6 6
Ruphia 19/20 8 11
Salacca 22/23 21
Calamoideae 399/659 58 292
A. Number of specics that exhibit...
Genus Shoot apical Shoot apical FALSE
dichotomy dichotomy with vivipary
lateral axillary
Calamus
Eleiodoxa
Eremospatha
Eugeissona 6
Korthalsia 28 *
Laccosperma
Lepidocaryum
Mauritia
Mauritiella
Metroxylon
Myrialepis
Oncocalamus
Pigafetta
Plectocomia
Plectocomiopsis
Ruphia
Salacca 2
Calamoideae 6 28 2
A. Number of specics that exhibit...
Genus False vivipary Abaxial Leaf-
with lateral opposed
axillary
Calamus 2 6
Eleiodoxa
Eremospatha
Eugeissona
Korthalsia
Laccosperma
Lepidocaryum
Mauritia
Mauritiella
Metroxylon
Myrialepis 1
Oncocalamus
Pigafetta
Plectocomia
Plectocomiopsis
Ruphia
Salacca
Calamoideae 2 7
A. References
Genus
Calamus Beccari, 1902; Beccari, 1914;
Dransfield, 1977; Dransfield, 1979;
Fisher & Dransfield. 1979;
Dransfield, 1982; Dransfield, 1984a;
Kramadibrata, 1992; Dransfield, 1997;
Evans et al., 2000; Rcnuka et al., 2001;
Baker & Dransfield, 2002a; Baker &
Dransfield, 2002b; Rustiami, 2002a;
Rustiami, 2002b; Baker et al., 2003;
Dransfield et al., 2005;
Henderson, 2005; Baker &
Dransfield; 2007; Henderson &
Henderson, 2007; Henderson et al.,
2008; Henderson, 2009;
Sunderland, 2012; Henderson & Dung,
2013; Rustiami et al., 2014;
Hcatubun et al., 2014; Baker &
Dransfield, 2014
Eleiodoxa Dransfield et al., 2008a. b
Eremospatha Dransfield et al., 2008a, b
Eugeissona Fisher etal., 1989;
Korthalsia Dransfield, 1981; Fisher &
Dransfield, 1979
Laccosperma Dransfield et al., 2008a, b
Lepidocaryum Dransfield et al., 2008a, b
Mauritia Dransfield et al., 2008a, b
Mauritiella Bernal & Galeano, 2010
Metroxylon Barrau. 1959; McClatchcy, 1998
Myrialepis Dransfield, 1982
Oncocalamus Dransfield et al., 2008a, b
Pigafetta Dransfield et al., 2008a, b
Plectocomia Dransfield, 1982
Plectocomiopsis Dransfield et al., 2008a, b
Ruphia Russell. 1965; Fisher et al., 1989
Salacca Fisher & Mogea, 1980
Calamoideae
Table 5 Genera, species counts and references for
the five branching types and their combinations for
subfamily Copryphoideae. Number under species give
species reviewed or examined/number of species in genus
B. Species Number of species that exhibit...
count
Genus No Lateral
branching axillary
Acoelorrhaphe 1/1 1
Arenga 20/24 3 17
Bismarkia 1/1 1
Borassodendron 2/2 2
Borassus 5/5 5
Brahea 11/11 10 1
Caryota 14/14 11 3
Chamaerops 1/1 1
Chelyocarpus 4/4 2 2
Chuniophoenix 2/2 2
Coccothrinax 50/53 46 4
Colpothrinax 3/3 3
Copemicia 22/22 21 1
Corypha 5/5 5
Cryosophila 10/10 10
Guihaia 2/2 2
Hemithrinax 3/3 3
Hyphaene 7/8 2
Itaya 1/1 1
Johannesteijsmannia 4/4 4
Kerriodoxa 1/1 1
Lanonia 8/8 1 7
Latania 3/3 3
Leucothrinax 1/1 1
Licuala 60/162 38 22
Livistona 27/27 27
Lodoicea 1/1 1
Maxburretia 2/3 2
Medemia 1/1 1
Nannorhops 1/1
Phoenix 13/13 6 7
Pholidocarpus 6/6 6
Pritchardia 30/30 30
Pritchardiopsis 1/1 1
Rhapidophyllum 1/1 1
Rhapis 10/10 10
Sabal 14/14 14
Sabinaria 1/1 1
Saribus 1/1 1
Satranala 1/1 1
Schippia 1/1 1
Serenoa 1/1 1
Tahina 1/1 1
Thrinax 3/3 3
Trachvcarpus 10/10 10
Trithrinax 3/3 2 1
Wallchia 8/8 1 7
Washingtonia 2/2 2
B. Number of species that exhibit...
Genus Shoot Shoot apical FALSE
apical dichotomy vivipary
dichotomy with lateral
axillary
Acoelorrhaphe
Arenga
Bismarkia
Borassodendron
Borassus
Brahea
Caryota
Chamaerops
Chelyocarpus
Chuniophoenix
Coccothrinax
Colpothrinax
Copemicia
Corypha
Cryosophila
Guihaia
Hemithrinax
Hyphaene 3 2
Itaya
Johannesteijsmannia
Kerriodoxa
Lanonia
Latania
Leucothrinax
Licuala
Livistona
Lodoicea
Maxburretia
Medemia
Nannorhops 1
Phoenix
Pholidocarpus
Pritchardia
Pritchardiopsis
Rhapidophyllum
Rhapis
Sabal
Sabinaria
Saribus
Satranala
Schippia
Serenoa
Tahina
Thrinax
Trachvcarpus
Trithrinax
Wallchia
Washingtonia
B. References
Genus
Acoelorrhaphe Personal observation
Arenga Dransfield et al., 2008a, b;
Jeanson & Guo, 2011
Bismarkia Dransfield et al., 2008a, b
Borassodendron Dransfield et al., 2008a, b
Borassus Dransfield et al., 2008a, b
Brahea Dransfield et al., 2008a, b
Caryota Dransfield et al., 2008a, b;
Personal observation
Chamaerops Dransfield et al., 2008a, b:
personal observation
Chelyocarpus Kahn & Mejia.1988;
Dransfield et al., 2008a, b
Chuniophoenix Dransfield et al., 2008a, b;
Personal observation
Coccothrinax Henderson et al., 1997;
Henderson, 2005; Moya, 1997b
Colpothrinax Dransfield et al., 2008a. b;
Personal observation
Copemicia Henderson et al., 1997; Moya, 1997a
Corypha Dransfield et al., 2008a, b;
Personal observation
Cryosophila Dransfield et al., 2008a, b;
Personal observation
Guihaia Dransfield et al., 1985;
Dransfield et al., 2008a, b;
Hemithrinax Dransfield et al., 2008a, b
Hyphaene Moore & Uhl, 1982;
van Valkenburg & Dransfield, 2004
Itaya Dransfield et al., 2008a, b;
personal observation
Johannesteijsmannia Dransfield et al., 2008a, b
Kerriodoxa Dransfield et al., 2008a. b;
Personal observation
Lanonia Henderson & Bacon, 2011
Latania Dransfield et al., 2008a, b;
Personal observation
Leucothrinax Dransfield et al., 2008a, b;
Personal observation
Licuala Henderson et al., 1997;
Takcnaka et al., 2001;
Dransfield et al., 2008a, b;
Henderson et al., 2008;
Livistona Dransfield et al., 2008a, b;
Dowe, 2009
Lodoicea Dransfield et al., 2008a, b
Maxburretia Dransfield et al., 2008a, b;
Henderson, 2009
Medemia Dransfield et al., 2008a, b
Nannorhops Tomlison & Moore Jr., 1968
Phoenix Davis, 1950; Chevalier, 1952;
Barrow, 1998; Dransfield et al.,
2008a, b; Barrett, 1973
Pholidocarpus Dransfield et al., 2008a, b
Pritchardia Dransfield et al., 2008a, b;
Personal observation
Pritchardiopsis Dransfield et al., 2008a, b
Rhapidophyllum Dransfield et al., 2008a, b;
Personal observation
Rhapis Dransfield et al., 2008a, b;
Personal observation
Sabal Dransfield et al., 2008a, b
Sabinaria Dransfield et al., 2008a, b
Saribus Bacon & Baker, 2011
Satranala Dransfield et al., 2008a. b
Schippia Dransfield et al., 2008a, b
Serenoa Fisher & Tomlison, 1973;
Bennet & Hicklin, 1998;
Abrahamson, 1999;
Personal observation
Tahina Dransfield et al., 2008a, b
Thrinax Dransfield et al., 2008a, b
Trachvcarpus Dransfield et al., 2008a, b
Trithrinax Dransfield et al., 2008a, b;
Personal observation
Wallchia Dransfield et al., 2008a, b;
Personal observation
Washingtonia Henderson et al., 1997;
Dransfield et al., 2008a, b
Table 6 Genera, species counts and references for
the four branching types and their combinations for
subfamily Ceroxyloideae. Number under species counts
give species reviewed or examined/number of species in genus.
C. Species Number of species that exhibit...
count
Genus No Lateral
branching axillary
Ammandra 1/1 1
Aphandra 1/1 1
Ceroxylon 12/12 12
Juania 1/1 1
Oraniopsis 1/1 1
Phytelephas 6/6 4 2
Pseudophoenix 4/4 4
Ravenea 21/21 20 1
Ceroxyloideae 47/47 46 1
C. Number of species that exhibit...
Genus Shoot apical Shoot apical FALSE
dichotomy dichotomy with vivipary
lateral axillary
Ammandra
Aphandra
Ceroxylon
Juania
Oraniopsis
Phytelephas
Pseudophoenix
Ravenea
Ceroxyloideae
C. Number of species that exhibit...
Genus False vivipary Abaxial Leaf-opposed
with lateral
axillary
Ammandra
Aphandra
Ceroxylon
Juania
Oraniopsis
Phytelephas
Pseudophoenix
Ravenea
Ceroxyloideae
C. References
Genus
Ammandra Dransfield et al.. 2008a, 2008b
Aphandra Dransfield et al., 2008a, 2008b
Ceroxylon Dransfield et al.. 2008a, 2008b
Juania Dransfield et al., 2008a, 2008b
Oraniopsis Dransfield et al., 2008a, 2008b
Phytelephas Dransfield et al.. 2008a, 2008b
Pseudophoenix Dransfield et al.. 2008a, 2008b
Ravenea Beentje, 1994a; Beentje. 1994b:
Ceroxyloideae Dransfield et al., 2008a, 2008b;
Rakotoarinivo, 2008;
Table 7 Genera, species counts references for the four
branching types and their combinations for subfamily Arecoideae
(A. Acanthophoenix-Beccariophoenix, B. Bentinckia--Drymophloeus,
C. Dypsis--Leopoldinia, D. Lepidorhachis-Prestoea,
E. Ptychococcus--Voaniola, F. Wallaceodoxa--Bodyetia.
Number under species counts give species reviewed or
examined/number of species in genus
D. Species Number of species that exhibit...
count
Genus No branching Lateral axillary
Acanlhophoenix 3
Acrocomia 8/8 8
Actinokentia 2/2 2
Actinorhytis 1/1 1
Adonidia 1/1 1
Aiphanes 23/29 11 12
Allagoptera 5/5 1
Archontophoenix 6/6 6
Areca 37/46 24 13
Asterogyne 5/5 5
Astrocuryum 32/38 24 8
Attalea 66/66 66
Bactris 72/79 5 67
Balaka 9/9 9
Barcella 1/1 1
Basselinia 14/14 10 3
Beccariophoenix 3/3 1
Bentinckia 2/2 2
Brassiophoenix 2/2 2
Bwretiokentia 5/5 5
Butia 17/20 14 3
Calyptrocaix 21/26 12 9
Calyptrogyne 10/17 10
Calyptronoma 3/3 3
Carpentaria 1/1 1
Carpoxvlon 1/1 1
Chamaedorea 91/104 73 17
Chambeyronia 2/2 2
Clinosperma 4/4 4
Clinostigma 11/11 11
Cocos 1/1 1
Cyphokentia 2/2 1 1
Cyphophoenix 4/4 4
Cyphosperma 5/5 5
Cyrtostachys 5/7 1 4
Deckenia 1/1 1
Desmoncus 24/24 24
Dictyocaryum 3/3 3
Dictyospertna 1/1 1
Dransfieldia 1/1 1
Drymophloeus 5/7 5
Dypsis 160/167 63 90
Elaeis 2/2 2
Euterpe 7/7 1 6
Gaussia 5/5 5
Geonoma 39/68 14 25
Hedyscepe l/l 1
Hetemspathe 22/41 18 4
Howea 2/2 2
Hydriastele 30/49 16 14
Hvophorbe 5/5 5
Hyospalhe 2/5 2
Iguanura 25/33 15 10
Irartea 1/1 1
Iriartella 2/2 2
Jailoloa 1/1 1
Jubaea 1/1 1
Jubaeopsis 1/1 1
Kentiopsis 4/4 4
Laccospadix 1/1 1
Lemurophoenix 1/1 1
Leopoldinia 2/2 2
Lepidorrhachis 1/1 1
Linospadix 7/7 1 6
Loxococcus 1/1 1
Lytocaryum 4/4 4
Manicaria 2/2 1
Manjekia 1/1 1
Marojejya 2/2 2
Masoala 2/2 2
Nenga 4/5 1 3
Neonicholsonia 1/1 1
Neoveitchia 2/2 2
Nephrosperma 1/1 1
Normanbya 1/1 1
Oertocarpus 9/9 8 1
Oncosperma 6/6
Orania 18/18 18
Parajubaea 3/3 3
Pelagodoxa 1/1 1
Phoenicophorium 1/1 1
Pholidostachys 4/8 4
Physokentia 7/7 7
Pinanga 60/139 12 48
Podococcus 2/2 2
Ponapea 4/4 4
Prestoea 10/10 2 8
Ptychococcus 2/2 3
Ptychosperma 19/29 7 12
Reihardtia 6/6 1 5
Rhopaloblaste 6/6 5 1
Rhopalostylis 2/2 2
Roscheria 1/1 1
Roystonea 10/10 1
Satakentia 1/1 1
Sclerosperma 3/3 3
Socratea 5/5 4
Solfia 1/1 1
Sommieria 1/1 1
Syagrus 36/61 23 12
Synechanthus 2/2 1 1
Tectiphiala 1/1 1
Veitchia 11/11 11
Verschaffeltia 1/1 1
Voaniola 1/1 1
Wallaceodoxa l/l 1
Welfia 1/1 1
Wendlandiella 1/1 1
Weltinia 21/21 19 2
Wodvetia 1/1 1
Arecoideae 1112/1376 657 423
D. Number of species that exhibit...
Genus Shoot apical Shoot apical False vivipary
dichotomy dichotomy with
lateral axillary
Acanlhophoenix
Acrocomia
Actinokentia
Actinorhytis
Adonidia
Aiphanes
Allagoptera 4
Archontophoenix
Areca
Asterogyne
Astrocuryum
Attalea
Bactris
Balaka
Barcella
Basselinia 1
Beccariophoenix
Bentinckia
Brassiophoenix
Bwretiokentia
Butia
Calyptrocaix
Calyptrogyne
Calyptronoma
Carpentaria
Carpoxvlon
Chamaedorea 1
Chambeyronia
Clinosperma
Clinostigma
Cocos
Cyphokentia
Cyphophoenix
Cyphosperma
Cyrtostachys
Deckenia
Desmoncus
Dictyocaryum
Dictyospertna
Dransfieldia
Drymophloeus
Dypsis 6
Elaeis
Euterpe
Gaussia
Geonoma
Hedyscepe
Hetemspathe
Howea
Hydriastele
Hvophorbe
Hyospalhe
Iguanura
Irartea
Iriartella
Jailoloa
Jubaea
Jubaeopsis
Kentiopsis
Laccospadix
Lemurophoenix
Leopoldinia
Lepidorrhachis
Linospadix
Loxococcus
Lytocaryum
Manicaria 1
Manjekia
Marojejya
Masoala
Nenga
Neonicholsonia
Neoveitchia
Nephrosperma
Normanbya
Oertocarpus
Oncosperma
Orania
Parajubaea
Pelagodoxa
Phoenicophorium
Pholidostachys
Physokentia
Pinanga
Podococcus
Ponapea
Prestoea
Ptychococcus
Ptychosperma
Reihardtia
Rhopaloblaste
Rhopalostylis
Roscheria
Roystonea
Satakentia
Sclerosperma
Socratea
Solfia
Sommieria
Syagrus 1
Synechanthus
Tectiphiala
Veitchia
Verschaffeltia
Voaniola
Wallaceodoxa
Welfia
Wendlandiella
Weltinia
Wodvetia
Arecoideae 13 1
D. Number of species that exhibit...
Genus False vivipary Abaxial Leaf-opposed
with lateral
axillary
Acanlhophoenix
Acrocomia
Actinokentia
Actinorhytis
Adonidia
Aiphanes
Allagoptera
Archontophoenix
Areca
Asterogyne
Astrocuryum
Attalea
Bactris
Balaka
Barcella
Basselinia
Beccariophoenix
Bentinckia
Brassiophoenix
Bwretiokentia
Butia
Calyptrocaix
Calyptrogyne
Calyptronoma
Carpentaria
Carpoxvlon
Chamaedorea
Chambeyronia
Clinosperma
Clinostigma
Cocos
Cyphokentia
Cyphophoenix
Cyphosperma
Cyrtostachys
Deckenia
Desmoncus
Dictyocaryum
Dictyospertna
Dransfieldia
Drymophloeus
Dypsis 1
Elaeis
Euterpe
Gaussia
Geonoma
Hedyscepe
Hetemspathe
Howea
Hydriastele
Hvophorbe
Hyospalhe
Iguanura
Irartea
Iriartella
Jailoloa
Jubaea
Jubaeopsis
Kentiopsis
Laccospadix
Lemurophoenix
Leopoldinia
Lepidorrhachis
Linospadix
Loxococcus
Lytocaryum
Manicaria
Manjekia
Marojejya
Masoala
Nenga
Neonicholsonia
Neoveitchia
Nephrosperma
Normanbya
Oertocarpus
Oncosperma 6
Orania
Parajubaea
Pelagodoxa
Phoenicophorium
Pholidostachys
Physokentia
Pinanga
Podococcus
Ponapea
Prestoea
Ptychococcus
Ptychosperma
Reihardtia
Rhopaloblaste
Rhopalostylis
Roscheria
Roystonea
Satakentia
Sclerosperma
Socratea 1
Solfia
Sommieria
Syagrus
Synechanthus
Tectiphiala
Veitchia
Verschaffeltia
Voaniola
Wallaceodoxa
Welfia
Wendlandiella
Weltinia
Wodvetia
Arecoideae 1 7 0
D. References
Genus
Acanlhophoenix Dransfield et al., 2008a, 2008b
Acrocomia Dransfield et al., 2008a, 2008b
Actinokentia Dransfield et al., 2008a, 2008b
Actinorhytis Dransfield et al., 2008a, 2008b
Adonidia Dransfield et al., 2008a, 2008b
Aiphanes Borchsenius & Bemal. 1996;
Henderson et al., 1997
Allagoptera Tomlison, 1967
Archontophoenix Personal observation
Areca Dransfield, 1984b;
Henderson, 2009;
Heatubun, 2011;
Heambun et al., 2012
Asterogyne Henderson & Steyermark, 1986;
de Granville & Henderson, 1988;
Stauffer et al., 2003;
Dransfield et al., 2008a, 2008b
Astrocuryum Kahn & Millan, 1992;
Henderson et al., 1997;
Borchsenius et al., 1998;
Kahn & de Granville, 1998;
Kahn, 2008
Attalea Dransfield et al., 2008a, 2008b
Bactris Tomlison. 1990; Henderson et al.,
1997; Henderson, 2000
Balaka Dransfield et al., 2008a, 2008b
Barcella Dransfield et al., 2008a, 2008b
Basselinia Moore & Uhl, 1984; Essig et al.,
1999; Pintaud & Baker, 2008;
Pintaud & Stauffer, 2015
Beccariophoenix Dransfield et al., 2008a, 2008b
Bentinckia Dransfield et al., 2008a, 2008b
Brassiophoenix Dransfield et al., 2008a, 2008b
Bwretiokentia Dransfield et al., 2008a, 2008b
Butia Gaiero et al., 2011
Calyptrocaix Dowe & Ferrero, 2001
Calyptrogyne Henderson et al., 1997;
Dransfield et al., 2008a, b
Calyptronoma Dransfield et al., 2008a, 2008b
Carpentaria Dransfield et al., 2008a, 2008b
Carpoxvlon Dransfield et al., 2008a, 2008b
Chamaedorea Fisher, 1974; Model, 1992
Chambeyronia Dransfield et al., 2008a, 2008b
Clinosperma Dransfield et al., 2008a, 2008b
Clinostigma Dransfield et al., 2008a, 2008b
Cocos Balaga. 1975; Dransfield et al.,
2008a, 2008b
Cyphokentia Moore & Uhl, 1984;
Jaffre & Veillon, 1989
Cyphophoenix Dransfield et al., 2008a, 2008b
Cyphosperma Dransfield et al., 2008a, 2008b
Cyrtostachys Dransfield, 1978;
Heatubun et al., 2009
Deckenia Dransfield et al., 2008a. 2008b
Desmoncus Putz, 1990; lsnard et al., 2005;
Tomlinson & Zimmerman, 2003
Dictyocaryum Henderson, 1990;
Dransfield et al., 2008a, 2008b
Dictyospertna Dransfield et al., 2008a, 2008b
Dransfieldia Baker et al., 2006
Drymophloeus Zona, 1999
Dypsis Dransfield & Beentje, 1995;
Fisher and Maidman, 1999;
Dransfield, 2003;
Britt & Dransfield, 2005;
Hodel et al., 2005;
Rakotoarinivo et al., 2009
Elaeis Dransfield et al., 2008a. 2008b
Euterpe Henderson & Galeano, 1996;
Dransfield et al., 2008a, 2008b
Gaussia Dransfield et al., 2008a, 2008b
Geonoma Henderson, 1995;
Henderson et al., 1997;
Dransfield et al., 2008a, 2008b;
Henderson. 2011 a
Hedyscepe Dransfield et al., 2008a, 2008b
Hetemspathe Fernando. 1990
Howea Dransfield et al., 2008a, 2008b
Hydriastele Baker & Dransfield, 2007
Hvophorbe Dransfield et al., 2008a. 2008b
Hyospalhe Skov & Balslev, 1989;
Borchsenius et al., 1998
Iguanura Kiew, 1976; Henderson, 2009
Irartea Dransfield et al., 2008a, 2008b
Iriartella Dransfield et al., 2008a, 2008b
Jailoloa Heatubun et al., 2014
Jubaea Dransfield et al., 2008a, 2008b
Jubaeopsis Dransfield, 1989
Kentiopsis Dransfield et al., 2008a, 2008b
Laccospadix Dowe, 2010
Lemurophoenix Dransfield et al., 2008a. 2008b
Leopoldinia Bemal & Galeano, 2010;
Henderson, 2011a, b
Lepidorrhachis Dransfield et al., 2008a, 2008b
Linospadix Dowe & Irvine, 1997;
Dowe & Ferrero. 2001
Loxococcus Dransfield et al., 2008a, 2008b
Lytocaryum Dransfield et al., 2008a, 2008b
Manicaria Bernal & Galeano, 2010:
Fisher & Zona, 2006
Manjekia Heatubun et al., 2014
Marojejya Dransfield et al., 2008a, 2008b
Masoala Dransfield et al., 2008a, 2008b
Nenga Fernando, 1983; Henderson, 2009
Neonicholsonia Henderson & Galeano, 1996;
Dransfield et al., 2008a, 2008b
Neoveitchia Dransfield et al., 2008a, 2008b
Nephrosperma Dransfield et al., 2008a, 2008b
Normanbya Dransfield et al., 2008a, 2008b
Oertocarpus Bemal et al., 1991;
Henderson et al., 1997;
Dransfield et al., 2008a, 2008b
Oncosperma Fisher et al., 1989;
Fisher and Maidman. 1999
Orania Dransfield et al., 2008a, 2008b
Parajubaea Dransfield et al., 2008a, 2008b
Pelagodoxa Dransfield et al., 2008a. 2008b
Phoenicophorium Dransfield et al., 2008a, 2008b
Pholidostachys Dransfield et al., 2008a, 2008b
Physokentia Dransfield et al., 2008a, 2008b
Pinanga Dransfield, 1978; Henderson, 2009
Podococcus Bullock, 1980;
Van Valkenburg et al., 2007
Ponapea Dransfield et al., 2008a, 2008b
Prestoea Henderson & deNevers, 1988;
Henderson & Galeano, 1996
Ptychococcus Dransfield et al., 2008a, 2008b
Ptychosperma Essig, 1977; Essig, 1978;
Dowe & Ferrero, 2001
Reihardtia Henderson et al., 1997;
Henderson, 2002b
Rhopaloblaste Banka & Baker, 2004
Rhopalostylis Dransfield et al., 2008a, 2008b
Roscheria Dransfield et al., 2008a, 2008b
Roystonea Dransfield et al., 2008a, 2008b
Satakentia Dransfield et al., 2008a, 2008b
Sclerosperma Van Valkenburg et al., 2007;
van Valkenburg, et al., 2008
Socratea Bernal-Gonzales & Henderson,
1986; Svenning & Balslev, 1998;
Pintaud & Millan, 2004
Solfia Dransfield et al., 2008a, 2008b
Sommieria Dransfield et al., 2008a, 2008b
Syagrus Henderson, 1995:
Pinheiro et al., 1996:
Noblick, 1996; Noblick. 2004;
Noblick & Lorenzi, 2010;
Noblick et al., 2014;
Noblick & Meerow, 2015
Synechanthus Dransfield et al., 2008a, b
Tectiphiala Moore, 1978
Veitchia Dransfield et al., 2008a, 2008b
Verschaffeltia Dransfield et al., 2008a, 2008b
Voaniola Dransfield, 1989;
Dransfield et al., 2008a, 2008b
Wallaceodoxa Heatubun et al., 2014
Welfia Dransfield et al., 2008a, 2008b
Wendlandiella Dransfield et al., 2008a, 2008b
Weltinia Henderson et al., 1997;
Borchsenius et al., 1998
Wodvetia Dransfield et al. 2008a, 2008b
Arecoideae
Sara M. Edelman (1,2,3) * Jennifer H. Richards (1,2)
(1) Florida International University, 11200 SW 8th Street, Miami, FL 33199, USA
(2) International Center for Tropical Botany, 4013 Douglas Road, Miami, FL 33133, USA
(3) Author for Correspondence; c-mail: Sedel003@fiu.edu Published online: 18 June 2018
Caption: Fig. 1 Vegetative branching types in the palms (arrows indicate vegetative branch): a No branching type (Hyophorbe laugenicaulis) or solitary: b Lateral axillary branching (Rhapis mulifida); c shoot apical division (Hyphaene dichotoma): d false vivipary (Socratea salazarii); D. abaxial branching (Dypsis lutescens); and E. leaf-opposed branching (Myrialepis paradoxa). Arrow points to branch
Caption: Fig. 2 Plan view of a palm leaf with locations of the three distinct types of stem nodal buds and thus branching types; the stem is not drawn but the encircling leaf base is shown, a Axillary branching--the meristem arises in the axil of the leaf; b Abaxial branching-the meristem is located on the base of the leaf sheath, on the abaxial surface of the leaf; and c Leaf-opposed branching-the meristem is borne on the stem of the palm, enclosed by the outer edges of the leaf sheath and opposite to the lamina and petiole
Caption: Fig. 3 Distribution of branching types in the palm family (Arecaceae) on a sub-family level cladogram (a key to branching types; b sub-family cladogram)
Caption: Fig. 4 Distribution of branching types in the Calamoideae on a genus level cladogram. Key the same as Fig. 3a
Caption: Fig. 5 Distribution of branching types in the Calamoidcac on a genus level cladogram. Key the same as Fig. 3a
Caption: Fig. 6 Distribution of branching types in the Arecoideae on a genus level cladogram (a entire cladogram showing further break down; b Socratea-Parajubaea; c Podococcus-Clinostigma d Chambeyronia-Neoveitchia; and e Ptychospemia-Normanbya). Key the same as Fig. 3a
Table 1 Definitions of branching terms used in this study.
In the first column terms in bold are the branching terms
used in this review with synonyms (non-bold terms listed
in parentheses directly below the bold); indented below the
new term arc terms from the literature that are included in
the new term. Additional columns provide references,
definitions of the branching type, and palm examples
Term (synonym(s)) Refercnce(s) Definition
Lateral axillary Tomlinson 1990 Branch originates in the
branch axil of the leaf
Basal sucker Tomlinson 1990 Lateral axillaiy branch
immediately grows
upward, limited to
basal internodes
Aerial lateral Tomlinson 1990 Lateral axillary branch
axillary branch is not limited to basal
intcmodcs
Dormant basal Tomlinson 1990 Basal sucker outgrowth
suckers is dormant until death
of parent stem
Rhizomatous Zimmermann Vegetative outgrowth of
branch and Tomlinson axillary meristcm at base
1967 of stem where monopodial
or sympodial units form
a plagiotropic rhizome
Sympodial Zimmermann Vegetative outgrowth of
rhizomatous and Tomlinson axillary meristem at base
branch 1967 of stem where sympodial
units form a plagiotropic
rhizome
Monopodial Bell & Tomlinson Vegetative outgrowth of
rhizomatous 1980 axillary meristcm at base
branch of stem where monopodial
units form a plagiotropic
rhizome
Shoot apical Tomlinson 1990 Branch originates in the
division apical meristcm, most
(Apical commonly as a division
branch) of the apical meristem
Apical division Gola 2014 More or less equal
division of apical meristem,
resulting in two independent
functioning axes
Apical isotomy Gola 2014 Equal division apical
meristem that results in
two independent functioning
axes of similar size and
morphology
Apical anisotomy Gola 2014 Unequal division apical
meristem that results in
two independent functioning
axes of different size and
morphology
Nannorhops * new term Equal division apical
branching meristem that results in
two independent functioning
axes of different size and
morphology
Adventitious bud/ Fisher 1973 Meristem not in typical
branching position
False vivipary Fisher and Adventitious vegetative
(prolification, Dransfield 1977; outgrowth at the shoot
vegetative Bell and Btyan apex of the inflorescence,
transformation 2008 growing independently
of of inflorescence axis
inflorescence,
broadly
as proliferation
(sensu latu))
Proliferation Bell and Bryan Adventitious mcristcm
(sensu stricto) 2008 originates from vegetative
material, usually leaves
Abaxial branch Fisher 1973, Vegetative branch meristem
Fisher et al. borne on the abaxial
1989 surface of leaf, on the
base of the leaf sheath
Leaf-opposed Fisher and Vegetative branch meristem
branch Dransfield 1979; borne on the stem opposite
Tillich 1998 of leaf and enclosed in the
leaf sheath
Term (synonym(s)) Palm example
Lateral axillary Serenoa repens
branch
Basal sucker Pytchosperma
macarthurii
Aerial lateral Geonoma baculifera,
axillary branch Hyospathe elegans
Dormant basal Plectomia spp.
suckers
Rhizomatous Rhapis excelsa
branch
Sympodial Rhapis exelsa
rhizomatous
branch
Monopodial No palm example
rhizomatous
branch
Shoot apical Hvphaene thebaica
division
(Apical
branch)
Apical division Hyphaene coriaceae
Apical isotomy Nypa fruticans
Apical anisotomy Eugeissona tiistis
Nannorhops Nannorhops richiana
branching
Adventitious bud/ Socratea salazarii
branching
False vivipary Calamus castaneiis
(prolification,
vegetative
transformation
of
inflorescence,
broadly
as proliferation
(sensu latu))
Proliferation No palm example
(sensu stricto)
Abaxial branch Dyipsis lutescens
Leaf-opposed Myrialepis
branch
Table 2 Palm subfamilies and their species counts for the
five branching types and their combinations. References for
sub-families can be found in the individual sub-family tables
Subfamily Species count Number of spcies that exhibit...
No Lateral
branching axillary
Arccoidcae 1112/1376 657 423
Calamoidcae 395/659 58 292
Ccroxyloideae 47/47 46 1
Coryphoidcae 381/492 283 92
Nypoidcae 1/1
Arccaceae (1903/2501) 1043 646
Subfamily Number of spcies that exhibit...
Shoot apical Shoot apical FALSE
dichotomy dichotomy with vivipary
lateral axillary
Arccoidcae 13 1
Calamoidcae 6 28 2
Ccroxyloideae
Coryphoidcae 3 3
Nypoidcae 1
Arccaceae 21 31 2
Table 3 Key to major branching types in the palms; palm branching
types were distinguished by location of the meristem
If there is more than one crown meristem used for branching is (a)
axillary, (b) apical, (c), adventitious (atypical position)
a. Axillary (1) Later axilary branching
b. Apical (2) Shoot apical division
c. Adventitious: bud borne on (a) inflorescence, (b) leaf sheath, (c)
sterm
a. Inflorescence (3) False vivipary
b. Leaf sheath, base (4) Abaxial
c. Stern, enclosed in leaf sheath (5) Leaf-opposed
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| |
| Author: | Edelman, Sara M.; Richards, Jennifer H. |
|---|---|
| Publication: | The Botanical Review |
| Article Type: | Report |
| Date: | Mar 1, 2019 |
| Words: | 13389 |
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