[en] We are currently facing a large decline in bee populations worldwide. Who are the winners and losers? Generalist bee species, notably those able to shift their diet to new or alternative floral resources, are expected to be among the least vulnerable to environmental change. However, studies of interactions between bees and plants over large temporal and geographical scales are limited by a lack of historical records. Here, we used a unique opportunistic century-old countrywide database of bee specimens collected on plants to track changes in the plant-bee interaction network over time. In each historical period considered, and using a network-based modularity analysis, we identified some major groups of species interacting more with each other than with other species (i.e. modules). These modules were related to coherent functional groups thanks to an a posteriory trait-based analysis. We then compared over time the ecological specialization of bees in the network by computing their degree of interaction within and between modules. "True" specialist species (or peripheral species) are involved in few interactions both inside and between modules. We found a global loss of specialist species and specialist strategies. This means that bee species observed in each period tended to use more diverse floral resources from different ecological groups over time, highly specialist species tending to enter/leave the network. Considering the role and functional traits of species in the network, combined with a long-term time series, provides a new perspective for the study of species specialization.
Violle, C.; CEFE, Univ Montpellier, CNRS, EPHE, IRD, Univ Paul Valéry Montpellier 3, Montpellier, France
Munoz, F.; Laboratoire d'Ecologie Alpine, Université Grenoble Alpes, Grenoble, France
Mahy, Grégory ; Université de Liège - ULiège > Département GxABT > Biodiversité et Paysage
Rasmont, P.; Laboratoire de Zoologie, Université de Mons, Mons, Belgium
Roberts, S. P. M.; Centre for Agri-Environmental Research, School of Agriculture, Policy and Development, University of Reading, Reading, United Kingdom
Vray, S.; Laboratoire de Zoologie, Université de Mons, Mons, Belgium, Département de Géographie, Université de Namur, Namur, Belgium
Dufrêne, Marc ; Université de Liège - ULiège > Département GxABT > Biodiversité et Paysage
Language :
English
Title :
Loss of pollinator specialization revealed by historical opportunistic data: Insights from network-based analysis
Ollerton J, Winfree R, Tarrant S. How many flowering plants are pollinated by animals? Oikos. 2011; 120: 321-326.
Winfree R, Gross BJ, Kremen C. Valuing pollination services to agriculture. Ecol Econ. 2011; 71: 80-88.
Williams PH, Colla S, Xie Z. Bumblebee Vulnerability: Common Correlates of Winners and Losers across Three Continents. Conserv Biol J Soc Conserv Biol. 2009; 23: 931-40.
Verburg PH, Schulp CJE, Witte N, Veldkamp A. Downscaling of land use change scenarios to assess the dynamics of European landscapes. Agric Ecosyst Environ. 2006; 114: 39-56.
Goulson D, Nicholls E, Botías C, Rotheray EL. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science. 2015; 347: 1255957. https://doi.org/10.1126/science.1255957 PMID: 25721506
Valiente-Banuet A, Aizen MA, Alcántara JM, Arroyo J, Cocucci A, Galetti M, et al. Beyond species loss: the extinction of ecological interactions in a changing world. Funct Ecol. 2015; 29: 299-307.
Morris RJ. Anthropogenic impacts on tropical forest biodiversity: a network structure and ecosystem functioning perspective. Philos Trans R Soc B Biol Sci. 2010; 365: 3709-3718.
Aizen MA, Sabatino M, Tylianakis JM. Specialization and Rarity Predict Nonrandom Loss of Interactions from Mutualist Networks. Science. 2012; 335: 1486-1489. https://doi.org/10.1126/science.1215320 PMID: 22442482
Waser NM. Plant-pollinator interactions: from specialization to generalization. Chicago: University of Chicago Press; 2006.
Biesmeijer JC, Roberts SPM, Reemer M, Ohlemüller R, Edwards M, Peeters T, et al. Parallel Declines in Pollinators and Insect-Pollinated Plants in Britain and the Netherlands. Science. 2006; 313: 351-354. https://doi.org/10.1126/science.1127863 PMID: 16857940
Murcia C. Forest fragmentation and the pollination of neotropical plants. In: Schelhas J and Greenberg R, editors. Forest patches in tropical landscapes. Washington: Island Press; 1996. pp. 19-36.
Roger N, Moerman R, Carvalheiro LG, Aguirre-Guitiérrez J, Jacquemart A-L, Kleijn D, et al. Impact of pollen resources drift on common bumblebees in NW Europe. Glob Change Biol. 2017; 23: 68-76.
Barnagaud JY, Devictor V, Jiguet F, Archaux F. When species become generalists: on-going largescale changes in bird habitat specialization. Glob Ecol Biogeogr. 2011; 20: 630-640.
Ings TC, Montoya JM, Bascompte J, Blüthgen N, Brown L, Dormann CF, et al. Ecological networks- beyond food webs. J Anim Ecol. 2009; 78: 253-269. https://doi.org/10.1111/j.1365-2656.2008.01460.x PMID: 19120606
Hagen M, Kissling WD, Rasmussen C, Carstensen DW, Dupont YL, Kaiser-Bunbury CN, et al. Biodiversity, species interactions and ecological networks in a fragmented world. Adv Ecol Res. 2012; 46: 89-120.
Fortuna MA, Bascompte J. The network approach in ecology. In: Valladares F, Camacho A, Elosegi A, Gracia C, Estrada M, Senar JC, Gili JP, editors. Unity in diversity: reflections on ecology after the legacy of Ramon Margalef. Bilbao: Fundación BBVA; 2008. pp. 371-392.
Blüthgen N, Menzel F, Blüthgen N. Measuring specialization in species interaction networks. BMC Ecol. 2006; 6: 9. https://doi.org/10.1186/1472-6785-6-9 PMID: 16907983
Jordano P. Patterns of mutualistic interactions in pollination and seed dispersal: connectance, dependence asymmetries, and coevolution. Am Nat. 1987; 129: 657-677.
Waser NM, Chittka L, Price MV, Williams NM, Ollerton J. Generalization in Pollination Systems, and Why it Matters. Ecology. 1996; 77: 1043-1060.
Olesen JM, Bascompte J, Dupont YL, Jordano P. The modularity of pollination networks. Proc Natl Acad Sci. 2007; 104: 19891-19896. https://doi.org/10.1073/pnas.0706375104 PMID: 18056808
Dupont YL, Olesen JM. Ecological modules and roles of species in heathland plant-insect flower visitor networks. J Anim Ecol. 2009; 78: 346-353. https://doi.org/10.1111/j.1365-2656.2008.01501.x PMID: 19021779
Watts S, Dormann CF, Martiń González AM, Ollerton J. The influence of floral traits on specialization and modularity of plant-pollinator networks in a biodiversity hotspot in the Peruvian Andes. Ann Bot. 2016; 118: 415-429. https://doi.org/10.1093/aob/mcw114 PMID: 27562649
Prado PI, Lewinsohn TM. Compartments in insect-plant associations and their consequences for community structure. J Anim Ecol. 2004; 73: 1168-1178.
Guimerà R, Amaral LAN. Cartography of complex networks: modules and universal roles. J Stat Mech Theory Exp. 2005; 2005: P02001.
Denelle P, Violle C, Munoz F. Generalist plants are more competitive and more functionally similar to each other than specialist plants: insights from network analyses. J Biogeogr. 2020; 0: 1-12.
Schleuning M, Fründ J, Schweiger O, Welk E, Albrecht J, Albrecht M, et al. Ecological networks are more sensitive to plant than to animal extinction under climate change. Nat Commun. 2016; 7: 13965. https://doi.org/10.1038/ncomms13965 PMID: 28008919
Kaiser-Bunbury CN, Muff S, Memmott J, Müller CB, Caflisch A. The robustness of pollination networks to the loss of species and interactions: a quantitative approach incorporating pollinator behaviour. Ecol Lett. 2010; 13: 442-452. https://doi.org/10.1111/j.1461-0248.2009.01437.x PMID: 20100244
Dupont YL, Padrón B, Olesen JM, Petanidou T. Spatio-temporal variation in the structure of pollination networks. Oikos. 2009; 118: 1261-1269.
Burkle LA, Marlin JC, Knight TM. Plant-Pollinator Interactions over 120 Years: Loss of Species, CoOccurrence, and Function. Science. 2013; 339: 1611-1615. https://doi.org/10.1126/science.1232728 PMID: 23449999
Petanidou T, Kallimanis AS, Tzanopoulos J, Sgardelis SP, Pantis JD. Long-term observation of a pollination network: fluctuation in species and interactions, relative invariance of network structure and implications for estimates of specialization. Ecol Lett. 2008; 11: 564-575. https://doi.org/10.1111/j.1461- 0248.2008.01170.x PMID: 18363716
Burkle LA, Alarcón R. The future of plant-pollinator diversity: Understanding interaction networks across time, space, and global change. Am J Bot. 2011; 98: 528-538. https://doi.org/10.3732/ajb. 1000391 PMID: 21613144
Senapathi D, Carvalheiro LG, Biesmeijer JC, Dodson C-A, Evans RL, McKerchar M, et al. The impact of over 80 years of land cover changes on bee and wasp pollinator communities in England. Proc R Soc B Biol Sci. 2015; 282: 20150294.
Kleijn D, Raemakers I. A retrospective analysis of pollen host plant use by stable and declining bumble bee species. Ecology. 2008; 89: 1811-1823. https://doi.org/10.1890/07-1275.1 PMID: 18705369
Wood TJ, Roberts SPM. An assessment of historical and contemporary diet breadth in polylectic Andrena bee species. Biol Conserv. 2017; 215: 72-80.
Scheper J, Reemer M, van Kats R, Ozinga WA, van der Linden GTJ, Schaminée JHJ, et al. Museum specimens reveal loss of pollen host plants as key factor driving wild bee decline in The Netherlands. Proc Natl Acad Sci U S A. 2014; 111: 17552-17557. https://doi.org/10.1073/pnas.1412973111 PMID: 25422416
Isaac NJB, Strien AJ van, August TA, Zeeuw MP de, Roy DB. Statistics for citizen science: extracting signals of change from noisy ecological data. Methods Ecol Evol. 2014; 5: 1052-1060.
Leclercq J, Gaspar C, Marchal JL, Verstraeten C, Wonville C. Analyse des 1600 premières cartes de l'atlas provisoire des insectes de Belgique, et première liste rouge d'insectes menaceś dans la faune belge. Notes Fauniques de Gembloux. 1980; 4: 1-104.
Rasmont P, Pauly A, Terzo M, Patiny S, Michez D, Iserbyt S, et al. The survey of wild bees (Hymenoptera, Apoidea) in Belgium and France. FAO. 2005, 1:78. Available from: https://pdfs.semanticscholar. org/f38a/5991db24d37ba77feb583752cdbcacdeaaef.pdf
Cirtwill AR, Roslin T, Rasmussen C, Olesen JM, Stouffer DB. Between-year changes in community composition shape species' roles in an Arctic plant-pollinator network. Oikos. 2018; 0: 1-14.
Bestová H, Munoz F, Svoboda P, Škaloud P, Violle C. Ecological and biogeographical drivers of freshwater green algae biodiversity: from local communities to large-scale species pools of desmids. Oecologia. 2018; 186: 1017-1030. https://doi.org/10.1007/s00442-018-4074-x PMID: 29368058
Carstensen DW, Trøjelsgaard K, Ollerton J, Morellato LPC. Local and regional specialization in plant- pollinator networks. Oikos. 2017; 531-537.
Bascompte J, Jordano P. Plant-Animal Mutualistic Networks: The Architecture of Biodiversity. Annu Rev Ecol Evol Syst. 2007; 38: 567-593.
Wright IR, Roberts SPM, Collins BE. Evidence of forage distance limitations for small bees (Hymenoptera: Apidae). Eur J Entomol. 2015; 112: 303-310.
Aguirre-Gutiérrez J, Kissling WD, Carvalheiro LG, WallisDeVries MF, Franzeń M, Biesmeijer JC. Functional traits help to explain half-century long shifts in pollinator distributions. Sci Rep. 2016; 6: 24451. https://doi.org/10.1038/srep24451 PMID: 27079784
Maglianesi MA, Blüthgen N, Böhning-Gaese K, Schleuning M. Morphological traits determine specialization and resource use in plant-hummingbird networks in the neotropics. Ecology. 2014; 95: 3325- 3334.
Donald PF, Pisano G, Rayment MD, Pain DJ. The Common Agricultural Policy, EU enlargement and the conservation of Europe's farmland birds. Agric Ecosyst Environ. 2002; 89: 167-182.
Beyaert M, Antrop M, De Maeyer P, Vandermotten C, Billen C, Decroly J-M, et al. La Belgique en cartes: l'évolution du paysage à travers trois siècles de cartographie. Tielt: Lannoo; 2006.
European Commission. Biogeographical Regions. 2014. Available from: http://ec.europa.eu/ environment/nature/natura2000/platform/knowledge_base/103_browse_categories_en.htm
Rasmont P, Iserbyt S. Atlas of the European Bees: genus Bombus. 3rd ed. Mons (Gembloux): STEP Project, Atlas Hymenoptera. 2014. Available from: http://www.zoologie.umh.ac.be//hymenoptera/page. asp?ID=169
Kleijn D, Sutherland WJ. How effective are European agri-environment schemes in conserving and promoting biodiversity? J Appl Ecol. 2003; 40: 947-969.
Crane E. Recent research on the world history of beekeeping. Bee World. 1999; 80: 174-186.
Michener CD. The Bees of the World. 2nd ed. Baltimore: Johns Hopkins University Press; 2007.
Dormann CF. How to be a specialist? Quantifying specialisation in pollination networks. Netw Biol. 2011; 1: 1-20.
Dormann CF, Gruber B, Fründ J. Introducing the bipartite package: analysing ecological networks. R News. 2008; 8: 8-12.
Blüthgen N, Fründ J, Vázquez DP, Menzel F. What do interaction network metrics tell us about specialization and biological traits. Ecology. 2008; 89: 3387-3399. https://doi.org/10.1890/07-2121.1 PMID: 19137945
Pellissier L, Albouy C, Bascompte J, Farwig N, Graham C, Loreau M, et al. Comparing species interaction networks along environmental gradients. Biol Rev. 2018; 93: 785-800. https://doi.org/10.1111/brv. 12366 PMID: 28941124
Doulcier G, Stouffer D. Rnetcarto: Fast Network Modularity and Roles Computation by Simulated Annealing. R package version 0.2.4. 2015.
Newman MEJ, Girvan M. Finding and evaluating community structure in networks. Phys Rev E. 2004; 69: 026113.
Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, et al. Picante: R tools for integrating phylogenies and ecology. Bioinformatics. 2010; 26: 1463-1464. https://doi.org/10.1093/ bioinformatics/btq166 PMID: 20395285
Cottet-Emard F. Probabiliteś et tests d'hypothèses. Louvain-La-Neuve: De Boeck Superieur; 2014.
R Core Team. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. 2018. Available from: https://www.R-project.org/
Dormann CF, Strauss R. A method for detecting modules in quantitative bipartite networks. Methods Ecol Evol. 2014; 5: 90-98.
Biella P, Ollerton J, Barcella M, Assini S. Network analysis of phenological units to detect important species in plant-pollinator assemblages: can it inform conservation strategies? Community Ecol. 2017; 18: 1-10.
Elton C. Competition and the Structure of Ecological Communities. J Anim Ecol. 1946; 15: 54-68.
Hegland SJ, Totland Ø. Relationships between species' floral traits and pollinator visitation in a temperate grassland. Oecologia. 2005; 145: 586-594. https://doi.org/10.1007/s00442-005-0165-6 PMID: 16028095
Westrich P. Die Wildbienen Baden-Württembergs. Stuttgart: E. Ulmer; 1989.
Moretti M, De Bello F, Roberts SPM, Potts SG. Taxonomical vs. functional responses of bee communities to fire in two contrasting climatic regions. J Anim Ecol. 2009; 78: 98-108. https://doi.org/10.1111/j. 1365-2656.2008.01462.x PMID: 18705629
Greenleaf SS, Williams NM, Winfree R, Kremen C. Bee foraging ranges and their relationship to body size. Oecologia. 2007; 153: 589-596. https://doi.org/10.1007/s00442-007-0752-9 PMID: 17483965
Klumpers SGT, Stang M, Klinkhamer PGL. Foraging efficiency and size matching in a plant-pollinator community: the importance of sugar content and tongue length. Ecol Lett. 2019; 22: 469-479. https:// doi.org/10.1111/ele.13204 PMID: 30609161
Goulson D. Bumblebees: Behaviour, Ecology, and Conservation. 2nd ed. Oxford: Oxford University Press; 2010.
Robertson C. Flowers and Insects: XXIV. Ecology. 1927; 8: 113-132.
Lambinon J, Delvosalle L, Duvigneaud J. Nouvelle flore de la Belgique, du Grand-Duchéde Luxembourd, du Nord de la France et des régions voisines (Ptéridophytes et Spermatophytes). 5th ed. Meise: Jardin botanique national de Belgique; 2008.
Julve P. Baseflor. Index botanique, ećologique et chorologique de la Flore de France. Version de 2018. Programme Catminat. 1998. Available from: http://perso.wanadoo.fr/philippe.julve/catminat.htm
Kühn I, Durka W, Klotz S. BiolFlor: A New Plant-Trait Database as a Tool for Plant Invasion Ecology. Divers Distrib. 2004; 10: 363-365.
McCall C, Primack RB. Influence of Flower Characteristics, Weather, Time of Day, and Season on Insect Visitation Rates in Three Plant Communities. Am J Bot. 1992; 79: 434-442.
Kugler H. Blütenökologie. Stuttgart: Gustav Fischer Verlag; 1970.
Cariveau DP, Nayak GK, Bartomeus I, Zientek J, Ascher JS, Gibbs J, et al. The Allometry of Bee Proboscis Length and Its Uses in Ecology. PLOS ONE. 2016; 11: e0151482. https://doi.org/10.1371/ journal.pone.0151482 PMID: 26986000
Guimerà R, Sales-Pardo M, Amaral LAN. Module identification in bipartite and directed networks. Phys Rev E. 2007; 76: 036102.
RevertéS, Retana J, Gómez JM, Bosch J. Pollinators show flower colour preferences but flowers with similar colours do not attract similar pollinators. Ann Bot. 2016; 118: 249-257. https://doi.org/10.1093/ aob/mcw103 PMID: 27325897
Rasheed SA, Harder LD. Economic motivation for plant species preferences of pollen-collecting bumble bees. Ecol Entomol. 2003; 22: 209-219.
Drossart M, Michez D, Vanderplanck M. Invasive plants as potential food resource for native pollinators: A case study with two invasive species and a generalist bumble bee. Sci Rep. 2017; 7: 16242. https:// doi.org/10.1038/s41598-017-16054-5 PMID: 29176720
Poisot T, Kéfi S, Morand S, Stanko M, Marquet PA, Hochberg ME. A Continuum of Specialists and Generalists in Empirical Communities. PLOS ONE. 2015; 10: e0114674. https://doi.org/10.1371/journal. pone.0114674 PMID: 25992798
Ashworth L, Aguilar R, Galetto L, Aizen MA. Why do pollination generalist and specialist plant species show similar reproductive susceptibility to habitat fragmentation? J Ecol. 2004; 92: 717-719.
Ollerton J, Erenler H, Edwards M, Crockett R. Extinctions of aculeate pollinators in Britain and the role of large-scale agricultural changes. Science. 2014; 346: 1360-1362. https://doi.org/10.1126/science. 1257259 PMID: 25504719
Gómez Reyes JM, Perfectti F, Jordano P. The Functional Consequences of Mutualistic Network Architecture. 2011; 6: e16143.
Bommarco R, Biesmeijer JC, Meyer B, Potts SG, Pöyry J, Roberts SPM, et al. Dispersal capacity and diet breadth modify the response of wild bees to habitat loss. Proc R Soc Lond B Biol Sci. 2010; rspb20092221.
Carvalheiro LG, Kunin WE, Keil P, Aguirre-Gutiérrez J, Ellis WN, Fox R, et al. Species richness declines and biotic homogenisation have slowed down for NW-European pollinators and plants. Ecol Lett. 2013; 16: 870-878. https://doi.org/10.1111/ele.12121 PMID: 23692632
Maes D, Isaac NJB, Harrower CA, Collen B, van Strien AJ, Roy DB. The use of opportunistic data for IUCN Red List assessments. Biol J Linn Soc. 2015; 115: 690-706.
Solan TD, Renner I, Cheylan M, Geniez P, Barnagaud J-Y. Opportunistic records reveal Mediterranean reptiles' scale-dependent responses to anthropogenic land use. Ecography. 2019; 42: 608-620.
Gibson RH, Knott B, Eberlein T, Memmott J. Sampling method influences the structure of plant-pollinator networks. Oikos. 2011; 120: 822-831.
King C, Ballantyne G, Willmer PG. Why flower visitation is a poor proxy for pollination: measuring single-visit pollen deposition, with implications for pollination networks and conservation. Methods Ecol Evol. 2013; 4: 811-818.
Thébault E, Fontaine C. Stability of Ecological Communities and the Architecture of Mutualistic and Trophic Networks. Science. 2010; 329: 853-856. https://doi.org/10.1126/science.1188321 PMID: 20705861