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Changes in plant community structure and decrease in floral resource availability lead to a high temporal β-diversity of plant–bee interactions

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Abstract

Biological communities are subject to spatiotemporal variations in community structure, i.e., species composition, richness, and abundance. Plant–pollinator interactions are affected by species composition and abundance, so that rapid changes in plant community structure can lead to critical impacts on plant–pollinator interactions at the community level. The extent of these impacts depends on how plants respond to different kinds of stressors, such as the disturbance caused by invading species. In this research, we conducted a before-and-after study to evaluate the potential effects of an invasive fast-growing alien grass species on the structure of a plant–pollinator interaction network. We described the changes in community structure and plant–pollinator interactions over two sampling periods, through the temporal β-diversity of plant and bee species, plant–bee interactions, and plant functional traits. Our results showed that changes in plant community composition (especially the plants in the network core) and decrease in plant species richness, as well as in floral resources availability impacted plant–pollinator interactions of a grassland community after the growth of a fast-growing alien grass species. These changes were accompanied by a decrease in plant–bee interaction diversity, and a high β-diversity of species interactions mainly due to interaction rewiring. However, we found no effect on the functional diversity of flowers. In conclusion, our study showed that a short-term change in plant species composition and floral resource abundance impacted plant–bee interactions, which markedly changed network structure and dynamics.

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References

  • Aizen MA, Morales CL, Morales JM (2008) Invasive mutualists erode native pollination webs. PLoS Biol 6:31

    Google Scholar 

  • Aizen MA, Sabatino M, Tylianakis JM (2012) Specialization and rarity predict nonrandom loss of interactions from mutualist networks. Science 335:1486–1489

    CAS  PubMed  Google Scholar 

  • Aizen MA, Morales CL, Vázquez DP et al (2014) When mutualism goes bad: density-dependent impacts of introduced bees on plant reproduction. N Phytol 204:322–328

    Google Scholar 

  • Almeida-Neto M, Ulrich W (2011) A straightforward computational approach for measuring nestedness using quantitative matrices. Environ Model Softw 26:173–178

    Google Scholar 

  • Almeida-Neto M, Prado PI, Kubota U et al (2010) Invasive grasses and native Asteraceae in the Brazilian Cerrado. Plant Ecol 209:109–122

    Google Scholar 

  • Anderson MJ, Ellingsen KE, McArdle BH (2006) Multivariate dispersion as a measure of beta diversity. Ecol Lett 9:683–693

    PubMed  Google Scholar 

  • Appezzato-da-Glória B, Cury G (2011) Morpho-anatomical features of underground systems in six Asteraceae species from the Brazilian Cerrado. An Acad Bras Cienc 3:981–992

    Google Scholar 

  • Araujo AC, Martin González AM, Sandel B et al (2018) Spatial distance and climate determine modularity in a cross-biomes plant–hummingbird interaction network in Brazil. J Biogeogr 45:1846–1858

    Google Scholar 

  • Barwell LJ, Isaac NJ, Kunin WE (2015) Measuring β-diversity with species abundance data. J Anim Ecol 84:1112–1122

    PubMed  PubMed Central  Google Scholar 

  • Bascompte J, Jordano P, Melián CJ, Olesen JM (2003) The nested assembly of plant–animal mutualistic networks. Proc Natl Acad Sci USA 100:9383–9387

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bascompte J, Jordano P, Olesen JM (2006) Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312:431–433

    CAS  PubMed  Google Scholar 

  • Beckett SJ (2016) Improved community detection in weighted bipartite networks. R Soc Open Sci 3:140536

    PubMed  PubMed Central  Google Scholar 

  • Biella P, Akter A, Ollerton J et al (2019) Experimental loss of generalist plants reveals alterations in plant–pollinator interactions and a constrained flexibility of foraging. Sci Rep UK 9:7376

    Google Scholar 

  • Blüthgen N, Menzel F, Blüthgen N (2006) Measuring specialization in species interaction networks. BMC Ecol 6:9

    PubMed  PubMed Central  Google Scholar 

  • Carstensen DW, Sabatino MT, Trøjelsgaard K et al (2014) Beta diversity of plant–pollinator networks and the spatial turnover of pairwise interactions. PLoS ONE 9:112903

    Google Scholar 

  • Chacoff NP, Vázquez DP, Lomáscolo SB et al (2012) Evaluating sampling completeness in a desert plant–pollinator network. J Anim Ecol 81:190–200

    PubMed  Google Scholar 

  • Chacoff NP, Resasco J, Vázquez DP (2018) Interaction frequency, network position, and the temporal persistence of interactions in a plant–pollinator network. Ecology 99:21–28

    PubMed  Google Scholar 

  • Chao A, Chazdon RL, Colwell RK et al (2005) A new statistical approach for assessing similarity of species composition with incidence and abundance data. Ecol Lett 8:148–159

    Google Scholar 

  • Chao A, Chazdon RL, Colwell RK et al (2006) Abundance-based similarity indices and their estimation when there are unseen species in samples. Biometrics 62:61–371

    Google Scholar 

  • Chao A, Gotelli NJ, Hsieh TC et al (2014) Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecol Monogr 84:45–67

    Google Scholar 

  • Chase MW, Christenhusz MJM, Fay MF et al (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc 181:1–20

    Google Scholar 

  • Craine JM, Dybzinski R (2013) Mechanisms of plant competition for nutrients, water and light. Funct Ecol 27:833–840

    Google Scholar 

  • Dáttilo W, Diaz-Castelazo C, Rico-Gray V (2014) Ant dominance hierarchy determines the nested pattern in ant–plant networks. Biol J Linn Soc 113:405–414

    Google Scholar 

  • De Bello F, Lepš J, Sebastià MT (2006) Variations in species and functional plant diversity along climatic and grazing gradients. Ecography 29:801–810

    Google Scholar 

  • Dixon P (2003) VEGAN, a package of R functions for community ecology. J Veg Sci 14:927–930

    Google Scholar 

  • Dormann CF (2008) Introducing the bipartite package: analysing ecological networks. R News 1:0-2413793

    Google Scholar 

  • Dormann CF, Strauss R (2014) A method for detecting modules in quantitative bipartite networks. Methods Ecol Evol 5:90–98

    Google Scholar 

  • Edwards KM, Schlesinger C, Ooi MK et al (2019) Invasive grass affects seed viability of native perennial shrubs in arid woodlands. Biol Invasions 21:1763–1774

    Google Scholar 

  • Fontaine C, Collin CL, Dajoz I (2008) Generalist foraging of pollinators: diet expansion at high density. J Ecol 96:1002–1010

    Google Scholar 

  • Goulson D (1999) Foraging strategies of insects for gathering nectar and pollen, and implications for plant ecology and evolution. Perspect Plant Ecol 2:185–209

    Google Scholar 

  • Gower JC (1971) A general coefficient of similarity and some of its properties. Biometrics 27:857–874

    Google Scholar 

  • Hendrickx F, Maelfait JP, Wingerden WV et al (2007) How landscape structure, land-use intensity and habitat diversity affect components of total arthropod diversity in agricultural landscapes. J Appl Ecol 44:340–351

    Google Scholar 

  • Hiraiwa MK, Ushimaru A (2017) Low functional diversity promotes niche changes in natural island pollinator communities. Proc R Soc B 284:20162218

    PubMed  PubMed Central  Google Scholar 

  • Horn HS (1966) Measurement of “overlap” in comparative ecological studies. Am Nat 100:419–424

    Google Scholar 

  • Hsieh TC, Ma KH, Chao A (2016) iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol Evol 7:1451–1456

    Google Scholar 

  • Hung KLJ, Kingston JM, Lee A et al (2019) Non-native honey bees disproportionately dominate the most abundant floral resources in a biodiversity hotspot. Proc R Soc B 286:20182901

    PubMed  PubMed Central  Google Scholar 

  • Karron JD, Holmquist KG, Flanagan RJ et al (2009) Pollinator visitation patterns strongly influence among-flower variation in selfing rate. Ann Bot Lond 103:1379–1383

    Google Scholar 

  • Kerr WE (1957) Introdução de abelhas africanas no Brasil. Bras Apic 3:2011–2213

    Google Scholar 

  • Kottek M (2006) World map of the Köppen-Geiger climate classification updated. Meteorol Z 15:259–263

    Google Scholar 

  • Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305

    PubMed  Google Scholar 

  • Lara-Romero C, Seguí J, Pérez-Delgado A et al (2019) Beta diversity and specialization in plant–pollinator networks along an elevational gradient. J Biogeogr 46:1598–1610

    Google Scholar 

  • Legendre P, Oksanen J, ter Braak CJ (2011) Testing the significance of canonical axes in redundancy analysis. Methods Ecol Evol 2:269–277

    Google Scholar 

  • Machado IC, Lopes AV (2004) Floral traits and pollination systems in the Caatinga, a Brazilian tropical dry forest. Ann Bot Lond 94:365–376

    Google Scholar 

  • Mack RN, Simberloff D, Mark Lonsdale W et al (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710

    Google Scholar 

  • Magrach A, González-Varo JP, Boiffier M et al (2017) Honeybee spillover reshuffles pollinator diets and affects plant reproductive success. Nat Ecol Evol 9:1299

    Google Scholar 

  • Martin PH, Canham CD, Marks PL (2009) Why forests appear resistant to exotic plant invasions: intentional introductions, stand dynamics, and the role of shade tolerance. Front Ecol Environ 7:142–149

    Google Scholar 

  • Maruyama PK, Vizentin-Bugoni J, Dalsgaard B et al (2015) Nectar robbery by a hermit hummingbird: association to floral phenotype and its influence on flowers and network structure. Oecologia 178:783–793

    PubMed  Google Scholar 

  • Maruyama PK, Nunes CE, Vizentin-Bugoni J et al (2018) Are native bees and Apis mellifera equally efficient pollinators of the Rupestrian grassland daisy Aspilia jolyana (Asteraceae)? Acta Bot Bras 32:386–391

    Google Scholar 

  • Melo AS, Melo MAS (2019) CommEcol: community ecology analyses. R package version 1.7.0. https://CRAN.R-project.org/package=CommEcol. Accessed 20 Mar 2020

  • Memmott J, Waser NM (2002) Integration of alien plants into a native flower–pollinator visitation web. Proc R Soc B 269:2395–2399

    PubMed  PubMed Central  Google Scholar 

  • Michener CD (2000) The bees of the world. Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Morales CL, Arbetman MP, Cameron SA et al (2013) Rapid ecological replacement of a native bumble bee by invasive species. Front Ecol Environ 11:529–534

    Google Scholar 

  • Olesen JM, Bascompte J, Dupont YL et al (2007) The modularity of pollination networks. Proc Natl Acad Sci USA 104:19891–19896

    CAS  PubMed  PubMed Central  Google Scholar 

  • Oliveira-Filho AT, Ratter JA (2002) The Cerrados of Brazil: ecology and natural history of a Neotropical savanna. Columbia University Press, New York

    Google Scholar 

  • Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326

    Google Scholar 

  • Pakeman RJ (2011) Functional diversity indices reveal the impacts of land use intensification on plant community assembly. J Ecol 99:1143–1151

    Google Scholar 

  • Patefield WM (1981) Algorithm AS 159: an efficient method of generating random R × C tables with given row and column totals. J R Stat Soc C 30:91–97

    Google Scholar 

  • Pausas JG, Lamont BB, Paula S et al (2018) Unearthing belowground bud banks in fire-prone ecosystems. N Phytol 217:1435–1448

    Google Scholar 

  • Pivello VR, Carvalho VMC, Lopes PF et al (1999a) Abundance and distribution of native and alien grasses in a “Cerrado” (Brazilian Savanna) Biological Reserve 1. Biotropica 31:71–82

    Google Scholar 

  • Pivello VR, Shida CN, Meirelles ST (1999b) Alien grasses in Brazilian savannas: a threat to the biodiversity. Biodivers Conserv 8:1281–1294

    Google Scholar 

  • Poisot T, Canard E, Mouillot D et al (2012) The dissimilarity of species interaction networks. Ecol Lett 15:1353–1361

    PubMed  Google Scholar 

  • Poisot T, Stouffer DB, Gravel D (2015) Beyond species: why ecological interaction networks vary through space and time. Oikos 124:243–251

    Google Scholar 

  • Potts SG, Ngo HT, Biesmeijer JC et al (2016) The assessment report of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services on pollinators, pollination and food production. Secretariat of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services, Bonn

    Google Scholar 

  • Ramírez-Burbano MB, Stiles FG, González C et al (2017) The role of the endemic and critically endangered Colorful Puffleg Eriocnemis mirabilis in plant–hummingbird networks of the Colombian Andes. Biotropica 49:555–564

    Google Scholar 

  • Silveira FA, Melo GA, Almeida EA (2002) Abelhas brasileiras Sistemática e Identificação. Fundação Araucária, Belo Horizonte

    Google Scholar 

  • Silvertown J (2004) Plant coexistence and the niche. Trends Ecol Evol 19:605–611

    Google Scholar 

  • Souza CS, Maruyama PK, Aoki C et al (2018) Temporal variation in plant–pollinator networks from seasonal tropical environments: higher specialization when resources are scarce. J Ecol 106:2409–2420

    Google Scholar 

  • Stout JC, Morales CL (2009) Ecological impacts of invasive alien species on bees. Apidologie 40:388–409

    Google Scholar 

  • Strayer DL, Eviner VT, Jeschke JM et al (2006) Understanding the long-term effects of species invasions. Trends Ecol Evol 21:645–651

    PubMed  Google Scholar 

  • Traveset A, Castro-Urgal R, Rotllàn-Puig X et al (2018) Effects of habitat loss on the plant–flower visitor network structure of a dune community. Oikos 127:45–55

    Google Scholar 

  • Valdovinos FS (2019) Mutualistic networks: moving closer to a predictive theory. Ecol Lett 22:1517–1534

    PubMed  Google Scholar 

  • Valdovinos FS, Moisset de Espanés PM, Flores JD et al (2013) Adaptive foraging allows the maintenance of biodiversity of pollination networks. Oikos 122:907–917

    Google Scholar 

  • Valdovinos FS, Berlow EL, Moisset de Espanés PM et al (2018) Species traits and network structure predict the success and impacts of pollinator invasions. Nat Commun 9:1–8

    CAS  Google Scholar 

  • Valido A, Rodríguez-Rodríguez MC, Jordano P (2019) Honeybees disrupt the structure and functionality of plant–pollinator networks. Sci Rep UK 9:1–11

    CAS  Google Scholar 

  • Valiente-Banuet A, Aizen MA, Alcántara JM et al (2015) Beyond species loss: the extinction of ecological interactions in a changing world. Funct Ecol 29:299–307

    Google Scholar 

  • Vanbergen AJ, Espíndola A, Aizen MA (2018) Risks to pollinators and pollination from invasive alien species. Nat Ecol Evol 2:16

    PubMed  Google Scholar 

  • Villéger S, Mason NW, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301

    PubMed  Google Scholar 

  • Vizentin-Bugoni J, Maruyama PK, Debastiani VJ et al (2016) Influences of sampling effort on detected patterns and structuring processes of a Neotropical plant–hummingbird network. J Anim Ecol 85:262–272

    PubMed  Google Scholar 

  • Whittaker RH (1960) Vegetation of the Siskiyou Mountains, Oregon and California. Ecol Monogr 30:279–338

    Google Scholar 

  • Williams DG, Baruch Z (2000) African grass invasion in the Americas: ecosystem consequences and the role of ecophysiology. Biol Invasions 2:123–140

    Google Scholar 

  • Yang GJ, Lü XT, Stevens CJ et al (2019) Mowing mitigates the negative impacts of N addition on plant species diversity. Oecologia 189:769–779

    PubMed  Google Scholar 

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Acknowledgements

We thank Antonio L. Castilho, Carine Emer, Jefferson Bugoni, Marcos Nogueira, Pedro Bergamo, Pietro K. Maruyama, two anonymous reviewers, and the Handling Editor Christina Mogren for critical reading and suggestions on the manuscript; Janet Reid for English editing and valuable suggestions. Ana Paula Fortuna and Eduardo Almeida for help in identification of plants and bees, respectively; and colleagues of the Laboratório de Ecologia da Polinização e Interações: LEPI, for their help during fieldwork and discussions. Luciano Ramos Cirne helped us with bee silhouettes. This study is part of L. Hachuy-Filho M.Sc. studies financed by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brazil (CAPES), Finance Code 001. C. S. Ballarin Ph.D. studies are also funded by CAPES (Finance Code 001), and his undergraduate studies (during which most of this research was conducted) was supported by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, Process Number 2017/27177-9).

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Hachuy-Filho, L., Ballarin, C.S. & Amorim, F.W. Changes in plant community structure and decrease in floral resource availability lead to a high temporal β-diversity of plant–bee interactions. Arthropod-Plant Interactions 14, 571–583 (2020). https://doi.org/10.1007/s11829-020-09774-5

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