The neglected importance of floral traits in trait‐based plant community assembly

Understanding the rules of community assembly and species coexistence is one of the oldest and most fundamental aims of ecological research (Götzenberger et al., 2012). To date, numerous potential ecological processes have been identified as drivers of species sorting into communities. Among these, abiotic conditions and biotic interactions, as well as dispersal, are generally agreed to have an important role, beside stochastic events (Cornwell and Ackerly, 2009). Abiotic and biotic processes act as a series of filters, selecting species from a regional species pool into local communities (Zobel, 2016) based on their functional characteristics which make them suitable for the particular habitat (Díaz et al., 1998). Such characteristics, i.e. “functional traits,” are defined as “any morphological, physiological or phenological feature measurable at the individual level, which impacts fitness indirectly via its effects on growth, reproduction and survival” (Violle et al., 2007). Although, by definition, reproduction is one of the three Received: 6 June 2019 | Revised: 14 February 2020 | Accepted: 26 February 2020 DOI: 10.1111/jvs.12877

[1]  K. N. Dollman,et al.  - 1 , 1743 .

[2]  H. G. Baker,et al.  SELF‐COMPATIBILITY AND ESTABLISHMENT AFTER ‘“LONG‐DISTANCE” DISPERSAL , 1955 .

[3]  Knut Faegri,et al.  The principles of pollination ecology , 1967 .

[4]  J. Wiens Spatial Scaling in Ecology , 1989 .

[5]  Alastair H. Fitter,et al.  The ecological flora database. , 1994 .

[6]  S. Barrett The Reproductive Biology and Genetics of Island Plants , 1996 .

[7]  J. Bosch,et al.  Flowering phenology, floral traits and pollinator composition in a herbaceous Mediterranean plant community , 1997, Oecologia.

[8]  Sandra Díaz,et al.  Plant functional traits and environmental filters at a regional scale , 1998 .

[9]  P. Chesson Mechanisms of Maintenance of Species Diversity , 2000 .

[10]  L. Chittka,et al.  Successful invasion of a floral market , 2001, Nature.

[11]  S. Lavorel,et al.  Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail , 2002 .

[12]  C. Körner,et al.  Altitudinal differences in flower traits and reproductive allocation , 2004 .

[13]  Mark Westoby,et al.  A leaf-height-seed (LHS) plant ecology strategy scheme , 1998, Plant and Soil.

[14]  W. Wilson,et al.  When can two plant species facilitate each other's pollination? , 2004 .

[15]  BiolFlor — a new plant‐trait database as a tool for plant invasion ecology , 2004 .

[16]  L. Gigord,et al.  Pollination of the European food-deceptive Traunsteinera globosa (Orchidaceae): the importance of nectar-producing neighbouring plants , 2007, Plant Systematics and Evolution.

[17]  Ingolf Kühn,et al.  Relating geographical variation in pollination types to environmental and spatial factors using novel statistical methods. , 2006, The New phytologist.

[18]  Sd Johnson,et al.  Geographical Variation in Diversity and Specificity of Pollination Systems , 2006 .

[19]  M. Potts,et al.  Character displacement among bat-pollinated flowers of the genus Burmeistera: analysis of mechanism, process and pattern , 2007, Proceedings of the Royal Society B: Biological Sciences.

[20]  Nils Blüthgen,et al.  Specialization, Constraints, and Conflicting Interests in Mutualistic Networks , 2007, Current Biology.

[21]  C. Violle,et al.  Let the concept of trait be functional , 2007 .

[22]  J. Losos Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. , 2008, Ecology letters.

[23]  D. Ackerly,et al.  Plant-pollinator interactions and the assembly of plant communities. , 2008, Trends in ecology & evolution.

[24]  D. Vokou,et al.  Flower morphology, phenology and visitor patterns in an alpine community on Mt Olympos, Greece , 2008 .

[25]  Ø. Totland,et al.  The relationships between floral traits and specificity of pollination systems in three Scandinavian plant communities , 2008, Oecologia.

[26]  N. Waser,et al.  New frontiers in competition for pollination. , 2009, Annals of botany.

[27]  Ignasi Bartomeus,et al.  Invasive plant integration into native plant–pollinator networks across Europe , 2009, Proceedings of the Royal Society B: Biological Sciences.

[28]  M. V. Price,et al.  A global test of the pollination syndrome hypothesis. , 2009, Annals of botany.

[29]  G. Mittelbach,et al.  Is There a Latitudinal Gradient in the Importance of Biotic Interactions , 2009 .

[30]  M. Devoto,et al.  Patterns of species turnover in plant‐pollinator communities along a precipitation gradient in Patagonia (Argentina) , 2009 .

[31]  F. Bello,et al.  CLO-PLA: the database of clonal and bud bank traits of Central European flora. , 2009 .

[32]  Elsevier Sdol,et al.  Flora - Morphology, Distribution, Functional Ecology of Plants , 2009 .

[33]  Luciano Cagnolo,et al.  Uniting pattern and process in plant-animal mutualistic networks: a review. , 2009, Annals of botany.

[34]  David D. Ackerly,et al.  Community assembly and shifts in plant trait distributions across an environmental gradient in coastal California , 2009 .

[35]  W. Durka,et al.  Pollination mode and life form strongly affect the relation between mating system and pollen to ovule ratios. , 2009, The New phytologist.

[36]  A. Ellis,et al.  Do pollinators influence the assembly of flower colours within plant communities? , 2011, Oecologia.

[37]  Peter W. McOwan,et al.  FReD: The Floral Reflectance Database — A Web Portal for Analyses of Flower Colour , 2010, PloS one.

[38]  Rebecca E. Irwin,et al.  Beyond biomass: measuring the effects of community‐level nitrogen enrichment on floral traits, pollinator visitation and plant reproduction , 2010 .

[39]  J. Vamosi,et al.  Floral colour versus phylogeny in structuring subalpine flowering communities , 2010, Proceedings of the Royal Society B: Biological Sciences.

[40]  P. Vittoz,et al.  Spatial pattern of floral morphology: possible insight into the effects of pollinators on plant distributions , 2010 .

[41]  J. Ollerton,et al.  How many flowering plants are pollinated by animals , 2011 .

[42]  N. Alvarez,et al.  Evolution of Plant-Pollinator Relationships: Pollinators as drivers of plant distribution and assemblage into communities , 2011 .

[43]  S. Ibanez,et al.  Optimizing size thresholds in a plant–pollinator interaction web: towards a mechanistic understanding of ecological networks , 2012, Oecologia.

[44]  J. HilleRisLambers,et al.  Rethinking Community Assembly through the Lens of Coexistence Theory , 2012 .

[45]  M. R. Whitehead,et al.  New perspectives on the evolution of plant mating systems. , 2012, Annals of botany.

[46]  M. Pärtel,et al.  Ecological assembly rules in plant communities—approaches, patterns and prospects , 2012, Biological reviews of the Cambridge Philosophical Society.

[47]  J. Craine,et al.  Flowering phenology as a functional trait in a tallgrass prairie. , 2012, The New phytologist.

[48]  Ø. Totland,et al.  Interactions for pollinator visitation and their consequences for reproduction in a plant community , 2012 .

[49]  Robert R. Junker,et al.  Specialization on traits as basis for the niche‐breadth of flower visitors and as structuring mechanism of ecological networks , 2013 .

[50]  Renée M. Bekker,et al.  Do plant traits retrieved from a database accurately predict on‐site measurements? , 2013 .

[51]  S. Lavorel,et al.  Herbivory mediated by coupling between biomechanical traits of plants and grasshoppers , 2013 .

[52]  J. Binkenstein,et al.  Increasing land-use intensity decreases floral colour diversity of plant communities in temperate grasslands , 2013, Oecologia.

[53]  T. Ashman,et al.  Toward a predictive understanding of the fitness costs of heterospecific pollen receipt and its importance in co-flowering communities. , 2013, American journal of botany.

[54]  Sandra Lavorel,et al.  A novel framework for linking functional diversity of plants with other trophic levels for the quantification of ecosystem services , 2013 .

[55]  P. Reich,et al.  New handbook for standardised measurement of plant functional traits worldwide , 2013 .

[56]  A. Ives,et al.  Phylogenetic trait-based analyses of ecological networks. , 2013, Ecology.

[57]  A. Pauw Can pollination niches facilitate plant coexistence? , 2013, Trends in ecology & evolution.

[58]  Elizabeth Elle,et al.  Traits and phylogenetic history contribute to network structure across Canadian plant–pollinator communities , 2014, Oecologia.

[59]  A. Ellis,et al.  Intraspecific divergence and convergence of floral tube length in specialized pollination interactions , 2014, Proceedings of the Royal Society B: Biological Sciences.

[60]  N. Blüthgen,et al.  Morphological traits determine specialization and resource use in plant–hummingbird networks in the neotropics , 2014 .

[61]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[62]  M. Burd,et al.  Flower colour and phylogeny along an altitudinal gradient in the Himalayas of Nepal , 2014 .

[63]  N. Blüthgen,et al.  Functional and phylogenetic diversity of plant communities differently affect the structure of flower-visitor interactions and reveal convergences in floral traits , 2015, Evolutionary Ecology.

[64]  A. Mooers,et al.  Pollinators visit related plant species across 29 plant–pollinator networks , 2014, Ecology and evolution.

[65]  M. Quesada,et al.  A quantitative review of pollination syndromes: do floral traits predict effective pollinators? , 2014, Ecology letters.

[66]  Eric Garnier,et al.  Are trait‐based species rankings consistent across data sets and spatial scales? , 2014 .

[67]  S. Johnsen,et al.  COMPETITION FOR HUMMINGBIRD POLLINATION SHAPES FLOWER COLOR VARIATION IN ANDEAN SOLANACEAE , 2014, Evolution; international journal of organic evolution.

[68]  X. Raynaud,et al.  Competition with wind-pollinated plant species alters floral traits of insect-pollinated plant species , 2015, Scientific Reports.

[69]  Richard G FitzJohn,et al.  Model Adequacy and the Macroevolution of Angiosperm Functional Traits , 2014, bioRxiv.

[70]  Ø. Totland,et al.  Pollen limitation, species’ floral traits and pollinator visitation: different relationships in contrasting communities , 2015 .

[71]  J. Lord Patterns in floral traits and plant breeding systems on Southern Ocean Islands , 2015, AoB PLANTS.

[72]  H. Müller Alpenblumen, Ihre Befruchtung Durch Insekten Und Ihre Anpassungen an Dieselben , 2015 .

[73]  Jochen Fründ,et al.  Predicting ecosystem functions from biodiversity and mutualistic networks: an extension of trait-based concepts to plant - animal interactions , 2015 .

[74]  Y. Buckley,et al.  Fast–slow continuum and reproductive strategies structure plant life-history variation worldwide , 2015, Proceedings of the National Academy of Sciences.

[75]  J. Ollerton,et al.  Is the notion that species interactions are stronger and more specialized in the tropics a zombie idea? , 2016 .

[76]  Jordi Bosch,et al.  Pollinators show flower colour preferences but flowers with similar colours do not attract similar pollinators. , 2016, Annals of botany.

[77]  I. Pen,et al.  Competition for pollinators and intra-communal spectral dissimilarity of flowers. , 2016, Plant biology.

[78]  P. Oliveira,et al.  Changes in floristic composition and pollination systems in a “Cerrado” community after 20 years of fire suppression , 2016, Brazilian Journal of Botany.

[79]  Andrew K. Skidmore,et al.  Mapping pollination types with remote sensing , 2016 .

[80]  G. Buffa,et al.  Does flowering synchrony contribute to the sustainment of dry grassland biodiversity , 2016 .

[81]  B. Dalsgaard,et al.  The macroecology of animal versus wind pollination: ecological factors are more important than historical climate stability , 2016 .

[82]  J. Funk,et al.  Regeneration: an overlooked aspect of trait‐based plant community assembly models , 2016 .

[83]  I. Kitching,et al.  Beyond neutral and forbidden links: morphological matches and the assembly of mutualistic hawkmoth-plant networks. , 2016, The Journal of animal ecology.

[84]  Nigel D. Boatman,et al.  Historical nectar assessment reveals the fall and rise of Britain in bloom , 2015, Nature.

[85]  M. Marques,et al.  Functional diversity of reproductive traits increases across succession in the Atlantic forest , 2016 .

[86]  M. Zobel The species pool concept as a framework for studying patterns of plant diversity , 2016 .

[87]  Jens Kattge,et al.  A global Fine-Root Ecology Database to address below-ground challenges in plant ecology. , 2017, The New phytologist.

[88]  B. Schatz,et al.  Understanding intraspecific variation of floral scent in light of evolutionary ecology. , 2017, Annals of botany.

[89]  G. Overbeck,et al.  Flowering phenology and plant-pollinator interactions in a grassland community of Southern Brazil , 2017 .

[90]  Tomáš Herben,et al.  CLO-PLA: a database of clonal and bud-bank traits of the Central European flora. , 2017, Ecology.

[91]  Y. Brandvain,et al.  Self-compatibility is over-represented on islands. , 2017, The New phytologist.

[92]  R. Ree,et al.  Global biogeography of mating system variation in seed plants. , 2017, Ecology letters.

[93]  L. Carvalheiro,et al.  Influence of plant–pollinator interactions on the assembly of plant and hummingbird communities , 2017 .

[94]  Grasiela Casas,et al.  Untangling the Tangled Bank: A Novel Method for Partitioning the Effects of Phylogenies and Traits on Ecological Networks , 2017, Evolutionary Biology.

[95]  J. Olesen,et al.  Community-wide integration of floral colour and scent in a Mediterranean scrubland , 2017, Nature Ecology & Evolution.

[96]  M. Lewis,et al.  How to be a good neighbour: Facilitation and competition between two co-flowering species. , 2017, Journal of theoretical biology.

[97]  C. Graham,et al.  Effects of hummingbird morphology on specialization in pollination networks vary with resource availability , 2017 .

[98]  R. Junker,et al.  Elevation predicts the functional composition of alpine plant communities based on vegetative traits, but not based on floral traits , 2018, Alpine Botany.

[99]  F. Hartig,et al.  Functional flower traits and their diversity drive pollinator visitation , 2017 .

[100]  Dominique Gravel,et al.  Species traits as drivers of food web structure , 2018 .

[101]  G. Buffa,et al.  New insights into plants co‐existence in species‐rich communities: The pollination interaction perspective , 2018 .

[102]  Wilfried Thuiller,et al.  Comparing species interaction networks along environmental gradients , 2017, Biological reviews of the Cambridge Philosophical Society.

[103]  J. Olesen,et al.  Disentangling the role of floral sensory stimuli in pollination networks , 2018, Nature Communications.

[104]  P. Maruyama,et al.  Temporal variation in plant–pollinator networks from seasonal tropical environments: Higher specialization when resources are scarce , 2018 .

[105]  J. H. Burns,et al.  GloPL, a global data base on pollen limitation of plant reproduction. , 2018 .

[106]  J. H. Burns,et al.  Reflections on, and visions for, the changing field of pollination ecology. , 2018, Ecology letters.

[107]  A. Pauw,et al.  Frequency dependence of pollinator visitation rates suggests that pollination niches can allow plant species coexistence , 2018, Journal of Ecology.

[108]  T. Knight,et al.  A review of European studies on pollination networks and pollen limitation, and a case study designed to fill in a gap , 2018, AoB PLANTS.

[109]  C. Lortie,et al.  Finding the bees knees: A conceptual framework and systematic review of the mechanisms of pollinator-mediated facilitation , 2019, Perspectives in Plant Ecology, Evolution and Systematics.

[110]  B. Schamp,et al.  Evidence of temporal niche separation via low flowering time overlap in an old-field plant community , 2019, Oecologia.

[111]  A. Ellis,et al.  Dominant pollinators drive non-random community assembly and shared flower colour patterns in daisy communities , 2018, Annals of botany.

[112]  A. Traveset,et al.  Pollination outcomes reveal negative density-dependence coupled with interspecific facilitation among plants. , 2019, Ecology letters.

[113]  Denis Bastianelli,et al.  TRY plant trait database - enhanced coverage and open access. , 2019, Global change biology.