Abstract
Pollen limitation can strongly influence reproduction of pollinator-dependent plants. Flower abundance can affect pollination ‘quantity’ and ‘quality’ due to its influence on pollen availability and foraging patterns of pollinators, ultimately impacting on seed production. We complemented individual-based measurements with landscape-level metrics to assess the influence of conspecific flower availability at different spatial scales on the quantity and quality components of pollination, and their impact on seed production in the invasive shrub Cytisus scoparius. In 2013–2014, we sampled 40 C. scoparius populations in Nahuel Huapi National Park, Patagonia (Argentina). In each population, we estimated the proportion of tripped flowers, fruit- and seed-set in five randomly selected individuals. The proportion of tripped flowers and the proportion of them setting fruit were used as proxies of pollination quantity and quality, respectively. Conspecific flower availability at distinct spatial scales (5–1000 m) was estimated as the area covered by flowering C. scoparius from color aerial photographs. Flower availability influenced seed output due to contrasting scale-dependent effects on pollination quantity and quality. Increasing flower availability at the landscape-scale reduced pollination quantity, whereas at the neighborhood-scale it increased pollination quality. The overall positive effect of flower availability on seed output at the neighborhood scale was slightly higher than the overall negative effect at the landscape scale. Moreover, pollination quality had a higher positive effect on seed output than pollination quantity. Our results demonstrate that pollination quality may severely limit plant reproduction. Pollination quality limitation can act independently of pollination quantity limitation because these factors operate at different spatial scales.
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References
Agren J (1996) Population size, pollinator limitation, and seed set in the self-incompatible herb Lythrum salicaria. Ecology 77:1779–1790. https://doi.org/10.2307/2265783
Aizen MA (1997) Influence of local floral density and sex ratio on pollen receipt and seed output: empirical and experimental results in dichogamous Alstroemeria aurea (Alstroemeriaceae). Oecologia 111:404–412. https://doi.org/10.1007/s004420050252
Aizen MA, Harder LD (2007) Expanding the limits of the pollen-limitation concept: effects of pollen quantity and quality. Ecology 88:271–281. https://doi.org/10.1890/06-1017
Aizen MA, Morales CL, Morales JM (2008) Invasive mutualists erode native pollination webs. PLoS Biol 6:e31. https://doi.org/10.1371/journal.pbio.0060031
Aizen MA, Smith-Ramírez C, Morales CL, Vieli L, Sáez A, Barahona-Segovia RM, Arbetman MP, Montalva J, Garibaldi LA, Inouye DW, Harder LD (2018) Coordinated global species-importation policies are needed to reduce serious invasions globally: the case of alien bumble bees in South America. J Appl Ecol 00:1–7. https://doi.org/10.1111/1365-2664.13121
Ashman TL, Knight TM, Steets JA, Amarasekare P, Burd M, Campbell DR, Dudash MR, Johnston MO, Mazer SJ, Mitchell RJ, Morgan MT, Wilson WG (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85:2408–2421. https://doi.org/10.1890/03-8024
Barros VR, Cordon V, Moyano C, Méndez R, Forquera J, Pizzio O (1983) Cartas de precipitación de la zona oeste de las provincias de Río Negro y Neuquén. Universidad Nacional del Comahue, Neuquén
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Soft 67:1–48
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
Bode RF, Tong R (2017) Pollinators exert positive selection on flower size on urban, but not on rural Scotch broom (Cytisus scoparius L. Link). J Plant Ecol. https://doi.org/10.1093/jpe/rtx024
Bolker BM, Fournier D, Skaug H, Magnusson A, Nielsen A (2012) Generalized linear mixed models using AD model builder. R package version 2.15
Bosch M, Waser NM (1999) Effects of local density on pollination and reproduction in Delphinium nuttallianum and Aconitum columbianum (Ranunculaceae). Am J Bot 86:871–879. https://doi.org/10.2307/2656707
Bosch M, Waser NM (2001) Experimental manipulation of plant density and its effect on pollination and reproduction of two confamilial montane herbs. Oecologia 126:76–83. https://doi.org/10.1007/s004420000488
Bossard CC, Rejmanek M (1994) Herbivory, growth, seed production, and resprouting of an exotic invasive shrub Cytisus scoparius. Biol Conserv 67:193–200. https://doi.org/10.1016/0006-3207(94)90609-2
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/10.1890/0012-9658(2002)083%5b2328:CFPBAI%5d2.0.CO;2
Caldwell BA (2006) Effects of invasive scotch broom on soil properties in a pacific coastal prairie soil. Appl Soil Ecol 32:149–152. https://doi.org/10.1016/j.apsoil.2004.11.008
Chittka L, Gumbert A, Kunze J (1997) Foraging dynamics of bumble bees: correlates of movements within and between plant species. Behav Ecol 8:239–249. https://doi.org/10.1093/beheco/8.3.239
Colling G, Reckinger C, Matthies D (2004) Effects of pollen quantity and quality on reproduction and offspring vigor in the rare plant Scorzonera humilis (Asteraceae). Am J Bot 91:1774–1782. https://doi.org/10.3732/ajb.91.11.1774
Cordero RL, Torchelsen FP, Overbeck GE, Anand M (2016) Cytisus scoparius (Fam. Fabaceae) in southern Brazil-first step of an invasion process? Anais Acad Brasileira Ciências 88:149–154. https://doi.org/10.1590/0001-3765201620140532
Downey PO, Smith JMB (2000) Demography of the invasive shrub scotch broom (Cytisus scoparius) at Barrington Tops, New South Wales: insights for management. Austral Ecol 25:477–485. https://doi.org/10.1046/j.1442-9993.2000.01083.x
Ehlers BK, Olesen JM, Ågren J (2002) Floral morphology and reproductive success in the orchid Epipactis helleborine: regional and local across-habitat variation. Plant Syst Evol 236:19–32. https://doi.org/10.1007/s00606-002-0197-x
Fernández N (2007) Plantas exóticas invasoras de los parques nacionales de Patagonia. Delegación Regional Patagonia (APN)-Universidad Nacional del Comahue (UNCOMA)
Fogarty G, Facelli JM (1999) Growth and competition of Cytisus scoparius, an invasive shrub, and australian native shrubs. Plant Ecol 144:27–35. https://doi.org/10.1023/A:1009808116068
Garibaldi LA, Steffan-Dewenter I, Kremen C, Morales JM, Bommarco R, Cunningham SA et al (2011) Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecol Lett 14:1062–1072. https://doi.org/10.1111/j.1461-0248.2011.01669.x
Garibaldi LA, Carvalheiro LG, Leonhardt SD, Aizen MA, Blaauw BR, Isaacs R et al (2014) From research to action: enhancing crop yield through wild pollinators. Front Ecol Environ 12:439–447. https://doi.org/10.1890/130330
Garibaldi LA, Gemmill-Herren B, D’Annolfo R, Graeub BE, Cunningham SA, Breeze TD (2017) Farming approaches for greater biodiversity, livelihoods, and food security. Trends Ecol Evol 32:68–80. https://doi.org/10.1016/j.tree.2016.10.001
Gavini SS, Farji-Brener AG (2015) La importancia del color: morfos florales, tasas de visita y éxito reproductivo en el arbusto Sarothamnus scoparius. Ecol Austral 25:204–211
Ghazoul J (2005) Pollen and seed dispersal among dispersed plants. Biol Rev Camb Philos Soc 80:413–443. https://doi.org/10.1017/S1464793105006731
Gillespie SD, Bayley J, Elle E (2017) Native bumble bee (Hymenoptera: Apidae) pollinators vary in floral resource use across an invasion gradient. Can Entomol 149:204–213. https://doi.org/10.4039/tce.2016.67
Goulson D (2005) Risks of increased weed problems associated with introduction of non-native bee species. J Food Agric Environ 3: 11–13. http://hdl.handle.net/1893/7325. Accessed 26 July 2018
Goverde M, Schweizer K, Baur B, Erhardt A (2002) Small-scale habitat fragmentation effects on pollinator behaviour: experimental evidence from the bumblebee Bombus veteranus on calcareous grasslands. Biol Conserv 104:293–299. https://doi.org/10.1016/S0006-3207(01)00194-X
Green DR, Cummins R, Right R, Miles J (1993) A methodology for acquiring information on vegetation succession from remotely sensed imagery. In: Haines-Young R, Green DR, Cousins S (eds) Landscape ecology and GIS. Taylor and Francis, London, pp 111–128
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. Proc R Soc Lond B Biol Sci. https://doi.org/10.1098/rspb.2011.0268
IPBES (2016) Chapter 1 - Background to pollinators, pollination and food production. In: Potts SG, Imperatriz-Fonseca VL, Ngo HT (eds) Secretariat of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services, Bonn, p 552
Jakobsson A, Lázaro A, Totland Ø (2009) Relationships between the floral neighborhood and individual pollen limitation in two self-incompatible herbs. Oecologia 160:707–719. https://doi.org/10.1007/s00442-009-1346-5
Kadmon R, Harari-Kremer R (1999) Studying long-term vegetation dynamics using digital processing of historical aerial photographs. Remote Sens Environ 68:164–176. https://doi.org/10.1016/S0034-4257(98)00109-6
Kandori I, Hirao T, Matsunaga S, Kurosaki T (2009) An invasive dandelion unilaterally reduces the reproduction of a native congener through competition for pollination. Oecologia 159:559–569. https://doi.org/10.1007/s00442-008-1250-4
Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241. https://doi.org/10.1016/S0169-5347(02)02489-8
Knight TM (2003) Floral density, pollen limitation, and reproductive success in Trillium grandiflorum. Oecologia 135:557–563. https://doi.org/10.1007/s00442-003-1371-8
Kolb A (2005) Reduced reproductive success and offspring survival in fragmented populations of the forest herb Phyteuma spicatum. J Ecol 93:1226–1237. https://doi.org/10.1111/j.1365-2745.2005.01049.x
Kunin WE (1993) Sex and the single mustard: population density and pollinator behavior effects on seed-set. Ecology 74:2145–2160. https://doi.org/10.2307/1940859
Kunin WE (1997) Population size and density effects in pollination: pollinator foraging and plant reproductive success in experimental arrays of Brassica kaber. J Ecol 85:225–234
Mayer C, Michez D, Chyzy A, Brédat E, Jacquemart AL (2012) The abundance and pollen foraging behaviour of bumble bees in relation to population size of whortleberry (Vaccinium uliginosum). PLoS ONE 7:e50353. https://doi.org/10.1371/journal.pone.0050353
Morales CL, Aizen MA (2002) Does invasion of exotic plants promote invasion of exotic flower visitors? A case study from the temperate forests of the southern Andes. Biol Invations 4:87–100. https://doi.org/10.1023/A:1020513012689
Morales CL, Traveset A (2008) Interspecific pollen transfer: magnitude, prevalence and consequences for plant fitness. Crit Rev Plant Sci 27:221–238. https://doi.org/10.1080/07352680802205631
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
Morales CL, Arbetman MP, Cameron SA, Aizen MA (2013) Rapid ecological replacement of a native bumble bee by invasive species. Front Ecol Environ 11:529–534. https://doi.org/10.1890/120321
Morales CL, Saez A, Arbetman MP, Cavallero L, Aizen MA (2014) Detrimental effects of volcanic ash deposition on bee fauna and plant-pollinator interactions. Ecol Austral 24:42–50
Muir JL, Vamosi JC (2015) Invasive Scotch broom (Cytisus scoparius, Fabaceae) and the pollination success of three Garry oak-associated plant species. Biol Invations 17:2429–2446. https://doi.org/10.1007/s10530-015-0886-3
Osborne JL, Clark SJ, Morris RJ, Williams IH, Riley JR, Smith AD, Reynolds DR, Edwards AS (1999) A landscape-scale study of bumble bee foraging range and constancy, using harmonic radar. J Appl Ecol 36:519–533. https://doi.org/10.1046/j.1365-2664.1999.00428.x
Parker IM (1997) Pollinator limitation of Cytisus scoparius (scotch broom), an invasive exotic shrub. Ecology 78:1457–1470. https://doi.org/10.1890/0012-9658(1997)078%5b1457:PLOCSS%5d2.0.CO;2
Parker IM (2000) Invasion dynamics of Cytisus scoparius: a matrix model approach. Ecol Appl 10:726–743. https://doi.org/10.1890/1051-0761(2000)010%5b0726:IDOCSA%5d2.0.CO;2
Parker IM, Haubensak KA (2002) Comparative pollinator limitation of two non-native shrubs: do mutualisms influence invasions? Oecologia 130:250–258. https://doi.org/10.1007/s004420100799
Paynter Q, Main A, Hugh Gourlay A, Peterson PG, Fowler SV, Buckley YM (2010) Disruption of an exotic mutualism can improve management of an invasive plant: varroa mite, honeybees and biological control of Scotch broom Cytisus scoparius in New Zealand. J Appl Ecol 47:309–317. https://doi.org/10.1111/j.1365-2664.2010.01784.x
Pérez A (2008) Reserva de la Biosfera Andino Norpatagonica. In: Karez CS, Schüttler E (eds) Especies exóticas invasoras en las Reservas de Biosfera de América Latina y el Caribe. Un informe técnico para fomentar el intercambio de experiencias entre las Reservas de Biosfera y promover el manejo efectivo de las invasiones biológicas. UNESCO, Montevideo
Potter KJB, Kriticos DJ, Watt MS, Leriche A (2009) The current and future potential distribution of Cytisus scoparius: a weed of pastoral systems, natural ecosystems and plantation forestry. Weed Res 49:271–282. https://doi.org/10.1111/j.1365-3180.2009.00697.x
R Development Core Team (2012) R: a language and environment forstatistical computing. Version 2.15.1. R Foundation for Statistical Computing, Vienna
Rathcke B (1983) Competition and facilitation among plants for pollination. In: Real E (ed) Pollination biology. Academic Press, Orlando, pp 305–329
Riedinger V, Renner M, Rundlöf M, Steffan-Dewenter I, Holzschuh A (2014) Early mass-flowering crops mitigate pollinator dilution in late-flowering crops. Landscape Ecol 29:425–435. https://doi.org/10.1007/s10980-013-9973-y
Sargent RD, Angert AL, Williams JL (2017) When are species invasions useful for addressing fundamental questions in plant biology? Am J Bot 104:797–799. https://doi.org/10.3732/ajb.1700087
Schmitt J (1980) Pollinator foraging behavior and gene dispersal in Senecio (Compositae). Evolution 34:934–943. https://doi.org/10.1111/j.1558-5646.1980.tb04031.x
Sheppard AW, Hodge P, Paynter Q, Rees M (2002) Factors affecting invasion and persistence of broom Cytisus scoparius in Australia. J Appl Ecol 39:721–734. https://doi.org/10.1046/j.1365-2664.2002.00750.x
Shipley B (2000) Cause and correlation in biology. A user’s guide to path analysis, structural equations and causal inference with R. Cambridge University Press, Cambridge, pp 1–63
Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Inv 1:21–32. https://doi.org/10.1023/A:1010086329619
Simpson SR, Gross CL, Silberbauer LX (2005) Broom and honeybees in Australia: an alien liaison. Plant Biol 7:541–548. https://doi.org/10.1055/s-2005-865855
Smith JMB, Harlen RL (1991) Preliminary observations on the seed dynamics of broom (Cytisus scoparius) at Barrington Tops, New South Wales. Plant Prot Q 6:73–78
Souto CP, Aizen MA, Premoli AC (2002) Effects of crossing distance and genetic relatedness on pollen performance in Alstroemeria aurea (Alstroemeriaceae). Am J Bot 89:427–432. https://doi.org/10.3732/ajb.89.3.427
Spigler RB, Chang SM (2008) Effects of plant abundance on reproductive success in the biennial Sabatia angularis (Gentianaceae): spatial scale matters. J Ecol 96:323–333. https://doi.org/10.1111/j.1365-2745.2007.01335.x
Steffan-Dewenter I, Münzenberg U, Tscharntke T (2001) Pollination, seed set and seed predation on a landscape scale. Proc R Soc Lond B Biol Sci 268:1685–1690. https://doi.org/10.1098/rspb.2001.1737
Steffan-Dewenter I, Münzenberg U, Bürger C, Thies C, Tscharntke T (2002) Scale-dependent effects of landscape context on three pollinator guilds. Ecology 83:1421–1432. https://doi.org/10.1890/0012-9658(2002)083%5b1421:SDEOLC%5d2.0.CO;2
Stout J (2000) Does size matter? Bumblebee behaviour and the pollination of Cytisus scoparius L. (Fabaceae). Apidologie 31:129–139. https://doi.org/10.1051/apido:2000111
Suzuki N (2000) Pollinator limitation and resource limitation of seed production in the scotch broom, Cytisus scoparius (Leguminosae). Plant Species Biol 15:187–193. https://doi.org/10.1046/j.1442-1984.2000.00038.x
Vamosi JC, Knight TM, Steets JA, Mazer SJ, Burd M, Ashman TL (2006) Pollination decays in biodiversity hotspots. Proc Nat Acad Sci 103:956–961. https://doi.org/10.1073/pnas.0507165103
Vázquez DP, Morris WF, Jordano P (2005) Interaction frequency as a surrogate for the total effect of animal mutualists on plants. Ecol Lett 8:1088–1094. https://doi.org/10.1111/j.1461-0248.2005.00810.x
Vitousek PM, D’Antonio CM, Loope LL, Rejmanek M, Westbroocks R (1997) Introduced species: a significant component of human-caused global change. NZ J Ecol 21:1–16
Waites AR, Ågren J (2004) Pollinator visitation, stigmatic pollen loads and among-population variation in seed set in Lythrum salicaria. J Ecol 92:512–526. https://doi.org/10.1111/j.0022-0477.2004.00893.x
Walther-Hellwig K, Frankl R (2000) Foraging habitats and foraging distances of bumblebees, Bombus spp. (Hym., Apidae), in an agricultural landscape. J Appl Entom 124:299–306. https://doi.org/10.1046/j.1439-0418.2000.00484.x
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York, 574 p
Acknowledgements
We thank Matías Carruitero and Mailén Latorre for helping with fieldwork, Gustavo Santamaria for providing the aerial photographs and Anabella Fantozzi for digitalization of aerial photographs. Gabriela Gleiser, Vanina Chalcoff and José Vesprini provided valuable comments and suggestions on an earlier draft. We also thank the National Park Administration of Argentina (APN) for allowing us to work in Nahuel Huapi National Park. This study was funded by PICT 2012-3015 to CLM and MAA. LC, CLM, JHG and MAA are researchers at the National Research Council of Argentina (CONICET). AMC was supported by a JAE-predoc fellowship and by an Alien Challenge COST-Action Short Term Scientific Mission.
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LC, CLM and MAA conceived the ideas and designed methodology; LC and AMC collected the data; LC and JHG analysed the data; LC, CLM and MAA led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.
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Communicated by Amy Parachnowitsch.
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Cavallero, L., Morales, C.L., Montero-Castaño, A. et al. Scale-dependent effects of conspecific flower availability on pollination quantity and quality in an invasive shrub. Oecologia 188, 501–513 (2018). https://doi.org/10.1007/s00442-018-4239-7
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DOI: https://doi.org/10.1007/s00442-018-4239-7