Climate Change Impacts on Pollinator-Plant Interaction Networks in Temperate Ecosystems
DOI:
https://doi.org/10.5281/zenodo.22688125Keywords:
pollinator-plant networks, phenological mismatch, climate change, network robustness, temperate ecosystems, systematic reviewAbstract
Temperate pollinator-plant interaction networks are widely predicted to be destabilised by climate-driven
phenological mismatch, but published evidence spans a wide range of taxa, geographic regions and network
metrics, making the overall strength and consistency of the effect difficult to judge from any single study. We
conducted a systematic review and quantitative synthesis, following PRISMA guidelines, of studies reporting
temporal change in temperate pollinator-plant network structure in relation to climatic warming. Searches of three
bibliographic databases identified 2,847 candidate records, of which 61 met full inclusion criteria after title-abstract
and full-text screening, spanning 19 countries and network observation periods from 4 to 43 years.
Random-effects meta-analysis of standardised effect sizes showed a significant mean decline in network
nestedness over time (Hedges' g = -0.34, 95% CI -0.48 to -0.20, k=44 studies) and in simulated robustness to
sequential pollinator extinction (g = -0.29, 95% CI -0.45 to -0.13, k=31), while connectance showed a smaller, only
marginally significant decline (g = -0.14, 95% CI -0.28 to 0.00, k=52). Effect sizes for nestedness decline were
significantly larger in studies from higher-latitude and higher-elevation sites (meta-regression P=0.008 and P=0.02
respectively), consistent with these settings experiencing more rapid relative warming and stronger phenological
shifts. Substantial residual heterogeneity remained after accounting for latitude, elevation and study duration
(I2=68%), and formal publication bias tests gave mixed results, with Egger's regression suggesting some
asymmetry for the nestedness outcome specifically. These findings support a real, geographically patterned
decline in temperate pollinator-plant network cohesion associated with recent climatic warming, while highlighting
substantial unexplained variability that single-site studies alone cannot resolve.
References
Bascompte J, Jordano P, Melian CJ, Olesen JM (2003) The nested assembly of plant-animal mutualistic networks. Proceedings of the National Academy of Sciences 100(16):9383-9387. https://doi.org/10.1073/pnas.1633576100
Bascompte J, Jordano P (2007) Plant-animal mutualistic networks: the architecture of biodiversity. Annual Review of Ecology, Evolution, and Systematics 38:567-593. https://doi.org/10.1146/annurev.ecolsys.38.091206.095818
Memmott J, Waser NM, Price MV (2004) Tolerance of pollination networks to species extinctions. Proceedings of the Royal Society B 271(1557):2605-2611. https://doi.org/10.1098/rspb.2004.2909
Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annual Review of Ecology, Evolution, and Systematics 37:637-669. https://doi.org/10.1146/annurev.ecolsys.37.091305.110100
Hegland SJ, Nielsen A, Lazaro A, Bjerknes AL, Totland O (2009) How does climate warming affect plant-pollinator interactions? Ecology Letters 12(2):184-195. https://doi.org/10.1111/j.1461-0248.2008.01269.x
Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant-pollinator interactions. Ecology Letters 10(8):710-717. https://doi.org/10.1111/j.1461-0248.2007.01061.x
Burkle LA, Marlin JC, Knight TM (2013) Plant-pollinator interactions over 120 years: loss of species, co-occurrence, and function. Science 339(6127):1611-1615. https://doi.org/10.1126/science.1232728
Willmer P (2012) Ecology: pollinator-plant synchrony tested by climate change. Current Biology 22(4):R131-R132. https://doi.org/10.1016/j.cub.2012.01.009
Bartomeus I, Ascher JS, Wagner D, Danforth BN, Colla S, Kornbluth S, Winfree R (2011) Climate-associated phenological advances in bee pollinators and bee-pollinated plants. Proceedings of the National Academy of Sciences 108(51):20645-20649. https://doi.org/10.1073/pnas.1115559108
Kudo G, Ida TY (2013) Early onset of spring increases the phenological mismatch between plants and pollinators. Ecology 94(10):2311-2320. https://doi.org/10.1890/12-2003.1
Thomson JD (2010) Flowering phenology, fruiting success and progressive deterioration of pollination in an early-flowering geophyte. Philosophical Transactions of the Royal Society B 365(1555):3187-3199. https://doi.org/10.1098/rstb.2010.0115
CaraDonna PJ, Iler AM, Inouye DW (2014) Shifts in flowering phenology reshape a subalpine plant community. Proceedings of the National Academy of Sciences 111(13):4916-4921. https://doi.org/10.1073/pnas.1323073111
Page ML, Nicholson CC, Brennan RM, Britzman AT, Greer J, Hemberger J, et al. (2021) A meta-analysis of single visit pollination effectiveness comparing honeybees and other floral visitors. American Journal of Botany 108(11):2196-2207. https://doi.org/10.1002/ajb2.1793
Petanidou T, Kallimanis AS, Tzanopoulos J, Sgardelis SP, Pantis JD (2008) Long-term observation of a pollination network: fluctuation in species and interactions, relative invariance of network structure and implications for estimates of specialization. Ecology Letters 11(6):564-575. https://doi.org/10.1111/j.1461-0248.2008.01170.x
Rafferty NE, Ives AR (2011) Effects of experimental shifts in flowering phenology on plant-pollinator interactions. Ecology Letters 14(1):69-74. https://doi.org/10.1111/j.1461-0248.2010.01557.x
Vazquez DP, Bluthgen N, Cagnolo L, Chacoff NP (2009) Uniting pattern and process in plant-animal mutualistic networks: a review. Annals of Botany 103(9):1445-1457. https://doi.org/10.1093/aob/mcp057
Devoto M, Bailey S, Craze P, Memmott J (2012) Understanding and planning ecological restoration of plant-pollinator networks. Ecology Letters 15(4):319-328. https://doi.org/10.1111/j.1461-0248.2012.01740.x
Miller-Struttmann NE, Geib JC, Franklin JD, Kevan PG, Holdo RM, Ebert-May D, et al. (2015) Functional mismatch in a bumble bee pollination mutualism under climate change. Science 349(6255):1541-1544. https://doi.org/10.1126/science.aab0868
Forrest JR (2015) Plant-pollinator interactions and phenological change: what can we learn about climate impacts from experiments and observations? Oikos 124(1):4-13. https://doi.org/10.1111/oik.01386
Renner SS, Zohner CM (2018) Climate change and phenological mismatch in trophic interactions among plants, insects, and vertebrates. Annual Review of Ecology, Evolution, and Systematics 49:165-182. https://doi.org/10.1146/annurev-ecolsys-110617-062535
Gerard M, Vanderplanck M, Wood T, Michez D (2020) Global warming and plant-pollinator mismatches. Emerging Topics in Life Sciences 4(1):77-86. https://doi.org/10.1042/ETLS20190139
Fabina NS, Abbott KC, Gilman RT (2010) Sensitivity of plant-pollinator-herbivore communities to changes in phenology. Ecological Modelling 221(3):453-458. https://doi.org/10.1016/j.ecolmodel.2009.10.030
Ovaskainen O, Skorokhodova S, Yakovleva M, Sukhov A, Kutenkov A, Kutenkova N, et al. (2013) Community-level phenological response to climate change. Proceedings of the National Academy of Sciences 110(33):13434-13439. https://doi.org/10.1073/pnas.1305533110
Robinson SVJ, Losapio G, Henry GHR (2018) Flower-power: flower diversity is a stronger predictor of network structure than insect diversity in an Arctic plant-pollinator network. Ecological Complexity 36:1-6. https://doi.org/10.1016/j.ecocom.2018.06.001
Dorado J, Vazquez DP, Willink EB, Chacoff NP (2011) Points of view of network approaches to forecast the sensitivity of ecosystem services to species loss. Ecological Applications 21(5):1554-1562. https://doi.org/10.1890/10-1150.1
Page CG, CaraDonna PJ, Ogilvie JE (2021) Extending the season: high summer flower availability supports increased pollinator abundance. Journal of Ecology 109(11):3776-3788. https://doi.org/10.1111/1365-2745.13756
Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. (2021) The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 372:n71. https://doi.org/10.1136/bmj.n71
Viechtbauer W (2010) Conducting meta-analyses in R with the metafor package. Journal of Statistical Software 36(3):1-48. https://doi.org/10.18637/jss.v036.i03
Nakagawa S, Santos ESA (2012) Methodological issues and advances in biological meta-analysis. Evolutionary Ecology 26:1253-1274. https://doi.org/10.1007/s10682-012-9555-5
Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315(7109):629-634. https://doi.org/10.1136/bmj.315.7109.629
IPCC (2021) Climate Change 2021: The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press. https://doi.org/10.1017/9781009157896
Pecl GT, Araujo MB, Bell JD, Blanchard J, Bonebrake TC, Chen IC, et al. (2017) Biodiversity redistribution under climate change: impacts on ecosystems and human well-being. Science 355(6332):eaai9214. https://doi.org/10.1126/science.aai9214
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(6):345-353. https://doi.org/10.1016/j.tree.2010.01.007
Goulson D, Nicholls E, Botias C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347(6229):1255957. https://doi.org/10.1126/science.1255957
Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120(3):321-326. https://doi.org/10.1111/j.1600-0706.2010.18644.x
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 of the Royal Society B 274(1608):303-313. https://doi.org/10.1098/rspb.2006.3721
Vazquez DP, Chacoff NP, Cagnolo L (2009) Evaluating multiple determinants of the structure of plant-animal mutualistic networks. Ecology 90(8):2039-2046. https://doi.org/10.1890/08-1837.1
Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecology Letters 11(12):1351-1363. https://doi.org/10.1111/j.1461-0248.2008.01250.x
Schweiger O, Biesmeijer JC, Bommarco R, Hickler T, Hulme PE, Klotz S, et al. (2010) Multiple stressors on biotic interactions: how climate change and alien species interact to affect pollination. Biological Reviews 85(4):777-795. https://doi.org/10.1111/j.1469-185X.2010.00125.x
Settele J, Kudrna O, Harpke A, Kuhn I, van Swaay C, Verovnik R, et al. (2008) Climatic Risk Atlas of European Butterflies. Biorisk 1:1-710. https://doi.org/10.3897/biorisk.1
Chen IC, Hill JK, Ohlemuller R, Roy DB, Thomas CD (2011) Rapid range shifts of species associated with high levels of climate warming. Science 333(6045):1024-1026. https://doi.org/10.1126/science.1206432
Aizen MA, Sabatino M, Tylianakis JM (2012) Specialization and rarity predict nonrandom loss of interactions from mutualist networks. Science 335(6075):1486-1489. https://doi.org/10.1126/science.1215320
Traveset A, Castro-Urgal R, Rotllan-Puig X, Lazaro A (2018) Effects of habitat loss on the plant-flower visitor network structure of a dune community. Oikos 127(1):45-55. https://doi.org/10.1111/oik.04154
Rader R, Bartomeus I, Garibaldi LA, Garratt MP, Howlett BG, Winfree R, et al. (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
Rasmussen C, Dupont YL, Madsen HB, Bogusch P, Goulson D, Herbertsson L, et al. (2021) Evaluating competition for forage plants between honey bees and wild bees in Denmark. PLOS ONE 16(4):e0250056. https://doi.org/10.1371/journal.pone.0250056
IPBES (2016) The assessment report of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services on pollinators, pollination and food production. Zenodo. https://doi.org/10.5281/zenodo.3402856
Kuppler J, Hoiss B, Albrecht M, Fritsch M, Bluthgen N, Boch S, et al. (2020) Response of flower visitation networks to climate change. Oecologia 194:387-399. https://doi.org/10.1007/s00442-020-04770-7
Iler AM, Inouye DW, Hoye TT, Miller-Rushing AJ, Burkle LA, Johnston EB (2013) Maintenance of temporal synchrony between syrphid flies and floral resources despite differential phenological responses to climate. Global Change Biology 19(8):2348-2359. https://doi.org/10.1111/gcb.12246
Hoiss B, Krauss J, Potts SG, Roberts S, Steffan-Dewenter I (2012) Altitude acts as an environmental filter on phylogenetic composition, traits and diversity in bee communities. Proceedings of the Royal Society B 279(1746):4447-4456. https://doi.org/10.1098/rspb.2012.1581
Warren MS, Hill JK, Thomas JA, Asher J, Fox R, Huntley B, et al. (2001) Rapid responses of British butterflies to opposing forces of climate and habitat change. Nature 414(6859):65-69. https://doi.org/10.1038/35102054
Descamps C, Quinet M, Baijot A, Jacquemart AL (2018) Temperature and water stress affect plant-pollinator interactions in Borago officinalis. Ecology and Evolution 8(6):3443-3456. https://doi.org/10.1002/ece3.3914
Wolkovich EM, Cook BI, Allen JM, Crimmins TM, Betancourt JL, Travers SE, et al. (2012) Warming experiments underpredict plant phenological responses to climate change. Nature 485(7399):494-497. https://doi.org/10.1038/nature11014
Gonzalez-Varo JP, Biesmeijer JC, Bommarco R, Potts SG, Schweiger O, Smith HG, et al. (2013) Combined effects of global change pressures on animal-mediated pollination. Trends in Ecology & Evolution 28(9):524-530. https://doi.org/10.1016/j.tree.2013.05.008
Bennett JM, Steets JA, Burns JH, Burkle LA, Vamosi JC, Wolowski M, et al. (2020) Land use and pollinator dependency drives global patterns of pollen limitation in the Anthropocene. Nature Communications 11:3999. https://doi.org/10.1038/s41467-020-17751-y
Kremen C, M'Gonigle LK, Ponisio LC (2018) Pollinator community assembly tracks changes in floral resources as restored hedgerows mature in agricultural landscapes. Frontiers in Ecology and Evolution 6:170. https://doi.org/10.3389/fevo.2018.00170
