Floral scent and pollination of the invasive plant Coreopsis lanceolata in Japan





Floral scent, Plant-pollinator interaction, Pollination success, Reproductive biology, Riparian ecosystem


The invasive plant Coreopsis lanceolata threatens ecosystems in Japan by competing for resources with native plants. This species is self-incompatible and requires pollinator agents for seed production; however, it is known to produce many seeds. Here, we document the pollination biology and plant-pollinator interactions that facilitate seed production of C. lanceolata in the introduced range. Results revealed that C. lanceolata attracted a wide array of floral visitors comprising 60 species from 20 families. Although most floral visitors could be potential pollinators, the functional groups of halictid bees appeared to be the most important pollinators of C. lanceolata in terms of visitation frequency and the ability to carry pollen. The floral scent emission of C. lanceolata consists predominantly of monoterpenes, sesquiterpenes, and benzenoids. Furthermore, the mean seed set was nearly 30% of the ovule mean. Our study confirmed that in the introduced range in Japan, C. lanceolata is integrated into the local pollinator community, especially with the functional group of halictid bees involved in the reproductive success.

Author Biographies

Muhammad Arifin, Gifu University



Tomoko Okamoto, Faculty of Applied Biological Sciences, Gifu University





Armbruster WS (2017) The specialization continuum in pollination systems: diversity of concepts and implications for ecology, evolution and conservation. Functional Ecology 31:88–100. https://doi.org/10.1111/1365-2435.12783

Azuma H, Toyota M, Asakawa Y (2001) lntraspecific variation of floral scent chemistry in Magnolia kobus DC. (Magnoliaceae). Journal of Plant Research 114:411–422. https://doi.org/10.1007/PL00014006

Banovetz SJ, Scheiner SM (1994a) The effects of seed mass on the seed ecology of Coreopsis lanceolata. The American Midland Naturalist 131:65–74. https://doi.org/10.2307/2426609

Banovetz SJ, Scheiner SM (1994b) Secondary seed dormancy in Coreopsis lanceolata. The American Midland Naturalist 131:75–83. https://doi.org/10.2307/2426610

Barrett SCH, Colautti RI, Eckert CG (2008) Plant reproductive systems and evolution during biological invasion. Molecular Ecology 17:373–383. https://doi.org/10.1111/j.1365-294X.2007.03503.x

Batianoff GAN, Halford DA (2002) Coreopsis lanceolata L. (Asteraceae): another environmental weed for Queensland and Australia. Plant Protection Quarterly 17:168–169.

Bernhardt CE, Mitchell RJ, Michaelsy HJ (2008) Effects of population size and density on pollinator visitation, pollinator behavior, and pollen tube abundance in Lupinus perennis. International Journal of Plant Sciences 169:944–953. 10.1086/589698

Bose T, Reina A, Marshall JA (2017) Collective decision-making. Current Opinion in Behavioral Sciences 16:30–34. https://doi.org/10.1016/j.cobeha.2017.03.004

Braunschmid H, Guilhot R, Dötterl S (2021) Floral scent and pollinators of Cypripedium calceolus L. at different latitudes. Diversity 13:1–15. https://doi.org/10.3390/d13010005

Burkle LA, Runyon JB (2017) The smell of environmental change: Using floral scent to explain shifts in pollinator attraction. Applications in Plant Sciences 5:1600123. https://doi.org/10.3732/apps.1600123

Cézar K, Franklin E, Pinto CE (2022) Temporal variation in pollinators’ visitation of Lantana camara in a tropical urban landscape: does butterfly abundance and richness drive the fruit set? Ekológia (Bratislava) 41:46–56. https://doi.org/10.2478/eko-2022-0006

Coffin DP, Lauenroth WK (1992) Spatial variability in seed production of the perennial bunchgrass Bouteloua gracilis (Gramineae). American Journal of Botany 79:347–353. https://doi.org/10.1002/j.1537-2197.1992.tb14558.x

Courtice B, Hoebee SE, Sinclair S, Morgan JW, Courtice B, Hoebee SE, Sinclair S, Morgan JW (2020) Local population density affects pollinator visitation in the endangered grassland daisy Rutidosis leptorhynchoides (Asteraceae). Australian Journal of Botany 67:638–648. https://doi.org/10.1071/BT18243

Dalsgaard B, Martín González AM, Olesen JM, Timmermann A, Andersen LH, Ollerton J (2008) Pollination networks and functional specialization: a test using Lesser Antillean plant-hummingbird assemblages. Oikos 117:789–793. https://doi.org/10.1111/j.0030-1299.2008.16537.x

Delle-Vedove R, Schatz B, Dufay M (2017) Understanding intraspecific variation of floral scent in light of evolutionary ecology. Annals of Botany 120:1–20. https://doi.org/10.1093/aob/mcx055

Fagua JC, Gonzalez VH (2007) Growth rates, reproductive phenology, and pollination ecology of Espeletia grandiflora (Asteraceae), a giant Andean caulescent rosette. Plant Biology 9:127–135. https://doi.org/10.1055/s-2006-924544

Fisogni A, Rossi M, Sgolastra F, Bortolotti L, Bogo G, de Manincor N, Quaranta M, Galloni M (2016) Seasonal and annual variations in the pollination efficiency of a pollinator community of Dictamnus albus L. Plant Biology 18:445–454. https://doi.org/10.1111/plb.12417

Fleming TH, Sahley CT, Holland JN, Nason JD, Hamrick JL (2001) Sonoran desert columnar cacti and the evolution of generalized pollination systems. Ecological Monographs 71:511–530. https://doi.org/10.1890/0012-9615(2001)071[0511:SDCCAT]2.0.CO;2

Friberg M, Schwind C, Guimarães PR, Raguso RA, Thompson JN (2019) Extreme diversification of floral volatiles within and among species of Lithophragma (Saxifragaceae). Proceedings of the National Academy of Sciences of the United States of America 116:4406–4415. https://doi.org/10.1073/pnas.1809007116

Gabel B, Thiéry D, Suchy V, Marion-Poll F, Hradsky P, Farkas P (1992) Floral volatiles of Tanacetum vulgare L. attractive to Lobesia botrana Den. et Schiff. females. Journal of Chemical Ecology 18:693–701. https://doi.org/10.1007/BF00994607

Giuliani C, Ascrizzi R, Lupi D, Tassera G, Santagostini L, Giovanetti M, Flamini G, Fico G (2018) Salvia verticillata: Linking glandular trichomes, volatiles and pollinators. Phytochemistry 155:53–60. https://doi.org/10.1016/j.phytochem.2018.07.016

Hao JH, Qiang S, Chrobock T, van Kleunen M, Liu QQ (2011) A test of baker’s law: Breeding systems of invasive species of Asteraceae in China. Biological Invasions 13:571–580. https://doi.org/10.1007/s10530-010-9850-4

Hao JH, Qiang S, Liu QQ, Cao F (2009) Reproductive traits associated with invasiveness in Conyza sumatrensis. Journal of Systematics and Evolution 47:245–254. https://doi.org/10.1111/j.1759-6831.2009.00019.x

Hatase Y, Oguri H, Matsue M (2007) Ecological characteristics of Coreopsis lanceolata which invaded native grassland on gravelly riverbeds at the Kiso River. Journal of The Japanese Institute of Landscape Architecture 70:467–470. https://doi.org/10.5632/jila.70.467

Heiduk A, Brake I, Tolasch T, Frank J, Jürgens A, Meve U, Dötterl S (2010) Scent chemistry and pollinator attraction in the deceptive trap flowers of Ceropegia dolichophylla. South African Journal of Botany 76:762–769. https://doi.org/10.1016/j.sajb.2010.07.022

Hilty J (2020) Flower-visiting insect of sand Coreopsis. Illinois wildflowers [online] URL: http://w.illinoiswildflowers.info/flower_insects/plants/sand_coreopsis.htm (accessed 19 May 2022).

Huber FK, Kaiser R, Sauter W, Schiestl FP (2005) Floral scent emission and pollinator attraction in two species of Gymnadenia (Orchidaceae). Oecologia 142:564–575. 10.1007/S00442-004-1750-9/FIGURES/4

Inoue K, Amano M (1986) Evolution of Campanula punctata Lam. in the Izu Islands: Changes of pollinators and evolution of breeding systems. Plant Species Biology 1:89–97. https://doi.org/10.1111/j.1442-1984.1986.tb00018.x

Inoue M, Mishima H, Fukaya H, Yahata K, Nobe K (2020) Distribution of an invasive alien species lanceleaf tickseed (Coreopsis lanceolata L.) in Oki Island, Shimane Prefecture. Bulletin of the Shimane Nature Museum of Mt. Sanbe (Sahimel) 18:73–77.

Issaly EA, Sérsic AN, Pauw A, Cocucci AA, Traveset A, Benítez-Vieyra SM, Paiaro V (2020) Reproductive ecology of the bird-pollinated Nicotiana glauca across native and introduced ranges with contrasting pollination environments. Biological Invasions 22:485–498. https://doi.org/10.1007/s10530-019-02104-8

Japan Butterfly Conservation Society (2012) Field Guide to the Butterflies of Japan Society JBC (ed). Seibundo Shinkosha, Tokyo.

Johnson SD, Hobbhahn N (2010) Generalized pollination, floral scent chemistry, and a possible case of hybridization in the African orchid Disa fragrans. South African Journal of Botany 76:739–748. https://doi.org/10.1016/j.sajb.2010.07.008

Johnson SD, Steiner KE (2000) Generalization versus specialization in plant pollination systems. Trends in Ecology and Evolution 15:140–143. https://doi.org/10.1016/S0169-5347(99)01811-X

Kaiser R (1993) The scent of orchids: Olfactory and chemical investigations. Elsevier Science Publishers, Amsterdam.

Kalaman H, Wilson SB, Mallinger RE, Knox GW, Van Santen E (2022) Evaluation of native and nonnative ornamentals as pollinator plants in Florida: I. Floral abundance and insect visitation. HortScience 57:126–136. https://doi.org/10.21273/HORTSCI16123-21

Kaneko Y (2012) Invasive alien plant species in the shore areas surrounding Lake Biwa. In: Kawanabe H, Nishino M, Maehata M (eds) Lake Biwa: Interactions between Nature and People. Springer, London, pp 487–490. https://doi.org/10.1007/978-94-007-1783-1

Kil JH, Shim KC, Park SH, Koh KS, Suh MH, Ku YB, Suh SU, Oh HK, Kong HY (2004) Distributions of naturalized alien plants in South Korea. Weed Technology 18:1493–1495. https://doi.org/10.1614/0890-037X(2004)018[1493:DONAPI]2.0.CO;2

Kishore K, Kalita H, Rinchen D, Lepcha B (2012) Evidence of functional specialization and pollination syndrome in Amomum subulatum Roxb. (Zingiberaceae). Current Science 103:193–198.

van Kleunen M, Dawson W, Maurel N (2015) Characteristics of successful alien plants. Molecular Ecology 24:1954–1968. https://doi.org/10.1111/mec.13013

Knudsen J (1993) Trends in floral scent chemistry in pollination syndromes: floral scent composition in moth-pollinated taxa. Botanical Journal of the Linnean Society 113:263–284. https://doi.org/10.1111/j.1095-8339.1993.tb00340.x

Knudsen JT (2002) Variation in floral scent composition within and between populations of Geonoma macrostachys (Arecaceae) in the western Amazon. American Journal of Botany 89:1772–1778. https://doi.org/10.3732/ajb.89.11.1772

Koike F, Clout MN, Kawamichi M, De Poorter M, Iwatsuki K (Eds) (2006) Assessment and control of biological invasion risks. Shoukadoh Book Sellers, Kyoto, Japan and the World Conservation Union (IUCN), Gland, Switzerland.

Komai F, Yoshiyasu Y, Nasu Y, Saito T (2011) A Guide to the Lepidoptera of Japan. Tokai University Press, Tokyo.

Layek U, Das A, Das U (2022) Floral biology, floral volatile organic compounds and floral visitors of Chromolaena odorata, an invasive alien species in West Bengal , India. Biodiversitas 23:2118–2129. https://doi.org/10.13057/biodiv/d230447

Lázaro A, Lundgren R, Totland Ø, La´zaro A, Lundgren R, Totland Ø (2009) Co-flowering neighbors influence the diversity and identity of pollinator groups visiting plant species. Oikos 118:691–702. https://doi.org/10.1111/j.1600-0706.2008.17168.x

Lemaitre AB, Pinto CF, Niemeyer HM (2014) Generalized pollination system: Are floral traits adapted to different pollinators? Arthropod-Plant Interactions 8:261–272. https://doi.org/10.1007/s11829-014-9308-1

Lemanski NJ, Cook CN, Ozturk C, Smith BH, Pinter-Wollman N (2021) The effect of individual learning on collective foraging in honey bees in differently structured landscapes. Animal Behaviour 179:113–123. https://doi.org/10.1016/j.anbehav.2021.06.033

Lindsey AH (1984) Reproductive biology of Apiacea. I. Floral vistors to Thaspium and Zizia and their importance in pollination. American Journal of Botany 71:375–387. https://doi.org/10.2307/2443496

Malayeri BE, Noori M, Jafari M (2012) Using the pollen viability and morphology for fluoride pollution biomonitoring. Biological Trace Element Research 147:315–319. https://doi.org/10.1007/s12011-011-9290-8

Maroyi A (2012) The casual, naturalised and invasive alien flora of Zimbabwe based on herbarium and literature records. Koedoe 54:1–6. https://doi.org/10.4102/koedoe.v54i1.1054

Martins C, Freitas L (2018) Functional specialization and phenotypic generalization in the pollination system of an epiphytic cactus. Acta Botanica Brasilica 32:359–366. https://doi.org/10.1590/0102-33062017abb0335

Maruyama PK, Nunes CEP, Vizentin-Bugoni J, Gustafsson S, Morellato LPC (2018) Are native bees and Apis mellifera equally efficient pollinators of the rupestrian grassland daisy Aspilia jolyana (Asteraceae)? Acta Botanica Brasilica 32:386–391. https://doi.org/10.1590/0102-33062018abb0143

Mencuccini M, Piussi P, Zanzi Sulli A (1995) Thirty years of seed production in a subalpine Norway spruce forest: Patterns of temporal and spatial variation. Forest Ecology and Management 76:109–125. https://doi.org/10.1016/0378-1127(95)03555-O

Miyawaki S, Washitani I (2004) Invasive alien plant species in riparian areas of Japan: The contribution of agricultural weeds, revegetation species and aquacultural species. Global Environmental Research 8:89–101.

Montero-Castaño A, Vilà M, Ortiz-Sánchez FJ (2014) Pollination ecology of a plant in its native and introduced areas. Acta Oecologica 56:1–9. https://doi.org/10.3391/bir.2022.11.1.03

Moshobane MC, Olowoyo JO, Middleton L (2022) Alien plant species of Haenertsburg Village, Limpopo Province, South Africa. BioInvasions Records 11:23–39. https://doi.org/10.3391/bir.2022.11.1.03

Nagasaki O (2021) Functional specialization for pollination by scoliid wasps and solitary bees of Ampelopsis glandulosa (Vitaceae). Flora: Morphology, Distribution, Functional Ecology of Plants 284:151921. https://doi.org/10.1016/j.flora.2021.151921

Olesen JM, Bascompte J, Elberling H, Jordano P (2008) Temporal dynamics in a pollination network. Ecology 89:1573–1582. https://doi.org/10.1890/07-0451.1

Ollerton J, Killick A, Lamborn E, Watts S, Whiston M (2007) Multiple meanings and modes: on the many ways to be a generalist flower. Taxon 56:717–728. https://doi.org/10.2307/25065855

Ollerton J, Watts S, Connerty S, Lock J, Parker L, Wilson I, Schueller S, Nattero J, Cocucci AA, Izahaki I, Geerts S, Pauw A, Stout JC (2012) Pollination ecology of the invasive tree tabacco Nicotiana glauca: comparisons across native and non-native ranges. Journal of Pollination Ecology 9:85–95. https://doi.org/10.26786/1920-7603(2012)12

Olsen KM (1997) Pollination effectiveness and pollinator importance in a population of Heterotheca subaxillaris (Asteraceae). Oecologia 109:114–121. https://doi.org/10.1007/PL00008811

Parker AJ, Tran JL, Ison JL, Bai JDK, Weis AE, Thomson JD (2015) Pollen packing affects the function of pollen on corbiculate bees but not non-corbiculate bees. Arthropod-Plant Interactions 9:197–203. https://doi.org/10.1007/s11829-015-9358-z

Pauw A, Stanway R (2015) Unrivalled specialization in a pollination network from South Africa reveals that specialization increases with latitude only in the Southern Hemisphere. Journal of Biogeography 42:652–661. https://doi.org/10.1111/jbi.12453

Pearse IS, LaMontagne JM, Koenig WD (2017) Inter-annual variation in seed production has increased over time (1900–2014). Proceedings of the Royal Society B: Biological Sciences 284:20171666. https://doi.org/10.1098/rspb.2017.1666

Petanidou T, Price M V., Bronstein JL, Kantsa A, Tscheulin T, Kariyat R, Krigas N, Mescher MC, De Moraes CM, Waser NM (2018) Pollination and reproduction of an invasive plant inside and outside its ancestral range. Acta Oecologica 89:11–20. https://doi.org/10.1016/j.actao.2018.03.008

Quinet M, Jacquemart A-L (2020) Troubles in pear pollination: Effects of collection and storage method on pollen viability and fruit production. Acta Oecologica 105:103558. https://doi.org/10.1016/j.actao.2020.103558

Raguso RA, Pellmyr O (1998) Dynamic headspace analysis of floral volatiles: a comparison of methods. Oikos 81:238–254. https://doi.org/10.2307/3547045

Randall RP (2007) The introduced flora of Australia and its weed status. CRC for Australian Weed Management, Australia.

Rech AR, Jorge LR, Ollerton J, Sazima M (2018) Pollinator availability, mating system and variation in flower morphology in a tropical savanna tree. Acta Botanica Brasilica 32:462–472. https://doi.org/10.1590/0102-33062018abb0220

Saito TI, Okubo K (2011) The relationship between alien herb Coreopsis lanceolata and soil texture types on gravelly floodplain vegetation in Central Japan. Vegetation Science 28:39–47. https://doi.org/10.15031/vegsci.28.39

Saito TI, Okubo K (2013) Influences of invasive herb Coreopsis lanceolata on riparian endemic herbs in relation to the understory light availability. Landscape and Ecological Engineering 9:271–280. https://doi.org/10.1007/s11355-011-0179-7

Sakai S, Kato M, Inoue T (1999) Three pollination guilds and variation in floral characteristics of Bornean gingers (Zingiberaceae and Costaceae). American Journal of Botany 86:646–658. https://doi.org/10.2307/2656573

da Santos RS, Carneiro LT, de Oliveira Santos JP, da Silva MM, de Oliveira Milfont M, Castro CC (2021) Bee pollination services and the enhancement of fruit yield associated with seed number in self-incompatible tangelos. Scientia Horticulturae 276:109743. https://doi.org/10.1016/j.scienta.2020.109743

Seeley TD, Camazine S, Sneyd J (1991) Collective decision-making in honey bees: how colonies choose among nectar sources. Behavioral Ecology and Sociobiology 28:277–290. https://doi.org/10.1007/BF00175101

Shorthouse DP (2010) SimpleMappr, an online tool to produce publication-quality point maps. [online] URL: https://www.simplemappr.net (accessed 19 June 2022).

Smith EB (1976) A biosystematic survey of Coreopsis in eastern United States and Canada. SIDA, Contributions to Botany 6:123–215.

Souza CS, Maruyama PK, Aoki C, Sigrist MR, Raizer J, Gross CL, de Araujo AC (2018) Temporal variation in plant–pollinator networks from seasonal tropical environments: Higher specialization when resources are scarce. Journal of Ecology 106:2409–2420. https://doi.org/10.1111/1365-2745.12978

Sowig P (1989) Effect of flowering plant’s patch size on species composition of pollinator communities, foraging strategies, and resource partitioning in bumblebees (Hymenoptera : Apidae). Oecologia 78:550–558. https://doi.org/10.1007/BF00378747

Sugita R, Itamiya H (2020) Discrimination of pollen of Asteroideae by spine and pollen size for forensic examination. Japanese Journal of Palynology 66:15–23.

Suinyuy TN, Donaldson JS, Johnson SD (2012) Geographical variation in cone volatile composition among populations of the African cycad Encephalartos villosus. Biological Journal of the Linnean Society 106:514–527. https://doi.org/10.1111/j.1095-8312.2012.01905.x

Svensson GP, Hickman MO, Bartram S, Boland W, Pellmyr O, Raguso RA (2005) Chemistry and geographic variation of floral scent in Yucca filamentosa (Agavaceae). American Journal of Botany 92:1624–1631. https://doi.org/10.3732/ajb.92.10.1624

Tadauchi O, Murao T (2014) An Illustrated Guide to Japanese Bees. Bunichi Sougou Shuppan, Tokyo.

Takahashi J, Yoshida T, Takagi T, Akimoto S, Woo K, Deowanish S, Hepburn R, Nakamura J, Matsuka M (2007) Geographic variation in the Japanese islands of Apis cerana japonica and in A. cerana populations bordering its geographic range. Apidologie 38:335–340. https://doi.org/10.1051/apido:2007018

Terayama M, Suda H (2016) A Guide to the Aculeate Wasps of Japan Terayama M, Suda H (eds). Tokai University Press, Tokyo.

The Ecological Society of Japan (Ed) (2002) Handbook of Alien Species in Japan. Chijin Shokan, Tokyo.

The Japan Coleopterological Society (1956) Coloured illustrations of the insects of Japan: Coleoptera Society JC (ed). Hoikusha Publishing Co., Osaka.

Theis N (2006) Fragrance of Canada thistle (Cirsium arvense) attracts both floral herbivores and pollinators. Journal of Chemical Ecology 32:917–927. https://doi.org/10.1007/s10886-006-9051-x

Traveset A, Sáez E (1997) Pollination of Euphorbia dendroides by lizards and insects: spatio-temporal variation in patterns of fower visitation. Oecologia 111:241–248. https://doi.org/10.1007/PL00008816

Wang D, Yu H, Chen G (2021) Scent chemistry and pollinators in the holoparasitic plant Cynomorium songaricum (Cynomoriaceae). Plant Biology 23:111–120. https://doi.org/10.1111/plb.13180

Waser NM, Chittka L, Price M V., Williams NM, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77:1043–1060. https://doi.org/10.2307/2265575

Wester P, Johnson SD, Pauw A (2019) Scent chemistry is key in the evolutionary transition between insect and mammal pollination in African pineapple lilies. New Phytologist 222:1624–1637. https://doi.org/10.1111/nph.15671

Wojcik VA, Frankie GW, Thorp RW, Hernandez JL (2008) Seasonality in bees and their floral resource plants at a constructed Urban bee habitat in Berkeley, California. Journal of the Kansas Entomological Society 81:15–28. https://doi.org/10.2317/JKES-701.17.1

Xu H, Qiang S, Genovesi P, Ding H, Wu J, Meng L, Han Z, Miao J, Hu B, Guo J, Sun H, Huang C, Lei J, Le Z, Zhang X, He S, Wu Y, Zheng Z, Chen L, Jarošik V, Pysek P, Pysek P (2012) An inventory of invasive alien species in China. NeoBiota 15:1–26. https://doi.org/10.3897/neobiota.15.3575

Yasunaga T, Takai M, Yamashita I, Kawamura M, Kawasawa T (1993) Terrestrial Heteropterans: A Field Guide to Japanese Bugs Series Tomokuni M (ed). Zenkoku Noson Kyoiku Kyokai Publishing Co., Tokyo.

Youngsteadt E, Irwin RE, Fowler A, Bertone MA, Giacomini SJ, Kunz M, Suiter D, Sorenson CE (2018) Venus flytrap rarely traps its pollinators. American Naturalist 191:539–546. https://doi.org/10.1086/696124

Zeng J-J, Xiao Y, Sun M, Zhou B (2014) Effect of clonal growth on mating system of invasive plant Coreopsis lanceolata. Bulletin of Botanical Research 34:650–654. 10.7525/j.issn.1673-5102.2014.05.011

Zeng J-J, Zhou B, Wang N (2021) Comparing the reproductive biological characteristics of the alien invasive Coreopsis lanceolata to those of the non-invasive alien congener Coreopsis tinctoria. Plant Species Biology 36:379–389. https://doi.org/10.1111/1442-1984.12323



How to Cite

Arifin, M., & Okamoto, T. (2023). Floral scent and pollination of the invasive plant Coreopsis lanceolata in Japan. Journal of Pollination Ecology, 33, 108–127. https://doi.org/10.26786/1920-7603(2023)740