Abstract
Invasive plants may decrease native plant density and disrupt interactions between native plants and their pollinators. We hypothesized that invasive Solidago canadensis (Asteraceae) competes for pollination services with two confamilial species, Ixeris chinensis and Sonchus arvensis. Breeding-system studies revealed that both native species are self-incompatible. In plots with all three species we found that Solidago received the highest visitation rates. To test the hypothesis of competition for pollination in the context of reduced native density, we established 3 plots for both native species with three Solidago densities (uninvaded, 50 and 75 % invaded) and corresponding decreases in native density. We investigated the effects of varying densities of Solidago on honeybee visitation rates, number of successive visits within individual ramets, pollen-load composition on bees, and seed set. For both native species, increasing Solidago density and decreasing native density resulted in bees carrying higher ratios of Solidago pollen and in bees visiting fewer capitula prior to departing from a plant. However, for other aspects of pollination, the native species responded very differently to Solidago. With increasing Solidago and decreasing native density, Ixeris received fewer honeybee visits and produced fewer seeds, demonstrating competition for pollination, but Sonchus attracted more honeybee visits and showed a non-significant trend toward setting more seeds, suggesting facilitation. These opposing effects occurred despite similarities in the native species’ floral morphology, suggesting that the effects of invasive plants are difficult to predict. In this case the different effects may relate to Sonchus being a taller plant with larger flowers.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Albert MJ, Iriondo JM, Escudero A, Torres E (2008) Dissecting components of flowering pattern: size effects on female fitness. Bot J Linn Soc 156:227–236. doi:10.1111/j.1095-8339.2007.00735.x
Andersson S (2008) Pollinator and nonpollinator selection on ray morphology in Leucanthemum vulgare (Oxeye daisy, Asteraceae). Am J Bot 95:1072–1078. doi:10.3732/ajb.0800087
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. doi:10.1890/03-8024
Bartomeus I, Bosch J, Vila M (2008a) High invasive pollen transfer, yet low deposition on native stigmas in a Carpobrotus-invaded community. Ann Bot 102:417–424. doi:10.1093/aob/mcn109
Bartomeus I, Vila M, Santamaria L (2008b) Contrasting effects of invasive plants in plant-pollinator networks. Oecologia 155:761–770. doi:10.1007/s00442-007-0946-1
Bartomeus I, Vila M, Steffan-Dewenter I (2010) Combined effects of Impatiens glandulifera invasion and landscape structure on native plant pollination. J Ecol 98:440–450. doi:10.1111/j.1365-2745.2009.01629.x
Benitez-Vieyra S, Medina AM, Glinos E, Cocucci AA (2006) Pollinator-mediated selection on floral traits and size of floral display in Cyclopogon elatus, a sweat bee-pollinated orchid. Func Ecol 20:948–957. doi:10.1111/j.1365-2435.2006.01179.x
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. doi:10.1016/j.biocon.2007.04.015
Brown BJ, Mitchell RJ, Graham SA (2002) Competition for pollination between an invasive species (purple loosestrife) and a native congener. Ecology 83:2328–2336. doi:10.2307/3072063
Burd M (1994) Bateman’s principle and plant reproduction, the role of pollen limitation in fruit and seed set. Bot Rev 60:83–139. doi:10.1007/BF02856594
Burkle LA, Alarcón R (2011) The future of plant–pollinator diversity: understanding interaction networks across time, space, and global change. Am J Bot 98:528–538. doi:10.3732/ajb.1000391
Carromero W, Hamrick JL (2005) Determinants of local abundance and range size in forest vascular plants. Int J Plant Sci 166:979–983. doi:10.1086/449315
Chen YC (1993) Apiculture in China. China Agriculture Press, Beijing
Chittka L, Schürkens S (2001) Successful invasion of a floral market—an exotic Asian plant has moved in on Europe’s river-banks by bribing pollinators. Nature 411:653. doi:10.1038/35079676
Chu S (1997) Flora of China: Compositae, vol 80. Science Publisher, Beijing
Dicks LV, Corbet SA, Pywell RF (2002) Compartmentalization in plant-insect flower visitor webs. J Anim Ecol 71:32–43. doi:10.1046/j.0021-8790.2001.00572.x
Dietzsch AC, Stanley DA, Stout JC (2011) Relative abundance of an invasive alien plant affects native pollination processes. Oecologia 167:469–479. doi:0.1007/s00442-011-1987-z
Dong M, Lu BR, Zhang HB, Chen JK, Li B (2006a) Role of sexual reproduction in the spread of an invasive clonal plant Solidago canadensis revealed using intersimple sequence repeat markers. Plant Spec Biol 21:13–18. doi:10.1111/j.1442-1984.2006.00146.x
Dong M, Lu JZ, Zhang WJ, Chen JK, Li B (2006b) Canada goldenrod (Solidago canadensis): an invasive alien weed rapidly spreading in China. Acta Phytotaxon Sin 44:72–85. doi:10.1360/aps050068
Feinsinger PH, Tiebout MI, Young BE (1991) Do tropical bird-pollinated plants exhibit density-dependent interactions? field experiments. Ecology 72:1953–1963. doi:10.2307/1941550
Feldman TS, Morris WF, Wilson WG (2004) When can two plant species facilitate each other’s pollination? Oikos 105:197–207. doi:10.1111/j.0030-1299.2004.12845.x
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. doi:10.3732/ajb.0800317
Flanagan RJ, Mitchell RJ, Karron JD (2010) Increased relative abundance of an invasive competitor for pollination, Lythrum salicaria, reduces seed number in Mimulus ringens. Oecologia 164:445–454. doi:10.1007/s00442-010-1693-2
Ghazoul J (2006) Floral diversity and the facilitation of pollination. J Ecol 94:295–304. doi:10.1111/j.1365-2745.2006.01098.x
Gibson MR, Richardson DM, Pauw A (2012) Can floral traits predict an invasive plant’s impact on native plant–pollinator communities? J Ecol 100:1216–1223. doi:10.1111/j.1365-2745.2012.02004.x
Gordon DR (1998) Effects of invasive, non-indigenous plant species on ecosystem processes, lessons from Florida. Ecol Appl 8:975–989. doi:10.2307/2640955
Gross RS, Werner PA (1983) Relationships among flowering phenology, insect visitors, and seed-set of individuals-experimental studies on 4 co-occurring species of goldenrod (Solidago, Compositae). Ecol Monogr 53:95–117. doi:10.2307/1942589
Kaiser-Bunbury CN, Valentin T, Mougal J, Matatiken D, Ghazoul J (2011) The tolerance of island plant-pollinator networks to alien plants. J Ecol 99:202–213. doi:10.1111/j.1365-2745.2010.01732.x
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. doi:10.1007/s00442-008-1250-4
Kearns CA, Inouye DW (1993) Techniques for pollination biologist. University Press of Colorado, Colorado
Kunin WE (1993) Sex and the single mustard: population density and pollinator behavior effects on seed-set. Ecology 74:2145–2160. doi:10.2307/1940859
Kunin WE, Shmida A (1997) Plant reproductive traits as a function of local, regional, and global abundance. Conserv Biol 11:183–192. doi:10.1046/j.1523-1739.1997.95469.x
Kwak MM, Jennersten O (1991) Bumblebee visitation and seed set in Melampyrum pratense and Viscaria vulgaris—heterospecific pollen and pollen limitation. Oecologia 86:99–104. doi:10.1007/BF00317395
Larson BMH, Barrett SCH (2000) A comparative analysis of pollen limitation in flowering plants. Biol J Linn Soc 69:503–520. doi:10.1111/j.1095-8312.2000.tb01221.x
Larson DL, Royer RA, Royer MR (2006) Insect visitation and pollen deposition in an invaded prairie plant community. Biol Conserv 130:148–159. doi:10.1016/j.biocon.2005.12.009
Laverty TM (1992) Plant interactions for pollinator visits—a test of the magnet species effect. Oecologia 89:502–508
Lema WK, Messersmith CG (1990) The biology of Canadian weeds. 94. Sonchus arvensis L. Can J Plant Sci 70:509–532
Li ZY, Xie Y (2002) Invasive alien species in China. China Forestry Publishing House, Beijing
Lopezaraiza-Mikel ME, Hayes RB, Whalley MR, Memmott J (2007) The impact of an alien plant on a native plant-pollinator network: an experimental approach. Ecol Let 10:539–550. doi:10.1111/j.1461-0248.2007.01055.x
Lortie CJ, Aarssen LW (1999) The advantage of being tall: higher flowers receive more pollen in Verbascum thapsus L. (Scrophulariaceae). Ecoscience 6:68–71
McKinney AM, Goodell K (2010) Shading by invasive shrub reduces seed production and pollinator services in a native herb. Biol Invasions 12:2751–2763. doi:10.1007/s10530-009-9680-4
McKinney AM, Goodell K (2011) Plant-pollinator interactions between an invasive and native plant vary between sites with different flowering phenology. Plant Ecol 212:1025–1035. doi:10.1007/s11258-010-9882-y
Meiners SJ, Pickett STA, Cadenasso ML (2001) Effects of plant invasions on the species richness of abandoned agricultural land. Ecography 24:633–644
Memmott J, Waser NM (2002) Integration of alien plants into a native flower-pollinator visitation web. Proc R Soc Lond B 269:2395–2399. doi:10.1098/rspb.2002.2174
Mitchell RJ, Flanagan RJ, Brown BJ, Waser NM, Karron JD (2009) New frontiers in competition for pollination. Ann Bot 103:1403–1413. doi:10.1093/aob/mcp062
Moeller DA (2004) Facilitative interactions among plants via shared pollinators. Ecology 85:3289–3301. doi:10.1890/03-0810
Montgomery BR (2009a) Do pollen carryover and pollinator constancy mitigate effects of competition for pollination? Oikos 118:1084–1092. doi:10.1111/j.1600-0706.2009.17064.x
Montgomery BR (2009b) Effect of introduced Euphorbia esula on the pollination of Viola pedatifida. Botany-Botanique 87:283–292. doi:10.1139/b08-139
Montgomery BR (2009c) Pollination of Sisyrinchium campestre (Iridaceae) in prairies invaded by the introduced pant Euphorbia esula (Euphorbiaceae). Am Midl Nat 162:239–252. doi:10.1674/0003-0031-162.2.239
Moragues E, Traveset A (2005) Effect of Carpobrotus spp. on the pollination success of native plant species of the Balearic Islands. Biol Conserv 122:611–619. doi:10.1016/j.biocon.2004.09.015
Morales CL, Traveset A (2009) A meta-analysis of impacts of alien versus native plants on pollinator visitation and reproductive success of co-flowering native plants. Ecol Let 12:716–728. doi:10.1111/j.1461-0248.2009.01319.x
Moron D, Lenda M, Skorka P, Szentgyorgyi H, Settele J, Woyciechowski M (2009) Wild pollinator communities are negatively affected by invasion of alien goldenrods in grassland landscapes. Biol Conserv 142:1322–1332. doi:10.1016/j.biocon.2008.12.036
Motten AF (1982) Autogamy and competition for pollinators in Hepatica americana (Ranunculaceae). Am J Bot 69:1296–1305. doi:10.2307/2442754
Muñoz AA, Cavieres LA (2008) The presence of a showy invasive plant disrupts pollinator service and reproductive output in native alpine species only at high densities. J Ecol 96:459–467. doi:10.1111/j.1365-2745.2008.01361.x
Page RG (2012) The Cistus and Halimium website. http://www.cistuspage.org.uk/. Accessed 1 Jan 2012
Powell KI, Krakos KN, Knight TM (2011) Comparing the reproductive success and pollination biology of an invasive plant to its rare and common native congeners: a case study in the genus Cirsium (Asteraceae). Biol Invasions 13:905–917. doi:10.1007/s10530-010-9878-5
Rathcke B (ed) (1983) Competition and facilitation among plants for pollination. Pollination biology. Academic Press, Orlando
Roy BA (1996) A plant pathogen influences pollinator behavior and may influence reproduction of nonhosts. Ecology 77:2445–2457. doi:10.2307/2265745
Shi Z, Chen YL, Chen YS, Lin YR, Liu SW, Ge XJ, Gao TG, et al. (2011) Asteraceae (Compositae). In: Wu ZY, Raven PH, Hong DY (ed) Flora of China vol 20–21. http://www.efloras.org/florataxon.aspx?flora_id=2&taxon_id=10074 Accessed 1 Feb 2012. Science Press, Beijing; Missouri Botanical Garden Press, St. Louis
Skórka P, Lenda M, Tryjanowski P (2010) Invasive alien goldenrods negatively affect grassland bird communities in Eastern Europe. Biol Conserv 143:856–861. doi:10.1016/j.biocon.2009.12.030
Sletvold N, Grindeland JM, Agren J (2010) Pollinator-mediated selection on floral display, spur length and flowering phenology in the deceptive orchid Dactylorhiza lapponica. New Phytol 188:385–392. doi:10.1111/j.1469-8137.2010.03296.x
Sun SG (2008) Reproductive strategy and adaptation of an invasive plant Solidago canadensis in China. Fudan University, Dissertation
Sundaram B, Hiremath AJ (2012) Lantana camara invasion in a heterogeneous landscape: patterns of spread and correlation with changes in native vegetation. Biol Invasions 14:1127–1141. doi:10.1007/s10530-011-0144-2
Tao HJ (1999) Divine Farmer’s Materia Medica: A Translation of the Shen Nong Ben Cao Jing (trans: Yang SZ). Blue Poppy Press, Boulder
Toräng P, Ehrlén J, Ågren J (2006) Facilitation in an insect-pollinated herb with a floral display dimorphism. Ecology 87:2113–2117. doi:10.1890/0012-9658(2006)87[2113:FIAIHW]2.0.CO;2
Totland O, Nielsen A, Bjerknes AL, Ohlson M (2006) Effects of an exotic plant and habitat disturbance on pollinator visitation and reproduction in a boreal forest herb. Am J Bot 93:868–873. doi:10.3732/ajb.93.6.868
Walck JL, Baskin JM, Baskin CC (1999) Relative competitive abilities and growth characteristics of a narrowly endemic and a geographically widespread Solidago species (Asteraceae). Am J Bot 86:820–828. doi:10.2307/2656703
Waser NM (1978) Interspecific pollen transfer and competition between co-occurring plant species. Oecologia 36:223–236. doi:10.1007/bf00349811
Weber E (1997) Morphological variation of the introduced perennial Solidago canadensis L sensu lato (Asteraceae) in Europe. Bot J Linn Soc 123:197–210. doi:10.1111/j.1095-8339.1997.tb01413.x
Yang SA, Ferrari MJ, Shea K (2011) Pollinator behavior mediates negative interactions between two congeneric invasive plant species. Am Nat 177:110–118. doi:10.1086/657433
Zavaleta ES, Hobbs RJ, Mooney HA (2001) Viewing invasive species removal in a whole-ecosystem context. Trends Ecol Evol 16:454–459. doi:10.1016/s0169-5347(01)02194-2
Zhang S et al (2006) Bioactive guaianolides from Siyekucai (Ixeris chinensis). J Nat Prod 69:1425–1428. doi:10.1016/S1875-5364(09)60008-X
Acknowledgments
We thank Li Guo, Long Tang and Meng Lu for assistance in the field and in the lab; Lvshen Plant Nursery for providing the study site; and Dr. Hong Liu and two anonymous reviewers for their insightful comments on the earlier versions of this paper, which greatly improved its quality. This work was financially supported by National Basic Research Program of China (Grant No. 2013CB430404), Leading Academic Discipline Project of Shanghai Municipal Education Commission (J50401), National Natural Sciences Foundation of China (Grant Nos. 30600036, 30930019 and 30910362).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Sun, SG., Montgomery, B.R. & Li, B. Contrasting effects of plant invasion on pollination of two native species with similar morphologies. Biol Invasions 15, 2165–2177 (2013). https://doi.org/10.1007/s10530-013-0440-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-013-0440-0