Langsdorffia : Creatures from the deep?

A spate of recent species discovery in the family Balanophoraceae, coupled with the difficulty in encountering these unpredictable and elusive plants, suggest further Langsdorffia taxa may await discovery. Future work should focus on refining our understanding of their host specificity with a view to propagating them, and introducing them into botanic gardens’ conservation collections.

sequence data to resolve its position in the sandalwood order.
The authors demonstrated that the family in fact comprises one slow-evolving clade that includes the genera Dactylantus, Hachettea, and Mystropetalon in the family Mystropetalaceae, and a relatively rapidly evolving clade comprising the remaining Balanophoraceae s.str., that includes the genus Langsdorffia. These data help to explain why morphology-based classifications of this family varied historically. Several new species have been described in the family, some very recently, such as Ombrophytum chilensis in Chile (Kuijt & Delprete, 2019), and O. villamariensis in Colombia (Guzmán-Guzmán, 2019). Meanwhile, Balanophora papuana was rediscovered recently in North Sumatra after 39 years without detection (Damayanto & Riastiwi, 2019). The scarcity, elusive nature, and remote locations of known Balanophoraceae indicate that further species may await discovery. Furthermore, little is understood about the biology of most of the species already known to science. Here we provide a brief review of the ecology and reproductive biology of one of the least examined genera in the family, Langsdorffia, and place emphasis on this highly unusual genus as a candidate for further research and conservation focus.

| LIFE HIS TORY AND ECOLOGY
The family Balanophoraceae comprises predominantly tropical subterranean root parasites of shrubs, herbs, and trees that are seldom encountered or collected, and generally preserve poorly (Hsiao, Mauseth, & Gomez, 1994). Little is known about the life history and ecology of most species in the family. All species of Langsdorffia are highly modified parasites comprising just a series of tubers and inflorescences, and lack an ordinary stem structure and all trace of functional apical meristems (Hsiao et al., 1994). The Balanophoraceae more broadly feature a particularly complicated host-parasite vascular interface, in which the parasitic tuber appears to engulf the host plant's roots ( Figure 2d) (Santos, Nascimento, Marzinek, Leiner, & Oliveira, 2017), the vascular tissues of which infiltrate the parasite tissue extensively (Hsiao, Mauseth, & Peng, 1995). Interestingly, all Balanophoraceae appear to lack stomata entirely, which is highly unusual in the plant kingdom beyond submerged aquatics (Kuijt & Dong, 1990).
Little research has been carried out to examine the host specificity of Langsdorffia. While holoparasites are generally host specific, L. hypogaea ( Figure 2) has been shown to parasitize over 20 host species including shrubs, trees, lianas, and even a cactus, from 16 families; however, an apparent preference for Miconia albicans (Melastomataceae) indicates at least a degree of specificity (Santos et al., 2017). This species occurs in various habitats including neo- in Papua New Guinea when it was first described (Geesink, 1972), This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. but this has not been revisited or confirmed to our knowledge. The host range of L. malagasica and the recently described L. heterotepala (Cardoso et al., 2011) have not been assessed in detail either.
Given the dependency of these parasites on their host plants, an assessment of the host range of all species of Langsdorffia will be an essential next step in their conservation.

| REPRODUC TIVE B IOLOGY
Little is known about the pollination biology, breeding systems, or seed dispersal of the Balanophoraceae (Kuijt & Delprete, 2019;Freitas et al., 2017), and in Langsdorffia in particular. All species in the family produce minute, unisexual flowers, borne in spike-like inflorescences on the dark forest floor; however, pollination mechanisms appear to be diverse (Goto, Yamakoshi, & Matsuzawa, 2012). Species in the genus Balanophora secrete nectar and are visited by ants, cockroaches, and moths in Japan (Kawakita & Kato, 2002) and Lophophytum mirabile is visited by beetles in the Ecuadorian Amazon (Borchsenius & Olesen, 1990). Here, B. kuroiwai appears to have evolved as a mutualistic pollination syndrome with pyralid moths, which use the plant as a brood site for their lar-  Hsiao et al., 1994;Santos et al., 2017). The flowers are brightly colored and sweetly scented during anthesis , and 259 species of floral visitor have been observed from a diversity of orders including Hymenoptera, Hemiptera, Dermaptera, Blattodea, Araneae, and Coleoptera . Ants (Brachymyrmex) are reported to visit this species most frequently; however, beetles (Stelidota) are suggested to be the principle pollinator in this species, and have been observed ovipositing in the flowers . The whitenaped jay (Cyanocorax cyanopogon) has also been observed visiting  (Irwin et al., 2007); pollination seems doubtful here. Together, the few data available suggest that Langsdorffia attract a diverse guild of floral visitors, including insects, birds, and mammals, and more broadly, that mutualistic pollination syndrome, involving moths, flies, and beetles, may be a common feature across the family Balanophoraceae.

| FUTURE WORK
Future work should focus on the effective propagation of Langsdorffia. The translocation and conservation of holoparasitic flowering plants are impeded significantly by the complete dependency on their host plants (Holzapfel, Dodgson, & Rohan, 2018). As a consequence of their difficulty of cultivation, parasitic plants seem to be underrepresented significantly in conservation collections.
Langsdorffia is no exception and at present, none of the four known species exist in cultivation to our knowledge. This is concerning because all species occur in habitats under threat, and at least one species, L. heteropetala, may be classified as Critically Endangered in the future, because it has such a limited distribution (Cardoso, 2020;Cardoso et al., 2011). Even species that are widespread, such as L.
hypogaea, which occurs across the Amazon, Caatinga, Cerrado, and Atlantic Forest eco-region, are considered at risk due to habitat loss . Placing emphasis on parasitic plants such as Langsdorffia in botanic gardens' conservation collections and seedbanking strategies will help safeguard the future of these extraordinary plants.