Passively crowdsourcing images online for measuring broad-scale fly (Diptera) floral interactions and biodiversity

Authors

  • Evelyn Blakeman Ohio University
  • Aydan B. Wilson
  • Sarah Romer Ohio University
  • Emi Olin Ohio University
  • Catherine Scott McGill University
  • Viorel Popescu Ohio University
  • Bekka Brodie Columbia University

DOI:

https://doi.org/10.26786/1920-7603(2023)724

Keywords:

Data mining, photos, fly pollinator, myophily, species richness

Abstract

Flies (Diptera) represent one of the largest and most important groups of pollinators on the planet; however, little is known about the interactions between flies and flowers compared to well-known pollinators, such as bees. Understanding pollinator assemblages is key to conserving biodiversity and ecosystem services, but monitoring Diptera is time and cost intensive. Using photographs of blooming flowers taken by photographers worldwide and uploaded on internet repositories, we built a dataset of 1,275 images of fly-flower visitations and extracted fly and flower taxonomic information, flower characteristics (shape and color), and fly activity (pollen carrying and foraging). The resulting dataset shows taxonomic and other biases but can still provide an initial overview of factors that affect pollination by Diptera. We identified 22 families of flies, with blow flies (Family Calliphoridae) most represented (29%) and 63 families of flowers, with Asteraceae (42%) and Apiaceae (21%) as the most common. Using logistic regression, we found that the likelihood of flies carrying pollen was determined by the interaction between flower color and shape: pollen-carrying was more likely when elongate cluster flowers were green-yellow. Fly foraging on flowers was determined by flower color: flies were more likely to feed on green-yellow and white flowers. Overall, Syrphidae flies were less likely to forage for nectar than non-Syrphidae, but were more likely to carry pollen. While biases exist in crowdsourced data, we show that data from photographs collected through citizen science offers potentially valuable information for monitoring pollinator-flower interactions and augment our understanding of pollinator ecology in an era of global insect declines.

Author Biographies

Evelyn Blakeman, Ohio University

Department of Biological Sciences, Undergraduate Student 

Sarah Romer, Ohio University

Department of Biological Sciences, Undergraduate Student

Emi Olin, Ohio University

University College, Undergraduate Student

Catherine Scott, McGill University

Department of Natural Resource Sciences, Post doc

Viorel Popescu, Ohio University

Department of Biological Sciences, Associate Professor

Bekka Brodie, Columbia University

Ecology, Evolution, and Environmental Biology (E3B), Director of the Masters Program

References

Arnold SEJ, Savolainen V, Chittka L (2009) Flower colours along an alpine altitude gradient, seen through the eyes of fly and bee pollinators. Arthropod-Plant Interactions 3:27–43. https://doi.org/10.1007/s11829-009-9056-9 DOI: https://doi.org/10.1007/s11829-009-9056-9

Bahlai CA, Landis DA (2016) Predicting plant attractiveness to pollinators with passive crowdsourcing. Royal Society Open Science 3:150677. http://dx.doi.org/10.1098/rsos.150677 DOI: https://doi.org/10.1098/rsos.150677

Biesmeijer JC, Roberts SPM, Reemer M, Ohlemüller R, Edwards M, Peeters T, Schaffers AP, Potts SG, Kleukers R, Thomas CD, Settele J, Kunin WE. (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science (1979) 313:351-354. https://doi.org/10.1126/science.1127863 DOI: https://doi.org/10.1126/science.1127863

Blakeman E, Aydan B. Wilson, Sarah Romer, Emi Olin, Catherine E. Scott, D. Viorel Popescu, & Bekka Brodie. (2023). Data set of 1,275 images capturing interactions between flies and blooming flowers [Data set]. Zenodo. https://doi.org/10.5281/zenodo.8221822

Brodie BS, Smith MA, Lawrence J, Gries G (2015) Effects of floral scent, colour and pollen on foraging decisions and oocyte development of common green bottle flies. PLoS ONE 10(12):e0145055 https://doi.org/10.1371/journal.pone.0145055 DOI: https://doi.org/10.1371/journal.pone.0145055

Cohn JP (2008) Citizen science: Can volunteers do real research? BioScience 58(3):192-197. https://doi.org/10.1641/B580303 DOI: https://doi.org/10.1641/B580303

Cooper CB, Shirk J, Zuckerberg B (2014) The invisible prevalence of citizen science in global research: Migratory birds and climate change. PLoS ONE 9(9):e106508 https://doi.org/10.1371/journal.pone.0106508 DOI: https://doi.org/10.1371/journal.pone.0106508

Courtney GW, Pape T, Skevington JH, Sinclair BJ (2017) Biodiversity of Diptera. In: (eds) Insect Biodiversity. John Wiley & Sons, Ltd, pp 229–278. DOI: https://doi.org/10.1002/9781118945568.ch9

Doyle T, Hawkes WLS, Massy R, Powney GD, Menz MHM, Wotton KR (2020) Pollination by hoverflies in the Anthropocene: Pollination by Hoverflies. Proceedings of the Royal Society B: Biological Sciences 287: 20200508. http://dx.doi.org/10.1098/rspb.2020.0508 DOI: https://doi.org/10.1098/rspb.2020.0508

Dwivedi AK (2021) Role of digital technology in freshwater biodiversity monitoring through citizen science during COVID-19 pandemic. River Research and Applications 37:1025–1031. https://doi.org/10.1002/rra.3820 DOI: https://doi.org/10.1002/rra.3820

Eitzel M. V, Cappadonna J.L., Santos-Lang C., Duerr R.E., Virapongse A., West S.E., et al. (2017). Citizen Science Terminology Matters: Exploring Key Terms. Citizen Science: Theory and Practice 2, 1. https://doi.org/10.5334/cstp.96 DOI: https://doi.org/10.5334/cstp.113

Fink D, Damoulas T, Bruns NE, La Sorte FA, Hochachka WM, Gomes CP, Kelling S (2014) Crowdsourcing meets ecology: hemisphere wide spatiotemporal species distribution models. AI Magazine 35:19–30 DOI: https://doi.org/10.1609/aimag.v35i2.2533

Forister ML, Pelton EM, Black SH (2019) Declines in insect abundance and diversity: We know enough to act now. Conservation Science and Practice 1:e80. https://doi.org/10.1111/csp2.80 DOI: https://doi.org/10.1111/csp2.80

Fründ J, Linsenmair KE, Blüthgen N (2010) Pollinator diversity and specialization in relation to flower diversity. Oikos 119:1581–1590. https://doi.org/10.1111/j.1600-0706.2010.18450.x DOI: https://doi.org/10.1111/j.1600-0706.2010.18450.x

Gardiner MM, Allee LL, Brown PMJ, Losey JE, Roy HE, Smyth RR (2012) Lessons from lady beetles: accuracy of monitoring data from US and UK citizen-scienc programs. Frontiers in Ecology and Evolution. 10: 471–476. https://doi.org.10.1890/110185 DOI: https://doi.org/10.1890/110185

Gilbert FS (1981) Foraging ecology of hoverflies: Morphology of the mouthparts in relation to feeding on nectar and pollen in some common urban species Ecological Entomology 6:245–262 https://doi.org/10.1111/j.1365-2311.1981.tb00612.x DOI: https://doi.org/10.1111/j.1365-2311.1981.tb00612.x

Hallmann CA, Sorg M, Jongejans E, Siepel H, Hofland N, Schwan H, Stenmans W, Müller A, Sumser H, Hörren T, Goulson D, de Kroon H (2017) More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS ONE 12(10):e0185809 https://doi.org/10.1371/journal.pone.0185809 DOI: https://doi.org/10.1371/journal.pone.0185809

Hannah L, Dyer AG, Garcia JE, Dorin A, Burd M (2019) Psychophysics of the hoverfly: Categorical or continuous colour discrimination? Current Zoology 65:483–492. https://doi.org/10.1093/cz/zoz008 DOI: https://doi.org/10.1093/cz/zoz008

Heigl F., Kieslinger B., Paul K.T., Uhlik J. & Dörler D. (2019). Toward an international definition of citizen science. Proceedings of the National Academy of Sciences of the United States of America 116, 8089–8092. https://doi.org/10.1073/pnas.1903393116 DOI: https://doi.org/10.1073/pnas.1903393116

Hickman JM, Lovei GL, Wratten SD (1995) Pollen feeding by adults of the hoverfly Melanostoma faciatum (Diptera: Syrphidae). New Zealand Journal of Zoology 22: 387-392 https://doi.org/10.1080/03014223.1995.9518057 DOI: https://doi.org/10.1080/03014223.1995.9518057

Inouye, DW, BMH Larson, A Ssymank, P.G. Kevan. (2015) Flies and flowers III: Ecology of foraging and pollination. Journal of Pollination Ecology 16(16): 115-133 https://doi.org/10.26786/1920-7603(2015)15 DOI: https://doi.org/10.26786/1920-7603(2015)15

Jacobs C (2016) Data quality in crowdsourcing for biodiversity research: issues and examples. In: European Handbook of Crowdsourced Geographic Information 75 https://doi.org/10.5334/bax.f DOI: https://doi.org/10.5334/bax.f

Jersáková J, Jürgens A, Šmilauer P, Johnson SD (2012) The evolution of floral mimicry: Identifying traits that visually attract pollinators. Functional Ecology 26:1381–1389. https://doi.org/10.1111/j.1365-2435.2012.02059.x DOI: https://doi.org/10.1111/j.1365-2435.2012.02059.x

Johnston A, Fink D, Hochachka WM, Kelling S (2018) Estimates of observer expertise improve species distributions from citizen science data. Methods in Ecology and Evolution 9:88–97. https://doi.org/10.1111/2041-210X.12838 DOI: https://doi.org/10.1111/2041-210X.12838

Joly A, Goëau H, Champ J, et al (2016) Crowdsourcing biodiversity monitoring: How sharing your photo stream can sustain our planet. In: MM 2016 - Proceedings of the 2016 ACM Multimedia Conference https://doi.org/10.1145/2964284.2976762 DOI: https://doi.org/10.1145/2964284.2976762

Kearns CA (2001) North American dipteran pollinators: Assessing their value and conservation status. Ecology and Society 5(1):5. http://www.consecol.org/vol5/iss1/art5/ DOI: https://doi.org/10.5751/ES-00262-050105

Kearns CA (1992) Anthophilous Fly Distribution Across an Elevation Gradient. American Midland Naturalist 127: 172-182. https://doi.org/10.2307/2426332 DOI: https://doi.org/10.2307/2426332

Kearns CA and DW Inouye. (1994) Fly pollination of Linum lewisii (Linaceae). American Journal of Botany. 81(9): 1091-1095. https://doi.org/10.1002/j.1537-2197.1994.tb15602.x DOI: https://doi.org/10.1002/j.1537-2197.1994.tb15602.x

Klecka J, Hadrava J, Biella P, Akter A (2018) Flower visitation by hoverflies (Diptera: Syrphidae) in a temperate plant-pollinator network. PeerJ 6:e6025. https://doi.org/10.7717/peerj.6025 DOI: https://doi.org/10.7717/peerj.6025

Klinkhamer PGL, Jong TJ (1990) Effects of plant size, plant density and sex differential nectar reward on pollinator visitation in the protandrous Echium vulgare (Boraginaceae). Oikos 57: 399-405. https://doi.org/10.2307/3565970 DOI: https://doi.org/10.2307/3565970

Larson B, Kevan P, Inouye D (2001) Flies and flowers: taxonomic diversity of anthophiles and pollinators. The Canadian Entomologists 133(4): 437-465. https://doi.org/10.4039/Ent133439-4 DOI: https://doi.org/10.4039/Ent133439-4

Lüdecke et al., (2021). performance: An R Package for Assessment, Comparison and Testing of Statistical Models. Journal of Open Source Software, 6(60), 3139. https://doi.org/10.21105/joss.03139 DOI: https://doi.org/10.21105/joss.03139

Lunau K, An L, Donda M, Hohmann M, Sermon L, Stegmanns V (2018) Limitations of learning in the proboscis reflex of the flower visiting syrphid fly Eristalis tenax. PLoS ONE 13(3): e0194167. https://doi.org/10.1371/journal.pone.0194167 DOI: https://doi.org/10.1371/journal.pone.0194167

Mitra B, Banerjee D (2007) Fly pollinators: assessing thir value in biodiversity conservation and food security in India. Records of the Zoological Survey of India 107(Part-1):33-48. https://doi.org/10.26515/rzsi/v107/i1/2007/159161 DOI: https://doi.org/10.26515/rzsi/v107/i1/2007/159161

Morante J, Desplan C (2008) The Colour-Vision Circuit in the Medulla of Drosophila. Current Biology 18:553–565. https://doi.org/10.1016/j.cub.2008.02.075 DOI: https://doi.org/10.1016/j.cub.2008.02.075

Motten AF, Campbell DR, Alexander DE, Miller HL (1981) Pollination effectiveness of specialist and generalist visitors to a North Carolina population of Claytonia virginiaca1. Ecology. 62(5) 1278-1287. https://doi.org/10.2307/1937292 DOI: https://doi.org/10.2307/1937292

Nguyen TTN, Le TL, Vu H, Hoang V, Tran T (2018) Crowdsourcing for botanical data collection towards to automatic plant identification: A review. Computers and Electronics in Agriculture 155:412–425. https://doi.org/10.1016/j.compag.2018.10.042 DOI: https://doi.org/10.1016/j.compag.2018.10.042

Niering WA, Olmstead NC (1979) The Audubon Society Field Guide to North American wildflowers (Eastern Region). Knopf, New York

Orford KA, Vaughan IP, Memmott J (2015) The forgotten flies: The importance of non-syrphid Diptera as pollinators. Proceedings of the Royal Society B: Biological Sciences 282:20142934. https://doi.org/10.1098/rspb.2014.2934 DOI: https://doi.org/10.1098/rspb.2014.2934

Peach DA, Gries G (2020). Mosquito phytophagy–sources exploited, ecological function, and evolutionary transition to haematophagy. Entomologia Experimentalis et Applicata 168(2): 120-136. https://doi.org/10.1111/eea.12852 DOI: https://doi.org/10.1111/eea.12852

Pocock MJO, Roy HE, Preston CD, Roy DB (2015) The Biological Records Centre: a pioneer of citizen science. Biological Journal of the Linnean Society 115(3):475-497. https://doi.org/10.1111/bij.12548 DOI: https://doi.org/10.1111/bij.12548

Potts SG, Biesmeijer JC, Kremen C, et al (2010) Global pollinator declines: Trends, impacts and drivers. Trends in Ecology and Evolution 25:345–353. https://doi.org/10.1016/j.tree.2010.01.007 DOI: https://doi.org/10.1016/j.tree.2010.01.007

Powney GD, Carvell C, Edwards M, Morris RKA, Roy HE, Woodcock BA, Isaac NJB (2019) Widespread losses of pollinating insects in Britain. Nature Communications 10:1018. https://doi.org/10.1038/s41467-019-08974-9 DOI: https://doi.org/10.1038/s41467-019-08974-9

R Core Team (2017). R: A language and environment for statistical computing. https://www.r-project.org/

Rader R, Bartomeus I, Garibaldi LA, Woyciechowski M (2016) Non-bee insects are important contributors to global crop pollination. Proceedings of the National Academy of Sciences 113(1):146–151. https://doi.org/10.1073/pnas.1517092112 DOI: https://doi.org/10.1073/pnas.1517092112

Rader R, Howlett BG, Cunningham SA, Westcott DA, Newstrom-Lloyd LE, Walker MK, Teulon DAJ, Edwards W (2009) Alternative pollinator taxa are equally efficient but not as effective as the honeybee in a mass flowering crop. Journal of Applied Ecology 46:1080–1087. https://doi.org/10.1111/j.1365-2664.2009.01700.x DOI: https://doi.org/10.1111/j.1365-2664.2009.01700.x

Raguso RA (2020) Don’t forget the flies: dipteran diversity and its consequences for floral ecology and evolution. Applied Entomology and Zoology 55:1-7. https://doi.org/10.1007/s13355-020-00668-9 DOI: https://doi.org/10.1007/s13355-020-00668-9

Rhodes CJ (2018) Pollinator decline – An ecological calamity in the making? Science Progress 101:121–160. https://doi.org/10.3184/003685018X15202512854527 DOI: https://doi.org/10.3184/003685018X15202512854527

Sánchez-Clavijo LM, Martínez-Callejas SJ, Acevedo-Charry O, Diaz-Pulido A, Gómez-Valencia B, Ocampo-Peñuela N, Ocampo D, Olaya-Rodríguez MH, Rey-Velasco JC, Soto-Vargas C, Ochoa-Quintero JM. Differential reporting of biodiversity in two citizen science platforms during COVID-19 lockdown in Colombia. Biological Conservation. 2021 256:109077. https://doi.org/10.1016/j.biocon.2021.109077 DOI: https://doi.org/10.1016/j.biocon.2021.109077

Sauermann H, Franzoni C (2015) Crowd science user contribution patterns and their implications. Proceedings of the National Academy of Sciences. https://doi.org/10.1073/pnas.1408907112 DOI: https://doi.org/10.1073/pnas.1408907112

Show H (2015) Rise of the citizen scientist. Nature. 524(7565): 265. https://doi.org/10.1038/524265a DOI: https://doi.org/10.1038/524265a

Silvertown J (2009) A new dawn for citizen science. Trends in Ecology and Evolution 24(9):467–471. https://doi.org/10.1016/j.tree.2009.03.017 DOI: https://doi.org/10.1016/j.tree.2009.03.017

Skevington JH, Dang PT (2002) Exploring the diversity of flies (Diptera). Biodiversity 3:3–27. https://doi.org/10.1080/14888386.2002.9712613 DOI: https://doi.org/10.1080/14888386.2002.9712613

Skevington JH (2019) Field guide to the flower flies of Northeastern North America. Princeton University Press, Princeton

Terry JCD, Roy HE, August TA (2020) Thinking like a naturalist: Enhancing computer vision of citizen science images by harnessing contextual data. Methods in Ecology and Evolution 11:303–315. https://doi.org/10.1111/2041-210X.13335 DOI: https://doi.org/10.1111/2041-210X.13335

Toivonen M, Karimaa AE, Herzon I, Kuussaari M (2022) Flies are important pollinators of mass-flowering caraway and respond to landscape and floral factors differently from honeybees. Agriculture, Ecosystems and Environment 323: 107698. https://doi.org/10.1016/j.agee.2021.107698 DOI: https://doi.org/10.1016/j.agee.2021.107698

Torney CJ, Lloyd-Jones DJ, Chevallier M, Moyer DC, Maliti HT, Mwita M, Kohi EM, Hopcraft GC (2019) A comparison of deep learning and citizen science techniques for counting wildlife in aerial survey images. Methods in Ecology and Evolution 10:779–787. https://doi.org/10.1111/2041-210X.13165 DOI: https://doi.org/10.1111/2041-210X.13165

Troje NF (1993) Spectral Categories in the Learning Behaviour of Blowflies. Zeitschrift für Naturforschung C 48: 104 - 96. https://doi.org/10.1515/znc-1993-1-218 DOI: https://doi.org/10.1515/znc-1993-1-218

Trouille L, Lintott CJ, Fortson LF (2019) Citizen science frontiers: Efficiency, engagement, and serendipitous discovery with human-machine systems. Proceedings of the National Academy of Sciences 116:1902–1909. https://doi.org/10.1073/pnas.1807190116 DOI: https://doi.org/10.1073/pnas.1807190116

van der Niet T, Hansen DM, Johnson SD (2011). Carrion mimicry in a South African orchid: flowers attract a narrow subset of the fly assemblage on animal carcasses. Annals of Botany 107(6):981-992. https://doi.org/10.1093/aob/mcr048 DOI: https://doi.org/10.1093/aob/mcr048

Van Horn G, mac Aodha O, Song Y, Cui Y, Sun C, Shepard A, Adam H, Perona P, Belongie S (2017) The iNaturalist Species Classification and Detection Dataset. Proceedings of the IEEE conference on computer vision and pattern recognition: pp. 8769-8778) https://doi.org/10.1109/CVPR.2018.00914 DOI: https://doi.org/10.1109/CVPR.2018.00914

Vanbergen AJ (2013) Insect Pollinators Initiative. Threats to an ecosystem service: Pressures on pollinators. Frontiers in Ecology and the Environment 11:251–259. https://doi.org/10.1890/120126 DOI: https://doi.org/10.1890/120126

Vaudo AD, Tooker JF, Grozinger CM, Patch HM (2015) Bee nutrition and floral resource restoration. Current Opinion in Insect Science.10:133-141. https://doi.org/10.1016/j.cois.2015.05.008 DOI: https://doi.org/10.1016/j.cois.2015.05.008

Wacht S, Lunau K, Hansen K (2000) Chemosensory control of pollen ingestion in the hoverfly Eristalis tenax by labellar taste hairs. Journal of Comparative Physiology A 186: 193-203. https://doi.org/10.1007/s003590050019 DOI: https://doi.org/10.1007/s003590050019

Wagner D, Grames E, Forister M, Berenbaum M, Stopak D (2021) Insect decline in the Anthropocene: Death by a thousand cuts. Proceedings of the National Academy of Sciences 118(2):e2023989118. https://doi.org/10.1073/PNAS.2023989118 DOI: https://doi.org/10.1073/pnas.2023989118

Willi M, Pitman RT, Cardoso AW, Locke C, Swanson A, Boyer A, Veldthuis M, Fortson L (2019) Identifying animal species in camera trap images using deep learning and citizen science. Methods in Ecology and Evolution 10:80–91. https://doi.org/10.1111/2041-210X.13099 DOI: https://doi.org/10.1111/2041-210X.13099

Woodcock TS, Larson BMH, Kevan PG, Inouye DW, Lunau K (2014) Flies and Flowers II: Floral attractants and rewards. Journal of Pollination Ecology 12: 63-94. https://doi.org/10.26786/1920-7603(2014)5 DOI: https://doi.org/10.26786/1920-7603(2014)5

Woodard S, Federman S, James R, Danforth B, Griswold T, Inouye D, McFederick Q, Morandin L, Paul D, Sellers E, Strange J, Vaughan M, Williams N, Branstetter M, Burns C, Cane J, Cariveau A, Cariveau D, Childers A, Childers C, Cox-Foster D, Evans E, Graham K, Hackett K, Huntzinger K, Irwin R, Jha S, Lawson S.Liang C, López-Uribe M, Melathopoulos A, Moyett H, Otto C, Ponisio L, Richardson L, Rose R, Singh R, Wehling W (2020) Towards a U.S. national program for monitoring native bees. Biological Conservation. 252: 108821. https://doi.org/10.1016/j.biocon.2020.108821 DOI: https://doi.org/10.1016/j.biocon.2020.108821

Additional Files

Published

2023-09-08

How to Cite

Blakeman, E., Wilson , A. B., Romer, S., Olin, E., Scott, C., Popescu, V., & Brodie, B. (2023). Passively crowdsourcing images online for measuring broad-scale fly (Diptera) floral interactions and biodiversity. Journal of Pollination Ecology, 35, 180–193. https://doi.org/10.26786/1920-7603(2023)724

Issue

Section

Articles

Similar Articles

1 2 3 4 5 6 7 8 9 10 > >> 

You may also start an advanced similarity search for this article.