Oxygyne is an exceptionally rare group of plants which are poorly known to science and are of critical conservation concern.

1 INTRODUCTION Oxygyne (Thismiaceae) is a rare and poorly known genus with a remarkably disjunct distribution, occurring only in a few places in Japan and West Central Africa (Cheek, Tsukaya, Rudall, & Suetsugu, 2018). Each of the six species is known from just one location, usually from a single specimen, two are believed to be extinct, and the remaining four are Critically Endangered (Figure 1). All species are mycoheterotropic—obtaining carbon from adjacent photosynthetic plants through a shared mycorrhizal fungal network, rather than from photosynthesis. As such, they are completely devoid of functional leaves and chlorophyll; combined with the blue coloration of some species, they have an appearance quite unique among flowering plants (Figure 2). Remarkably little is known about the biology of the genus and they are completely unknown in cultivation. Indeed like many mycoheterotropic plants, they are elusive and seldom seen, because they grow in deep shade, often under leaf litter, where they are easily overlooked (see Movie S1 and Infographic S1). Figure 1 Open in figure viewer PowerPoint The genus Oxygyne comprises six species: (a) O. duncanii; (b) O. frankei; (c) O. triandra; (d) O. hyodoi; (e) O. shinzatoi; (f) O. yamashitae. Illustrations not to scale (all flowers are small, ≤30 mm high) Figure 2 Open in figure viewer PowerPoint The genus Oxygyne has a disjunct distribution with species in Japan, such as (a) O. shinzatoi and in West‐Central Africa, such as (b) O. duncanii. All species are exceptionally rare, and seldom photographed: (c,d) O. shinzatoi; (e,f) O. yamashitae; and (g) O. hyodoi. Illustrations (a,b) by Chris J. Thorogood. Photographs (c,d) by Tazuko Watanabe; (e,f) by Kenji Suetsugu; (g) by Syoji Hyodo Genera in the family Thismiaceae are renowned for their extreme scarcity (Franke, 2004) and many species have been discovered only recently. Oxygyne yamashitae was described in 2008 (Yahara & Tsukaya, 2008); indeed, the first taxonomic monograph of Oxygyne was published only in 2018 (Cheek et al., 2018) and raised the number of recognized species from four to six. Meanwhile, recent discoveries in the related genus Thismia include T. cornuta, T. pallida (Hroneš et al., 2018), and T. hexagona (Dančák et al., 2013) in Borneo; T. filiformis in Thailand (Chantanaorrapint, 2012); T. clavarioides in Australia (Thiele & Jordan, 2002); the rediscovery of T. neptunis—not seen for 151 years—in Borneo in 2017 (Sochor, Egertová, Hroneš, & Dančák, 2018); and T. kobensis found preserved in a Japanese natural history museum, and probably now extinct (Suetsugu, Nakanishi, Kobayashi, & Kurosaki, 2018). This remarkable spate of recent discoveries, coupled with elusive life history, suggests more species await discovery in the Thismiaceae.

2 EVOLUTION AND LIFE HISTORY Approximately 10% of plant species use carbon from a fungal partner (mycorrhizal association) at some stage of their life cycle, although the true extent of dependency on fungal carbon across the plant kingdom is unclear (Leake & Cameron, 2010). This relationship is most dramatic in achlorophyllous mycoheterotrophic plants, such as Oxygyne, which often have a ghostly appearance (Bolin, Tennakoon, Majid, & Cameron, 2017) and grow in deep shade, in contrast with most photosynthetic plants (Bidartondo, Burghardt, Gebauer, Bruns, & Read, 2004). Mycoheterotrophy has evolved independently multiple times (Merckx, Bakkerb, Huysmansa, & Smets, 2009) and is prominent in monocot families, especially orchids (Orchidaceae) (Lam et al., 2018). However, elucidating the evolutionary origins of these “ghostly,” morphologically reduced plants across the plant kingdom has proved challenging (Lam et al., 2018; Merckx et al., 2009). This is because many have lost traits shared with their photosynthetic ancestors (such as functional leaves), and because plastid genes used in DNA sequencing are either highly divergent or absent (Lam et al., 2018; Lam, Merckx, & Graham, 2016; Leake, 1994; Schelkunov, Penin, & Logacheva, 2018). Furthermore, mycoheterotrophs show a strong evolutionary convergence of adaptations to their life history, making the identification of their photosynthetic ancestors challenging (Leake, 1994). The Thismiaceae is a particularly problematic family. All species are small, reduced, achlorophyllous mycoheterotrophic herbs, often completely devoid of leaves. Most species occur in dense tropical rainforest and can only be seen when they appear above ground to flower through leaf litter. Because of its scarcity, Oxygyne is poorly represented in phylogenetic analyses. Broadly sampled phylogenetic trees of mycoheterotrophs, including scarce taxa such as Oxygyne, will be crucial for testing hypotheses relating to the evolutionary origins of mycoheterotrophy in flowering plants (Lam et al., 2018).

3 REPRODUCTIVE BIOLOGY Despite the unusual appearance of the flowers of Oxygyne, nothing is known about their reproductive biology. Interestingly, Japanese species are all blue, whereas African species are brownish‐orange (Cheek et al., 2018) (Figure 2a, b). All are small and inconspicuous. For example, although the flowers of the newly described species O. yamashitae are a vibrant shade of blue, they are small (just 5 mm high and 5 mm across) and often at least partially concealed by leaf litter (Yahara & Tsukaya, 2008). The authors suggest that this species is self‐compatible; however, empirical data on its pollination biology (indeed for all species of Oxygyne) are completely lacking (Cheek et al., 2018) and are scant across genera in the Thismiaceae more broadly. Tiputinia foetida, a recently discovered achlorophyllous mycoheterotroph in the related family Burmanniaceae (which includes the Thismiaceae in the views of some authors), attracts flies with the smell of carrion in Amazonian Ecuador (Woodward, Berry, Maas‐van de Kamer, & Swing, 2007). Since fetid odors are capable of attracting pollinators from long distances in carrion insect‐pollinated plants, deceit pollination is suggested by Woodward et al. (2007) to be effective in rare, inconspicuous forest herbs such as Thismiaceae. Preliminary observations of O. yamashitae suggest that the flowers have no discernible odor (Yahara & Tsukaya, 2008); however, unidentified Diptera have been observed visiting the flowers of this species (Suetsugu K., unpublished data). Another related achlorophyllous mycoheterotroph, Thismia hongkongensis, described only in 2015, appears to be pollinated by fungus gnats (Myctophilidae or Sciaridae) and scuttle flies (Phoridae). These insects are suggested to enter the perianth tube via the annulus below the filiform tepal appendages and exit via small apertures between the filaments of the pendent stamens. The flowers are inferred to be protandrous (the male reproductive phase preceding the female), and flies are possibly trapped within the flower, increasing chances of pollen deposition on the receptive stigma (Mar & Saunders, 2015). Given that T. hongkongensis shares morphological features with Oxygyne (perianth tubes with an annulus and tepal extensions), a similar pollination syndrome is possible for Oxygyne. Meanwhile, Mitrastemon yamamotoi (Mitrastemonaceae), a holoparasitic species (a parasite devoid of chlorophyll) which also produces flowers close to the ground in dark understorey environments, was recently established to be pollinated by social wasps, crickets, and cockroaches (Suetsugu, 2018). Suetsugu (2018) suggests that pollination systems involving unusual and unexpected taxa might be more widespread than previously thought, especially in non‐photosynthetic plants with highly modified floral morphology. These recent studies show that investigation into the pollination syndrome of the genus Oxygyne warrants much further attention.

4 CONCLUDING REMARKS In summary, virtually nothing is known about the biology of the genus Oxygyne, including its life history, mycorrhizal partners, and reproductive biology. Only six species have been described, but given the inconspicuous nature of Oxygyne, and the recent spate of species discovery of related Thismiaceae in Southeast Asia, it is possible that further taxa await discovery. Such discoveries are most likely to be in areas of high rainfall with exceptional species diversity and endemism, in regions where Oxygyne is already known to occur (Cheek et al., 2018). Two species (O. triandra and O. hyodoi) have not been encountered during numerous targeted searches and have been assessed as extinct (Cheek et al., 2018); coupled with the potential for habitat loss and degradation in areas where Oxygyne occurs, the identification and conservation of new species are an urgent priority. Investigations into the biology of this extraordinary genus will enhance our knowledge of the elusive family Thismiaceae and the evolution of mycoheterotrophy in flowering plants more broadly.

ACKNOWLEDGMENTS The author thanks Kenji Suetsugu for critically reviewing the manuscript and providing useful suggestions.

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