Abstract
Florivores directly decrease the reproductive success of plants by consuming pollen and seeds; thus, plants often have defense mechanisms against florivory. Here, we show that the recurved phyllaries of an agamospermous hybrid dandelion, Taraxacum japonicum × officinale, function as a physical barrier to slug florivory. We allowed Lehmannia valentiana, a European slug naturalized in Japan, to feed on eight pairs of the hybrid dandelion and T. japonicum, a Japanese species with erect phyllaries. Consequently, the slugs only damaged T. platycarpum flowers. The slugs either moved back from recurved phyllaries or spent more than twice as long on recurved than on erect phyllaries. When we removed the recurved phyllaries, the slugs stayed on hybrid and T. japonicum phyllaries for equal lengths of time. In addition to recurved outer phyllaries, the hybrid dandelion has erect inner phyllaries that are longer than those of T. japonicum, which effectively conceal the florets at night protecting them from slug florivory. Using the taxonomic literature, we have confirmed that recurved phyllaries evolved in many species in several parts of Europe, but are rare in East Asia. These findings suggest that European dandelions acquired recurved phyllaries as a defense mechanism under antagonistic coevolution with florivorous slugs, but this coevolution did not occur in East Asia.
Similar content being viewed by others
References
Abedin S (2007) New species of Taraxacum Weber ex Wigg from Pakistan. Pak J Bot 39:1417–1433
Adler LS, Karban R, Strauss SY (2001) Direct and indirect effect of alkaloid on plant fitness via herbivory and pollination. Ecology 82:2004–2032
Aquaro G, Caparelli KF, Peruzzi L (2009) The genus Taraxacum (Asteraceae) in Italy. II. Five new species of Taraxacum sect. Erythrocarpa. Proceedings of the IV Balkan Botanical Congress, Sofia, 20–26 June 2006, pp 160–168
Aquaro G, Caparelli KF, Peruzzi L (2008) The genus Taraxacum (Asteraceae) in Italy. I. A systematic study of Taraxacum sect. Palustria. Phytol Balcan 14:61–67
Asker SE, Jerling L (1992) Apomixis in plants. CRC Press, Boca Raton
Breadmore KN, Kirk WDJ (1998) Factors affecting floral herbivory in a limestone grassland. Acta Oecol 19:501–506
Breedlove DE, Ehrlich PR (1968) Plant-herbivore coevolution: lupines and lycaenids. Science 162:671–672
Bremer K (1994) Asteraceae, cladistics and classification. Timber Press, Portland
Cardel YJ, Koptur S (2010) Effects of florivory on the pollination of flowers: an experimental field study with a perennial plant. Int J Pl Sci 171:283–292
Dudman AA, Richards AJ (1994) Seven new species of Taraxacum Wigg. (Asteraceae), native to the British Isles. Watsonia 20:119–132
Ferreira CA, Torezan-Silingardi HM (2013) Implications of the floral herbivory on malpighiacea plant fitness: visual aspect of the flower affects the attractiveness to pollinators. Sociobiology 60:323–328
Forsyth RG (2001) First records of the European land slug Lehmannia valentiana in British Columbia, Canada. Festivus 33:75–78
Funk VA, Susanna A, Stuessy T, Bayer R (2009) Systematics, evolution, and biogeography of the compositae. IAPT, Vienna
Galán de Mera A (2016) Taraxacum. In: Castroviejo et al. (eds) Flora Ibérica vol. 16, http://www.rjb.csic.es/floraiberica/. Accessed 19 Aug 2016
Galán de Mera A, Vicente Orellana JA (2010) Taraxacum decastroi and T. lacianense (Asteraceae), two new species from the Iberian Peninsula. Ann Bot Fenn 47:307–311
Galán de Mera A, Linares Perea E, Vicente Orellana JA (2012) Taraxacum penyalarense (Asteraceae), a new species from the central mountains of Spain. Ann Bot Fenn 49:91–94
Ge XJ, Kirschner J, Štěpánek J (2011) Taraxacum. Flora of China 20–21: 270–325. http://www.efloras.org/browse.aspx?flora_id=2&name_str=taraxacum&btnSearch=Search. Accessed 17 Aug 2016
Honěk A, Martinková Z (2014) Floral herbivory of an invasive slug on a native weed. Pl Prot Sci 50:151–156
Horvitz CC, Schemske DW (1984) Effects of ants and an ant-tended herbivore on seed production of a neotropical herb. Ecology 65:1369–1378
Hoya A, Shibaike H, Morita T, Ito M (2004) Germination and seedling survivorship characteristics of hybrids between native and alien species of dandelion (Taraxacum). Plant Species Biol 19:81–90
Jafari E, Assadi M (2007) Taraxacum aurantiacum (Asteraceae), a new record for the flora of Iran. Iran J Bot 13:47–48
Kessler D, Diezel C, Clark DG, Colquhoun TA, Baldwin IT (2013) Petunia flowers solve the defence/apparency dilemma of pollinator attraction by deploying complex floral blends. Ecol Lett 16:299–306
Kirschner J, Štěpánek J (2005) Dandelions in central Asia: taraxacum sect. Suavia. Preslia Praha 77:263–276
Kirschner J, Štěpánek J, Mes THM, den Nijs JCM, Oosterveld P, Štorchová H, Kuperus P (2003) Principal features of the cpDNA evolution in Taraxacum (Asteraceae, Lactuceae): a conflict with taxonomy. Plant Syst Evol 239:231–255
Kirschner J, Drábková LZ, Štěpánek J, Uhlemann I (2015) Towards a better understanding of the Taraxacum evolution (Compositae–Cichorieae) on the basis of nrDNA of sexually reproducing species. Plant Syst Evol 301:1135–1156
Klooster MR, Clark DL, Culley TM (2009) Cryptic bracts facilitate herbivore avoidance in the mycoheterotrophic plant Monotropsis odorata (Ericaceae). Am J Bot 96:2197–2205
Kurozumi T (2002) Lehmannia valentiana. In: Ecological Society of Japan (ed) Handbook of alien species in Japan. Chijinshokan, Tokyo, p 164 (in Japanese)
Lundevall C-F, Øllgaard H (2006) Seven new Taraxacum species (Asteraceae, Cichorieae) from Norden. Willdenowia 36:671–688
Makino T (1904) Nihon no tanpopo (Taraxacum of Japan). Bot Mag Tokyo 18:92–93 (in Japanese)
McCall AC, Irwin RE (2006) Florivory: the intersection of pollination and herbivory. Ecol Lett 9:1351–1365
Meza-Lopez MM, Siemann E (2015) Experimental test of the invasional meltdown hypothesis: an exotic herbivore facilitates an exotic plant, but the plant does not reciprocally facilitate the herbivore. Freshwater Biol 60:1475–1482
Mitsuyuki C, Hoya A, Shibaike H, Watanabe M, Yahara T (2014) Formation of a hybrid triploid agamosperm on a sexual diploid plant: evidence from progeny tests in Taraxacum platycarpum Dahlst. Plant Syst Evol 300:863–870
Morita T (1995) Taraxacum. In: Iwatsuki K, Yamazaki T, Boufford DE, Ohba H (eds) Flora of Japan, vol IIIb. Kodansha, Tokyo, pp 7–13
Morita T, Menken SBJ, Strek AA (1990) Hybridization between European and Asian dandelions (Taraxacum section Ruderalia and section Mongolica) 1. Crossability and breakdown of self-incompatibily. New Phytol 114:519–529
Nishida S, Takakura K-I, Nishida T, Matsumoto T, Kanaoka MM (2012) Differential effects of reproductive interference by an alien congener on native Taraxacum species. Biol Invas 14:439–447
Ogawa K (2002) Alien dandelions. In: Ecological Society of Japan (ed) Handbook of alien species in Japan. Chijinshikan, Tokyo, p 192 (in Japanese)
Ogawa K, Mototani I (1985) Invasion of the introduced dandelions and survival of the native ones in the Tokyo metropolitan area of Japan. Jpn J Ecol 35:443–452
Øllgaard H (2006) Further new Taraxacum species (Asteraceae, Cichorieae) from northern Europe. Willdenowia 36:693–706
Penet L, Collin CL, Ashman T-L (2009) Florivory increases selfing: an experimental study in the wild strawberry, Fragaria virginiana. Plant Biol 11:38–45
Peng CI, Chung KF, Li HL (1998) Compositae. In: Editorial Committee of the Flora of Taiwan (ed) Flora of Taiwan, 2nd edn, vol 4. Editorial Committee of the Flora of Taiwan, Taipei, pp 1079–1081
Peruzzi L, Aquaro G, Caparelli KF, Raimondo FM (2009) The genus Taraxacum (Asteraceae) in Italy III. A new species of T. sect. Erythrocarpa from Sicily. Fl Medit 19:73–79
Primack RB (1985) Longevity of individual flowers. Annu Rev Ecol Syst 16:15–37
Richards AJ (1973) The origin of Taraxacum agamospecies. Bot J Linn Soc 66:189–211
Richards AJ, Sell PD (1976) Taraxacum. Fl Eur 4:332–343
Roulston T, Cane JH, Buchmann SL (2000) What governs protein content of pollen: pollinator preferences, pollen–pistil interactions, or phylogeny? Ecol Monog 70:617–643
Safavi SR, NasehY, Jafari E, Tavakoli Z, Heidarnia N (2013) Taraxacum. In: Flora of Iran 77. Research Institute of Forests & Rangelands Press, Iran
Schaffner U, Ridenour WM, Wolf VC, Bassett T, Müller C, Müller-Schärer H, Sutherland S, Lortie CJ, Callaway RM (2011) Plant invasions, generalist herbivores, and novel defense weapons. Ecology 92:829–835
Shibaike H (2005) Agamospermous triploids meet sexual diploids: a case study of Taraxacum officinale in Japan. Biol Sci 56:74–82 (in Japanese)
Sonck CE (1999) New Taraxacum species from Greece V. Ann Bot Fenn 36(3):211–217
Takakura K, Nishida T, Matsumoto T, Nishida S (2009) Alien dandelion reduces the seed-set of a native congener through frequency-dependent and one-sided effects. Biol Invas 11:973–981
Textor S, Gershenzon J (2009) Herbivore induction of the glucosinolate-myrosinase defense system: major trends, biochemical bases and ecological significance. Phytochem Rev 8:149–170
Theis N, Adler LS (2012) Advertising to the enemy: enhanced floral fragrance increases beetle attraction and reduces plant reproduction. Ecolology 93:430–435
Trávníček B, Vašut RJ (2011) Notes on the genus Taraxacum in Slovakia I. Taraxacum sect. Hamata: a new group of dandelion in Slovakia. Biologia 66:595–603
Trávníček B, Marciniuk J, Žíla V (2007) New localities of Taraxacum species from S Poland (with nine new species to polish flora). Acta Soc Bot Polon 76:209–224
Trávníček B, Kirschner J, Štěpánek J (2008) Five new species of Taraxacum sect. Ruderalia from central Europe and Denmark. Preslia 80:27–59
Udaka H, Numata H (2010) Comparison of the life cycle and photoperiodic response between northern and southern populations of the terrestrial slug Lehmannia valentiana in Japan. Zool Sci 27:735–739
Uhlemann I (2007) New species of the genus Taraxacum (Asteraceae, Cichorieae) from Croatia. Willdenowia 37:115–121
Waldén HW (1961) On the variation, nomenclature, distribution and taxonmical position of Limax (Lehmannia) valentiana Férussac (Gastropoda, Pulmonata). Arkiv Zool 15:71–95
Yamano M, Shibaike H, Hamaguch T, Ide M (2002) Analysis on the distribution patterns of hybrid dandelions (Taraxacum) in Japan collaborated with the ‘‘Environmental Indicator Species Survey (Survey of Common Wildlife)’’. Environ Inform Sci 16:357–362 (in Japanese with English summary)
Yamano M, Shibaike H, Ide M (2004) Analysis on relationships between landscape structure and distribution patterns for native and hybrid dandelions (Taraxacum) in Tsukuba City, Ibaraki Pref. Jap Inst Landsc Archit 67:587–590 (in Japanese with English summary)
Yamawo A, Hada Y (2010) Effects of light on direct and indirect defences against herbivores of young plants of Mallotus japonicus demonstrate a trade-off between two indirect defense traits. Ann Bot 106:143–148
Acknowledgements
We thank Firouzeh Javadi for help in obtaining data on the flora of Iran and Chika Mitsuyuki for help with sampling the Japanese and hybrid dandelions. Thanks also to KC Hung and SF Chan for data analysis, ZF Tang for drawing Fig. 2, and our colleagues in the Laboratory of Ecological Science, Kyushu University for their helpful comments on our findings and constructive discussion throughout this study.
Author information
Authors and Affiliations
Corresponding author
About this article
Cite this article
Wu, FY., Yahara, T. Recurved Taraxacum phyllaries function as a floral defense: experimental evidence and its implication for Taraxacum evolutionary history. Ecol Res 32, 313–329 (2017). https://doi.org/10.1007/s11284-017-1444-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11284-017-1444-5