Pollinator effectiveness and pollination dependency of bilberry (Vaccinium myrtillus) in Swedish hemi-boreal forests
DOI:
https://doi.org/10.26786/1920-7603(2024)791Keywords:
bilberry, forest pollinators, pollination effectiveness, dwarf shrubAbstract
Intensification of forest management to increase production of biomass has resulted in considerable habitat degradation with negative impacts on insect biodiversity, including beneficial insect groups such as pollinators. Yet, little is known about how reliant forest understory plants, such as bilberry (Vaccinium myrtillus), are on insect pollinators for reproduction. Here, we quantified the structure of the bilberry flower visitor community, compared the pollination effectiveness of the most common pollinators, and experimentally quantified bilberry pollination dependency. The bilberry pollinator community was comprised of several bee and hoverfly taxa. Bumblebees were the most important pollinators due to their high abundance and pollination effectiveness. Other bees, in particular, Andrena spp., and to a smaller extent, hoverflies, were also effective pollinators. Furthermore, bilberry was strongly pollen-limited, with only 40% of open-pollinated flowers setting fruit. Bilberry supports a diverse flower visitor community within hemi-boreal forests, for which it is highly dependent for reproduction. Given the ecological and cultural value of bilberry, the importance of insect pollinators for understory plants should be considered within forest management strategies.
References
Andresen JL (2019) Bilberry as an important resource for bumblebees within the forest-tundra ecotone. Master Master, University of South-Eastern Norway, Kongsberg
Angelstam P, Manton M, Green M, Jonsson B-G, Mikusiński G, Svensson J, Maria Sabatini F (2020) Sweden does not meet agreed national and international forest biodiversity targets: A call for adaptive landscape planning. Landscape and Urban Planning 202:103838. https://doi.org/10.1016/j.landurbplan.2020.103838 DOI: https://doi.org/10.1016/j.landurbplan.2020.103838
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. https://doi.org/10.1002/ece3.924 DOI: https://doi.org/10.1002/ece3.924
Bartholomée O, Dwyer C, Tichit P, Caplat P, Baird E, Smith HG (2023) Shining a light on species coexistence: visual traits drive bumblebee communities. Proceedings of the Royal Society B. https://doi.org/10.1098/rspb.2022.2548 DOI: https://doi.org/10.1098/rspb.2022.2548
Benjamin FE, Reilly JR, Winfree R, Osborne J (2014) Pollinator body size mediates the scale at which land use drives crop pollination services. Journal of Applied Ecology 51:440-449. https://doi.org/10.1111/1365-2664.12198 DOI: https://doi.org/10.1111/1365-2664.12198
Berg A, Ehnstrom B, Gustafsson L, Hallingback T, Jonsell M, Weslien J (1995) Threat Levels and Threats to Red-Listed Species in Swedish Forests. Conservation Biology 9:1629-1633 https://doi.org/10.1046/j.1523-1739.1995.09061629.x DOI: https://doi.org/10.1046/j.1523-1739.1995.09061629.x
Berglund H, Kuuluvainen T (2021) Representative boreal forest habitats in northern Europe, and a revised model for ecosystem management and biodiversity conservation. Ambio 50:1003-1017. https://doi.org/10.1007/s13280-020-01444-3 DOI: https://doi.org/10.1007/s13280-020-01444-3
Bernauer OM, Tierney SM, Cook JM (2022) Efficiency and effectiveness of native bees and honey bees as pollinators of apples in New South Wales orchards. Agriculture, Ecosystems & Environment 337:108063. https://doi.org/10.1016/j.agee.2022.108063 DOI: https://doi.org/10.1016/j.agee.2022.108063
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 https://doi.org/10.1002/ecs2.1654 DOI: https://doi.org/10.1002/ecs2.1654
Brooks ME, Kristensen K, Benthem KJv, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Maechler M, Bolker BM (2017) glmmTMB Balances Speed and Flexibility Among Packages for Zero-inflated Generalized Linear Mixed Modeling. The R Journal 9:378-400 https://doi.org/10.32614/RJ-2017-066 DOI: https://doi.org/10.32614/RJ-2017-066
Burton P, Bergeron Y, Bogdanski B, Juday G, Kuuluvainen T, McAfee B, Ogden A, Teplyakov V, Alfaro R, Francis DA, Gauthier S, Hantula J (2010) Sustainability of boreal forests and forestry in a changing environment. In: G. Mery PK, G. Galloway, R.I. Alfaro, M. Kanninen, M. Lobovikov, J. Varjo (ed) Forests and Society - Responding to Global Drivers of Change. International Union of Forest Research Organizations, Vienna, Austria, pp 249-282
Carolan JC, Murray TE, Fitzpatrick Ú, Crossley J, Schmidt H, Cederberg B, McNally L, Paxton RJ, Williams PH, Brown MJF (2012) Colour Patterns Do Not Diagnose Species: Quantitative Evaluation of a DNA Barcoded Cryptic Bumblebee Complex. PLOS ONE 7:e29251. https://doi.org/10.1371/journal.pone.0029251 DOI: https://doi.org/10.1371/journal.pone.0029251
Courcelles DMM, Button L, Elle E (2013) Bee visit rates vary with floral morphology among highbush blueberry cultivars (Vaccinium corymbosum L.). Journal of Applied Entomology 137:693-701. https://doi.org/10.1111/jen.12059 DOI: https://doi.org/10.1111/jen.12059
De Luca PA, Vallejo-Marín M (2013) What's the ‘buzz’ about? The ecology and evolutionary significance of buzz-pollination. Current Opinion in Plant Biology 16:429-435. https://doi.org/10.1016/j.pbi.2013.05.002 DOI: https://doi.org/10.1016/j.pbi.2013.05.002
Doyle T, Hawkes WLS, Massy R, Powney GD, Menz MHM, Wotton KR (2020) Pollination by hoverflies in the Anthropocene. Proceedings of The Royal Society B: Biological Sciences 287:20200508. https://doi.org/10.1098/rspb.2020.0508 DOI: https://doi.org/10.1098/rspb.2020.0508
Eckerter T, Buse J, Bauhus J, Förschler MI, Klein AM (2021) Wild bees benefit from structural complexity enhancement in a forest restoration experiment. Forest Ecology and Management 496:119412. https://doi.org/10.1016/j.foreco.2021.119412 DOI: https://doi.org/10.1016/j.foreco.2021.119412
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. https://doi.org/10.1016/j.foreco.2018.10.059 DOI: https://doi.org/10.1016/j.foreco.2018.10.059
Ekroos J, Rundlöf M, Smith HG (2013) Trait-dependent responses of flower-visiting insects to distance to semi-natural grasslands and landscape heterogeneity. Landscape Ecology 28:1283-1292. https://doi.org/10.1007/s10980-013-9864-2 DOI: https://doi.org/10.1007/s10980-013-9864-2
Eldegard K, Scholten J, Stokland JN, Granhus A, Lie M (2019) The influence of stand density on bilberry (Vaccinium myrtillus L.) cover depends on stand age, solar irradiation, and tree species composition. Forest Ecology and Management 432:582-590. https://doi.org/10.1016/j.foreco.2018.09.054 DOI: https://doi.org/10.1016/j.foreco.2018.09.054
Gustafsson L, Hannerz M, Koivula M, Shorohova E, Vanha-Majamaa I, Weslien J (2020) Research on retention forestry in Northern Europe. Ecological Processes 9:3. https://doi.org/10.1186/s13717-019-0208-2 DOI: https://doi.org/10.1186/s13717-019-0208-2
Hanski I (2011) Habitat Loss, the Dynamics of Biodiversity, and a Perspective on Conservation. Ambio 40:248-255. https://doi.org/10.1007/s13280-011-0147-3 DOI: https://doi.org/10.1007/s13280-011-0147-3
Hartig F (2022) DHARMa: Residual Diagnostics for Hierarchical (Multi-level/Mixed) Regression Models https://cran.r-project.org/web/packages/DHARMa/index.html
Hedwall P-O, Brunet J, Nordin A, Bergh J (2013) Changes in the abundance of keystone forest floor species in response to changes of forest structure. Journal of Vegetation Science 24:296-306. https://doi.org/10.1111/j.1654-1103.2012.01457.x DOI: https://doi.org/10.1111/j.1654-1103.2012.01457.x
Heikkala O, Seibold S, Koivula M, Martikainen P, Müller J, Thorn S, Kouki J (2016) Retention forestry and prescribed burning result in functionally different saproxylic beetle assemblages than clear-cutting. Forest Ecology and Management 359:51-58. https://doi.org/10.1016/j.foreco.2015.09.043 DOI: https://doi.org/10.1016/j.foreco.2015.09.043
Holzschuh A, Dormann CF, Tscharntke T, Steffan-Dewenter I (2011) Expansion of mass-flowering crops leads to transient pollinator dilution and reduced wild plant pollination. Proceedings of The Royal Society B: Biological Sciences 278:3444-3451. https://doi.org/10.1098/rspb.2011.0268 DOI: https://doi.org/10.1098/rspb.2011.0268
Hyvärinen E, Kouki J, Martikainen P (2009) Prescribed fires and retention trees help to conserve beetle diversity in managed boreal forests despite their transient negative effects on some beetle groups. Insect Conservation and Diversity 2:93-105. https://doi.org/10.1111/j.1752-4598.2009.00048.x DOI: https://doi.org/10.1111/j.1752-4598.2009.00048.x
Jacquemart A-L (1993) Floral visitors of Vaccinium species in the High Ardennes, Belgium. Flora 188:263-273. https://doi.org/10.1016/S0367-2530(17)32276-4 DOI: https://doi.org/10.1016/S0367-2530(17)32276-4
Jones MS, Vanhanen H, Peltola R, Drummond F (2014) A global review of arthropod-mediated ecosystem-services in Vaccinium berry agroecosystems. Terrestrial Arthropod Reviews 7:41-78. https://doi.org/10.1163/18749836-06041074 DOI: https://doi.org/10.1163/18749836-06041074
Jonsson BG, Dahlgren J, Ekström M, Esseen P-A, Grafström A, Ståhl G, Westerlund B (2021) Rapid Changes in Ground Vegetation of Mature Boreal Forests—An Analysis of Swedish National Forest Inventory Data. Forests 12:475 https://doi.org/10.3390/f12040475 DOI: https://doi.org/10.3390/f12040475
Kangas K, Markkanen P (2001) Factors affecting participation in wild berry picking by rural and urban dwellers. Silva Fennica 35:487-495 https://doi.org/10.14214/sf.582 DOI: https://doi.org/10.14214/sf.582
Kendall LK, Mola JM, Portman ZM, Cariveau DP, Smith HG, Bartomeus I (2022) The potential and realized foraging movements of bees are differentially determined by body size and sociality. Ecology 103:e3809. https://doi.org/10.1002/ecy.3809 DOI: https://doi.org/10.1002/ecy.3809
Klein AM, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proceedings in Biological Science 274:303-313. https://doi.org/10.1098/rspb.2006.3721 DOI: https://doi.org/10.1098/rspb.2006.3721
Larsson A, Bjelke U, Dahlberg A, Sandström J (2011) Tillståndet i skogen–rödlistade arter i ett nordiskt perspektiv. ArtDatabanken rapporterar 9:4-13
Lõhmus A, Remm L (2017) Disentangling the effects of seminatural forestry on an ecosystem good: Bilberry (Vaccinium myrtillus) in Estonia. Forest Ecology and Management 404:75-83. https://doi.org/10.1016/j.foreco.2017.08.035 DOI: https://doi.org/10.1016/j.foreco.2017.08.035
Moquet L, Bruyère L, Pirard B, Jacquemart AL (2017a) Nectar foragers contribute to the pollination of buzz-pollinated plant species. American Journal of Botany 104:1451-1463. https://doi.org/10.3732/ajb.1700090 DOI: https://doi.org/10.3732/ajb.1700090
Moquet L, Laurent E, Bacchetta R, Jacquemart A-L (2018) Conservation of hoverflies (Diptera, Syrphidae) requires complementary resources at the landscape and local scales. Insect Conservation and Diversity 11:72-87. https://doi.org/10.1111/icad.12245 DOI: https://doi.org/10.1111/icad.12245
Moquet L, Vanderplanck M, Moerman R, Quinet M, Roger N, Michez D, Jacquemart A-L (2017b) Bumblebees depend on ericaceous species to survive in temperate heathlands. Insect Conservation and Diversity 10:78-93. https://doi.org/10.1111/icad.12201 DOI: https://doi.org/10.1111/icad.12201
Naturvårdsverket (2023) Fördjupad utvärdering av Sveriges miljömål 2023, p 108
Ne'eman G, Jürgens A, Newstrom-Lloyd L, Potts SG, Dafni A (2010) A framework for comparing pollinator performance: effectiveness and efficiency. Biological Reviews 85:435-451. https://doi.org/10.1111/j.1469-185X.2009.00108.x DOI: https://doi.org/10.1111/j.1469-185X.2009.00108.x
Nestby R, Percival D, Martinussen I, Opstad N, Rohloff J (2011) The European blueberry (Vaccinium myrtillus L.) and the potential for cultivation. A review. European Journal of Plant Science and Biotechnology 5:5-16
Nilsson P, Roberge C, Fridman J (2021) Skogsdata 2021: aktuella uppgifter om de svenska skogarna från SLU Riksskogstaxeringen.
Nuortila C, Tuomi J, Aspi J, Laine K (2006) Early-acting inbreeding depression in a clonal dwarf shrub, Vaccinium myrtillus, in a northern boreal forest. Annales Botanici Fennici 43:36-48. https://doi.org/10.1139/b02-079
Nuortila C, Tuomi J, Laine K (2002) Inter-parent distance affects reproductive success in two clonal dwarf shrubs, Vaccinium myrtillus and Vaccinium vitis-idaea (Ericaceae). Canadian Journal of Botany 80:875-884. https://doi.org/10.1139/b02-079 DOI: https://doi.org/10.1139/b02-079
Oksanen J, Simpson G, Blanchet F, Kindt R, Legendre P, Minchin P, O'Hara R, Solymos P, Stevens M, Szoecs E, Wagner H, Barbour M, Bedward M, Bolker B, Borcard D, Carvalho G, Chirico M, De Caceres M, Durand S, Evangelista H, FitzJohn R, Friendly M, Furneaux B, Hannigan G, Hill M, Lahti L, McGlinn D, Ouellette M, Ribeiro Cunha E, Smith T, Stier A, Ter Braak C, Weedon J (2022) vegan: Community Ecology Package. R package version 2.6-4
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 DOI: https://doi.org/10.1111/j.1600-0706.2010.18644.x
Persson AS, Rundlof M, Clough Y, Smith HG (2015) Bumble bees show trait-dependent vulnerability to landscape simplification. Biodiversity and Conservation 24:3469-3489. https://doi.org/10.1007/s10531-015-1008-3 DOI: https://doi.org/10.1007/s10531-015-1008-3
Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends in Ecology & 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
R Core Team (2023) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria
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
Raderschall CA, Bommarco R, Lindström SAM, Lundin O (2021) Landscape crop diversity and semi-natural habitat affect crop pollinators, pollination benefit and yield. Agriculture, Ecosystems & Environment 306:107189. https://doi.org/10.1016/j.agee.2020.107189 DOI: https://doi.org/10.1016/j.agee.2020.107189
Ram D, Axelsson A-L, Green M, Smith HG, Lindström Å (2017) What drives current population trends in forest birds – forest quantity, quality or climate? A large-scale analysis from northern Europe. Forest Ecology and Management 385:177-188. https://doi.org/10.1016/j.foreco.2016.11.013 DOI: https://doi.org/10.1016/j.foreco.2016.11.013
Rivers JW, Galbraith SM, Cane JH, Schultz CB, Ulyshen MD, Kormann UG (2018) A Review of Research Needs for Pollinators in Managed Conifer Forests. Journal of Forestry 116:563-572. https://doi.org/10.1093/jofore/fvy052 DOI: https://doi.org/10.1093/jofore/fvy052
Rodríguez A, Kouki J (2015) Emulating natural disturbance in forest management enhances pollination services for dominant Vaccinium shrubs in boreal pine-dominated forests. Forest Ecology and Management 350:1-12. https://doi.org/10.1016/j.foreco.2015.04.029 DOI: https://doi.org/10.1016/j.foreco.2015.04.029
Ruckstuhl KE, Johnson EA, Miyanishi K (2008) Introduction. The boreal forest and global change. Philosophical Transactions of the Royal Society B: Biological Sciences 363:2243-2247. https://doi.org/10.1098/rstb.2007.2196 DOI: https://doi.org/10.1098/rstb.2007.2196
SLU Artdatabanken (2020) Rödlistade arter i Sverige 2020. SLU, Uppsala
SMHI (2021) Ladda ner meteorologiska observationer.
Statistics Sweden (2019) Land use in Sweden, seventh edition
Swedish NFI (2022) Forest Statistics, vol. 2022
Söderman AME, Ekroos J, Hedlund K, Olsson O, Smith HG (2016) Contrasting effects of field boundary management on three pollinator groups. Insect Conservation and Diversity 9:427-437. https://doi.org/10.1111/icad.12179 DOI: https://doi.org/10.1111/icad.12179
Ulyshen MD (2016) Wood decomposition as influenced by invertebrates. Biological Reviews 91:70-85. https://doi.org/10.1111/brv.12158 DOI: https://doi.org/10.1111/brv.12158
Vallejo-Marín M, Vallejo GC (2021) Comparison of defence buzzes in hoverflies and buzz-pollinating bees. Journal of Zoology 313:237-249. https://doi.org/10.1111/jzo.12857 DOI: https://doi.org/10.1111/jzo.12857
Öckinger E, Smith HG (2006) Semi-natural grasslands as population sources for pollinating insects in agricultural landscapes. Journal of Applied Ecology 44:50-59. https://doi.org/10.1111/j.1365-2664.2006.01250.x DOI: https://doi.org/10.1111/j.1365-2664.2006.01250.x
Östlund L (2004) Fire, death and disorder in the forest: 150 years of change in critical ecological structures and processes in boreal Scandinavia. Forest Biodiversity: Lessons from History for Conservation:55-65. https://doi.org/10.1079/9780851998022.0055 DOI: https://doi.org/10.1079/9780851998022.0055
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