Abstract
Thismia (commonly known as fairy lanterns) is a genus of strange-looking, elusive, and non-photosynthetic plants. Thismia kobensis was first discovered in Kobe City, Hyogo Prefecture, Japan in 1992, but it was believed to be extinct, given that its type locality was destroyed during the construction of an industrial complex. Here, we have reported the rediscovery of T. kobensis in Sanda City, Hyogo Prefecture, which is located approximately 30 km from the type locality. The new locality of T. kobensis is the northernmost distributional limit of Asian Thismiaceae species. As the original description of the species was based on a single museum specimen that lacked two of the three inner perianth lobes, we have provided an amended description of T. kobensis, highlighting its differences from the morphologically similar species T. huangii. Specifically, our morphological re-examination has revealed that T. kobensis is distinguishable from T. huangii by its short but expanded annulus and many short hairs on each stigma lobe. We have also demonstrated that the genetic distance between these taxa is comparable to that between other closely related species pairs. Finally, we have provided brief notes on the taxonomy, biogeography, evolutionary history, and conservation of T. kobensis and its closely related species, including an enigmatic species T. americana.
References
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<p>Capella-Gutiérrez, S., Silla-Martínez, J.M. & Gabaldón, T. (2009) trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. <em>Bioinformatics</em> 25: 1972–1973. https://doi.org/10.1093/bioinformatics/btp348</p>
<p>Chiang, P.-Y. & Hsieh, T.-H. (2011) <em>Thismia huangii</em> (Thismiaceae), a new species from Taiwan. <em>Taiwania</em> 56: 138–142.</p>
<p>Dančák, M., Hroneš, M. & Sochor, M. (2020) <em>Thismia</em>: the rarest of the rare? Ranges of some Bornean species are much larger than previously believed. <em>Phytotaxa</em> 455 (4): 245–261. https://doi.org/10.11646/phytotaxa.455.4.2</p>
<p>Dančák, M., Hroneš, M., Sochor, M. & Sochorová, Z. (2018) <em>Thismia kelabitiana</em> (Thismiaceae), a new unique fairy lantern from Borneo potentially threatened by commercial logging. <em>PLoS ONE:</em> 13. https://doi.org/10.1371/journal.pone.0203443</p>
<p>Don, D. (1839) Descriptions of two genera of the natural family of plants called <em>Coniferae</em>. <em>Transactions of the Linnean Society of London</em> 18: 167–179. https://doi.org/10.1111/j.1095-8339.1838.tb00169.x</p>
<p>Donoghue, M.J. & Smith, S.A. (2004) Patterns in the assembly of temperature forests around the Northern Hemisphere. <em>Philosophical Transactions of the Royal Society B: Biological Sciences</em> 359: 1633–1644. https://doi.org/10.1098/rstb.2004.1538</p>
<p>Gomes, S.I.F., Aguirre-Gutierrez, J., Bidartondo, M.I. & Merckx, V. (2017) Arbuscular mycorrhizal interactions of mycoheterotrophic <em>Thismia</em> are more specialized than in autotrophic plants. <em>New Phytologist</em> 213: 1418–1427. https://doi.org/10.1111/nph.14249</p>
<p>Gomes, S.I.F., van Bodegom, P.M., Merckx, V.S.F.T. & Soudzilovskaia, N. (2019) Environmental drivers for cheaters of arbuscular mycorrhizal symbiosis in tropical rainforests. <em>New Phytologist</em> 223: 1575–1583. https://doi.org/10.1111/nph.15876</p>
<p>Griffith, W. (1844) On the root parasites referred by authors to Rhizantheae and their allies. <em>Proceedings of the Linnean Society of London</em> 1: 216–221.</p>
<p>Guo, X., Zhao, Z., Mar, S.S., Zhang, D. & Saunders, R.M.K. (2019) A symbiotic balancing act: arbuscular mycorrhizal specificity and specialist fungus gnat pollination in the mycoheterotrophic genus <em>Thismia</em> (Thismiaceae). <em>Annals of Botany</em> 124: 331–342. https://doi.org/10.1093/aob/mcz087</p>
<p>Hatusima, S. (1976) Two new species of Burmanniaceae from Japan. <em>Journal of Geobotany</em> 24: 2–10.</p>
<p>Hoang, D.T., Chernomor, O., Von Haeseler, A., Minh, B.Q. & Vinh, L.S. (2018) UFBoot2: Improving the ultrafast bootstrap approximation. <em>Molecular Biology and Evolution</em> 35: 518–522. https://doi.org/10.1093/molbev/msx281</p>
<p>Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. <em>Nature Methods</em> 14: 587–589. https://doi.org/10.1038/nmeth.4285</p>
<p>Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. <em>Molecular Biology and Evolution</em> 30: 772–780. https://doi.org/10.1093/molbev/mst010</p>
<p>Kumar, P., Gale, S.W., Li, J.-H., Bouamanivong, S. & Fischer, G.A. (2017) <em>Thismia nigricoronata</em>, a new species of Burmanniaceae (Thismieae, Dioscoreales) from Vang Vieng, Vientiane Province, Laos, and a key to subgeneric classification. <em>Phytotaxa</em> 319 (3): 225–240. https://doi.org/10.11646/phytotaxa.319.3.2</p>
<p>Linnaeus, C. (1782) <em>Supplementum plantarum</em>. Impensis Orphanotrophei, Brunsvigae, 421 pp.</p>
<p>Linnaeus, C. & Murray, J.A. (1784) <em>Systema vegetabilium</em>. Typis et impensis Jo. Christ. Dieterich, Gottingae, 858 pp.</p>
<p>Merckx, V.S.F.T. (2013) <em>Mycoheterotrophy: The biology of plants living on fungi</em>. 1st ed. Springer, Berlin, Germany, 356 pp. https://doi.org/10.1007/978-1-4614-5209-6</p>
<p>Merckx, V.S.F.T. & Smets, E.F. (2014) <em>Thismia americana</em>, the 101st anniversary of a botanical mystery. <em>International Journal of Plant Sciences</em> 175: 165–175. https://doi.org/10.1086/674315</p>
<p>Mueller, F.J.H.V. (1890) Description of new Australian plants with occasional, other annotations. <em>The Victorian Naturalist</em> 7: 114–116.</p>
<p>Nguyen, L.-T., Schmidt, H.A., Von Haeseler, A. & Minh, B.Q. (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. <em>Molecular Biology and Evolution</em> 32: 268–274. https://doi.org/10.1093/molbev/msu300</p>
<p>Nuraliev, M., Beer, A., Kuznetsov, A. & Kuznetsova, S. (2015) <em>Thismia puberula</em> (Thismiaceae), a new species from Southern Vietnam. <em>Phytotaxa</em> 234 (2): 133–142. https://doi.org/10.11646/phytotaxa.234.2.3</p>
<p>Pfeiffer, N.E. (1914) Morphology of <em>Thismia americana</em>. <em>Botanical gazette</em> 57: 122–135. https://doi.org/10.1086/331235</p>
<p>Roberts, N., Wapstra, E., Duncan, F., Woolley, A., Morley, J. & Fitzgerald, N.B. (2003) Shedding some light on <em>Thismia rodwayi</em> F. Muell. (fairy lanterns) in Tasmania: distribution, habitat and conservation status. <em>Papers and Proceedings of the Royal Society of Tasmania</em> 137: 55–66. https://doi.org/10.26749/rstpp.137.55</p>
<p>Rogers, R.S. (1928) A new genus of Australian orchid. <em>Journal of the Royal Society of Western Australia</em> 15: 1–7.</p>
<p>Schlechter, R. (1919) Die Thismiae. <em>Notizblatt des Botanischen Gartens und Museums zu Berlin-Dahlem</em>: 31–45.</p>
<p>Shepeleva, E.A., Schelkunov, M.I., Hroneš, M., Sochor, M., Dančák, M., Merckx, V.S., Kikuchi, I.A., Chantanaorrapint, S., Suetsugu, K. & Tsukaya, H. (2020) Phylogenetics of the mycoheterotrophic genus <em>Thismia</em> (Thismiaceae: Dioscoreales) with a focus on the Old World taxa: delineation of novel natural groups and insights into the evolution of morphological traits. <em>Botanical Journal of the Linnean Society</em> 193: 287–315. https://doi.org/10.1093/botlinnean/boaa017</p>
<p>Sochor, M., Egertová, Z., Hroneš, M. & Dancák, M. (2018) Rediscovery of <em>Thismia neptunis</em> (Thismiaceae) after 151 years. <em>Phytotaxa</em> 340 (1): 71–78. https://doi.org/10.11646/phytotaxa.340.1.5</p>
<p>Suetsugu, K., Nakanishi, O., Kobayashi, T. & Kurosaki, N. (2018a) <em>Thismia kobensis</em> (Burmanniaceae), a new and presumably extinct species from Hyogo Prefecture, Japan. <em>Phytotaxa</em> 369 (2): 121–125. https://doi.org/10.11646/phytotaxa.369.2.6</p>
<p>Suetsugu, K., Nishigaki, H., Fukushima, S., Ishitani, E., Kakishima, S. & Sueyoshi, M. (2022a) Thread-like appendix on <em>Arisaema urashima</em> (Araceae) attracts fungus gnat pollinators. <em>Ecology</em> 103: e3782. https://doi.org/10.1002/ecy.3782</p>
<p>Suetsugu, K., Okada, H., Hirota, S.K. & Suyama, Y. (2022b) Evolutionary history of mycorrhizal associations between Japanese <em>Oxygyne</em> (Thismiaceae) species and Glomeraceae fungi. <em>New Phytologist</em> 235: 836–841. https://doi.org/10.1111/nph.18163</p>
<p>Suetsugu, K. & Sueyoshi, M. (2021) Fairy lanterns may lure pollinators by mimicking fungi. <em>Frontiers in Ecology and the Environment </em>19: 233–233. https://doi.org/10.1002/fee.2342</p>
<p>Suetsugu, K., Tsukaya, H., Tagane, S., Chhang, P., Yukawa, T. & Yahara, T. (2018b) Flora of Bokor National Park VII: <em>Thismia bokorensis</em> (Burmanniaceae), a new species representing a new generic record. <em>Phytotaxa</em> 334 (1): 65. https://doi.org/10.11646/phytotaxa.334.1.10</p>
<p>Swarts, N.D. & Dixon, K.W. (2009) Terrestrial orchid conservation in the age of extinction. <em>Annals of Botany</em> 104: 543–556. https://doi.org/10.1093/aob/mcp025</p>
<p>Thiele, K.R. & Jordan, P. (2002) <em>Thismia clavarioides</em> (Thismiaceae), a new species of fairy lantern from New South Wales. <em>Telopea</em> 9: 765–771. https://doi.org/10.7751/telopea20024015</p>
<p>Thorogood, C.J., Bougoure, J.J. & Hiscock, S.J. (2019) <em>Rhizanthella</em>: Orchids unseen. <em>Plants, People, Planet</em> 1: 153–156. https://doi.org/10.1002/ppp3.45</p>
<p>Thorogood, C.J. & Mat Yunoh, S.-M. (2021) Fairy lanterns in focus. <em>Plants, People, Planet</em> 3: 680–684. https://doi.org/10.1002/ppp3.10217</p>
<p>Warming, E. (1901) Sur quelques Burmanniacées recueillies au Brésil par le Dr. A. Glaziou. <em>Oversigt Over Det Kgl. Danse Videnskabernes Selskabs Forhandlinger</em> 1901: 173–188.</p>
<p>Capella-Gutiérrez, S., Silla-Martínez, J.M. & Gabaldón, T. (2009) trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. <em>Bioinformatics</em> 25: 1972–1973. https://doi.org/10.1093/bioinformatics/btp348</p>
<p>Chiang, P.-Y. & Hsieh, T.-H. (2011) <em>Thismia huangii</em> (Thismiaceae), a new species from Taiwan. <em>Taiwania</em> 56: 138–142.</p>
<p>Dančák, M., Hroneš, M. & Sochor, M. (2020) <em>Thismia</em>: the rarest of the rare? Ranges of some Bornean species are much larger than previously believed. <em>Phytotaxa</em> 455 (4): 245–261. https://doi.org/10.11646/phytotaxa.455.4.2</p>
<p>Dančák, M., Hroneš, M., Sochor, M. & Sochorová, Z. (2018) <em>Thismia kelabitiana</em> (Thismiaceae), a new unique fairy lantern from Borneo potentially threatened by commercial logging. <em>PLoS ONE:</em> 13. https://doi.org/10.1371/journal.pone.0203443</p>
<p>Don, D. (1839) Descriptions of two genera of the natural family of plants called <em>Coniferae</em>. <em>Transactions of the Linnean Society of London</em> 18: 167–179. https://doi.org/10.1111/j.1095-8339.1838.tb00169.x</p>
<p>Donoghue, M.J. & Smith, S.A. (2004) Patterns in the assembly of temperature forests around the Northern Hemisphere. <em>Philosophical Transactions of the Royal Society B: Biological Sciences</em> 359: 1633–1644. https://doi.org/10.1098/rstb.2004.1538</p>
<p>Gomes, S.I.F., Aguirre-Gutierrez, J., Bidartondo, M.I. & Merckx, V. (2017) Arbuscular mycorrhizal interactions of mycoheterotrophic <em>Thismia</em> are more specialized than in autotrophic plants. <em>New Phytologist</em> 213: 1418–1427. https://doi.org/10.1111/nph.14249</p>
<p>Gomes, S.I.F., van Bodegom, P.M., Merckx, V.S.F.T. & Soudzilovskaia, N. (2019) Environmental drivers for cheaters of arbuscular mycorrhizal symbiosis in tropical rainforests. <em>New Phytologist</em> 223: 1575–1583. https://doi.org/10.1111/nph.15876</p>
<p>Griffith, W. (1844) On the root parasites referred by authors to Rhizantheae and their allies. <em>Proceedings of the Linnean Society of London</em> 1: 216–221.</p>
<p>Guo, X., Zhao, Z., Mar, S.S., Zhang, D. & Saunders, R.M.K. (2019) A symbiotic balancing act: arbuscular mycorrhizal specificity and specialist fungus gnat pollination in the mycoheterotrophic genus <em>Thismia</em> (Thismiaceae). <em>Annals of Botany</em> 124: 331–342. https://doi.org/10.1093/aob/mcz087</p>
<p>Hatusima, S. (1976) Two new species of Burmanniaceae from Japan. <em>Journal of Geobotany</em> 24: 2–10.</p>
<p>Hoang, D.T., Chernomor, O., Von Haeseler, A., Minh, B.Q. & Vinh, L.S. (2018) UFBoot2: Improving the ultrafast bootstrap approximation. <em>Molecular Biology and Evolution</em> 35: 518–522. https://doi.org/10.1093/molbev/msx281</p>
<p>Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. <em>Nature Methods</em> 14: 587–589. https://doi.org/10.1038/nmeth.4285</p>
<p>Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. <em>Molecular Biology and Evolution</em> 30: 772–780. https://doi.org/10.1093/molbev/mst010</p>
<p>Kumar, P., Gale, S.W., Li, J.-H., Bouamanivong, S. & Fischer, G.A. (2017) <em>Thismia nigricoronata</em>, a new species of Burmanniaceae (Thismieae, Dioscoreales) from Vang Vieng, Vientiane Province, Laos, and a key to subgeneric classification. <em>Phytotaxa</em> 319 (3): 225–240. https://doi.org/10.11646/phytotaxa.319.3.2</p>
<p>Linnaeus, C. (1782) <em>Supplementum plantarum</em>. Impensis Orphanotrophei, Brunsvigae, 421 pp.</p>
<p>Linnaeus, C. & Murray, J.A. (1784) <em>Systema vegetabilium</em>. Typis et impensis Jo. Christ. Dieterich, Gottingae, 858 pp.</p>
<p>Merckx, V.S.F.T. (2013) <em>Mycoheterotrophy: The biology of plants living on fungi</em>. 1st ed. Springer, Berlin, Germany, 356 pp. https://doi.org/10.1007/978-1-4614-5209-6</p>
<p>Merckx, V.S.F.T. & Smets, E.F. (2014) <em>Thismia americana</em>, the 101st anniversary of a botanical mystery. <em>International Journal of Plant Sciences</em> 175: 165–175. https://doi.org/10.1086/674315</p>
<p>Mueller, F.J.H.V. (1890) Description of new Australian plants with occasional, other annotations. <em>The Victorian Naturalist</em> 7: 114–116.</p>
<p>Nguyen, L.-T., Schmidt, H.A., Von Haeseler, A. & Minh, B.Q. (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. <em>Molecular Biology and Evolution</em> 32: 268–274. https://doi.org/10.1093/molbev/msu300</p>
<p>Nuraliev, M., Beer, A., Kuznetsov, A. & Kuznetsova, S. (2015) <em>Thismia puberula</em> (Thismiaceae), a new species from Southern Vietnam. <em>Phytotaxa</em> 234 (2): 133–142. https://doi.org/10.11646/phytotaxa.234.2.3</p>
<p>Pfeiffer, N.E. (1914) Morphology of <em>Thismia americana</em>. <em>Botanical gazette</em> 57: 122–135. https://doi.org/10.1086/331235</p>
<p>Roberts, N., Wapstra, E., Duncan, F., Woolley, A., Morley, J. & Fitzgerald, N.B. (2003) Shedding some light on <em>Thismia rodwayi</em> F. Muell. (fairy lanterns) in Tasmania: distribution, habitat and conservation status. <em>Papers and Proceedings of the Royal Society of Tasmania</em> 137: 55–66. https://doi.org/10.26749/rstpp.137.55</p>
<p>Rogers, R.S. (1928) A new genus of Australian orchid. <em>Journal of the Royal Society of Western Australia</em> 15: 1–7.</p>
<p>Schlechter, R. (1919) Die Thismiae. <em>Notizblatt des Botanischen Gartens und Museums zu Berlin-Dahlem</em>: 31–45.</p>
<p>Shepeleva, E.A., Schelkunov, M.I., Hroneš, M., Sochor, M., Dančák, M., Merckx, V.S., Kikuchi, I.A., Chantanaorrapint, S., Suetsugu, K. & Tsukaya, H. (2020) Phylogenetics of the mycoheterotrophic genus <em>Thismia</em> (Thismiaceae: Dioscoreales) with a focus on the Old World taxa: delineation of novel natural groups and insights into the evolution of morphological traits. <em>Botanical Journal of the Linnean Society</em> 193: 287–315. https://doi.org/10.1093/botlinnean/boaa017</p>
<p>Sochor, M., Egertová, Z., Hroneš, M. & Dancák, M. (2018) Rediscovery of <em>Thismia neptunis</em> (Thismiaceae) after 151 years. <em>Phytotaxa</em> 340 (1): 71–78. https://doi.org/10.11646/phytotaxa.340.1.5</p>
<p>Suetsugu, K., Nakanishi, O., Kobayashi, T. & Kurosaki, N. (2018a) <em>Thismia kobensis</em> (Burmanniaceae), a new and presumably extinct species from Hyogo Prefecture, Japan. <em>Phytotaxa</em> 369 (2): 121–125. https://doi.org/10.11646/phytotaxa.369.2.6</p>
<p>Suetsugu, K., Nishigaki, H., Fukushima, S., Ishitani, E., Kakishima, S. & Sueyoshi, M. (2022a) Thread-like appendix on <em>Arisaema urashima</em> (Araceae) attracts fungus gnat pollinators. <em>Ecology</em> 103: e3782. https://doi.org/10.1002/ecy.3782</p>
<p>Suetsugu, K., Okada, H., Hirota, S.K. & Suyama, Y. (2022b) Evolutionary history of mycorrhizal associations between Japanese <em>Oxygyne</em> (Thismiaceae) species and Glomeraceae fungi. <em>New Phytologist</em> 235: 836–841. https://doi.org/10.1111/nph.18163</p>
<p>Suetsugu, K. & Sueyoshi, M. (2021) Fairy lanterns may lure pollinators by mimicking fungi. <em>Frontiers in Ecology and the Environment </em>19: 233–233. https://doi.org/10.1002/fee.2342</p>
<p>Suetsugu, K., Tsukaya, H., Tagane, S., Chhang, P., Yukawa, T. & Yahara, T. (2018b) Flora of Bokor National Park VII: <em>Thismia bokorensis</em> (Burmanniaceae), a new species representing a new generic record. <em>Phytotaxa</em> 334 (1): 65. https://doi.org/10.11646/phytotaxa.334.1.10</p>
<p>Swarts, N.D. & Dixon, K.W. (2009) Terrestrial orchid conservation in the age of extinction. <em>Annals of Botany</em> 104: 543–556. https://doi.org/10.1093/aob/mcp025</p>
<p>Thiele, K.R. & Jordan, P. (2002) <em>Thismia clavarioides</em> (Thismiaceae), a new species of fairy lantern from New South Wales. <em>Telopea</em> 9: 765–771. https://doi.org/10.7751/telopea20024015</p>
<p>Thorogood, C.J., Bougoure, J.J. & Hiscock, S.J. (2019) <em>Rhizanthella</em>: Orchids unseen. <em>Plants, People, Planet</em> 1: 153–156. https://doi.org/10.1002/ppp3.45</p>
<p>Thorogood, C.J. & Mat Yunoh, S.-M. (2021) Fairy lanterns in focus. <em>Plants, People, Planet</em> 3: 680–684. https://doi.org/10.1002/ppp3.10217</p>
<p>Warming, E. (1901) Sur quelques Burmanniacées recueillies au Brésil par le Dr. A. Glaziou. <em>Oversigt Over Det Kgl. Danse Videnskabernes Selskabs Forhandlinger</em> 1901: 173–188.</p>