Abstract
Interactions between a native plant species and its pollinators, herbivores, or microbiome can be affected by the presence of non-native plant species. Non-native plant species are altering plant-pollinator interactions, yet we know little about how these non-native species influence natural selection. In addition, year-to-year variation in flowering could influence the impacts of non-native species on reproductive success in native plants and the strength and direction of pollinator-mediated selection. We examined whether the presence of the highly invasive plant Linaria vulgaris influenced average pollinator visitation, species composition of floral visitors, or pollinator-mediated selection in the native Penstemon strictus. In the field, we conducted small scale L. vulgaris inflorescence removals, that were repeated through 3 years. Pollinator-mediated selection on the floral trait of platform length was examined by determining the relationships between platform length and visitation, between visitation and seed production, and by calculating net selection based on seed production. We found that the presence of L. vulgaris on a small spatial scale facilitated pollinator visitation rates to P. strictus but did not influence pollinator-mediated selection on platform length. Pollinator visitation varied across years, as did the relationship between seed production and pollinator visitation, and the relationship between pollinator visitation and platform length. Although components of selection varied across years, no net selection on platform length was detected in any of the 3 years. Our results show how the presence of an invasive plant and year-to-year variation in plant-pollinator interactions affect the pollination and components of pollinator-mediated selection in native plants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data is available in Dryad https://datadryad.org/stash/dataset/doi:10.7280/D1JM40.
References
Albor C, García-Franco JG, Parra-Tabla V et al (2019) Taxonomic and functional diversity of the co-flowering community differentially affect Cakile edentula pollination at different spatial scales. J Ecol 107:2167–2181. https://doi.org/10.1111/1365-2745.13183
Albrecht M, Ramis MR, Traveset A (2016) Pollinator-mediated impacts of alien invasive plants on the pollination of native plants: the role of spatial scale and distinct behaviour among pollinator guilds. Biol Invasions 18:1801–1812. https://doi.org/10.1007/s10530-016-1121-6
Arnold SJ, Wade MJ (1984) On the measurement of natural and sexual selection. Evolution 38:709–719. https://doi.org/10.2307/2408383
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Beans CM, Roach DA (2015) An invasive plant alters pollinator-mediated phenotypic selection on a native congener. Am J Bot 102:50–57. https://doi.org/10.3732/ajb.1400385
Benitez-Vieyra S, Glinos E, Medina AM, Cocucci AA (2012) Temporal variation in the selection on floral traits in Cyclopogon elatus (Orchidaceae). Evol Ecol 26:1451–1468. https://doi.org/10.1007/s10682-012-9565-3
Berthon K (2015) How do native species respond to invaders? Mechanistic and trait-based perspectives. Biol Invasions 17:2199–2211. https://doi.org/10.1007/s10530-015-0874-7
Bezemer TM, Harvey JA, Cronin JT (2014) Response of native insect communities to invasive plants. Annu Rev Entomol 59:119–141. https://doi.org/10.1146/annurev-ento-011613-162104
Bjerknes AL, Totland Ø, Hegland SJ, Nielsen A (2007) Do alien plant invasions really affect pollination success in native plant species? Biol Conserv 138:1–12. https://doi.org/10.1016/j.biocon.2007.04.015
Blankinship JC, Meadows MW, Lucas RG, Hart SC (2014) Snowmelt timing alters shallow but not deep soil moisture in the Sierra Nevada. Water Resour Res 50:1448–1456. https://doi.org/10.1002/2013WR014541
Brown BJ, Mitchell RJ (2001) Competition for pollination: effects of pollen of an invasive plant on seed set of a native congener. Oecologia 129:43–49. https://doi.org/10.1007/s004420100700
Brown BJ, Mitchell RJ, Graham SA (2002) Competition for pollination between an invasive species (purple loosestrife) and a native congener. Ecology 83:2328–2336. https://doi.org/10.2307/3072063
Bruckman D, Campbell DR (2016) Pollination of a native plant changes with distance and density of invasive plants in a simulated biological invasion. Am J Bot 103:1458–1465. https://doi.org/10.3732/ajb.1600153
Burkle LA, Irwin RE, Newman DA (2007) Predicting the effects of nectar robbing on plant reproduction: implications of pollen limitation and plant mating system. Am J Bot 94:1935–1943. https://doi.org/10.3732/ajb.94.12.1935
Callaway RM, Ridenour WM, Laboski T et al (2005) Natural selection for resistance to the allelopathic effects of invasive plants. J Ecol 93:576–583. https://doi.org/10.1111/j.1365-2745.2005.00994.x
Campbell DR (1985) Pollinator sharing and seed set of Stellaria pubera: competition for pollination. Ecology 66:544–553. https://doi.org/10.2307/1940403
Campbell DR, Motten AF (1985) The mechanism of competition for pollination between two forest herbs. Ecology 66:554–563. https://doi.org/10.2307/1940404
Campbell DR, Waser NM, Price MV et al (1991) Components of phenotypic selection: pollen export and flower corolla width in Ipomopsis aggregata. Evolution 45:1458–1467. https://doi.org/10.1111/j.1558-5646.1991.tb02648.x
Campbell DR, Waser NM, Price MV (1996) Mechanisms of hummingbird-mediated selection for flower width in Ipomopsis aggregata. Ecology 77:1463–1472. https://doi.org/10.2307/2265543
Campbell DR, Brody AK, Price MV et al (2017) Is plant fitness proportional to seed set? An experiment and a spatial model. Am Nat 190:818–827. https://doi.org/10.1086/694116
Caruso CM (2000) Competition for pollination influences selection on floral traits of Ipomopsis aggregata. Evolution 54:1546–1557. https://doi.org/10.1111/j.0014-3820.2000.tb00700.x
Castellanos MC, Wilson P, Thomson JD (2003) Pollen transfer by hummingbirds and bumblebees, and the divergence of pollination modes in Penstemon. Evolution 57:2742–2752. https://doi.org/10.1111/j.0014-3820.2003.tb01516.x
Castellanos MC, Wilson P, Thomson JD (2004) “Anti-bee” and “pro-bird” changes during the evolution of hummingbird pollination in Penstemon flowers. J Evol Biol 17:876–885. https://doi.org/10.1111/j.1420-9101.2004.00729.x
Charlebois JA, Sargent RD (2017) No consistent pollinator-mediated impacts of alien plants on natives. Ecol Lett 20:1479–1490
Coats VC, Rumpho ME (2014) The rhizosphere microbiota of plant invaders: an overview of recent advances in the microbiomics of invasive plants. Front Microbiol 5:1–10. https://doi.org/10.3389/fmicb.2014.00368
Fenster CB, Dudash MR (2001) Spatiotemporal variation in the role of hummingbirds as pollinators of Silene virginica. Ecology 82:844–851. https://doi.org/10.2307/2680202
Fishbein M, Venable DL (1996) Diversity and temporal change in the effective pollinators of Asclepias tuberosa. Ecology 77:1061–1073. https://doi.org/10.2307/2265576
Fishman L, Wyatt R (1999) Pollinator-mediated competition, reproductive character displacement, and the evolution of selfing in Arenaria uniflora (Caryophyllaceae). Evolution 53:1723–1733. https://doi.org/10.2307/2640435
Flanagan RJ, Mitchell RJ, Knutowski D, Karron JD (2009) Interspecific pollinator movements reduce pollen deposition and seed production in Mimulus ringens (Phrymaceae). Am J Bot 96:809–815. https://doi.org/10.3732/ajb.0800317
Galen C (1989) Measuring pollinator-mediated selection on morphometric floral traits: bumblebees and the alpine sky pilot, Polemonium viscosum. Evolution 43:882–890. https://doi.org/10.2307/2409315
Goergen EM, Leger EA, Espeland EK (2011) Native perennial grasses show evolutionary response to Bromus tectorum (cheatgrass) invasion. PLoS One 6:e18145. https://doi.org/10.1371/journal.pone.0018145
Gómez JM (2000) Phenotypic selection and response to selection in Lobularia maritima: importance of direct and correlational components of natural selection. J Evol Biol 13:689–699. https://doi.org/10.1046/j.1420-9101.2000.00196.x
Grant PR, Grant R (2002) Unpredictable evolution in a 30-year study of Darwin’s finches. Science 296:707–711. https://doi.org/10.1126/science.1070315
Harder LD, Johnson SD (2009) Darwin’s beautiful contrivances: evolutionary and functional evidence for floral adaptation. New Phytol 183:530–545. https://doi.org/10.1111/j.1469-8137.2009.02914.x
Hegland SJ, Grytnes J-A, Totland Ø (2009) The relative importance of positive and negative interactions for pollinator attraction in a plant community. Ecol Res 24:929–936. https://doi.org/10.1007/s11284-008-0572-3
Herrera CM (1988) Variation in mutualisms: the spatio-temporal mosaic of a pollinator assemblage. Biol J Linn Soc 35:95–125. https://doi.org/10.1111/j.1095-8312.1988.tb00461.x
Horvitz CC, Schemske DW (1990) Spatiotemporal variation in insect mutualists of a neotropical herb. Ecology 71:1085–1097. https://doi.org/10.2307/1937377
Iwao K, Rausher MD (1997) Evolution of plant resistance to multiple herbivores: quantifying diffuse coevolution. Am Nat 149:316–335. https://doi.org/10.1086/285992
Jakobsson A, Padrón B (2014) Does the invasive Lupinus polyphyllus increase pollinator visitation to a native herb through effects on pollinator population sizes? Oecologia 174:217–226. https://doi.org/10.1007/s00442-013-2756-y
Kingsolver JG, Hoekstra HE, Hoekstra JM et al (2001) The strength of phenotypic selection in natural populations. Am Nat 157:245–261. https://doi.org/10.1086/319193
Lau JA (2008) Beyond the ecological: biological invasions alter natural selection on a native plant species. Ecology 89:1023–1031. https://doi.org/10.1890/06-1999.1
Lau JA (2012) Evolutionary indirect effects of biological invasions. Oecologia 170:171–181. https://doi.org/10.1007/s00442-012-2288-x
Molina-Montenegro MA, Badano EI, Cavieres LA (2008) Positive interactions among plant species for pollinator service: assessing the ‘magnet species’ concept with invasive species. Oikos 117:1833–1839. https://doi.org/10.1111/j.0030-1299.2008.16896.x
Morales CL, Traveset A (2009) A meta-analysis of impacts of alien vs. native plants on pollinator visitation and reproductive success of co-flowering native plants. Ecol Lett 12:716–728. https://doi.org/10.1111/j.1461-0248.2009.01319.x
Oduor AMO (2013) Evolutionary responses of native plant species to invasive plants: a review. New Phytol 200:986–992. https://doi.org/10.1111/nph.12429
Ogilvie JE, Griffin SR, Gezon ZJ et al (2017) Interannual bumble bee abundance is driven by indirect climate effects on floral resource phenology. Ecol Lett 20:1507–1515. https://doi.org/10.1111/ele.12854
Ogle D, Peterson S, St. John L (2013) Plant guide for Rocky Mountain penstemon (Penstemon strictus). USDA-Natural Resources Conservation Service, Plant Materials Center, Aberdeen
Price MV, Waser NM, Irwin RE et al (2005) Temporal and spatial variation in pollination of a montane herb: a seven-year study. Ecology 86:2106–2116. https://doi.org/10.1890/04-1274
Rafferty NE, Ives AR (2012) Pollinator effectiveness varies with experimental shifts in flowering time. Ecology 93:803–814. https://doi.org/10.1890/11-0967.1
R Core Team (2018) R: a language and environment for statistical computing
Recart W, Ottoson B, Campbell DR (2019) Water influences how seed production responds to conspecific and heterospecific pollen. Am J Bot 106:1–9. https://doi.org/10.1002/ajb2.1273
Sahli HF, Conner JK (2007) Visitation, effectiveness, and efficiency of 15 genera of visitors to wild radish, Raphanus raphanistrum (Brasicaceae). Am J Bot 94:203–209. https://doi.org/10.3732/ajb.94.2.203
Saner MA, Clements DR, Hall MR et al (1995) The biology of Canadian weeds. 105. Linaria vulgaris Mill. Can J Plant Sci 75:525–537. https://doi.org/10.4141/cjps76-052
Stanton ML, Snow AA, Handel SN (1986) Floral evolution: attractiveness to pollinators increases male fitness. Science 232:1625–1627. https://doi.org/10.1126/science.232.4758.1625
Thomson JD (1996) Trapline foraging by bumblebees: I. Persistence of flight-path geometry. Behav Ecol 7:158–164. https://doi.org/10.1093/beheco/7.2.158
Traveset A, Richardson DM (2006) Biological invasions as disruptors of plant reproductive mutualisms. Trends Ecol Evol 21:208–216. https://doi.org/10.1016/j.tree.2006.01.006
USDA, NRCS (2020) The PLANTS database. In: National plant data team, Greensboro, NC, 27401-4901, USA. http://plants.usda.gov. Accessed 5 Mar 2020
Waser NM, Price MV (2016) Drought, pollen and nectar availability, and pollination success. Ecology 97:1400–1409. https://doi.org/10.1890/15-1423.1
Wassink E, Caruso CM (2013) Effect of coflowering Mimulus ringens on phenotypic selection on floral traits of gynodioecious Lobelia siphilitica. Botany 91:745–751. https://doi.org/10.1139/cjb-2013-0112
Wilson P, Castellanos MC, Hogue JN et al (2004) A multivariate search for pollination syndromes among Penstemons. Oikos 104:345–361. https://doi.org/10.1111/j.0030-1299.2004.12819.x
Yang CF, Wang QF, Guo YH (2013) Pollination in a patchily distributed lousewort is facilitated by presence of a co-flowering plant due to enhancement of quantity and quality of pollinator visits. Ann Bot 112:1751–1758. https://doi.org/10.1093/aob/mct228
Zung JL, Forrest JRK, Castellanos MC, Thomson JD (2015) Bee- to bird-pollination shifts in Penstemon: effects of floral-lip removal and corolla constriction on the preferences of free-foraging bumble bees. Evol Ecol 29:341–354. https://doi.org/10.1007/s10682-014-9716-9
Acknowledgements
We thank Ashley Morse, Alexandra Faidiga, M. Kate Gallagher, Hannah Clements, Paula Sosenski, Victoria Luizzi, Victor Prestinary, Amanda Barth and Judith Trunschke for aiding with data collection, and M. Kate Gallagher, Heather Briggs, Steve Weller, John Powers, and two anonymous reviewers for providing feedback on this manuscript. We thank the Rocky Mountain Biological Laboratory for providing access to facilities and instrumentation and the Crested Butte Land Trust for access to the field sites. This work was supported by the Rocky Mountain Biological Laboratory Graduate Student Research Fellowships, Colorado Mountain Club Foundation Student Research Awards, Botanical Society of America Graduate Student Research Award, National Science Foundation Graduate Research Fellowship under Grant No. [DGE-1321846], and the University of California Eugene Cota-Robles Fellowship.
Funding
This work was supported by the Rocky Mountain Biological Laboratory Graduate Student Research Fellowships, Colorado Mountain Club Foundation Student Research Awards, Botanical Society of America Graduate Student Research Award, National Science Foundation Graduate Research Fellowship under Grant No. [DGE-1321846], and the University of California Eugene Cota-Robles Fellowship.
Author information
Authors and Affiliations
Contributions
WRG developed the questions; WRG and DRC contributed to the experimental design; WRG conducted fieldwork experiments and collected data; WRG and DRC contributed to the data analysis and interpretation; WRG led the writing of the manuscript, with revisions by DRC. Both authors gave final approval for publication.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Recart, W., Campbell, D.R. Unraveling the ecological and evolutionary impacts of a plant invader on the pollination of a native plant. Biol Invasions 23, 1533–1547 (2021). https://doi.org/10.1007/s10530-021-02457-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-021-02457-z