How accurate are estimates of flower visitation rates by pollinators? Lessons from a spatially explicit agent-based model

Abstract Despite the relevant services associated with insect pollinators, several species are considered to have undergone severe and widespread declines, which raise concerns about the future sustainability of ecosystems. Reliable estimates of pollinators' visitation rates to flowers are thus fundamental for supporting management and mitigation actions. A spatially explicit agent-based model was developed to investigate how plant species richness and pollinators' specialisation degree, within a gradient of pollinators abundance and landscape types, might influence accuracy of estimates of visitation rates. Visitation of plants by a generalist-specialist continuum within variable conditions was simulated with the purpose of reproducing pollination studies. Our results indicate that the accuracy of estimates of pollinators' visitation rates is influenced by the interplay between pollinators' specialisation, pollinators' abundances and type of landscape. We highlight the importance of fieldwork investigation to complement our results and compute adjustments in sampling effort for comparable estimates of pollinators' visitation rates from different landscapes and pollinator communities.

[1]  D. Naugle,et al.  Vegetation sampling and measurement , 1994 .

[2]  N. Blüthgen,et al.  Measuring specialization in species interaction networks , 2006, BMC Ecology.

[3]  A. Rosas,et al.  Effect of Landscape Structure on Species Diversity , 2013, PloS one.

[4]  P. Holme,et al.  Agent-based model approach to optimal foraging in heterogeneous landscapes: effects of patch clumpiness , 2007 .

[5]  J. Biesmeijer,et al.  Exploring the relationships between landscape complexity, wild bee species richness and reproduction, and pollination services along a complexity gradient in the Netherlands , 2017 .

[6]  Uta Berger,et al.  17. Anticipating Invasions and Managing Impacts: A Review of Recent Spatiotemporal Modelling Approaches , 2015 .

[7]  Theodora Petanidou,et al.  Spatio‐temporal variation in the structure of pollination networks , 2009 .

[8]  D. Vázquez,et al.  Rareness and specialization in plant-pollinator networks. , 2011, Ecology.

[9]  Birgit Müller,et al.  A standard protocol for describing individual-based and agent-based models , 2006 .

[10]  A. P. Schaffers,et al.  Parallel Declines in Pollinators and Insect-Pollinated Plants in Britain and the Netherlands , 2006, Science.

[11]  A. S. Hedayat,et al.  Statistical Tools for Measuring Agreement , 2011 .

[12]  Uta Berger,et al.  Linking landscape futures with biodiversity conservation strategies in northwest Iberia - A simulation study combining surrogates with a spatio-temporal modelling approach , 2016, Ecol. Informatics.

[13]  J. Gareth Polhill,et al.  The ODD protocol: A review and first update , 2010, Ecological Modelling.

[14]  Robert B. McBride,et al.  A proposal for strength-of-agreement criteria for Lins Concordance Correlation Coefficient , 2005 .

[15]  Hongchun Qu,et al.  A spatially explicit agent-based simulation platform for investigating effects of shared pollination service on ecological communities , 2013, Simul. Model. Pract. Theory.

[16]  Julian Resasco,et al.  Interaction frequency, network position, and the temporal persistence of interactions in a plant-pollinator network. , 2018, Ecology.

[17]  D. Goulson,et al.  Bee declines driven by combined stress from parasites, pesticides, and lack of flowers , 2015, Science.

[18]  Katherine C. R. Baldock,et al.  Constructing more informative plant–pollinator networks: visitation and pollen deposition networks in a heathland plant community , 2015, Proceedings of the Royal Society B: Biological Sciences.

[19]  P. Royston A Toolkit for Testing for Non‐Normality in Complete and Censored Samples , 1993 .

[20]  Carsten F Dormann,et al.  Fragmentation of nest and foraging habitat affects time budgets of solitary bees, their fitness and pollination services, depending on traits: Results from an individual-based model , 2018, PloS one.

[21]  Steven L Chown,et al.  The effect of network size and sampling completeness in depauperate networks , 2018, The Journal of animal ecology.

[22]  F. Schiestl,et al.  Bees use honest floral signals as indicators of reward when visiting flowers. , 2015, Ecology letters.

[23]  Kevin McGarigal,et al.  Landscape Pattern Metrics , 2014 .

[24]  R. O’Hara,et al.  Dealing with Varying Detection Probability, Unequal Sample Sizes and Clumped Distributions in Count Data , 2012, PloS one.

[25]  C. Neinhuis,et al.  Spatio-temporal patterns in pollination of deceptive Aristolochia rotunda L. (Aristolochiaceae). , 2016, Plant biology.

[26]  H. Sahli,et al.  Characterizing ecological generalization in plant-pollination systems , 2006, Oecologia.

[27]  W. Armbruster,et al.  The specialization continuum in pollination systems: diversity of concepts and implications for ecology, evolution and conservation , 2017 .

[28]  J. Fox,et al.  The relative importance of pollinator abundance and species richness for the temporal variance of pollination services. , 2017, Ecology.

[29]  S. Roberts,et al.  Associations between plant and pollinator communities under grassland restoration respond mainly to landscape connectivity , 2018, Journal of Applied Ecology.

[30]  J. A. Cabral,et al.  A spatial explicit agent based model approach to evaluate the performance of different monitoring options for mortality estimates in the scope of onshore windfarm impact assessments , 2017 .

[31]  Jordi Bosch,et al.  Weather-Dependent Pollinator Activity in an Apple Orchard, with Special Reference to Osmia cornuta and Apis mellifera (Hymenoptera: Megachilidae and Apidae) , 2000 .

[32]  Pedro Jordano,et al.  Beyond species loss: The extinction of ecological interactions in a changing world , 2015 .

[33]  Jessica Gurevitch,et al.  Transparency in Ecology and Evolution: Real Problems, Real Solutions. , 2016, Trends in ecology & evolution.

[34]  Jeff Ollerton,et al.  Pollinator Diversity: Distribution, Ecological Function, and Conservation , 2017 .

[35]  V. Wolters,et al.  Partitioning wild bee and hoverfly contributions to plant-pollinator network structure in fragmented habitats. , 2019, Ecology.

[36]  Y. Dumont,et al.  Modeling oil palm pollinator dynamics using deterministic and agent‐based approaches. Applications on fruit set estimates. Some preliminary results , 2018 .

[37]  P. Willmer,et al.  Why flower visitation is a poor proxy for pollination: measuring single‐visit pollen deposition, with implications for pollination networks and conservation , 2013 .

[38]  D. Michez,et al.  Early spring floral foraging resources for pollinators in wet heathlands in Belgium , 2015, Journal of Insect Conservation.

[39]  Dave Goulson,et al.  Why do pollinators visit proportionally fewer flowers in large patches , 2000 .

[40]  Jochen Fründ,et al.  What do interaction network metrics tell us about specialization and biological traits? , 2008, Ecology.

[41]  Shucun Sun,et al.  Relative species abundance successfully predicts nestedness and interaction frequency of monthly pollination networks in an alpine meadow , 2019, PloS one.

[42]  Albert-László Barabási,et al.  Universal resilience patterns in complex networks , 2016, Nature.

[43]  J. Schenk,et al.  Staminode evolution in Mentzelia section Bartonia (Loasaceae) and its impact on insect visitation rates , 2019, Botanical Journal of the Linnean Society.

[44]  A. Cocucci,et al.  Factors affecting pollinator movement and plant fitness in a specialized pollination system , 2011, Plant Systematics and Evolution.

[45]  Carla J Essenberg,et al.  A benefit to providing information? Flower size cues, plant attractiveness, and plant visit length , 2019, Behavioral Ecology.

[46]  Milton Abramowitz,et al.  Handbook of Mathematical Functions with Formulas, Graphs, and Mathematical Tables , 1964 .

[47]  Ruben H. Heleno,et al.  Fine‐tuning the nested structure of pollination networks by adaptive interaction switching, biogeography and sampling effect in the Galápagos Islands , 2019, Oikos.

[48]  Frank Drummond,et al.  Simulation-based modeling of wild blueberry pollination , 2018, Comput. Electron. Agric..

[49]  Matthew S. Heard,et al.  Network size, structure and mutualism dependence affect the propensity for plant–pollinator extinction cascades , 2017 .

[50]  Measurement of Biodiversity (MoB): A method to separate the scale‐dependent effects of species abundance distribution, density, and aggregation on diversity change , 2018, Methods in Ecology and Evolution.

[51]  B. Ebenman,et al.  A potential role for rare species in ecosystem dynamics , 2019, Scientific Reports.

[52]  Jane E. Ogilvie,et al.  Site fidelity by bees drives pollination facilitation in sequentially blooming plant species. , 2016, Ecology.

[53]  William Rand,et al.  An Introduction to Agent-Based Modeling: Modeling Natural, Social, and Engineered Complex Systems with NetLogo , 2015 .

[54]  Ørjan Totland,et al.  How does climate warming affect plant-pollinator interactions? , 2009, Ecology letters.

[55]  J. Vamosi,et al.  Specialization in plant–pollinator networks: insights from local-scale interactions in Glenbow Ranch Provincial Park in Alberta, Canada , 2019, BMC Ecology.

[56]  S. Johnson,et al.  Specialized mutualisms may constrain the geographical distribution of flowering plants , 2017, Proceedings of the Royal Society B: Biological Sciences.

[57]  L. Moquet,et al.  Diversity of the Insect Visitors on Calluna vulgaris (Ericaceae) in Southern France Heathlands , 2015, Journal of insect science.

[58]  N. Blüthgen,et al.  Pollinator diversity and specialization in relation to flower diversity , 2010 .

[59]  Charles M. Macal,et al.  Everything you need to know about agent-based modelling and simulation , 2016, J. Simulation.

[60]  Fred L. Collopy,et al.  Error Measures for Generalizing About Forecasting Methods: Empirical Comparisons , 1992 .

[61]  B. Brosi Pollinator specialization: from the individual to the community. , 2016, The New phytologist.

[62]  C. Pirk,et al.  Economic and ecological implications of geographic bias in pollinator ecology in the light of pollinator declines , 2014 .

[63]  Myles H. M. Menz,et al.  Pollinator rarity as a threat to a plant with a specialized pollination system , 2015 .

[64]  M. Vilà,et al.  Plant–pollinator networks in semi‐natural grasslands are resistant to the loss of pollinators during blooming of mass‐flowering crops , 2018 .

[65]  J. Christopher D. Terry,et al.  Finding missing links in interaction networks , 2019, bioRxiv.

[66]  Ana M. Martín González,et al.  Abundance drives broad patterns of generalisation in plant–hummingbird pollination networks , 2019, Oikos.

[67]  Asko Lõhmus,et al.  A simple survey protocol for assessing terrestrial biodiversity in a broad range of ecosystems , 2018, PloS one.

[68]  A. Holzschuh,et al.  Desynchronizations in bee–plant interactions cause severe fitness losses in solitary bees , 2018, The Journal of animal ecology.

[69]  Myles H. M. Menz,et al.  Reconnecting plants and pollinators: challenges in the restoration of pollination mutualisms. , 2011, Trends in plant science.

[70]  M. Forister,et al.  Revisiting the evolution of ecological specialization, with emphasis on insect-plant interactions. , 2012, Ecology.

[71]  D. Potter,et al.  Quantifying bee assemblages and attractiveness of flowering woody landscape plants for urban pollinator conservation , 2018, PloS one.

[72]  J. C. Marlin,et al.  Plant-Pollinator Interactions over 120 Years: Loss of Species, Co-Occurrence, and Function , 2013, Science.

[73]  Owen L. Petchey,et al.  Biodiversity and Resilience of Ecosystem Functions. , 2015, Trends in ecology & evolution.

[74]  Michael J. O. Pocock,et al.  Estimating sampling completeness of interactions in quantitative bipartite ecological networks: incorporating variation in species’ specialisation , 2017, bioRxiv.

[75]  Martin Wikelski,et al.  Space Use of Bumblebees (Bombus spp.) Revealed by Radio-Tracking , 2011, PloS one.

[76]  D. Inouye,et al.  Variation in composition of two bumble bee species across communities affects nectar robbing but maintains pollinator visitation rate to an alpine plant, Salvia przewalskii , 2018 .

[77]  É. Thébault,et al.  Plant Pollinator Networks along a Gradient of Urbanisation , 2013, PloS one.

[78]  M. Zimmerman Optimal foraging: Random movement by pollen collecting bumblebees , 1982, Oecologia.

[79]  N. Cox,et al.  A Note on the Concordance Correlation Coefficient , 2002 .

[80]  Jennifer A. Dunne,et al.  How to monitor ecological communities cost-efficiently: The example of plant–pollinator networks , 2010 .

[81]  H. de Kroon,et al.  More than 75 percent decline over 27 years in total flying insect biomass in protected areas , 2017, PloS one.

[82]  Michael J. O. Pocock,et al.  Potential landscape-scale pollinator networks across Great Britain: structure, stability and influence of agricultural land cover. , 2018, Ecology letters.

[83]  Jair E. Garcia,et al.  Pollination in a new climate: Assessing the potential influence of flower temperature variation on insect pollinator behaviour , 2018, PloS one.

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

[85]  Víctor M Eguíluz,et al.  Plant survival and keystone pollinator species in stochastic coextinction models: role of intrinsic dependence on animal-pollination , 2017, Scientific Reports.

[86]  J. Nichols,et al.  IMPROVING INFERENCES IN POPULATION STUDIES OF RARE SPECIES THAT ARE DETECTED IMPERFECTLY , 2005 .

[87]  H. Briggs,et al.  Single pollinator species losses reduce floral fidelity and plant reproductive function , 2013, Proceedings of the National Academy of Sciences.

[88]  T. Chai,et al.  Root mean square error (RMSE) or mean absolute error (MAE)? – Arguments against avoiding RMSE in the literature , 2014 .

[89]  J. VanDerWal,et al.  Ecological specialization and population size in a biodiversity hotspot: How rare species avoid extinction , 2009, Proceedings of the National Academy of Sciences.

[90]  Sandra M. Rehan,et al.  Wild bee pollination networks in northern New England , 2016, Journal of Insect Conservation.

[91]  Steiner,et al.  Generalization versus specialization in plant pollination systems. , 2000, Trends in ecology & evolution.

[92]  David Kleijn,et al.  How to efficiently obtain accurate estimates of flower visitation rates by pollinators , 2017 .

[93]  D. Vázquez,et al.  Evaluating sampling completeness in a desert plant-pollinator network. , 2012, The Journal of animal ecology.

[94]  M. Weiss Floral colour changes as cues for pollinators , 1991, Nature.

[95]  A. Newton,et al.  Impacts of deforestation on plant-pollinator networks assessed using an agent based model , 2018, PloS one.

[96]  Xiaohong Li,et al.  The diverse effects of habitat fragmentation on plant–pollinator interactions , 2016, Plant Ecology.

[97]  Mathilde Baude,et al.  How much flower‐rich habitat is enough for wild pollinators? Answering a key policy question with incomplete knowledge , 2015, Ecological entomology.

[98]  J. Biesmeijer,et al.  Safeguarding pollinators and their values to human well-being , 2016, Nature.

[99]  L. Fahrig,et al.  Landscape configurational heterogeneity by small-scale agriculture, not crop diversity, maintains pollinators and plant reproduction in western Europe , 2018, Proceedings of the Royal Society B: Biological Sciences.

[100]  Regina Santos,et al.  Do habitat characteristics determine mortality risk for bats at wind farms? Modelling susceptible species activity patterns and anticipating possible mortality events , 2015, Ecol. Informatics.

[101]  B. Haegeman,et al.  A general sampling formula for community structure data , 2017 .

[102]  Paulo R. Guimarães,et al.  The Robustness of Plant-Pollinator Assemblages: Linking Plant Interaction Patterns and Sensitivity to Pollinator Loss , 2015, PloS one.

[103]  J. A. Cabral,et al.  Is wind energy increasing the impact of socio-ecological change on Mediterranean mountain ecosystems? Insights from a modelling study relating wind power boost options with a declining species. , 2019, Journal of environmental management.

[104]  Lars Chittka,et al.  Recognition of flowers by pollinators. , 2006, Current opinion in plant biology.

[105]  M. Herrera,et al.  A survey of heath vegetation of the Iberian Peninsula and Northern Morocco: a biogeographic and bioclimatic approach , 2007 .

[106]  Jochen Fründ,et al.  Sampling bias is a challenge for quantifying specialization and network structure: lessons from a quantitative niche model , 2016 .

[107]  Haldre S. Rogers,et al.  Defaunation leads to interaction deficits, not interaction compensation, in an island seed dispersal network , 2018, Global change biology.

[108]  D. King,et al.  Optimizing landscape selection for estimating relative effects of landscape variables on ecological responses , 2013, Landscape Ecology.

[109]  J. Osborne,et al.  Bumble‐BEEHAVE: A systems model for exploring multifactorial causes of bumblebee decline at individual, colony, population and community level , 2018, The Journal of applied ecology.