Phylogenetic relationships among arecoid palms (Arecaceae: Arecoideae)

Background and Aims

The Arecoideae is the largest and most diverse of the five subfamilies of palms (Arecaceae/Palmae), containing >50 % of the species in the family. Despite its importance, phylogenetic relationships among Arecoideae are poorly understood. Here the most densely sampled phylogenetic analysis of Arecoideae available to date is presented. The results are used to test the current classification of the subfamily and to identify priority areas for future research.

Methods

DNA sequence data for the low-copy nuclear genes PRK and RPB2 were collected from 190 palm species, covering 103 (96 %) genera of Arecoideae. The data were analysed using the parsimony ratchet, maximum likelihood, and both likelihood and parsimony bootstrapping.

Key Results and Conclusions

Despite the recovery of paralogues and pseudogenes in a small number of taxa, PRK and RPB2 were both highly informative, producing well-resolved phylogenetic trees with many nodes well supported by bootstrap analyses. Simultaneous analyses of the combined data sets provided additional resolution and support. Two areas of incongruence between PRK and RPB2 were strongly supported by the bootstrap relating to the placement of tribes Chamaedoreeae, Iriarteeae and Reinhardtieae; the causes of this incongruence remain uncertain. The current classification within Arecoideae was strongly supported by the present data. Of the 14 tribes and 14 sub-tribes in the classification, only five sub-tribes from tribe Areceae (Basseliniinae, Linospadicinae, Oncospermatinae, Rhopalostylidinae and Verschaffeltiinae) failed to receive support. Three major higher level clades were strongly supported: (1) the RRC clade (Roystoneeae, Reinhardtieae and Cocoseae), (2) the POS clade (Podococceae, Oranieae and Sclerospermeae) and (3) the core arecoid clade (Areceae, Euterpeae, Geonomateae, Leopoldinieae, Manicarieae and Pelagodoxeae). However, new data sources are required to elucidate ambiguities that remain in phylogenetic relationships among and within the major groups of Arecoideae, as well as within the Areceae, the largest tribe in the palm family.     

Non-axillary branching in the palms Eugeissona and Oncosperma (Arecaceae)

FISHER, J. B., GOH, C. J. & RAO, A. N., 1989. Non-axillary branching in the palms Eugeissona and Oncosperma (Arecaceae). The south-east Asian palms, Eugeissona (Calamoideae) and Oncosperma (Arecoideae) are multiple-stemmed. The morphology and development of branching in two species of each genus were examined in Singapore, Borneo, and the Malay Peninsula. Cultivated seedling and adult plants of 0. tigillarium were also observed in Florida. A new shoot arises most often from a longitudinal abaxial groove at the base of an enclosing leaf sheath. In some instances, especially in E. tristis , the enclosing leaf has two equal, adjacent grooves such that any distinction between an original mother shoot and a lateral daughter shoot is impossible. No axillary buds occur in Eugeissona which is hapaxanthic. In Oncosperma , which is pleonanthic, axillary buds are absent from young pre-flowering stems, but an inflorescence bud occurs in the axil of each leaf in older aerial stems. Early ontogenetic stages of vegetative branching, as seen in sectioned apices, indicate that a new vegetative shoot is present on the abaxial base of the first (youngest) leaf primordium. There is no ontogenetic evidence for the displacement of an originally axillary meristem as previously described for the palm Salacca (Calamoideae). Shoot development in Eugeissona is interpreted as a putative dichotomy of the apical meristem in which the meristem centres commonly develop unequally. In Oncosperma the smaller sucker bud meristem may be described as an abaxial leaf base bud, but ontogenetic variations indicate this form of branching is close to dichotomous branching. These new examples of non-axillary branching are compared to similar cases previously reported for palms and other monocotyledons.     

Neither insects nor wind: ambophily in dioecious Chamaedorea palms (Arecaceae)

Pollination of Neotropical dioecious trees is commonly related to generalist insects. Similar data for non‐tree species with separated genders are inconclusive. Recent studies on pollination of dioecious Chamaedorea palms (Arecaceae) suggest that species are either insect‐ or wind‐pollinated. However, the wide variety of inflorescence and floral attributes within the genus suggests mixed pollination mode involving entomophily and anemophily. To evaluate this hypothesis, we studied the pollination of Chamaedorea costaricana, C. macrospadix, C. pinnatifrons and C. tepejilote in two montane forests in Costa Rica. A complementary morphological analysis of floral traits was carried out to distinguish species groups within the genus according to their most probable pollination mechanism. We conducted pollinator exclusion experiments, field observations on visitors to pistillate and staminate inflorescences, and trapped airborne pollen. A cluster analysis using 18 floral traits selected for their association with wind and insect pollination syndromes was carried out using 52 Chamaedorea species. Exclusion experiments showed that both wind and insects, mostly thrips (Thysanoptera), pollinated the studied species. Thrips used staminate inflorescences as brood sites and pollinated pistillate flowers by deception. Insects caught on pistillate inflorescences transported pollen, while traps proved that pollen is wind‐borne. Our empirical findings clearly suggest that pollination of dioecious Chamaedorea palms is likely to involve both insects and wind. A cluster analysis showed that the majority of studied species have a combination of floral traits that allow for both pollination modes. Our pollination experiments and morphological analysis both suggest that while some species may be completely entomophilous or anemophilous, ambophily might be a common condition within Chamaedorea. Our results propose a higher diversity of pollination mechanisms of Neotropical dioecious species than previously suggested.     

Leaf anatomy and its taxonomic significance in phytelephantoid palms (Arecaceae)

The leaf anatomy of the genera Phytelephas, Palandra and Ammandra (Arecaceae) is described and compared. The anatomical features considered to be of taxonomic importance include: the distribution of fibre bundles and minor veins in mesophyll and hypodermis, the relative size of the cells of the stomatal complex and whether the costal bands of eleongated cells are conspicuous in surface view or not. Species of Palandra and Phytelephas form an anatomically homogenous group. The two species of Ammandra differ in their anatomy, although they have several xeromorphic adaptations in common. This is peculiar as they both grow in humid habitats.     

Floral scent chemistry and pollination ecology in phytelephantoid palms (Arecaceae)

The subfamilyPhytelephantoideae comprises three genera (Ammandra, Aphandra, andPhytelephas) and seven species of dioecious palms. The floral scents ofAmmandra dasyneura, A. decasperma, Aphandra natalia, Phytelephas aequatorialis, P. macrocarpa, andP. seemannii were analyzed by gas chromatography-mass spectrometry. We studied the pollination biology ofA. natalia, P. aequatorialis, andP. macrocarpa, and tested how the synthetically produced main constituents of the floral scents ofAphandra andPhytelephas attracted insects in two natural populations ofPhytelephas. The genera are distinct in terms of floral scents.Ammandra has sesquiterpenes,Aphandra (+)-2-methoxy-3-sec-butylpyrazine, andPhytelephas p-methyl anisol. These constituents dominated the scents quantitatively and qualitatively. The similarity between scents of male and female inflorescences was 76.5% inAmmandra, 84.2% inAphandra, and >99% inPhytelephas. Different species ofAleocharinae (Staphylinidae) pollinateAphandra natalia andPhytelephas species and reproduce in their male inflorescences.Derelomini (Curculinoidae) andMystrops (Nitidulidae) only visit and pollinatePhytelephas in which male inflorescences they reproduce. A species ofBaridinae (Curculionidae) only visits and pollinatesAphandra natalia, and reproduces in its female inflorescence. The apparent reliance on one or a few floral scent constituents as attractants and few and specific pollinators may indicate co-evolution. Sympatric species ofPhytelephantoideae have different scents. We suggest that species with similar scents have allopatric distributions due to the absence of a pollinator isolation mechanism.     

A monograph of the betel nut palms (Areca: Arecaceae) of East Malesia

The palm genus Areca is widespread in tropical Asia and includes the economically important betel nut palm, A. catechu. The genus has three centres of high species diversity: the Sunda Region, the Philippines and East Malesia (to the east of Wallace's line). The taxonomy of the genus in East Malesia has been neglected. Prior to this study, 19 species were accepted for this area, all but one endemic, but their limits and differences were not understood. Here, we provide a taxonomic monograph of East Malesian Areca spp., based on an extensive study of the genus in herbaria and in the field. We recognize six species of Areca in East Malesia, including the widespread cultivated A. catechu. Five wild species are accepted, namely A. macrocalyx, A. mandacanii, A. novohibernica, A. oxycarpa and A. vestiaria. We place 12 of the previously accepted species into synonymy, and provide additional new synonymy in A. catechu. © 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2012, 168 , 147–173.     

Diversity,distribution and conservation status assessment of Paraguayan palms (Arecaceae)

Indigenous palm species of Paraguay are presented with data on their diversity, distribution, threats and conservation status. The Paraguayan palm flora consists of 23 native species in 11 genera, representing two of the five subfamilies recognized in the group. The palm distribution in the country is strongly related to the different ecoregions present in Paraguay, with number of species by ecoregion being as follow: Cerrado (18), Upper Parana Atlantic forest (6), Wet Chaco (4), Pantanal (2), and Dry Chaco (1). Half of the species display an acaulescent habit reflecting an interesting ecological adaptation to natural fires in the Cerrado. The alarming rate of habitat modification that the country is undergoing since 1940s has put palms under a high risk of extinction in the wild. A GIS model was used to calculate the extent of occurrence and the area of occupancy of the species in order to assess their conservation status applying the IUCN Red List Categories and Criteria. This analysis shows that about 30% of the species are threatened; one species is Critically Endangered, three of them are Endangered, and three are Vulnerable. One species (Acrocomia hassleri) is considered Near Threatened, 13 are Least Concern whereas two species are insufficiently known and therefore unable to be assessed. Important areas for palm conservation in Paraguay were identified, revealing the importance of the Amambay department. Conservation measures for the threatened species identified are proposed.     

Functional and historical drivers of leaf shape evolution in palms (Arecaceae)

Aim

Leaves display a remarkable variety of shapes, each with potential ecological advantages in specific climates. While the relations between leaf shape and either climate or height have been relatively well studied in eudicots, the macroecological drivers of shape remain poorly known in monocots. Here, we investigated the associations between climate and plant height with the evolution of leaf shape in a clade with high species and morphological diversity.

Location

Global.

Time period

Cretaceous to contemporary.

Major taxa studied

Palms (Arecaceae).

Methods

We apply a Bayesian phylogenetic mixed model to test for associations between climate and leaf shape (all – entire-leaved, pinnate-dissected, palmate-dissected and costapalmate). We further reconstruct the ancestral leaf shape using multistate speciation and extinction models and compare the frequency of shapes with global temperatures through time.

Results

We find that plant height associates with dissected leaves and that annual precipitation associates with pinnate shapes. The ancestral leaf shape is unclear, but early diversification was dominated by pinnate-dissected palms, which has remained the most species-rich form of leaves throughout palm history.

Main Conclusions

Palms that are tall and live in humid regions are more likely to have pinnate leaves. Through geological time scales, temperature did not play an obvious role in determining leaf shapes. This study contributes to our understanding of how the diversity of leaf shapes is linked to biological and climatic factors.     

Geographical ecology of the palms (Arecaceae): determinants of diversity and distributions across spatial scales

Background

The palm family occurs in all tropical and sub-tropical regions of the world. Palms are of high ecological and economical importance, and display complex spatial patterns of species distributions and diversity.

Scope

This review summarizes empirical evidence for factors that determine palm species distributions, community composition and species richness such as the abiotic environment (climate, soil chemistry, hydrology and topography), the biotic environment (vegetation structure and species interactions) and dispersal. The importance of contemporary vs. historical impacts of these factors and the scale at which they function is discussed. Finally a hierarchical scale framework is developed to guide predictor selection for future studies.

Conclusions

Determinants of palm distributions, composition and richness vary with spatial scale. For species distributions, climate appears to be important at landscape and broader scales, soil, topography and vegetation at landscape and local scales, hydrology at local scales, and dispersal at all scales. For community composition, soil appears important at regional and finer scales, hydrology, topography and vegetation at landscape and local scales, and dispersal again at all scales. For species richness, climate and dispersal appear to be important at continental to global scales, soil at landscape and broader scales, and topography at landscape and finer scales. Some scale–predictor combinations have not been studied or deserve further attention, e.g. climate on regional to finer scales, and hydrology and topography on landscape and broader scales. The importance of biotic interactions – apart from general vegetation structure effects – for the geographic ecology of palms is generally underexplored. Future studies should target scale–predictor combinations and geographic domains not studied yet. To avoid biased inference, one should ideally include at least all predictors previously found important at the spatial scale of investigation.     

Diversity of use and local knowledge of palms (Arecaceae) in eastern Amazonia

Ethnobotanical information can clarify how dependent a community is on local plant resources and provide evidence about the consequences of resource exploitation. We performed a quantitative analysis on different aspects of knowledge and use of palms by the residents of the surrounding the Tucuruí Hydroelectric Power Station reservoir, eastern Amazonia, and their relationship with socioeconomic factors, adopting the methodology of consensus among informants. We based the study on accidental sampling of the 232 families and data were gathered through semi-structured forms. We evaluated correlations between the effective use and importance of species and the effect of socioeconomic factors on the knowledge and use of palms as cited by the informants. Informants know 27 species of palms and use 20 of these in eight different categories, the main ones being for food, utensils and construction. The species most widely used and cited as most important were Attalea speciosa, Oenocarpus bacaba, Euterpe oleracea, A. maripa and Socratea exorrhiza. For the informants, the value of a palm species is directly related to the different types of uses that it offers. The knowledge about palms is greater among farmers than fishermen and, when considering the medicinal aspect, it is greater among women than among men.     

Testing the water-energy theory on American palms (Arecaceae) using geographically weighted regression

Water and energy have emerged as the best contemporary environmental correlates of broad-scale species richness patterns. A corollary hypothesis of water-energy dynamics theory is that the influence of water decreases and the influence of energy increases with absolute latitude. We report the first use of geographically weighted regression for testing this hypothesis on a continuous species richness gradient that is entirely located within the tropics and subtropics. The dataset was divided into northern and southern hemispheric portions to test whether predictor shifts are more pronounced in the less oceanic northern hemisphere. American palms (Arecaceae, n = 547 spp.), whose species richness and distributions are known to respond strongly to water and energy, were used as a model group. The ability of water and energy to explain palm species richness was quantified locally at different spatial scales and regressed on latitude. Clear latitudinal trends in agreement with water-energy dynamics theory were found, but the results did not differ qualitatively between hemispheres. Strong inherent spatial autocorrelation in local modeling results and collinearity of water and energy variables were identified as important methodological challenges. We overcame these problems by using simultaneous autoregressive models and variation partitioning. Our results show that the ability of water and energy to explain species richness changes not only across large climatic gradients spanning tropical to temperate or arctic zones but also within megathermal climates, at least for strictly tropical taxa such as palms. This finding suggests that the predictor shifts are related to gradual latitudinal changes in ambient energy (related to solar flux input) rather than to abrupt transitions at specific latitudes, such as the occurrence of frost.     

Phylogeny and character evolution in the Indo-Pacific genus Ctenogobiops (Gobiiformes: Gobiidae)

Ctenogobiops is a genus of Indo-Pacific gobies that form obligate, mutualistic associations with shrimp in the genus Alpheus. This study provides a molecular phylogenetic analysis of eight Ctenogobiops species: C. aurocingulus, C. crocineus, C. feroculus, C. formosa, C. maculosus, C. mitodes, C. tangaroai, and C. tongaensis. We recover two clades within the genus, one consisting of C. feroculus and C. aurocingulus, the second including the remaining species arrayed as follows: (C. tongaensis (C. mitodes (C. formosa (C. maculosus (C. crocineus, C. tangaroai))))). Recovery of C. maculosus and C. crocineus as distinct taxa suggests that these species are not synonymous, although sampling in this study is limited. Species of Ctenogobiops are morphologically very similar to each other, with generally consistent meristic character states present throughout the genus. Recognition of species is based primarily on slight variations in color pattern, shape of the dorsal fin, and size of the gill opening. Comparison of our specimens of C. mitodes with accounts of C. pomastictus confirms that color pattern variations and lateral scale counts are more reliable indicators of species identity than relative dorsal fin spine length, particularly for smaller specimens. We evaluate the distribution of morphological characters in the context of the new phylogenetic hypothesis, and provide a summary of distinguishing characters for Ctenogobiops species. In this case, as in other instances of diverse reef-dwelling fish taxa, molecular data are ideal for inferring phylogenetic relationships, whereas morphological data remain the most expedient way to identify species.     

Inflorescence structure and generic delimitation of Triplaris and Ruprechtia (Polygonaceae)

A revision of the generic limits between Triplaris and Ruprechtia (Polygonaceae), which were confused in earlier literature, led to the conclusion that the two genera should be maintained. Triplaris is characterized by 1–flowered pistillate partial inflorescences, absence of a basal pedicel–like extension of the fruiting perianth–tube, which is always as long as or longer than the achene, bracteoles completely fissured on the abaxial side, and sessile or subsessile male flowers with perianth segments always connate for more than half of their length.
Ruprechtia has 2–3–flowered monochasial pistillate part–inflorescences (except the 1–flowered R. triflora) , a basal pedicel–like extension of the fruiting perianth–tube, which is at most 3/4 as long as the achene, more or less tubular bracteoles only exceptionally fissured down on the abaxial side, and pedicellate male flowers with perianth segments never connate for more than one third of their lenght. Preliminary paly–nological studies have shown that the pollen of Triplaris are microreticulate or punc–tate–microreticulate while Ruprechtia pollen have perforate–rugulose surfaces.     

On the role of microenvironmental heterogeneity in the ecology and diversification of neotropical rain-forest palms (Arecaceae)

Microenvironmental heterogeneity is important in the ecology and diversification of the rich palm flora that inhabits neotropical rain forests. At small-0.1-10² m-scales, neotropical rain forests exhibit high heterogeneity in numerous environmental factors: canopy conditions, conspecifics, other plants, litter, soil factors, topography, and animal mutualists and pests. These aspects of microenvironmental heterogeneity affect the performance and the small-scale distribution of palms in numerous ways, often affecting different species differently. Notably, even subtle environmental variation can be of crucial ecological importance. Microenvironmental heterogeneity promotes the local coexistence of palm species by niche differences among the species and probably also by mass effects and negative density dependence. Sympatric species of the same growth form often differ in terms of light requirements, edaphic-topographic preferences, and possibly also in seed-dispersal patterns, whereas mass effects are likely to account for the local occurrence of a share of the rare species. Density dependence seems to be frequent among large-seeded palms, but its importance needs to be assessed. Microenvironmental heterogeneity is proposed to be an important diversity-generating factor in the neotropical palm flora through the process of parapatric speciation. This hypothesis is based on the observation that, in species-rich palm genera and species complexes, sympatric species or morphs often differ in edaphic-topographic preferences or in characteristics that confer differing light requirements and in traits that favor reproductive isolation.     

Floral anatomy in Dypsis (Arecaceae–Areceae): a case of complex synorganization and stamen reduction

Male (staminate) flowers of Dypsis possess either six or three stamens and/or staminodes, in contrast to most other palms, in which the basic stamen number is six (although polyandry is also common in palms). Significant variation among the tristaminate forms, both in stamen morphology and stamen position with respect to the perianth parts, indicates that stamen reduction from six to three has occurred more than once, and possibly several times within Dypsis. A few species include teratological forms with zygomorphic flowers; for example, Dypsis lantzeana normally possesses three antesepalous stamens, but in some specimens only the median outer (abaxial) stamen is expressed, perhaps indicating incipient zygomorphy correlated with complex synorganization. Inclusion of earlier historic genera such as Neophloga and Chrysalidocarpus within a broadly circumscribed Dypsis appears to be justified, although the informal taxonomic groupings within Dypsis require review, in particular the taxonomic significance of the different types of anther morphology. The discovery here that adnation of staminodes to the pistillode (complex synorganization) occurs in species other than D. mirabilis opens further questions about the taxonomic utility of this character in Dypsis, in which stamen/staminode development and adnation are apparently unusually labile. Such androecial–gynoecial adnation is otherwise rare in palms, as also in other monocots, in which probably the best‐known example occurs in orchids. Septal nectaries are present in some, but not all, staminate flowers in species of Dypsis. Dypsis bejofo is exceptional in that in staminate flowers the pistillode is distally bulbous and bears three prominent modified supralocular septal nectaries. Female (pistillate) flowers in Dypsis are syncarpous, normally pseudomonomerous (as in many other Arecoideae), and possess septal nectaries that effectively delimit the carpel margins and indicate insect pollination. There is a central solid transmitting tissue that extends from the placenta to three stylar canals. The stylar canals of the two sterile carpels are apparently functional, in addition to that of the fertile carpel. © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 143 , 115?133.     

Phylogenetics of Eulophiinae (Orchidaceae: Epidendroideae): evolutionary patterns and implications for generic delimitation

Eulophiinae comprise c. 270 species divided into nine genera, with the species‐rich terrestrial genus Eulophia representing 60% of this diversity. Remarkable ecological and morphological variation, and an absence of clear diagnostic characters have led to uncertain generic delimitation in the subtribe. Using a combination of new and previously published DNA sequences, we created a dataset representing 122 taxa and all genera of Eulophiinae and inferred a complete generic‐level phylogeny for the subtribe for the first time. Our sampling focused on analysing Afro‐Madagascan taxa and therefore included representatives of the four mostly epiphytic Madagascan endemic genera, the near Madagascan endemic Oeceoclades and additional sampling of the predominantly African genera Eulophia and Orthochilus. In total, 104 new accessions were collected for this study in Zambia and Madagascar (88 of which represented 36 Eulophia spp. and 12 Oeceoclades spp.). Independent plastid and nuclear phylogenetic trees were inferred using Bayesian and maximum‐likelihood algorithms, which recovered strong support for a monophyletic Eulophiinae, the first‐branching position of the mostly epiphytic Madagascan endemic genera, and increased support for recognition of the terrestrial genera Oeceoclades and Orthochilus. Eulophia, the largest genus in the group, was recovered as polyphyletic, but with implications for its classification and that of Geodorum, that was nested in the main Eulophia clade. Although relationships among several genera were resolved with some confidence, the positions of the South African endemic genus Acrolophia and the epiphytic Madagascan endemic Paralophia require further work. Taxon sampling of Asian Eulophia is a priority for future work on the systematics of this group. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 179 , 43–56.     

Geographical variation and environmental correlates of functional trait distributions in palms (Arecaceae) across the New World

Functional traits play a key role in driving biodiversity effects on ecosystem functioning. Here, we examine the geographical distributions of three key functional traits in New World palms (Arecaceae), an ecologically important plant group, and their relationships with current climate, soil and glacial–interglacial climate change. We combined range maps for the New World (N = 541 palm species) with data on traits (leaf size, stem height and fruit size), representing the leaf–height–seed plant strategy scheme of Westoby, to estimate median trait values for palm species assemblages in 110 × 110‐km grid cells. Spatial and non‐spatial multi‐predictor regressions were used with the Akaike Information Criterion to identify minimum adequate models. Present‐day seasonality in temperature and precipitation played a major role in explaining geographical variation of all traits. Mean annual temperature and annual precipitation were additionally important for median leaf size. Glacial–interglacial temperature change was the most important predictor for median fruit size. Large‐scale soil gradients played only a minor role overall. These results suggest that current climate (larger median trait values with increasing seasonality) and glacial–interglacial temperature change (larger median fruit size with increasing Quaternary temperature anomaly) are important drivers for functional trait distributions of New World palms. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 179 , 602–617.     

Micromorphological characters and generic delimitation of some New World Senecioneae (Asteraceae)

Some recent systematic investigations have placed great reliance on micromorphological floral features in generic delimitation in the Senecioneae. In order to test the taxonomic value of those features, 31 species of New World “Cacalioid” and “Senecionoid” Senecioneae were examined for five micromorphological characters: 1) configuration and distribution of the stigmatic area on the style branches, 2) stylopodial structure, 3) cellular structure of the carpopodium, 4) configuration of the anther collar, and 5) form of the endothecial cells in the anther. LM or SEM photographs were made for each character for each species. Variation was found to exist with age and geographical range for each of these characters and sometimes between florets on one capitulum. Differences in these five microcharacters were found between the “Cacalioid” and “Senecionoid” genera, but they were no more consistent than the differences in traditional characters employed in generic delimitation.