Abstract
Arisaema sect. Pistillata (Araceae) is a rapidly diversifying taxon in the Japanese archipelago. Several sympatric Arisaema species selectively attract different fungus gnats (Mycetophilidae and Sciaridae), suggesting that frequent pollinator shifts induce adaptive radiation. Since no study has compared pollinator species between sister Arisaema species, we examined the floral visitor assemblages of two closely related species (Ar. nagiense and Ar. ovale) in sympatric, parapatric, and allopatric populations. In all six sites, at the level of genus, male Anatella spp. (Mycetophilidae) dominated the floral visitors in both Arisaema species, but Ar. nagiense and Ar. ovale selectively attracted different Anatella species. The pollinator shift during the allopatric speciation of the two sister Arisaema species suggests the contribution of a species-specific pollination system to the rapid diversification of Japanese Arisaema species.
This is a preview of subscription content, log in via an institution to check access.
Data availability
The list of all floral visitors is provided in Online Resource 1.
References
Blanco MA, Barboza G (2005) Pseudocopulatory pollination in Lepanthes (Orchidaceae: Pleurothallidinae) by fungus gnats. Ann Bot (Oxford) 95:763–772. https://doi.org/10.1093/aob/mci090
Bohman B, Flematti GR, Barrow RA, Pichersky E, Peakall R (2016) Pollination by sexual deception—it takes chemistry to work. Curr Opin Pl Biol 32:37–46. https://doi.org/10.1016/j.pbi.2016.06.004
Buggs RJA, Pannell JR (2006) Rapid displacement of a monoecious plant lineage is due to pollen swamping by a dioecious relative. Curr Biol 16:996–1000. https://doi.org/10.1016/j.cub.2006.03.093
Chandler PJ (1977) Studies of some fungus gnats (Diptera: Mycetophilidae) including nine additions to the British list. Syst Entomol 2:67–93. https://doi.org/10.1111/j.1365-3113.1977.tb00362.x
Dafni A (1984) Mimicry and deception in pollination. Annual Rev Ecol Syst 15:259–278. https://doi.org/10.1146/annurev.es.15.110184.001355
Dell’Olivo A, Hoballah MR, Gübitz T, Kuhlemeler C (2011) Isolation barriers between Petunia axillaris and Petunia integrifolia (Solanaceae). Evolution 65:1979–1991. https://doi.org/10.1111/j.1558-5646.2011.01279.x
Hayashi T, Bohman B, Scaffidi A, Peakall R, Flematti GR (2021) An unusual tricosatriene is crucial for male fungus gnat attraction and exploitation by sexually deceptive Pterostylis orchids. Curr Biol 31:1954–1961. https://doi.org/10.1016/j.cub.2021.01.095
Hooper SD, Brown AP (2007) A revision of Australia’s hammer orchids (Drakaea: Orchidaceae), with some field data on species-specific sexually deceived wasp pollinators. Aust Syst Bot 20:252–285. https://doi.org/10.1071/SB06033
Hu J, Xie C, Shi C, Wang S, Wu Q, Li C, Zhang Y (2019) Effect of sex and air temperature on the flight capacity of Bradysia odoriphaga (Diptera: Sciaridae). J Econ Entomol 112:2161–2166. https://doi.org/10.1093/jee/toz152
Ishihara Y, Tagami Y (2020) Estimating the dispersal ability of Bradysia odoriphaga (Diptera: Sciaridae). Jap J Appl Entomol Zool 64:107–113. https://doi.org/10.1303/jjaez.2020.107
Kakishima S, Sueyoshi M, Okuyama Y (2020) Floral visitors of critically endangered Arisaema cucullatum (Araceae) endemic to Kinki region of Japan. Bull Natl Mus Nat Sci Ser B 46:47–53
Kobayashi T (2016) Research notes on Japanese Arisaema (Araceae)—its taxonomy with special reference to plumular leaf, number of ovules per ovary, and chromosome numbers. J Jap Bot 91 (Suppl):128–137. https://doi.org/10.51033/jjapbot.91_suppl_10726
Kobayashi T (2021) The genus Arisaema (Araceae) in Hyogo Prefecture—revised edition. Plants Hyogo 31:1–30
Kobayashi T, Murata J, Watanabe K (2005) Two new putative natural hybrids in Japanese Arisaema (Araceae). Acta Phytotax Geobot 56:105–110. https://doi.org/10.18942/apg.KJ00004622917
Kobayashi T, Sasamura K, Watanabe K, Murata J (2008) Arisaema inaense and A. nagiense, two diploid species of the A. ovale group (Araceae). Acta Phytotax Geobot 59:37–43. https://doi.org/10.18942/apg.KJ00004899885
Kurina O, Grootaert P (2016) Fungus gnats in the Botanical garden Jean Massart on the outskirts of Brussels: 52 new country records and a pictorial atlas of the genera (Diptera: Sciaroidea). Belg J Entomol 44:1–34
Lounibos LP, Escher RL (2008) Sex ratios of mosquitoes from long-term censuses of Florida tree holes. J Amer Mosquito Control Assoc 24:11–15. https://doi.org/10.2987/5656.1
Lowry DB, Modliszewski JL, Wright KM, Wu CA, Willis JH (2008) The strength and genetic basis of reproductive isolating barriers in flowering plants. Phil Trans Roy Soc London B 363:3009–3021. https://doi.org/10.1098/rstb.2008.0064
Matile L (1975) Un nouveau cas de brachyptérisme chez les Diptères Mycetophilidae: la femelle de Macrocera crozetensis Colless. Bull Soc Entomol France 80:2–6
Matile L (1976) Un genre nouveau de Mycomyini à nervation alaire réduite; diagnose préliminaire. Bull Soc Entomol France 81:139–140
Matsumoto TK (2021) Application of multivariate morphometrics to delimit three Japanese species of Arisaema sect. Pistillata (Araceae). Nordic J Bot 39:e03075. https://doi.org/10.1111/njb.03075
Matsumoto TK, Hirobe M, Sueyoshi M, Miyazaki Y (2021) Selective pollination by fungus gnats potentially functions as an alternative reproductive isolation among five Arisaema species. Ann Bot (Oxford) 127:633–644. https://doi.org/10.1093/aob/mcaa204
Moe AM, Weiblen GD (2012) Pollinator-mediated reproductive isolation among dioecious fig species (Ficus, Moraceae). Evolution 66:3710–3721. https://doi.org/10.1111/j.1558-5646.2012.01727.x
Murata J (1993) Differentiation and taxonomy of Arisaema ovale Nakai and allies. Bull Bot Soc Yamanashi 6:2–8
Murata J (1995) Diversity in the Arisaema serratum group. Acta Phytotax Geobot 46:185–208. https://doi.org/10.18942/bunruichiri.KJ00001079100
Murata J, Ohno J, Kobayashi T, Ohi-Toma T (2018) The Genus Arisaema in Japan. Hokuryukan, Tokyo
Ohi-Toma T, Wu S, Murata H, Murata J (2016) An updated genus-wide phylogenetic analysis of Arisaema (Araceae) with reference to sections. Bot J Linn Soc 182:100–114. https://doi.org/10.1111/boj.12459
Økland B (1996) Unlogged forests: important sites for preserving the diversity of mycetophilids (Diptera: Sciaroidea). Biol Conservation 76:297–310. https://doi.org/10.1016/0006-3207(95)00129-8
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O-Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2018) Package ‘vegan’ version 2.5–2.
Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120: 321–326. https://doi.org/10.1111/j.1600-0706.2010.18644.x
Okayama Prefecture (2020) Red Data Book in Okayama. Okayama Prefecture, Okayama
Peakall R, Ebert D, Poldy J, Barrow RA, Francke W, Bower CC, Schiestl FP (2010) Pollinator specificity, floral odour chemistry and the phylogeny of Australian sexually deceptive Chiloglottis orchids: implications for pollinator-driven speciation. New Phytol 188:437–450. https://doi.org/10.1111/j.1469-8137.2010.03308.x
Phillips RD, Scaccabarozzi D, Retter BA, Hayes C, Brown GR, Dixon KW, Peakall R (2014) Caught in the act: pollination of sexually deceptive trap-flowers by fungus gnats in Pterostylis (Orchidaceae). Ann Bot (Oxford) 113:629–641. https://doi.org/10.1093/aob/mct295
R Development Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Ramsey J, Bradshaw HD Jr, Schemske DW (2003) Components of reproductive isolation between the monkeyflowers Mimulus lewisii and M. cardinalis (Phrymaceae). Evolution 57:1520–1534. https://doi.org/10.1111/j.0014-3820.2003.tb00360.x
Reiter N, Freestone M, Brown G, Peakall R (2019) Pollination by sexual deception of fungus gnats (Keroplatidae and Mycetophilidae) in two clades of Pterostylis (Orchidaceae). Bot J Linn Soc 190:101–116. https://doi.org/10.1093/botlinnean/boz009
Sasakawa M, Ishizaki H (2003) Fungus gnats of the genera Anatella, Allodia and Cordyla in Japan (Diptera: Mycetophilidae). Entomol Sci 6:97–109. https://doi.org/10.1046/j.1343-8786.2003.00013.x
Sasamura K, Murata J, Ohi-Toma T (2021) Ploidy diversity in the Arisaema ovale group and the A. nikoense group (Araceae). J Jap Bot 96:67–73. https://doi.org/10.51033/jjapbot.96_2_11081
Schiestl FP (2005) On the success of a swindle: pollination by deception in orchids. Naturwissenschaften 92:255–264. https://doi.org/10.1007/s00114-005-0636-y
Seno J (2021) A new record and feature for Arisaema inaense (Araceae) from Ishikawa prefecture, Japan. J Jap Bot 96:348–351. https://doi.org/10.51033/jjapbot.96_6_11139
Suetsugu K, Sato R, Kakishima S, Okuyama Y, Sueyoshi M (2021) The sterile appendix of two sympatric Arisaema species lures each specific pollinator into deadly trap flowers. Ecology 102:e03242. https://doi.org/10.1002/ecy.3242
Sutou M, Maruyama M, Komatsu T, Kanao T (2012) Discovery of a remarkable new species of black fungus gnat (Diptera, Sciaridae) from termite nests in Malaysia. J Nat Hist 46:969–978. https://doi.org/10.1080/00222933.2012.654478
Tabadkani SM, Ashouri A, Rahimi-Alangi V, Fathi-Moghaddam M (2013) When to estimate sex ratio in natural populations of insects? A study on sex ratio variations of gall midges within a generation. Entomol Sci 16:54–59. https://doi.org/10.1111/j.1479-8298.2012.00537.x
Toft RJ, Harris RJ, Williams PA (2001) Impacts of the weed Tradescantia fluminensis on insect communities in fragmented forests in New Zealand. Biol Conservation 102:31–46. https://doi.org/10.1016/S0006-3207(01)00091-X
van der Niet T, Johnson SD (2012) Phylogenetic evidence for pollinator-driven diversification of angiosperms. Trends Ecol Evol 27:353–361. https://doi.org/10.1016/j.tree.2012.02.002
van der Niet T, Johnson SD, Linder HP (2006) Macroevolutionary data suggest a role for reinforcement in pollination system shifts. Evolution 60:1596–1601. https://doi.org/10.1554/05-705.1
Vereecken NJ, Wilson CA, Hötling S, Schulz S, Banketov SA, Mardulyn P (2012) Pre-adaptations and the evolution of pollination by sexual deception: cope’s rule of specialization revisited. Proc Roy Soc London B 279:4786–4794. https://doi.org/10.1098/rspb.2012.1804
Vereecken NJ, Dorchin A, Dafni A, Hötling S, Schulz S, Watts S (2013) A pollinators’ eye view of a shelter mimicry system. Ann Bot (Oxford) 111:1155–1165. https://doi.org/10.1093/aob/mct081
Vogel S, Martens J (2000) A survey of the function of the lethal kettle traps of Arisaema (Araceae), with records of pollinating fungus gnats from Nepal. Bot J Linn Soc 133:61–100. https://doi.org/10.1006/bojl.1999.0317
Weber MG, Strauss SY (2016) Coexistence in close relatives: beyond competition and reproductive isolation in sister taxa. Annual Rev Ecol Evol Syst 47:359–381. https://doi.org/10.1146/annurev-ecolsys-112414-054048
Whitehead MR, Peakall R (2014) Pollinator specificity drives strong prepollination reproductive isolation in sympatric sexually deceptive orchids. Evolution 68:1561–1575. https://doi.org/10.1111/evo.12382
Wolf DE, Takebayashi N, Rieseberg LH (2001) Predicting the risk of extinction through hybridization. Conservation Biol 15:1039–1053. https://doi.org/10.1046/j.1523-1739.2001.0150041039.x
Wong BBM, Schiestl FP (2002) How an orchid harms its pollinator. Proc Roy Soc London B 269:1529–1532. https://doi.org/10.1098/rspb.2002.2052
Zaitzev AI (2003) Fungus gnats (Diptera, Sciaroidea) of the fauna of Russia and adjacent regions. Part II. Int J Dipterol Res 14:77–386. https://doi.org/10.33338/ef.4693
Acknowledgements
We thank Shungo Kariyama and Tomiki Kobayashi for providing information on Ar. nagiense populations and three anonymous reviewers and Associate Editor for helpful comments on our manuscript.
Funding
This study was supported by a Grant-in-Aid for JSPS Research Fellow (grant number JP19J10090) and a Research Grant for Encouragement of Students, Graduate School of Environmental and Life Science, Okayama University, to T.K.M. and the Wesco Scientific Promotion Foundation to M.H.
Author information
Authors and Affiliations
Contributions
T.K.M. constructed study concept and design, and conducted field survey, insect identification and manuscript drafting. M.S. conducted insect identification and manuscript drafting. S.S. supported field survey. Y.M. and M.H. conducted supervision and manuscript drafting.
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare that they have no conflicts of interest.
Additional information
Handling Editor: Mario Fernández-Mazuecos.
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.
Information on Electronic Supplementary Material. Online Resource 1
. Floral visitor assemblages of the Arisaema species (DOCX 44 kb)
Information on Electronic Supplementary Material
Information on Electronic Supplementary Material
Online Resource 1. Floral visitor assemblages of the Arisaema species.
Rights and permissions
About this article
Cite this article
Matsumoto, T.K., Sueyoshi, M., Sakata, S. et al. Two closely related species of the Arisaema ovale group (Araceae) selectively attract male fungus gnats of different Anatella species (Diptera: Mycetophilidae). Plant Syst Evol 309, 4 (2023). https://doi.org/10.1007/s00606-022-01839-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00606-022-01839-7