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  • The long-tongued hawkmoth pollinator niche for native and invasive plants in Africa
    savanna plant species in Africa belong to the Agrius pollination guild In South Africa at least 23 native species have very long floral tubes and pollination by A convolvuli or rarely by the closely related hawkmoth Coelonia fulvinotata has been confirmed for 11 of these species The guild is strikingly absent from the species rich Cape floral region and now includes at least four non native invasive species with long tubed flowers that are pre adapted for pollination by A convolvuli Conclusions This study highlights the value of a niche perspective on pollination which provides a framework for making predictions about the ecological importance of keystone pollinators and for understanding patterns of convergent evolution and the role of floral traits in plant colonization Key words Agrius convolvuli biological invasions ecological opportunity flower colour functional traits long tongued hawkmoth moth pollination mutualism nectar plant pollinator interactions pollination ecology proboscis length regeneration niche specialization The Author 2015 Published by Oxford University Press on behalf of the Annals of Botany Company All rights reserved For Permissions please email journals permissions oup com Related articles ContentSnapshots Content Snapshots Ann Bot 2016 117 1 i iii doi 10 1093 aob mcv183 Extract Full Text HTML Full Text PDF Previous Next Article Table of Contents This Article Ann Bot 2016 117 1 25 36 doi 10 1093 aob mcv137 First published online September 7 2015 Abstract Free Free Figures Free Full Text HTML Free Full Text PDF Free Supplementary Data All Versions of this Article mcv137v1 117 1 25 most recent Classifications Original Article Services Article metrics Alert me when cited Alert me if corrected Alert me if commented Find similar articles Similar articles in Web of Science Similar articles in PubMed Add to my archive Download citation Request Permissions Responses Submit a response No responses published Citing Articles Load citing article information Citing articles via CrossRef Citing articles via Scopus Citing articles via Web of Science Google Scholar Articles by Johnson S D Articles by Raguso R A PubMed PubMed citation Articles by Johnson S D Articles by Raguso R A Agricola Articles by Johnson S D Articles by Raguso R A Related Content Related articles in this journal Load related web page information Share Email this article CiteULike Delicious Facebook Google Mendeley Twitter What s this Search this journal Advanced Current Issue February 2016 117 2 Alert me to new issues The Journal About this journal Annals of Botany Collections AoB article attracts media coverage We are mobile find out more Journals Career Network Published on behalf of The Annals of Botany Company Impact factor 3 654 5 Yr impact factor 4 338 Eigenfactor 0 02603 Rank 10 200 SCImago Score 1 461 Rank 124 1873 Chief Editor Professor J S Pat Heslop Harrison View full editorial board International Review Board For Authors Submitting a manuscript online Self archiving policy Instructions for authors Low Rate Open Access Fees Open access options for authors visit Oxford Open Visit HighWire Press 3hWaciBYRk30rSOQ7UOpP6viAxsZnEle true Looking for your

    Original URL path: https://aob.oxfordjournals.org/content/117/1/25.abstract (2016-02-18)
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  • The long-tongued hawkmoth pollinator niche for native and invasive plants in Africa
    Crinum delagoanse they reflect light of wavelengths ranging from 400 to 700 nm and absorb UV wavelengths 300 399 nm Fig 3 Older flowers of Cladostemon kirkii Rangaeris muscicola Gardenia thunbergii Oxyanthus speciosa and Sesamothamnus lugardii undergo a colour change in human perception from white to yellow as illustrated by the contrasting spectra for C kirkii Fig 3 View larger version In this window In a new window Download as PowerPoint Slide F ig 3 Spectral reflectance of long tubed flowers in the flora of South Africa Pollinator observations We observed hawkmoths to visit the flowers of 13 plant species with long tubed flowers Figs 4 and 5 Supplementary Data Table S3 Almost all of the visits to these species were by the convolvulus hawkmoth A convolvuli This hawkmoth species was the only observed visitor for ten of the 13 plant species Supplementary Data Table S3 The only other hawkmoth species recorded were the fulvous hawkmoth Coelonia fulvinotata observed on flowers of two of the species and a single individual of the accented hawkmoth Nephele accentifera accentifera observed on flowers of one species Hawkmoths generally carried large pollen loads of the flowers they visited and these were visible even in photographs Figs 4 and 5 View larger version In this window In a new window Download as PowerPoint Slide F ig 4 Long tongued hawkmoth visitors to native South African plant species with long tubed flowers A The convolvulus hawkmoth Agrius convolvuli feeding on Crinum macowanii B A convolvuli on Crinum bulbispermum C D A convolvuli on Gardenia thunbergia E A convolvuli on Harveya speciosa F The fulvous hawkmoth Coelonia fulvinotata on Cladostemon kirkii View larger version In this window In a new window Download as PowerPoint Slide F ig 5 Long tongued hawkmoth visitors to long tubed flowers of exotic plant species that are invasive in South Africa A The convolvulus hawkmoth Agrius convolvuli feeding on Hedychium gardnerianum B C A convolvuli on Ipomoea alba D A convolvuli on Lilium formosanum Video footage of G thunbergii showed that convolvulus hawkmoths feed from flowers through most of the night We obtained video footage of ten foraging bouts between 19 00 and 21 00 h 16 bouts between 21 00 and 23 00 h zero bouts between 23 00 and 01 00 h two bouts between 01 00 and 03 00 h and two bouts between 03 00 and 05 00 h Floral tube length as a mechanical filter Combining the data from this study with those of other studies of hawkmoth pollination in South Africa showed that the number of hawkmoth visitor species declines with increasing floral tube length Fig 6 A This closely matches a similar trend in Kenya Fig 6 B In both South Africa and Kenya flowers visited by hawkmoths show a strong linear relationship between floral tube length and the volume of nectar available just before dusk Fig 6 C D View larger version In this window In a new window Download as PowerPoint Slide F ig 6 Relationships between floral tube length and the number of hawkmoth visitor species for plants in South Africa A and Kenya B and between floral tube length and the volume of nectar available at the start of moth foraging for plants in South Africa C and Kenya D Data for Kenya from Martins and Johnson 2013 Biogeography Plant species with long floral tubes 8 cm are found only in the eastern half of South Africa and are conspicuously absent from the Cape floral region Fig 7 The density of species with long tubed flowers is greatest along the sub tropical coastal belt and far eastern regions of South Africa Fig 7 The distribution of invasive species with long tubed flowers closely matches that of the native species with long tubed flowers Supplementary Data Fig S1 Although hawkmoth collection records are not available for all degree squares in South Africa available data indicate that A convolvuli makes up a high percentage of hawkmoth museum accessions frequently in excess of 50 from degree grid squares in the east but has only very rarely been recorded in the Greater Cape Floral region in the west Supplementary Data Fig S2 View larger version In this window In a new window Download as PowerPoint Slide F ig 7 The geographical distribution of native plant species with long tubed flowers in South Africa The number of species is indicated in each quarter degree grid square and is also indicated by the depth of the pink shading Previous Section Next Section DISCUSSION This study conducted in South Africa together with the findings of Martins and Johnson 2013 in East Africa demonstrates the existence of a guild of African plants that appears to rely almost exclusively on the long tongued convolvulus hawkmoth Agrius convolvuli for pollination This guild of plants is characterized by the shared possession of a very long approx 10 cm floral tube or spur or androphore in the case of Cladostemon kirkii Fig 1 Previous studies cf Alexandersson and Johnson 2002 have shown that the nectar column in these guild members typically occupies about 10 of the tube length meaning that a tongue of at least 9 cm would be required for moths to obtain any nectar The long floral tubes thus appear to act as a mechanical filter that excludes shorter tongued moths from flowers Fig 6 A B as was shown to be the case for long tubed flowers visited by hawkmoths in Costa Rica Agosta and Janzen 2005 Apart from A convolvuli the only other local hawkmoth species that appeared to be able to access nectar in deep tubular flowers at our study sites was the fulvous hawkmoth Coelonia fulvinotata but this species was seldom recorded either among light trapped specimens Fig 2 A or in observations made at flowers Supplementary Data Table S2 and appears to be restricted to wooded habitats while the convolvulus hawkmoth is common in open grassland and savanna habitat In the geographical range of the study plant species there are no other insect groups that compete with the convolvulus and fulvous hawkmoths in terms of proboscis length There is one long proboscid fly species in Africa that has a proboscis with a length of up to 85 mm in some populations but this species is localized to the south western Cape and pollinates a guild of plants with day opening unscented flowers with floral tubes that are typically about 40 80 mm in length Johnson and Steiner 1997 Pauw et al 2009 The maximum length of the proboscis among long proboscid fly species in the eastern part of South Africa is about 50 mm Anderson and Johnson 2009 The convolvulus and fulvous hawkmoths have proboscides that are more than twice as long as those of all other hawkmoths at the study sites Fig 2 A and thus seem to represent a distinct pollinator niche to which a wide range of unrelated plants have become adapted The importance of floral tube length as an adaptation for pollination by A convolvuli is evident not only from convergent evolution among guild members but also from selection studies that show that plants of the iris Gladious longicollis that have floral tubes that match or exceed the proboscis length of A convolvuli have higher fitness than those that have shorter floral tubes Alexandersson and Johnson 2002 Further supporting our contention that there are at least two different hawkmoth pollination systems in South Africa recent studies have identified two largely geographically separated ecotypes of G longicollis one with short floral tubes adapted to short tongued hawkmoths e g Hippotion celerio and another with very long floral tubes adapted to A convolvuli Anderson et al 2010 The results of this study are consistent with our contention that mouthpart bill proboscis tongue length is a key aspect of the pollinator niche For groups of animals that have similar sensory systems and therefore select for similar floral advertising traits mouthpart length is the key niche axis that determines plant floral adaptations and specialization Animals belonging to the same higher taxon e g hummingbirds but that vary in the length of their mouthparts are in most cases likely to act as different functional groups This has become evident from studies of specialized pollination systems involving bumble bees Ranta and Lundberg 1980 Harder 1985 euglossine bees Borrell 2005 long proboscid flies Johnson and Steiner 1997 hummingbirds Maglianesi et al 2014 bats Muchhala and Thomson 2009 and hawkmoths Anderson et al 2010 Martins and Johnson 2013 This simple niche axis of mouthpart length obviously applies mainly to relatively specialized pollination systems Pollinator niche dimensions for plants with generalized pollination systems are far more complex and also much less stable in time and mainly involve the relative abundance of different pollinator functional groups in local assemblages Gomez et al 2015 Besides having very long floral tubes plants pollinated by A convolvuli have strong similarities in spectral reflectance Fig 3 However similar spectra are known from plants pollinated by other insects Kevan et al 1996 and so we cannot be certain that our study species possess these spectral reflectance traits as a result of specific adaptations to long tongued moths It does however seem likely that white floral coloration is important for attraction of A convolvuli A simple experiment decoupling the olfactory and visual display of invasive Datura inoxia Solanaceae flowers in the former Yugoslavia revealed a strong attraction and probing response of wild A convolvuli moths to white objects Kugler 1971 a preference that is shared by the closely related American species Agrius cingulatus Ippolito et al 2004 as well as other long tongued hawkmoths in the sub family Sphinginae Raguso and Willis 2003 Volumes of nectar in the long tubed flowers of guild members are much larger than those in shorter tubed flowers pollinated by other hawkmoths Fig 6 C D Observations by Martins and Johnson 2013 in East Africa showed that A convolvuli is an extremely polyphagous insect that feeds from both short and long tubed flowers The higher volume of nectar in long tubed flowers can thus be interpreted as selection for traits that entice A convolvuli to visit long tubed flowers in communities where these hawkmoths also have access to short tubed flowers This enticement is particularly critical given that these long tubed flowers filter out shorter tongued hawkmoths and thus rely solely on long tongued hawkmoths for pollination Although we did not attempt to control for phylogeny in our analyses of the South African flora analysis of a similar data set for Kenyan plants showed that the trend for flowers with longer tubes to have more nectar was still evident after phylogenetic correction Martins and Johnson 2013 Agrius convolvuli appears to be an exceptionally common hawkmoth throughout sub Saharan Africa Of the 1199 individual hawkmoths that were captured in light traps in South Africa 535 44 6 were individuals of A convolvulus Even museum accessions for particular degree grid squares are often dominated by this species Supplementary Data Fig S2 A similar high proportion of individuals of A convolvuli was found among light trapped catches of hawkmoths in Tanzania Robertson 1977 and in direct observations of flowers by Martins and Johnson 2013 Agrius convolvuli has also been recorded as an important pollinator of orchids and baobabs that occur in open woodland habitats in Madagascar Nilsson and Rabakonandrianina 1988 Baum 1995 Ryckewaert et al 2011 In contrast A convolvuli made up a very small percentage of the hawkmoths light trapped in a forest in Madagascar by Nilsson et al 1985 This may reflect the fact that A convolvuli prefers open habitats Pinhey 1962 In studies performed by D F Owen at forested sites in Sierra Leone A convolvuli made up 3 3 of the hawkmoth individuals trapped at mercury vapour lamps and showed strong seasonal and potentially migratory patterns of abundance Owen 1969 1972 Hawkmoth pollination has not been studied in the closed canopy forests of central Africa and it is possible that other hawkmoth species play a role in the pollination of long tubed flowers in this habitat The nominal subspecies of Xanthopan morgani the famous long tongued hawkmoth that fitted Darwin s prediction of a pollinator for the orchid Angraecum sesquipedale in Madagascar occurs on the African mainland Pinhey 1962 Owen 1969 and together with the fulvous hawkmoth C fulvinotata is likely to play a role in the pollination of long tubed forest plant species in tropical Africa The total number of species reliant on A convolvuli for pollination is hard to estimate on account of the fragmentary nature of the botanical literature for many African countries We identified 23 native species in South Africa with floral tubes longer than 8 cm while Martins and Johnson 2013 identified 51 species with floral tubes longer than 8 cm that are native to Kenya Supplementary Data Table S4 Four taxa Crinum macowanii Cladostemon kirkii Bonatea steudneri and Gardenia volkensii are common to both countries so there are at least 70 distinct native taxa that are either known or likely to be pollinated by A convolvuli in these two countries alone These taxa represent 15 plant families and 30 genera suggesting that the guild had multiple evolutionary origins Given that South Africa and Kenya make up just a small fraction of the landmass and flora of Africa we consider it likely that several hundred African plant species are pollinated by A convolvuli In South Africa the Agrius plant guild is distributed in the eastern sub tropical regions Fig 7 The guild is absent from the Cape floral region and the arid south west This appears to be a general pattern for hawkmoth pollination systems in the region as previous studies have shown that hawkmoth pollinated Amaryllidaceae are concentrated in the east of South Africa Manning and Snijman 2002 It is notable that the Cape fynbos vegetation lacks families such as Rubiaceae Balsaminaceae Vitaceae Convolvulaceae and Loganiaceae that comprise the larval food plants for many hawkmoths Attie et al 2010 The scarcity of A convolvuli in the semi arid region is somewhat harder to explain as this hawkmoth species is known to have considerable ability to disperse beyond its natal habitat Ballesteros Mejia et al 2011 and has been observed to pollinate white long tubed flowers in the semi arid Mediterranean habitats of Israel Eisikowitch and Galil 1971 The niche concept for pollinators applied using the idea of unique morphospace Fig 2 may be a powerful way of predicting whether or not plants are likely to co opt functionally equivalent substitute pollinators when introduced to new regions Data from this study and that by Rodger et al 2010 show that at least four introduced plants with floral tubes approx 10 cm in length are pollinated by A convolvuli in Africa Two of these species Ipomoea alba and Datura stramonium originate from the Americas which are outside of the range of A convolvuli while two others Hedychium gardnerianum and Lilium formosanum originate from Asia within the range of A convolvuli Some of these invasive species are facultative selfers Rodger et al 2013 so we cannot exclude the possibility that invasion by these species would have occurred even without hawkmoth pollination Nevertheless outcrossing by hawkmoths is likely to lead to genetic recombinations and accelerate the pace of invasion The distribution of the four long tubed invasive species is tightly correlated with that of the native species in the guild Supplementary Data Fig S1 although this may be due to adaptations of the invasive species to sub tropical climates rather than to interactions with long tongued hawkmoths and guild members The impacts of invasive long tubed plant species on the native guild members pollinated by A convolvuli are unknown and worth examining in future studies The presence of a guild of long tubed night blooming flowers provides a potential niche for invasion by other hawkmoths with a very long proboscis The long tubed flowers of guild members have relatively large amounts of nectar that can only be accessed by long tongued animals The long tongued American hawkmoth species A cingulata has recently become naturalized in West Africa and bioclimatic models suggest that it could spread across much of Africa Ballesteros Mejia et al 2011 Given the availability of larval food plants and a guild of nectar rich long tubed flowers for this hawkmoth such an invasion scenario seems highly likely In conclusion this study shows that the hawkmoth A convolvuli and to a much lesser extent the related species C fulvinotata comprise a distinct long tongued pollinator niche in Africa that is occupied by a large guild of plant species The key functional trait that enables both native and introduced plants to exploit this ecological opportunity is the possession of a very long approx 10 cm floral tube Shorter tubed plants are also visited by long tongued hawkmoths but this seldom results in efficient pollination Alexandersson and Johnson 2002 From the patterns of convergent evolution among guild members it seems likely that white floral coloration and copious amounts of nectar are also important for establishing mutualisms with long tongued hawkmoths The functional roles of these floral traits as well as of floral scent remain to be investigated This study highlights the value of a niche perspective for understanding the geographical context and functional significance of floral traits This perspective may also have value for predicting patterns of species sorting when plants become naturalized in new regions Previous Section Next Section SUPPLEMENTARY DATA Supplementary data are available online at www aob oxfordjournals org and consist of the following Table S1 localities of study sites plant species studied and methods used Table S2 corolla dimensions and nectar properties of plant species in South Africa with long tubed flowers Table S3 hawkmoths observed on long tubed flowers of plant species in South Africa indicating their proboscis length and site of pollen placement Table S4 plant species in Kenya with floral tubes greater than 80 mm in length adapted from Martins and Johnson 2013

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  • The long-tongued hawkmoth pollinator niche for native and invasive plants in Africa

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  • The long-tongued hawkmoth pollinator niche for native and invasive plants in Africa
    Crinum bulbispermum C D A convolvuli on Gardenia thunbergia E A convolvuli on Harveya speciosa F The fulvous hawkmoth Coelonia fulvinotata on Cladostemon kirkii View larger version In this window In a new window Download as PowerPoint Slide F ig 5 Long tongued hawkmoth visitors to long tubed flowers of exotic plant species that are invasive in South Africa A The convolvulus hawkmoth Agrius convolvuli feeding on Hedychium gardnerianum B C A convolvuli on Ipomoea alba D A convolvuli on Lilium formosanum View larger version In this window In a new window Download as PowerPoint Slide F ig 6 Relationships between floral tube length and the number of hawkmoth visitor species for plants in South Africa A and Kenya B and between floral tube length and the volume of nectar available at the start of moth foraging for plants in South Africa C and Kenya D Data for Kenya from Martins and Johnson 2013 View larger version In this window In a new window Download as PowerPoint Slide F ig 7 The geographical distribution of native plant species with long tubed flowers in South Africa The number of species is indicated in each quarter degree grid square and is also indicated by the depth of the pink shading The Author 2015 Published by Oxford University Press on behalf of the Annals of Botany Company All rights reserved For Permissions please email journals permissions oup com Related articles ContentSnapshots Content Snapshots Ann Bot 2016 117 1 i iii doi 10 1093 aob mcv183 Extract Full Text HTML Full Text PDF Previous Next Article Table of Contents This Article Ann Bot 2016 117 1 25 36 doi 10 1093 aob mcv137 First published online September 7 2015 Abstract Free Free Figures Free Full Text HTML Free Full Text PDF Free Supplementary Data All Versions of this Article mcv137v1 117 1 25 most recent Classifications Original Article Services Article metrics Alert me when cited Alert me if corrected Alert me if commented Find similar articles Similar articles in Web of Science Similar articles in PubMed Add to my archive Download citation Request Permissions Responses Submit a response No responses published Citing Articles Load citing article information Citing articles via CrossRef Citing articles via Scopus Citing articles via Web of Science Google Scholar Articles by Johnson S D Articles by Raguso R A PubMed PubMed citation Articles by Johnson S D Articles by Raguso R A Agricola Articles by Johnson S D Articles by Raguso R A Related Content Related articles in this journal Load related web page information Share Email this article CiteULike Delicious Facebook Google Mendeley Twitter What s this Search this journal Advanced Current Issue February 2016 117 2 Alert me to new issues The Journal About this journal Annals of Botany Collections AoB article attracts media coverage We are mobile find out more Journals Career Network Published on behalf of The Annals of Botany Company Impact factor 3 654 5 Yr impact factor 4 338 Eigenfactor 0 02603 Rank 10

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  • The long-tongued hawkmoth pollinator niche for native and invasive plants in Africa — Supplementary Data
    25 36 Abstract Free Free Figures Full Text HTML Free Full Text PDF Supplementary Data Search this journal Advanced Current Issue February 2016 117 2 Alert me to new issues The Journal About this journal Annals of Botany Collections AoB article attracts media coverage We are mobile find out more Journals Career Network Published on behalf of The Annals of Botany Company Impact factor 3 654 5 Yr impact factor 4 338 Eigenfactor 0 02603 Rank 10 200 SCImago Score 1 461 Rank 124 1873 Chief Editor Professor J S Pat Heslop Harrison View full editorial board International Review Board For Authors Submitting a manuscript online Self archiving policy Instructions for authors Low Rate Open Access Fees Open access options for authors visit Oxford Open Visit HighWire Press 3hWaciBYRk30rSOQ7UOpP6viAxsZnEle true Looking for your next opportunity Looking for jobs Alerting Services Email table of contents Email Advance Access CiteTrack XML RSS feed Rights Permissions This journal is a member of the Committee on Publication Ethics COPE Corporate Services Advertising sales Reprints Supplements Widget Get a Widget Most Most Read Calcium in Plants Pollen Tube Distribution in the Kiwifruit Actinidia deliciosaA Chev C F Liang Pistil in Relation to its Reproductive Process Homeosis in Araceae Flowers The Case of Philodendron melinonii The Supramolecular Organization of Red Algal Vacuole Membrane Visualized by Freeze fracture Biological nitrogen fixation in non legume plants View all Most Read articles Most Cited An update on receptor like kinase involvement in the maintenance of plant cell wall integrity Arrangement of mixed linkage glucan and glucuronoarabinoxylan in the cell walls of growing maize roots Understanding polysaccharide production and properties using seed coat mutants future perspectives for the exploitation of natural variants Molecular control of seasonal flowering in rice arabidopsis and temperate cereals A footprint of past climate change on

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  • Phylogeography and modes of reproduction in diploid and tetraploid halophytes of Limonium species (Plumbaginaceae): evidence for a pattern of geographical parthenogenesis
    species of each ploidy group namely diploid L ovalifolium and tetraploid L multiflorum using plants from greenhouse collections Key Results and Conclusions Genetic analyses showed that diploid species have a higher haplotype diversity and a higher number of unique endemic haplotypes than tetraploid species Network analysis revealed correlations between cpDNA haplotype distribution and ploidy groups species groups and geographical origin and haplotype sharing within and among species with distinct ploidy levels Reproductive biology analyses showed that diploid L ovalifolium mainly forms meiotically reduced tetrasporic embryo sacs of Gagea ova Adoxa and Drusa types Limonium multiflorum however has only unreduced diplosporic apomictic embryo sacs of Rudbeckia type and autonomous apomictic development seems to occur Taken together the findings provide evidence of a pattern of geographical parthenogenesis in which quaternary climatic oscillations appear to be involved in the geographical patterns of coastal diploid and tetraploid Limonium species Key words Apomixis cytoplasmic markers cpDNA female gametophyte development floral biology geographical parthenogenesis Limonium phylogeography polyploidy reproductive modes The Author 2015 Published by Oxford University Press on behalf of the Annals of Botany Company All rights reserved For Permissions please email journals permissions oup com Related articles ContentSnapshots Content Snapshots Ann Bot 2016 117 1 i iii doi 10 1093 aob mcv183 Extract Full Text HTML Full Text PDF Previous Next Article Table of Contents This Article Ann Bot 2016 117 1 37 50 doi 10 1093 aob mcv138 First published online September 30 2015 Abstract Free Free Figures Free Full Text HTML Full Text PDF Supplementary Data All Versions of this Article mcv138v1 117 1 37 most recent Classifications Original Article Services Article metrics Alert me when cited Alert me if corrected Alert me if commented Find similar articles Similar articles in Web of Science Similar articles in PubMed Add to my archive Download citation Request Permissions Responses Submit a response No responses published Citing Articles Load citing article information Citing articles via CrossRef Citing articles via Scopus Citing articles via Web of Science Google Scholar Articles by Róis A S Articles by Caperta A D PubMed PubMed citation Articles by Róis A S Articles by Sádio F Articles by Paulo O S Articles by Teixeira G Articles by Paes A P Articles by Espírito Santo D Articles by Sharbel T F Articles by Caperta A D Agricola Articles by Róis A S Articles by Caperta A D Related Content Related articles in this journal Load related web page information Share Email this article CiteULike Delicious Facebook Google Mendeley Twitter What s this Search this journal Advanced Current Issue February 2016 117 2 Alert me to new issues The Journal About this journal Annals of Botany Collections AoB article attracts media coverage We are mobile find out more Journals Career Network Published on behalf of The Annals of Botany Company Impact factor 3 654 5 Yr impact factor 4 338 Eigenfactor 0 02603 Rank 10 200 SCImago Score 1 461 Rank 124 1873 Chief Editor Professor J S Pat Heslop Harrison View full editorial

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