Pollinator dependence and pollination deficit in Hedera helix, and effects on frugivore feeding choices

Pollination and frugivory in ivy Hedera helix





Pollinator dependence, Pollination deficit, Ivy, Hedera Helix, Frugivory


English ivy (Hedera helix) is an important resource for wildlife in rural and urban ecosystems. It provides pollen and nectar for flower-visiting insects during autumn and fruits for frugivores during winter and spring. A requirement of insect pollination for fruit set in ivy implies that recent declines in pollinator populations can threaten food supply for frugivores. This study investigated the link between pollination services and the quantity and quality of fruit produced in ivy, and how that could in turn influence frugivore feeding choices, in a mixed woodland and an urban garden habitat respectively. Surveys on pollinator community and activity were conducted to assess the overall level of pollination. A set of experiments involving insect exclusion, open pollination, and extra pollen supplementation was performed to reveal the level of pollinator dependence and pollination deficit in ivy. Additionally, the removal of these fruits by frugivores was measured to test whether frugivore feeding preferences are influenced by the initial level of pollination. Our results showed that the quantity and quality (size) of fruit produced in ivy were significantly reduced under insect exclusion, which is strong evidence for pollinator dependence. Pollination deficit was also identified at both sites. Furthermore, the data indicate that frugivores can display some degree of preference for well-pollinated ivy fruits. Taken together, our study shows that declines in pollination services will have direct impacts on the availability and quality of ivy fruits for frugivores. Maintaining the health of pollinator communities in both urban and rural habitats could therefore ensure healthy ecosystem functioning.


Abrol DP, Gorka AK, Ansari MJ, Al-Ghamdi A, Al-Kahtani S (2019) Impact of insect pollinators on yield and fruit quality of strawberry. Saudi Journal of Biological Sciences 26:524–530. https://doi.org/10.1016/j.sjbs.2017.08.003

Baldock KCR, Goddard MA, Hicks DM, Kunin WE, Mitschunas N, Morse H, Osgathorpe LM, Potts SG, Robertson KM, Scott A V., Staniczenko PPA, Stone GN, Vaughan IP, Memmott J (2019) A systems approach reveals urban pollinator hotspots and conservation opportunities. Nature Ecology and Evolution 3:363–373. https://doi.org/10.1038/s41559-018-0769-y

Baldock KCR, Goddard MA, Hicks DM, Kunin WE, Mitschunas N, Osgathorpe LM, Potts SG, Robertson KM, Scott A V., Stone GN, Vaughan IP, Memmott J (2015) Where is the UK’s pollinator biodiversity? The importance of urban areas for flower-visiting insects. Proceedings of the Royal Society B: Biological Sciences 282:20142849. https://doi.org/10.1098/rspb.2014.2849

Bates AJ, Sadler JP, Fairbrass AJ, Falk SJ, Hale JD, Matthews TJ (2011) Changing Bee and Hoverfly Pollinator Assemblages along an Urban-Rural Gradient Stout JC (ed). PLoS ONE 6:e23459. https://doi.org/10.1371/journal.pone.0023459

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 313:351–354. https://doi.org/10.1126/science.1127863

Bonier F, Martin PR, Wingfield JC (2007) Urban birds have broader environmental tolerance. Biology Letters 3:670–673. https://doi.org/10.1098/rsbl.2007.0349

Bottema S (2001) A note on the pollen representation of ivy (Hedera helix L.). Review of Palaeobotany and Palynology 117:159–166. https://doi.org/10.1016/S0034-6667(01)00084-7

Buchmann SL, Nabhan GP (1997) The forgotten pollinators. Island Press.

Callaghan CT, Major RE, Lyons MB, Martin JM, Kingsford RT (2018) The effects of local and landscape habitat attributes on bird diversity in urban greenspaces. Ecosphere 9:e02347. ttps://doi.org/10.1002/ecs2.2347

Cambridge University Botanic Garden (2021) About the Garden. Cambridge University Botanic Garden Website [online] URL: https://www.botanic.cam.ac.uk/the-garden/about-the-garden/ (accessed 9 April 2022).

Cariveau DP, Winfree R (2015) Causes of variation in wild bee responses to anthropogenic drivers. Current Opinion in Insect Science 10:104–109. https://doi.org/10.1016/j.cois.2015.05.004

Chace JF, Walsh JJ (2006) Urban effects on native avifauna: a review. Landscape and Urban Planning 74:46–69. https://doi.org/10.1016/j.landurbplan.2004.08.007

Clark JR (1983) Age-related changes in trees. J. Arboriculture 9:201–205. https://doi.org/10.48044/jauf.1983.050

Concepción ED, Moretti M, Altermatt F, Nobis MP, Obrist MK (2015) Impacts of urbanisation on biodiversity: the role of species mobility, degree of specialisation and spatial scale. Oikos 124:1571–1582. https://onlinelibrary.wiley.com/doi/10.1111/oik.02166

Crall JD, Brokaw J, Gagliardi SF, Mendenhall CD, Pierce NE, Combes SA (2020) Wind drives temporal variation in pollinator visitation in a fragmented tropical forest. Biology Letters 16:20200103. https://doi.org/10.1098/rsbl.2020.0103

Daniels B, Jedamski J, Ottermanns R, Ross-Nickoll M (2020) A “plan bee” for cities: Pollinator diversity and plant-pollinator interactions in urban green spaces Dyer AG (ed). PLOS ONE 15:e0235492. https://doi.org/10.1371/journal.pone.0235492

Dung CD, Wallace HM, Bai SH, Ogbourne SM, Trueman SJ (2021) Cross-pollination affects fruit colour, acidity, firmness and shelf life of self-compatible strawberry Borges RM (ed). PLOS ONE 16:e0256964. https://doi.org/10.1371/journal.pone.0256964

Evans KL, Chamberlain DE, Hatchwell BJ, Gregory RD, Gaston KJ (2011) What makes an urban bird? Global Change Biology 17:32–44. https://doi.org/10.1111/j.1365-2486.2010.02247.x

Fenoglio MS, Calviño A, González E, Salvo A, Videla M (2021) Urbanisation drivers and underlying mechanisms of terrestrial insect diversity loss in cities. Ecological Entomology 46:757–771. https://doi.org/10.1111/een.13041

Fortel L, Henry M, Guilbaud L, Guirao AL, Kuhlmann M, Mouret H, Rollin O, Vaissière BE (2014) Decreasing Abundance, Increasing Diversity and Changing Structure of the Wild Bee Community (Hymenoptera: Anthophila) along an Urbanization Gradient Smith MA (ed). PLoS ONE 9:e104679. https://doi.org/10.1371/journal.pone.0104679

Galimberti A, Spinelli S, Bruno A, Mezzasalma V, De Mattia F, Cortis P, Labra M (2016) Evaluating the efficacy of restoration plantings through DNA barcoding of frugivorous bird diets. Conservation Biology 30:763–773. https://doi.org/10.1111/cobi.12687

Garbuzov M, Ratnieks FLW (2014) Ivy: an underappreciated key resource to flower-visiting insects in autumn Leather SR, Roubik D (eds). Insect Conservation and Diversity 7:91–102. https://doi.org/10.1111/icad.12033

Gardiner MM, Burkman CE, Prajzner SP (2013) The Value of Urban Vacant Land to Support Arthropod Biodiversity and Ecosystem Services. Environmental Entomology 42:1123–1136. https://doi.org/10.1603/EN12275

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, Dudenhoffer JH, Freitas BM, Ghazoul J, Greenleaf S, Hipolito 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, Rundlof M, Seymour CL, Schuepp C, Szentgyorgyi 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. https://doi.org/10.1126/science.1230200

Garratt MPD, Breeze TD, Jenner N, Polce C, Biesmeijer JC, Potts SG (2014) Avoiding a bad apple: Insect pollination enhances fruit quality and economic value. Agriculture, Ecosystems & Environment 184:34–40. https://doi.org/10.1016/j.agee.2013.10.032

Grosbois M (1976) Changes in the Amount of Complex Lipids in the Seeds and in the Pericarp during the Development of Ivy Fruit (Hedera helix). Physiologia Plantarum 36:145–149. https://doi.org/10.1111/j.1399-3054.1976.tb03925.x

Halder S, Chandra B, Viswavidyalaya K, Khan R, Perween T, Hasan A, Khan AA, Hasan MA, Ghosh S, Khan A (2019) Role of pollination in fruit crops: A review. The Pharma Innovation Journal 8:695–702.

Hall DM, Camilo GR, Tonietto RK, Ollerton J, Ahrné K, Arduser M, Ascher JS, Baldock KCR, Fowler R, Frankie G, Goulson D, Gunnarsson B, Hanley ME, Jackson JI, Langellotto G, Lowenstein D, Minor ES, Philpott SM, Potts SG, Sirohi MH, Spevak EM, Stone GN, Threlfall CG (2017) The city as a refuge for insect pollinators. Conservation Biology 31:24–29. https://doi.org/10.1111/cobi.12840

Harris JG, Harris MW (2001) Plant identification terminology: an illustrated glossary, 2nd edn. Spring Lake Publishing.

van Heezik Y, Smyth A, Mathieu R (2008) Diversity of native and exotic birds across an urban gradient in a New Zealand city. Landscape and Urban Planning 87:223–232. https://doi.org/10.1016/j.landurbplan.2008.06.004

Hennig EI, Ghazoul J (2012) Pollinating animals in the urban environment. Urban Ecosystems 15:149–166. https://doi.org/10.1007/s11252-011-0202-7

Hernández Á (2005) Blackcaps, Sylvia atricapilla and blackbirds, Turdus merula, feeding their nestlings and fledglings on fleshy fruit. Folia Zoologica 54:379–388.

Hothorn T, Bretz F, Westfall P (2008) Simultaneous Inference in General Parametric Models. Biometrical Journal 50:346–363. https://doi.org/10.1002/bimj.200810425

Hsieh TC, Ma KH, Chao A (2016) iNEXT: an R package for rarefaction and extrapolation of species diversity ( Hill numbers) McInerny G (ed). Methods in Ecology and Evolution 7:1451–1456. https://doi.org/10.1111/2041-210X.12613

Jackson D, Looney N, Morley-Bunker M (2011) Temperate and subtropical fruit production, 3rd edn. CABI. https://doi.org/10.1079/9781845935016.0003

Jacobs JH, Clark SJ, Denholm I, Goulson D, Stoate C, Osborne JL (2009) Pollination biology of fruit-bearing hedgerow plants and the role of flower-visiting insects in fruit-set. Annals of Botany 104:1397–1404. https://doi.org/10.1093/aob/mcp236

Jacobs JH, Clark SJ, Denholm I, Goulson D, Stoate C, Osborne JL (2010) Pollinator effectiveness and fruit set in common ivy, Hedera helix (Araliaceae). Arthropod-Plant Interactions 4:19–28. https://doi.org/10.1007/s11829-009-9080-9

Kaluza BF, Wallace H, Heard TA, Klein A, Leonhardt SD (2016) Urban gardens promote bee foraging over natural habitats and plantations. Ecology and Evolution 6:1304–1316. https://doi.org/10.1002/ece3.1941

Kark S, Iwaniuk A, Schalimtzek A, Banker E (2007) Living in the city: Can anyone become an “urban exploiter”? Journal of Biogeography 34:638–651. https://doi.org/10.1111/j.1365-2699.2006.01638.x

Kassambara A, Kosinski M, Biecek P (2021) survminer: a package for drawing survival curves using ‘ggplot2.’ [online] URL: https://cran.r-project.org/package=survminer

Katumo DM, Liang H, Ochola AC, Lv M, Wang QF, Yang CF (2022) Pollinator diversity benefits natural and agricultural ecosystems, environmental health, and human welfare. Plant Diversity 44:429–435. https://doi.org/10.1016/j.pld.2022.01.005

Kearns CA, Inouye DW, Waser NM (1998) endangered mutualisms: The Conservation of Plant-Pollinator Interactions. Annual Review of Ecology and Systematics 29:83–112. https://doi.org/10.1146/annurev.ecolsys.29.1.83

Kishore J, Goel M, Khanna P (2010) Understanding survival analysis: Kaplan-Meier estimate. International Journal of Ayurveda Research 1:274. https://doi.org/10.4103/0974-7788.76794

Klatt BK, Holzschuh A, Westphal C, Clough Y, Smit I, Pawelzik E, Tscharntke T (2013) Bee pollination improves crop quality, shelf life and commercial value. Proceedings of the Royal Society B: Biological Sciences 281:20132440. https://doi.org/10.1098/rspb.2013.2440

Klein A-M, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences 274:303–313. https://doi.org/10.1098/rspb.2006.3721

Knuth P, Ainsworth-Davis JR, Müller H (1906) Handbook of flower pollination: based upon Hermann Müller’s work ʻThe fertilisation of flowers by insectsʼ. Clarendon Press, Oxford. https://doi.org/10.5962/bhl.title.160107

Konarska A (2014) Characteristics of flower nectaries of Hedera helix L. (Araliaceae). Acta Scientiarum Polonorum-hortorum Cultus 13:109–122.

Kosior A, Celary W, Olejniczak P, Fijał J, Król W, Solarz W, Płonka P (2007) The decline of the bumble bees and cuckoo bees (Hymenoptera: Apidae: Bombini) of Western and Central Europe. Oryx 41:79–88. https://doi.org/10.1017/S0030605307001597

Lata S, Shrama G, Garg S, Mishra G (2018) Effect of different modes of pollination on fruit set and malformation of strawberry cultivars. Research on Crops 19:430–435.

McCall C, Primack RB (1992) Influence of Flower Characteristics, Weather, Time of Day, and Season on Insect Visitation Rates in Three Plant Communities. American Journal of Botany 79:434. https://doi.org/10.1002/j.1537-2197.1992.tb14571.x

Metcalfe DJ (2005) Hedera helix L. Journal of Ecology 93:632–648. https://doi.org/10.1111/j.1365-2745.2005.01021.x

Ollerton J, Killick A, Lamborn E, Watts S, Whiston M (2007) Multiple meanings and modes: on the many ways to be a generalist flower. Taxon 56:717–728. https://doi.org/10.2307/25065855

Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326. https://doi.org/10.1111/j.1600-0706.2010.18644.x

Pacini E, Nepi M, Vesprini JL (2003) Nectar biodiversity: a short review. Plant Systematics and Evolution 238:7–21. https://doi.org/10.1007/s00606-002-0277-y

Persson AS, Ekroos J, Olsson P, Smith HG (2020) Wild bees and hoverflies respond differently to urbanisation, human population density and urban form. Landscape and Urban Planning 204:103901. https://doi.org/10.1016/j.landurbplan.2020.103901

Potts SG, Imperatriz-Fonseca V, Ngo HT, Aizen MA, Biesmeijer JC, Breeze TD, Dicks L V., Garibaldi LA, Hill R, Settele J, Vanbergen AJ (2016) Safeguarding pollinators and their values to human well-being. Nature 540:220–229. https://doi.org/10.1038/nature20588

R Core Team (2022) R: A Language and Environment for Statistical Computing. [online] URL: https://www.r-project.org/

Ratto F, Simmons BI, Spake R, Zamora-Gutierrez V, MacDonald MA, Merriman JC, Tremlett CJ, Poppy GM, Peh KSH, Dicks L V. (2018) Global importance of vertebrate pollinators for plant reproductive success: a meta-analysis. Frontiers in Ecology and the Environment 16:82–90. https://doi.org/10.1002/fee.1763

Ricketts TH, Regetz J, Steffan-Dewenter I, Cunningham SA, Kremen C, Bogdanski A, Gemmill-Herren B, Greenleaf SS, Klein AM, Mayfield MM, Morandin LA, Ochieng’ A, Viana BF (2008) Landscape effects on crop pollination services: are there general patterns? Ecology Letters 11:499–515. https://doi.org/10.1111/j.1461-0248.2008.01157.x

Rodger JG, Bennett JM, Razanajatovo M, Knight TM, van Kleunen M, Ashman TL, Steets JA, Hui C, Arceo-Gómez G, Burd M, Burkle LA, Burns JH, Durka W, Freitas L, Kemp JE, Li J, Pauw A, Vamosi JC, Wolowski M, Xia J, Ellis AG (2021) Widespread vulnerability of flowering plant seed production to pollinator declines. Science Advances 7:eabd3524 https://doi.org/10.1126/sciadv.abd3524

Samnegård U, Hambäck PA, Smith HG (2019) Pollination treatment affects fruit set and modifies marketable and storable fruit quality of commercial apples. Royal Society Open Science 6:190326. https://doi.org/10.1098/rsos.190326

Snow BK, Snow D (1988) Birds and berries: a study of an ecological interaction, 1st edn. T & A D Poyser.

Sorensen AE (1981) Interactions between birds and fruit in a temperate woodland. Oecologia 50:242–249. https://doi.org/10.1007/BF00348046

Stavert JR, Liñán-Cembrano G, Beggs JR, Howlett BG, Pattemore DE, Bartomeus I (2016) Hairiness: the missing link between pollinators and pollination. PeerJ 4:e2779. https://doi.org/10.7717/peerj.2779

Stel VS, Dekker FW, Tripepi G, Zoccali C, Jager KJ (2011) Survival Analysis I: The Kaplan-Meier Method. Nephron Clinical Practice 119:c83–c88. https://doi.org/10.1159/000324758

Theodorou P, Albig K, Radzevičiūtė R, Settele J, Schweiger O, Murray TE, Paxton RJ (2017) The structure of flower visitor networks in relation to pollination across an agricultural to urban gradient Kudo G (ed). Functional Ecology 31:838–847. https://doi.org/10.1111/1365-2435.12803

Theodorou P, Radzevičiūtė R, Lentendu G, Kahnt B, Husemann M, Bleidorn C, Settele J, Schweiger O, Grosse I, Wubet T, Murray TE, Paxton RJ (2020) Urban areas as hotspots for bees and pollination but not a panacea for all insects. Nature Communications 11:576. https://doi.org/10.1038/s41467-020-14496-6

Therneau TM (2022) A Package for Survival Analysis in R. [online] URL: https://cran.r-project.org/package=survival

Thomson JD (2001) Using pollination deficits to infer pollinator declines: Can theory guide us? Ecology and Society 5(1): 6. https://doi.org/10.5751/ES-00270-050106

UK Pollinator Monitoring Scheme (2021) FIT Counts: help us monitor pollinators. [online] URL: https://ukpoms.org.uk/fit-counts (accessed 28 March 2022).

Vezza M, Nepi M, Guarnieri M, Artese D, Rascio N, Pacini E (2006) Ivy (Hedera helix l.) flower nectar and nectary ecophysiology. International Journal of Plant Sciences 167:519–527. https://doi.org/10.1086/501140

Wenzel A, Grass I, Belavadi V V., Tscharntke T (2020) How urbanization is driving pollinator diversity and pollination – A systematic review. Biological Conservation 241:108321. https://doi.org/10.1016/j.biocon.2019.108321

Wilcock C, Neiland R (2002) Pollination failure in plants: why it happens and when it matters. Trends in Plant Science 7:270–277. https://doi.org/10.1016/S1360-1385(02)02258-6

Wildlife Trust BCN (2018) Trumpington Meadows. [online] URL: https://www.wildlifebcn.org/nature-reserves/trumpington-meadows (accessed 9 April 2022).

Willcox BK, Aizen MA, Cunningham SA, Mayfield MM, Rader R (2017) Deconstructing pollinator community effectiveness. Current Opinion in Insect Science 21:98–104. https://doi.org/10.1016/j.cois.2017.05.012

Winfree R, Aguilar R, Vázquez DP, LeBuhn G, Aizen MA (2009) A meta-analysis of bees’ responses to anthropogenic disturbance. Ecology 90:2068–2076. https://doi.org/10.1890/08-1245.1

A female ivy bee (Colletes hederae) feeding on ivy flower (Photo by Steven Falk)



How to Cite

Lam, M., Ryan, I., & Dicks, L. (2024). Pollinator dependence and pollination deficit in Hedera helix, and effects on frugivore feeding choices: Pollination and frugivory in ivy Hedera helix. Journal of Pollination Ecology, 35, 14–28. https://doi.org/10.26786/1920-7603(2024)748



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