Editor’s Choice @Biotropica 48(1): White Sand Forests & the Evolutionary History of Pagamea
I am pleased to announce the Editor’s Choice Article for Biotropica 48(1): Vicentini, A. (2016), The evolutionary history of Pagamea (Rubiaceae), a white-sand specialist lineage in tropical South America. Biotropica, 48: 58–69.
The first issue of Biotropica Vol. 48 is a special issueon Neotropical White Sand Forests — unusual environments found throughout tropical South America that often occur as habitat islands surrounded by rain forests. Their namesake sandy soils can greatly reduce nutrient and water availability, leading to stunted forests with unique physiognomies and endemic species assemblages. Although white-sand forests have fascinated biologists for >100 years, it is only recently that major advances have been made in describing their unique biology. Our thanks to Dr. Paul Fine, who edited the Special Issue, to all the authors who contributed.
This issue’s Editor’s Choice article by Alberto Vicentini highlights both what makes these ecosystems fascinating and challenging to study, and advances our understanding of the evolution of their unique flora through a combination of contemporary techniques and arduous but spectacular expeditionary botany. His results on the genus Pagamea and how he came to them are described in the essay below. Congratulations Beto!
In 1998 I participated in a multidisciplinary field expedition to an island of white-sand vegetation in the Jaú National Park, Amazonas, Brazil, the Campina do Patauá (Borges et al. 2004). There, I encountered for the first time a white-sand vegetation that becomes completely flooded during the rainy season. In the previous year, during an extreme “El Ninõ drought”, this patch had been almost completely burned, and during the expedition the shrubby vegetation was resprouting. This kind of white-sand vegetation, whose physiognomy was clearly shaped by a combination of soil, fire and flooding, was quite different from the white-sand forests I knew nearby Manaus, described by Anderson (1981). These areas share many plant species with the Patauá area, but represent a less extreme portion of the flooding gradients that characterize these systems (e.g. Damasco et al. 2013). Both forests and scrublands at the Patauá area had many floristic elements from the Upper Rio Negro and the Guiana Shield Highlands, like Euphronia and Cyrilla, which were new to me and by which I learned about the floristic connections between lowland white-sands and the “Tepui” vegetation (Kubitzki 1990). We collected many species in the Patuá area that pointed to these biogeographical connections (Vicentini 2004), including a new grass species that dominated the area and was likely the major fuel for the fire that had burned the area in 1997. This grass species, still unpublished, belonged to a monospecific genus (Arundoclaytonia) only known beforehand from the Serra do Cachimbo in southern Amazonia, more than 2000 km away. I had also visited two mountains a few years back, the Neblina and Roraima tepuis, and by learning and experiencing the physionomic and floristic similarities among lowland and highland white-sand ecossystems, I decided to conduct my PhD on this topic. I was interested in biogeography and wanted to explore the Tepui landscape, and naively thought that these would be easy tasks – it was just a matter of using molecular phylogenetics for a historical reconstruction.
In 1999 I was accepted as a PhD student at the University of Missouri Saint Louis (UMSL) and the Missouri Botanical Garden, and with this idea in mind I searched for a plant lineage that would allow me to explore the tepui landscape and to learn the theoretical and empirical aspects of plant evolutionary biology. The genus Pagamea was not my first choice as a focal group for this study, but it was a good one. Pagamea was always mentioned as a genus from white-sand systems in the Amazon (Anderson 1981), with species in both the lowlands and highlands (Steyermark 1986). Simon Malcomber, who I had the pleasure to interact with at UMSL, was finishing his study on the genus Gaertnera, the sister-lineage to Pagamea that occurs in the Paleotropics and has undergone rapid radiation (Malcomber 2002), which made Pagamea even more interesting. Although we have not explored the comparison between these sister clades, Gaertnera may have twice the number of species than Pagamea and a younger (relatively) diversification history, reinforcing the idea that Gaertnera has undergone rapid radiation, with more species, greater ecological variation and broader geographical distribution (Africa to South East Asia).
During the development of the study it became clear to me that it would not be an easy task to study the genus Pagamea: sequencing single molecular markers showed to be difficult, both to amplify and to find variation (NextGen was not available at that time); sampling in the Guyana Highlands was impossible because of the complexity for obtaining permits, both in Venezuela and also in my home country (my samples were retained for 4 years in Brazil); and early in the process I realized that there were too many undescribed species of Pagamea and that it would be impossible to collect on the Tepui landscape, my motivation in the first place. In a single trip to the Upper Rio Negro I encountered three previously uncollected species. How to reconstruct the biogeographical history of a lineage if species limits are unclear and current diversity undescribed or unsampled? My first molecular results were promising, I found more variation than Malcomber did with the same markers, but I also found incongruence among nuclear and chloroplast data, which together with a lack of great morphological differences among species made it extremely complicated to untangle. Challenges are good and many interesting questions arose from this study.
This Biotropica paper summarizes the major results I found during my PhD study, with a focus on biogeography and diversification, but it include little of the complexity I found on species limits and much more work is still needed on this matter. The endemic species from the Guyana Highlands remain largely unsampled, many new species remain underscribed, not because we lack samples, but because species limits are not easy to establish, mostly due to the lack of morphological gaps among closely related clades. For example, the Guianensis Clade, with three species, contain great cryptic variation that are now being resolved by a phylogeographical study (Eduardo Prata, INPA, in prep) and may turn out to contain six reproductively isolated species, and the Coriaceae clade also contain cryptic species (Esteves & Vicentini 2013). Biogeographical and phylogenetic reconstructions rely on having the taxonomy resolved, and we still do not have a good taxonomic definition for many species in Pagamea.
I consider the results of this study to have raised more questions than provided answers. But this is how science works. With current technology, particularly the possibility of having good sequence data from next-generation sequencing, many of the questions raised during this study can now be addressed. Pagamea is an excelent model to study diversification within white-sand systems in the Amazon, but the more interesting questions regarding speciation can only be answered by population level studies. For example, the incongruence between chloroplast and nuclear data may be caused by hybridization, but we need such sampling to address this question. The Thyrsiflora clade may contain a ring-species, Pagamea thyrsiflora, which show great morphological variation in sympatry in western Amazon (Andes) that point to independent colonization events to this area by this clade, one from the Western Guyana Shield (North) and another from the Brazilian Shield (South) in Acre. I am also interested in assessing the rate of dispersal and gene flow among islands of white-sand vegetation in the lowlands at a fine scale. To which extent limited dispersal is really the major cause of diversification in Pagamea as the results seem to suggest? Few-flowered species of Pagamea, which correlate with larger fruits, have smaller geographical ranges than species with smaller fruits and higher fecundity (i.e., number of fruits per infructesence; Vicentini 2007). Are species with smaller fruits more vagile? Who disperses them? We know too little about the ecology of these species at finer scales, and it is clear to me that understanding plant speciation in this system would require more detailed studies at the population level. We are now working on this direction.
Anderson, A. B. 1981. White-sand vegetation of Brazilian Amazonia. Biotropica 13: 199–210.
Borges, S.H., S. Iwanaga, C.C. Durigan, M.R. Pinheiro. 2004. Janelas para a biodiversidade no Parque Nacional do Jaú: uma estratégia para o estudo da biodiversidade na Amazônia. Fundação Vitória Amazônica (FVA), WWF, IBAMA, Manaus, pp. 117-143.
Damasco, G., A. Vicentini, C. V. Castilho, T. P. Pimentel, And H. E. M. Nascimento. 2012. Disentangling the role of edaphic variability, flooding regime and topography of Amazonian white-sand vegetation. J Veg Sci 24: 384-394.
Esteves, S. D. M., And A. Vicentini. 2013. Cryptic species in Pagamea coriacea sensu lato (Rubiaceae): evidence from morphology, ecology and reproductive behavior in a sympatric context. Acta Amazonica 43: 415-428.
Kubitzki, K. 1990. The psammophilous flora of northern South America. Memoirs of the New York Botanical Garden 64: 248-253.
Malcomber, S. T. 2002. Phylogeny of Gaertnera Lam. (Rubiaceae) based on multiple DNA markers: evidence of a rapid radiation in a widespread, morphologically diverse genus. Evolution 56: 42-57.
Steyermark, J. A. 1986. High Altitude Tropical Biogeography. In F. Vuilleumier and M. Monasterio (Eds.), pp. 317-373 Speciation and endemism in the flora of the Venezuelan tepuis. Oxford University Press, New York, USA.
Vicentini, A. 2007. Pagamea Aubl. (Rubiaceae), from species to processes, building the bridge. Doctoral Thesis, University of Missouri Saint Louis. 330 pp. (https://apps.umsl.edu/webapps/weboffice/ETD/search.cfm). Accessed on 02-06-2015.