Experimental loss of generalist plants reveals alterations in plant-pollinator interactions and a constrained flexibility of foraging
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
31089144
PubMed Central
PMC6517441
DOI
10.1038/s41598-019-43553-4
PII: 10.1038/s41598-019-43553-4
Knihovny.cz E-zdroje
- MeSH
- distribuce rostlin MeSH
- druhová specificita MeSH
- extinkce biologická * MeSH
- hmyz fyziologie MeSH
- květy MeSH
- migrace zvířat fyziologie MeSH
- opylení fyziologie MeSH
- pilotní projekty MeSH
- potravní řetězec * MeSH
- stravovací zvyklosti fyziologie MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Species extinctions undermine ecosystem functioning, with the loss of a small subset of functionally important species having a disproportionate impact. However, little is known about the effects of species loss on plant-pollinator interactions. We addressed this issue in a field experiment by removing the plant species with the highest visitation frequency, then measuring the impact of plant removal on flower visitation, pollinator effectiveness and insect foraging in several sites. Our results show that total visitation decreased exponentially after removing 1-4 most visited plants, suggesting that these plants could benefit co-occurring ones by maintaining high flower visitor abundances. Although we found large variation among plant species, the redistribution of the pollinator guild affected mostly the other plants with high visitor richness. Also, the plant traits mediated the effect of removal on flower visitation; while visitation of plants which had smaller inflorescences and more sugar per flower increased after removal, flower visitors did not switch between flower shapes and visitation decreased mostly in plants visited by many morpho-species of flower visitors. Together, these results suggest that the potential adaptive foraging was constrained by flower traits. Moreover, pollinator effectiveness fluctuated but was not directly linked to changes of flower visitation. In conclusion, it seems that the loss of generalist plants alters plant-pollinator interactions by decreasing pollinator abundance with implications for pollination and insect foraging. Therefore, generalist plants have high conservation value because they sustain the complex pattern of plant-pollinator interactions.
Czech Academy of Sciences Biology Centre Institute of Entomology České Budějovice Czech Republic
Department of Ecology Faculty of Science Charles University Viničná 7 Praha CZ 12844 Czech Republic
Faculty of Arts Science and Technology University of Northampton Northampton UK
University of Milano Bicocca Department of Biotechnology and Biosciences Milan Italy
University of South Bohemia Faculty of Science Department of Zoology České Budějovice Czech Republic
Zobrazit více v PubMed
Grime JP. Declining plant diversity: empty niches or functional shifts? J. Veg. Sci. 2002;13:457–460. doi: 10.1111/j.1654-1103.2002.tb02072.x. DOI
Smith MD, Knapp AK. Dominant species maintain ecosystem function with non-random species loss. Ecol. Lett. 2003;6:509–517. doi: 10.1046/j.1461-0248.2003.00454.x. DOI
Dupont YL, Hansen DM, Olesen JM. Structure of a plant–flower-visitor network in the high-altitude sub-alpine desert of Tenerife, Canary Islands. Ecography. 2003;26:301–310. doi: 10.1034/j.1600-0587.2003.03443.x. DOI
Ollerton J, Johnson SD, Cranmer L, Kellie S. The pollination ecology of an assemblage of grassland asclepiads in South Africa. Ann. Bot. 2003;92:807–834. doi: 10.1093/aob/mcg206. PubMed DOI PMC
Martín González AM, Dalsgaard B, Olesen JM. Centrality measures and the importance of generalist species in pollination networks. Ecol. Complex. 2010;7:36–43. doi: 10.1016/j.ecocom.2009.03.008. DOI
Gross K. Positive interactions among competitors can produce species-rich communities. Ecol. Lett. 2008;11:929–936. doi: 10.1111/j.1461-0248.2008.01204.x. PubMed DOI
Faegri, K. & van der Pijl, L. The principles of pollination ecology. (Pergamon Press, 1979).
Brosi BJ. Pollinator specialization: from the individual to the community. New Phytol. 2016;210:1190–1194. doi: 10.1111/nph.13951. PubMed DOI
Alaux, C., Ducloz, F., Crauser, D. & Conte, Y. L. Diet effects on honeybee immunocompetence. Biol. Lett. rsbl20090986, 10.1098/rsbl.2009.0986 (2010). PubMed PMC
Filipiak M, et al. Ecological stoichiometry of the honeybee: Pollen diversity and adequate species composition are needed to mitigate limitations imposed on the growth and development of bees by pollen quality. PLOS ONE. 2017;12:e0183236. doi: 10.1371/journal.pone.0183236. PubMed DOI PMC
Biella P, Ollerton J, Barcella M, Assini S. Network analysis of phenological units to detect important species in plant-pollinator assemblages: can it inform conservation strategies? Community Ecol. 2017;18:1–10. doi: 10.1556/168.2017.18.1.1. DOI
Seabloom EW, Dobson AP, Stoms DM. Extinction rates under nonrandom patterns of habitat loss. Proc. Natl. Acad. Sci. 2002;99:11229–11234. doi: 10.1073/pnas.162064899. PubMed DOI PMC
Gross K, Cardinale BJ. The functional consequences of random vs. ordered species extinctions. Ecol. Lett. 2005;8:409–418. doi: 10.1111/j.1461-0248.2005.00733.x. DOI
Smith KG, Lips KR, Chase JM. Selecting for extinction: nonrandom disease-associated extinction homogenizes amphibian biotas. Ecol. Lett. 2009;12:1069–1078. doi: 10.1111/j.1461-0248.2009.01363.x. PubMed DOI
Santamaría S, Galeano J, Pastor JM, Méndez M. Removing interactions, rather than species, casts doubt on the high robustness of pollination networks. Oikos. 2016;125:526–534. doi: 10.1111/oik.02921. DOI
Kaiser-Bunbury CN, Muff S, Memmott J, Müller CB, Caflisch A. The robustness of pollination networks to the loss of species and interactions: a quantitative approach incorporating pollinator behaviour. Ecol. Lett. 2010;13:442–452. doi: 10.1111/j.1461-0248.2009.01437.x. PubMed DOI
Lopezaraiza–Mikel ME, Hayes RB, Whalley MR, Memmott J. The impact of an alien plant on a native plant–pollinator network: an experimental approach. Ecol. Lett. 2007;10:539–550. doi: 10.1111/j.1461-0248.2007.01055.x. PubMed DOI
Ferrero V, et al. Effect of invader removal: pollinators stay but some native plants miss their new friend. Biol. Invasions. 2013;15:2347–2358. doi: 10.1007/s10530-013-0457-4. DOI
Goldstein J, Zych M. What if we lose a hub? Experimental testing of pollination network resilience to removal of keystone floral resources. Arthropod-Plant Interact. 2016;10:263–271. doi: 10.1007/s11829-016-9431-2. DOI
Brosi BJ, Briggs HM. Single pollinator species losses reduce floral fidelity and plant reproductive function. Proc. Natl. Acad. Sci. 2013;110:13044–13048. doi: 10.1073/pnas.1307438110. PubMed DOI PMC
Hallett, A. C., Mitchell, R. J., Chamberlain, E. R. & Karron, J. D. Pollination success following loss of a frequent pollinator: the role of compensatory visitation by other effective pollinators. AoB PLANTS9 (2017). PubMed PMC
Memmott J, Waser NM, Price MV. Tolerance of pollination networks to species extinctions. Proc. R. Soc. Lond. B Biol. Sci. 2004;271:2605–2611. doi: 10.1098/rspb.2004.2909. PubMed DOI PMC
Dafni, A., Kevan, P. G. & Husband, B. C. Practical pollination biology. (Enviroquest Ltd, 2005).
Waser NM, Chittka L, Price MV, Williams NM, Ollerton J. Generalization in pollination systems, and why it matters. Ecology. 1996;77:1043–1060. doi: 10.2307/2265575. DOI
Dormann CF. How to be a specialist? Quantifying specialisation in pollination networks. Netw. Biol. 2011;1:1–20.
Gómez JM, Bosch J, Perfectti F, Fernández J, Abdelaziz M. Pollinator diversity affects plant reproduction and recruitment: the tradeoffs of generalization. Oecologia. 2007;153:597–605. doi: 10.1007/s00442-007-0758-3. PubMed DOI
Alonso C, Herrera CM, Ashman T-L. A piece of the puzzle: a method for comparing pollination quality and quantity across multiple species and reproductive events. New Phytol. 2012;193:532–542. doi: 10.1111/j.1469-8137.2011.03932.x. PubMed DOI
Martin FW. Staining and observing pollen tubes in the style by means of fluorescence. Stain Technol. 1959;34:125–128. doi: 10.3109/10520295909114663. PubMed DOI
Kugler, H. Blütenökologie. (G. Fischer, 1970).
Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 2015;67:1–48. doi: 10.18637/jss.v067.i01. DOI
R Core Team. R: A language and environment for statistical computing. (ISBN 3-900051-07-0, 2017).
Hothorn T, Bretz F, Westfall P. Simultaneous inference in general parametric models. Biom. J. 2008;50:346–363. doi: 10.1002/bimj.200810425. PubMed DOI
Reitan T, Nielsen A. Do not divide count data with count data; a story from pollination ecology with implications beyond. PLOS ONE. 2016;11:e0149129. doi: 10.1371/journal.pone.0149129. PubMed DOI PMC
Osenberg CW, Sarnelle O, Cooper SD. Effect size in ecological experiments: the application of biological models in meta-analysis. Am. Nat. 1997;150:798–812. doi: 10.1086/286095. PubMed DOI
Pianka, E. R. The structure of lizard communities. Annu Rev Ecol Syst4, 53–74 (1973).
Dormann, C. F., Gruber, B. & Fründ, J. Introducing the bipartite package: analysing ecological networks. R news8, 8–11 (2008).
Gotelli, N. J., Hart E. M. & Ellison, A. M. EcoSimR: Null model analysis for ecological data. R package version 0.1.0. http://github.com/gotellilab/EcoSimR (2015).
Valdovinos FS, de Espanés M, Flores P, Ramos-Jiliberto JD. R. Adaptive foraging allows the maintenance of biodiversity of pollination networks. Oikos. 2013;122:907–917. doi: 10.1111/j.1600-0706.2012.20830.x. DOI
Kondoh M. Foraging adaptation and the relationship between food-web complexity and stability. Science. 2003;299:1388–1391. doi: 10.1126/science.1079154. PubMed DOI
Gilpin, A.-M., Denham, A. J. & Ayre, D. J. Are there magnet plants in Australian ecosystems: pollinator visits to neighbouring plants are not affected by proximity to mass flowering plants. Basic Appl. Ecol. 35, 34–44 (2019).
Akter A, Biella P, Klecka J. Effects of small-scale clustering of flowers on pollinator foraging behaviour and flower visitation rate. PLOS ONE. 2017;12:e0187976. doi: 10.1371/journal.pone.0187976. PubMed DOI PMC
Vizentin-Bugoni J, Maruyama PK, Sazima M. Processes entangling interactions in communities: forbidden links are more important than abundance in a hummingbird–plant network. Proc. R. Soc. Lond. B Biol. Sci. 2014;281:20132397. doi: 10.1098/rspb.2013.2397. PubMed DOI PMC
Janovský Z, et al. Conspecific and heterospecific plant densities at small-scale can drive plant-pollinator interactions. PLOS ONE. 2013;8:e77361. doi: 10.1371/journal.pone.0077361. PubMed DOI PMC
Lázaro A, Nielsen A, Totland Ø. Factors related to the inter-annual variation in plants’ pollination generalization levels within a community. Oikos. 2010;119:825–834. doi: 10.1111/j.1600-0706.2009.18017.x. DOI
Ye Z-M, et al. Competition and facilitation among plants for pollination: can pollinator abundance shift the plant–plant interactions? Plant Ecol. 2014;215:3–13. doi: 10.1007/s11258-013-0274-y. DOI
Carstensen DW, Sabatino M, Trøjelsgaard K, Morellato LPC. Beta diversity of plant-pollinator networks and the spatial turnover of pairwise interactions. PLOS ONE. 2014;9:e112903. doi: 10.1371/journal.pone.0112903. PubMed DOI PMC
Peters VE, et al. Using plant–animal interactions to inform tree selection in tree-based agroecosystems for enhanced biodiversity. BioScience. 2016;66:1046–1056. doi: 10.1093/biosci/biw140. DOI
Menz MH, et al. Reconnecting plants and pollinators: challenges in the restoration of pollination mutualisms. Trends Plant Sci. 2011;16:4–12. doi: 10.1016/j.tplants.2010.09.006. PubMed DOI
Montoya D, Rogers L, Memmott J. Emerging perspectives in the restoration of biodiversity-based ecosystem services. Trends Ecol. Evol. 2012;27:666–672. doi: 10.1016/j.tree.2012.07.004. PubMed DOI