Camera-trap monitoring reveals flower visitor diversity and diel activity patterns in the forest understory: bramble patches (Rubus fruticosus agg.) as a model system

Louise Bonneau-Chloup; Cécile Hignard; Baptiste Lemaire; Sophie Pasek; Sylvie Meyer; Laurence Walch

doi:10.26786/1920-7603(2026)940

Authors

Louise Bonneau-Chloup https://orcid.org/0009-0006-0302-4149
Cécile Hignard
Baptiste Lemaire
Sophie Pasek https://orcid.org/0009-0005-4701-7592
Sylvie Meyer
Laurence Walch CNRS https://orcid.org/0009-0004-3093-731X

DOI:

https://doi.org/10.26786/1920-7603(2026)940

Keywords:

floral visitor community, temperate forest, temproal niches, microclimate, video monitoring, Rubus

Abstract

Pollinator communities in deciduous temperate forest understories remain poorly understood, particularly regarding the relative roles of temporal activity patterns and microclimatic conditions in structuring flower visitor assemblages. We developed a non-invasive video monitoring system to investigate flower visitor communities on brambles (Rubus fruticosus agg.) across four forest patches in the Fontainebleau forest (Île-de-France, France), recording 3,636 visits from 17 morphotype groups during 369 hours. Ants dominated visits (45%), followed by non-syrphid flies (10%), whereas bees, hoverflies, and Lepidoptera together accounted for 32%. Visitor assemblages exhibited substantial spatial and temporal variation, with evidence of temporal niche partitioning. Generalized additive mixed models (GAMMs) revealed taxon-specific diurnal activity patterns, with most taxa peaking during late morning to afternoon (10:00–18:00), though ants showed crepuscular activity and some groups including non-syrphid flies and hoverflies displayed bimodal distributions in certain patches. Nocturnal activity was observed for several taxa. Microclimatic effects on visitor occurrence were taxon-specific and limited: non-syrphid flies and ants responded negatively to light intensity. In addition, non-syrphid flies and hoverflies showed shorter visit durations under higher light intensity, and non-syrphid flies additionally showed temperature-dependent foraging behavior, reducing visit duration by 57% per 10°C increase. Visit duration varied markedly among taxa, ranging from a few seconds in bumblebees and hoverflies to over an hour in some Coleoptera and Orthoptera. These findings reveal that forest flower visitors partition temporal niches more strongly than microclimatic niches. This non-lethal monitoring approach successfully captured complex ecological patterns, demonstrating brambles' potential as a model system for forest pollination ecology while preserving natural environmental contexts and enabling continuous day-night observations.

References

Alison J, Botham M, Maskell LC, Garbutt A, Seaton FM, Skates J, Smart SM, Thomas ARC, Tordoff G, Williams BL, Wood CM, Emmett BA (2022) Woodland, cropland and hedgerows promote pollinator abundance in intensive grassland landscapes, with saturating benefits of flower cover. Journal of Applied Ecology 59:342–354. DOI: https://doi.org/10.1111/1365-2664.14058

Anderson M, Rotheray EL, Mathews F (2023) Marvellous moths! pollen deposition rate of bramble (Rubus futicosus L. agg.) is greater at night than day Del-Claro K (ed). PLOS ONE 18:e0281810. DOI: https://doi.org/10.1371/journal.pone.0281810

Bailey S, Requier F, Nusillard B, Roberts SPM, Potts SG, Bouget C (2014) Distance from forest edge affects bee pollinators in oilseed rape fields. Ecology and Evolution 4:370–380. DOI: https://doi.org/10.1002/ece3.924

Barragán‐Fonseca KY, Van Loon JJA, Dicke M, Lucas‐Barbosa D (2020) Use of visual and olfactory cues of flowers of two brassicaceous species by insect pollinators. Ecological Entomology 45:45–55. DOI: https://doi.org/10.1111/een.12775

Barrett M, Fischer B (2024) Ethical issues in lethal insect monitoring. Current Opinion in Insect Science 66:101279. DOI: https://doi.org/10.1016/j.cois.2024.101279

Bartholomée O, Jie VW, Caplat P, Smith HG, Baird E (2025) Warm or bright – Temperature and light microhabitat use in insect pollinators. Ecological Entomology 50:853–864. DOI: https://doi.org/10.1111/een.13452

Bates D, Mächler M, Bolker B, Walker S (2015) Fitting Linear Mixed-Effects Models Using lme4. Journal of Statistical Software 67 [online] URL: http://www.jstatsoft.org/v67/i01/ (accessed 17 October 2025). DOI: https://doi.org/10.18637/jss.v067.i01

Baude M, Kunin WE, Boatman ND, Conyers S, Davies N, Gillespie MAK, Morton RD, Smart SM, Memmott J (2016) Historical nectar assessment reveals the fall and rise of floral resources in Britain. Nature 530:85–88. DOI: https://doi.org/10.1038/nature16532

Beattie AJ (1971) Itinerant pollinators in a forest. West American journal of botany 21:120–124.

Beattie AJ, Turnbull C, Knox RB, Williams EG (1984) Ant inhibition of pollen function: a possible reason why ant pollination is rare. American Journal of Botany 71:421–426. DOI: https://doi.org/10.1002/j.1537-2197.1984.tb12527.x

Bjerge K, Mann HMR, Høye TT (2022) Real‐time insect tracking and monitoring with computer vision and deep learning Sankey T, Ahumada J (eds). Remote Sensing in Ecology and Conservation 8:315–327. DOI: https://doi.org/10.1002/rse2.245

Blareau E, Gabard C, Riva C, Dajoz I, Requier F (2025) Automated 24-h surveys of flower-visiting communities reveal temporal complementarities and overlaps among strawberry pollinators. Global Ecology and Conservation 62:e03727. DOI: https://doi.org/10.1016/j.gecco.2025.e03727

Bloch G, Bar-Shai N, Cytter Y, Green R (2017) Time is honey: circadian clocks of bees and flowers and how their interactions may influence ecological communities. Philosophical Transactions of the Royal Society B: Biological Sciences 372:20160256. DOI: https://doi.org/10.1098/rstb.2016.0256

Blüthgen N, Klein A-M (2011) Functional complementarity and specialisation: The role of biodiversity in plant–pollinator interactions. Basic and Applied Ecology 12:282–291. DOI: https://doi.org/10.1016/j.baae.2010.11.001

Boulanger‐Lapointe N, Järvinen A, Partanen R, Herrmann TM (2017) Climate and herbivore influence on Vaccinium myrtillus over the last 40 years in northwest Lapland, Finland. Ecosphere 8:e01654. DOI: https://doi.org/10.1002/ecs2.1654

Brown AO, McNeil JN (2009) Pollination ecology of the high latitude, dioecious cloudberry ( Rubus chamaemorus ; Rosaceae). American Journal of Botany 96:1096–1107. DOI: https://doi.org/10.3732/ajb.0800102

Carvalheiro LG, Barbosa ERM, Memmott J (2008) Pollinator networks, alien species and the conservation of rare plants: Trinia glauca as a case study. Journal of Applied Ecology 45:1419–1427. DOI: https://doi.org/10.1111/j.1365-2664.2008.01518.x

Corbet SA, Saville NM, Fussell M, Prys-Jones OE, Unwin DM (1995) The Competition Box: A Graphical Aid to Forecasting Pollinator Performance. The Journal of Applied Ecology 32:707. DOI: https://doi.org/10.2307/2404810

Díaz‐Calafat J, Öckinger E, Felton A, Frenne PD, Cousins SAO, Uria‐Diez J, Hedwall P (2026) Fly pollinator foraging in boreal forests is shaped by climate, forest structure and flower resources. Oikos 2026:e11405. DOI: https://doi.org/10.1002/oik.11405

Eckerter T, Buse J, Förschler M, Pufal G (2019) Additive positive effects of canopy openness on European bilberry (Vaccinium myrtillus) fruit quantity and quality. Forest Ecology and Management 433:122–130. DOI: https://doi.org/10.1016/j.foreco.2018.10.059

Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination Syndromes and Floral Specialization. Annual Review of Ecology, Evolution, and Systematics 35:375–403. DOI: https://doi.org/10.1146/annurev.ecolsys.34.011802.132347

Fründ J, Dormann CF, Holzschuh A, Tscharntke T (2013) Bee diversity effects on pollination depend on functional complementarity and niche shifts. Ecology 94:2042–2054. DOI: https://doi.org/10.1890/12-1620.1

Garibaldi LA, Steffan-Dewenter I, Winfree R, Aizen MA, Bommarco R, Cunningham SA, Kremen C, Carvalheiro LG, Harder LD, Afik O, Bartomeus I, Benjamin F, Boreux V, Cariveau D, Chacoff NP, Dudenhöffer JH, Freitas BM, Ghazoul J, Greenleaf S, Hipólito J, Holzschuh A, Howlett B, Isaacs R, Javorek SK, Kennedy CM, Krewenka KM, Krishnan S, Mandelik Y, Mayfield MM, Motzke I, Munyuli T, Nault BA, Otieno M, Petersen J, Pisanty G, Potts SG, Rader R, Ricketts TH, Rundlöf M, Seymour CL, Schüepp C, Szentgyörgyi H, Taki H, Tscharntke T, Vergara CH, Viana BF, Wanger TC, Westphal C, Williams N, Klein AM (2013) Wild Pollinators Enhance Fruit Set of Crops Regardless of Honey Bee Abundance. Science 339:1608–1611. DOI: https://doi.org/10.1126/science.1230200

Goulard R, Julien-Laferriere A, Fleuriet J, Vercher J-L, Viollet S (2015) Behavioural evidence for a visual and proprioceptive control of head roll in hoverflies ( Episyrphus balteatus , Dipteran). Journal of Experimental Biology:jeb.127043. DOI: https://doi.org/10.1242/jeb.127043

Gyan KY, Woodell SRJ (1987a) Analysis of Insect Pollen Loads and Pollination Efficiency of Some Common Insect Visitors of Four Species of Woody Rosaceae. Functional Ecology 1:269. DOI: https://doi.org/10.2307/2389430

Gyan KY, Woodell SRJ (1987b) Nectar Production, Sugar Content, Amino Acids and Potassium in Prunus spinosa L., Crataegus monogyna Jacq. and Rubus fruticosus L. at Wytham, Oxfordshire. Functional Ecology 1:251. DOI: https://doi.org/10.2307/2389428

Hartig F (2024) DHARMa: Residual Diagnostics for Hierarchical (Multi-Level / Mixed) Regression Models. [online] URL: https://CRAN.R-project.org/package=DHARMa

Herrera CM (1995) Microclimate and Individual Variation in Pollinators: Flowering Plants are More than Their Flowers. Ecology 76:1516–1524. DOI: https://doi.org/10.2307/1938153

Herrera CM (1997) Thermal Biology and Foraging Responses of Insect Pollinators to the Forest Floor Irradiance Mosaic. Oikos 78:601. DOI: https://doi.org/10.2307/3545623

Hofmann MM, Fleischmann A, Renner SS (2020) Foraging distances in six species of solitary bees with body lengths of 6 to 15 mm, inferred from individual tagging, suggest 150 m-rule-of-thumb for flower strip distances. Journal of Hymenoptera Research 77:105–117. DOI: https://doi.org/10.3897/jhr.77.51182

Houlihan PR, Stone M, Clem SE, Owen M, Emmel TC (2019) Pollination ecology of the ghost orchid (Dendrophylax lindenii): A first description with new hypotheses for Darwin’s orchids. Scientific Reports 9:12850. DOI: https://doi.org/10.1038/s41598-019-49387-4

Høye TT, Montagna M, Oteman B, Roy DB (2025) Emerging technologies for pollinator monitoring. Current Opinion in Insect Science 69:101367. DOI: https://doi.org/10.1016/j.cois.2025.101367

Jacobson MM, Pilkey HC (2024) Flower-Visiting Insects of American Chestnut Orchards in New York, and First Contemporary State Record of Andrena rehni Viereck. Northeastern Naturalist 31 [online] URL: https://bioone.org/journals/northeastern-naturalist/volume-31/issue-3/045.031.0305/Flower-Visiting-Insects-of-American-Chestnut-Orchards-in-New-York/10.1656/045.031.0305.full (accessed 3 December 2025). DOI: https://doi.org/10.1656/045.031.0305

Kremen C, Williams NM, Thorp RW (2002) Crop pollination from native bees at risk from agricultural intensification. Proceedings of the National Academy of Sciences 99:16812–16816. DOI: https://doi.org/10.1073/pnas.262413599

Kudo G, Ida TY, Tani T (2008) Linkages between phenology, pollination, photosynthesis, and reproduction in deciduous forest understory plants. Ecology 89:321–331. DOI: https://doi.org/10.1890/06-2131.1

Larue C, Austruy E, Basset G, Petit RJ (2021) Revisiting pollination mode in chestnut ( Castanea spp .): an integrated approach. Botany Letters 168:348–372. DOI: https://doi.org/10.1080/23818107.2021.1872041

Mildner S, Roces F (2017) Plasticity of Daily Behavioral Rhythms in Foragers and Nurses of the Ant Camponotus rufipes: Influence of Social Context and Feeding Times Yamazaki S (ed). PLOS ONE 12:e0169244. DOI: https://doi.org/10.1371/journal.pone.0169244

Miner MC, Wilson Rankin EE (2025) Bees modulate behavior during nectar foraging in response to direct ant aggression (Hymenoptera: Apidae and Formicidae) Roeder K (ed). Journal of Insect Science 25:ieaf076. DOI: https://doi.org/10.1093/jisesa/ieaf076

Mola JM, Hemberger J, Kochanski J, Richardson LL, Pearse IS (2021) The Importance of Forests in Bumble Bee Biology and Conservation. BioScience 71:1234–1248. DOI: https://doi.org/10.1093/biosci/biab121

Motten AF (1986) Pollination Ecology of the Spring Wildflower Community of a Temperate Deciduous Forest. Ecological Monographs 56:21–42. DOI: https://doi.org/10.2307/2937269

Narendra A, Reid SF, Hemmi JM (2010) The twilight zone: ambient light levels trigger activity in primitive ants. Proceedings of the Royal Society B: Biological Sciences 277:1531–1538. DOI: https://doi.org/10.1098/rspb.2009.2324

Neuschulz EL, Mueller T, Schleuning M, Böhning-Gaese K (2016) Pollination and seed dispersal are the most threatened processes of plant regeneration. Scientific Reports 6:29839. DOI: https://doi.org/10.1038/srep29839

Nybom H (1985) Active self‐pollination in blackberries (Rubus subgen. Rubus, Rosaceae). Nordic Journal of Botany 5:521–525. DOI: https://doi.org/10.1111/j.1756-1051.1985.tb01689.x

Osborne JL, Martin AP, Carreck NL, Swain JL, Knight ME, Goulson D, Hale RJ, Sanderson RA (2008) Bumblebee flight distances in relation to the forage landscape. Journal of Animal Ecology 77:406–415. DOI: https://doi.org/10.1111/j.1365-2656.2007.01333.x

Percival MS (1946) Observations on the flowering and nectar secretion of Rubus fructicosus (Agg.). New Phytologist 45:111–123. DOI: https://doi.org/10.1111/j.1469-8137.1946.tb05048.x

Proctor E, Nol E, Burke D, Crins WJ (2012) Responses of insect pollinators and understory plants to silviculture in northern hardwood forests. Biodiversity and Conservation 21:1703–1740. DOI: https://doi.org/10.1007/s10531-012-0272-8

Proctor M, Yeo P, Lack A (1996) The natural history of pollination, 1. publ. HarperCollin, London.

R Core Team (2023) R: A Language and Environment for Statistical Computing., R Foundation for Statistical Computing.

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. DOI: https://doi.org/10.1007/s13355-020-00668-9

Requier F, Leonhardt SD (2020) Beyond flowers: including non-floral resources in bee conservation schemes. Journal of Insect Conservation 24:5–16. DOI: https://doi.org/10.1007/s10841-019-00206-1

Ridout MS, Linkie M (2009) Estimating overlap of daily activity patterns from camera trap data. Journal of Agricultural, Biological, and Environmental Statistics 14:322–337. DOI: https://doi.org/10.1198/jabes.2009.08038

Rostás M, Bollmann F, Saville D, Riedel M (2018) Ants contribute to pollination but not to reproduction in a rare calcareous grassland forb. PeerJ 6:e4369. DOI: https://doi.org/10.7717/peerj.4369

Saunders ME (2018) Insect pollinators collect pollen from wind‐pollinated plants: implications for pollination ecology and sustainable agriculture Packer L (ed). Insect Conservation and Diversity 11:13–31. DOI: https://doi.org/10.1111/icad.12243

Schaffer WM, Zeh DW, Buchmann SL, Kleinhans S, Schaffer MV, Antrim J (1983) Competition for Nectar between Introduced Honey Bees and Native North American Bees and Ants. Ecology 64:564–577. DOI: https://doi.org/10.2307/1939976

Schürch S, Pfunder M, Roy BA (2000) Effects of ants on the reproductive success of Euphorbia cyparissias and associated pathogenic rust fungi. Oikos 88:6–12. DOI: https://doi.org/10.1034/j.1600-0706.2000.880102.x

Serra‐Marin PE, Solé‐Ribalta A, Lana A, Borge‐Holthoefer J, Hervías‐Parejo S, Traveset A (2025) Comparative assessment of automated and manual monitoring in comprehensive plant–pollinator communities. Methods in Ecology and Evolution 16:2960–2978. DOI: https://doi.org/10.1111/2041-210X.70165

Sochor M, Vašut RJ, Sharbel TF, Trávníček B (2015) How just a few makes a lot: Speciation via reticulation and apomixis on example of European brambles (Rubus subgen. Rubus, Rosaceae). Molecular Phylogenetics and Evolution 89:13–27. DOI: https://doi.org/10.1016/j.ympev.2015.04.007

Ștefan V, Workman A, Cobain JC, Rakosy D, Knight TM (2025) Utilising affordable smartphones and open-source time-lapse photography for pollinator image collection and annotation. Journal of Pollination Ecology 38:1–21. DOI: https://doi.org/10.26786/1920-7603(2025)778

Ulyshen M, Urban‐Mead KR, Dorey JB, Rivers JW (2023) Forests are critically important to global pollinator diversity and enhance pollination in adjacent crops. Biological Reviews 98:1118–1141. DOI: https://doi.org/10.1111/brv.12947

Urban-Mead KR, Muñiz P, Gillung J, Espinoza A, Fordyce R, Van Dyke M, McArt SH, Danforth BN (2021) Bees in the trees: Diverse spring fauna in temperate forest edge canopies. Forest Ecology and Management 482:118903. DOI: https://doi.org/10.1016/j.foreco.2020.118903

Urban‐Mead KR, Van Dyke M, Muñiz P, Young AD, Danforth BN, McArt SH (2023) Early spring orchard pollinators spill over from resource‐rich adjacent forest patches. Journal of Applied Ecology 60:553–564. DOI: https://doi.org/10.1111/1365-2664.14350

Van Klink R, August T, Bas Y, Bodesheim P, Bonn A, Fossøy F, Høye TT, Jongejans E, Menz MHM, Miraldo A, Roslin T, Roy HE, Ruczyński I, Schigel D, Schäffler L, Sheard JK, Svenningsen C, Tschan GF, Wäldchen J, Zizka VMA, Åström J, Bowler DE (2022) Emerging technologies revolutionise insect ecology and monitoring. Trends in Ecology & Evolution 37:872–885. DOI: https://doi.org/10.1016/j.tree.2022.06.001

Van Klink R, Bowler DE, Gongalsky KB, Swengel AB, Gentile A, Chase JM (2020) Meta-analysis reveals declines in terrestrial but increases in freshwater insect abundances. Science 368:417–420. DOI: https://doi.org/10.1126/science.aax9931

Vicens N, Bosch J (2000) Weather-Dependent Pollinator Activity in an Apple Orchard, with Special Reference to Osmia cornuta and Apis mellifera (Hymenoptera: Megachilidae and Apidae). Environmental Entomology 29:413–420. DOI: https://doi.org/10.1603/0046-225X-29.3.413

Visscher PK, Seeley TD (1982) Foraging Strategy of Honeybee Colonies in a Temperate Deciduous Forest. Ecology 63:1790. DOI: https://doi.org/10.2307/1940121

Walther-Hellwig K, Frankl R (2000) Foraging Distances of Bombus muscorum, Bombus lapidarius, and Bombus terrestris (Hymenoptera, Apidae). Journal of Insect Behavior 13:239–246. DOI: https://doi.org/10.1023/A:1007740315207

Wignall VR, Arscott NA, Nudds HE, Squire A, Green TO, Ratnieks FLW (2020) Thug life: bramble ( Rubus fruticosus L. agg.) is a valuable foraging resource for honeybees and diverse flower‐visiting insects. Insect Conservation and Diversity 13:543–557. DOI: https://doi.org/10.1111/icad.12436

Willmer PG (1983) Thermal constraints on activity patterns in nectar‐feeding insects. Ecological Entomology 8:455–469. DOI: https://doi.org/10.1111/j.1365-2311.1983.tb00524.x

Wood SN (2011) Fast Stable Restricted Maximum Likelihood and Marginal Likelihood Estimation of Semiparametric Generalized Linear Models. Journal of the Royal Statistical Society Series B: Statistical Methodology 73:3–36. DOI: https://doi.org/10.1111/j.1467-9868.2010.00749.x

Żmihorski M, Ślipiński P (2016) The importance of diurnal and nocturnal activity and interspecific interactions for space use by ants in clear‐cuts. Ecological Entomology 41:276–283. DOI: https://doi.org/10.1111/een.12297