Distribution of Sapria
In Vietnam, Sapria himalayana is thus far known only on the Lang Biang Plateau, at Tuyền Lâm Lake, Cam Ly and Nam Ban Protection Forest. Outside of Vietnam, the known range of Sapria himalayana includes India and Thailand, where the forma himalayana (distinguished by yellow warts on blood-red perigone lobes) occurs in India (Assam), Myanmar and Thailand (Elliott 1992; Bendiksby et al. 2010) and the forma albovinosa Bänziger and Hansen (distinguished by white warts on wine-red perigone lobes) is documented from Phu Khiew Wildlife Sanctuary, Chaiyaphum Province, Thailand (Bänziger et al. 2000). This distribution is likely to be very incomplete because there are generally very few careful documentations of Sapria and their colour expression or variation.
The other two species of Sapria known include S. poilanei, so far known from the Cardamom mountains area in Cambodia and Chanthaburi in Thailand, and S. ram documented from Dawna-Bilauktaung, Phangnga and Suratthani in Thailand (Bänziger and Hansen 1997).
Identification of the Lang Biang Sapria
By its size attributes, morphological details (Table 1) and colour patterns (Figs. 3, 4), we were able to identify the Vietnamese taxon as Sapria himalayana f. albovinosa according to the excellent key and attributes of fresh material provided by Bänziger and Hansen (1997) and Bänziger et al. (2000). Fresh open flowers of Sapria himalayana are distinctly larger (previously documented floral span 95–200 mm) than either Sapria poilanei (floral span 65–120 mm) or Sapria ram (floral span 55–110 mm) (Bänziger and Hansen 1997), and our Vietnamese taxon has a floral span of 110–165 mm, falling in the range for S. himalayana. The ramenta apices of the Vietnamese taxon are also bilobed or multilobed (especially in female specimens), or crateriform (i.e., with a shallow recess, especially in males). The aperture of the diaphragm is 14–21 mm, distinctly smaller than the disk of 51–61 mm diameter, as also documented by Bänziger and Hansen for Sapria himalayana. The disk is somewhat flat and thins out towards its periphery so that it does not have a distinctive “wall” between upper and lower surfaces, as noted by Bänziger and Hansen (1997) for S. himalayana; in contrast, the other two species have a pan- to bowl-shaped (female) or cup-shaped (male) disk with a distinct wall. Other morphological details (Table 1) are also consistent with those of Sapria himalayana as described by Bänziger and Hansen (1997). Comparison between these three Sapria species is summarized in Table 2.
Table 1 Measurements (in mm) of female and male flowers of Sapria himalayana f. albovinosa sampled on Lang Biang Plateau for the present study
Table 2 Floral characters and known flowering period compared for three Sapria species
The colour patterns of the Vietnam taxon (Figs. 3, 4, 5 and 7) are those documented for Sapria himalayana f. albovinosa. The warts are white against the distinctive wine-red colour of the perigone lobes as described for this form.
Description of the Lang Biang Sapria
In the following description, the key morphological parts are provided with abbreviations in brackets that correspond to Fig. 2.
Holoparasitic plant on Tetrastigma laoticum roots. Flower buds c. 8 cm in diameter near to opening stage. Cupule (CP) 10–16.6 mm high in female, 2–6 mm high in male. Bracts (A) of outer whorl 5, (14–)20–35 mm long; those of inner whorl 5, (39–)43–62 mm long. Diameter (C) × height (HE) of fully open flowers: 130–165 × 71–90 mm in female, 110–142 × 97–107 mm in male. Perigone lobes 10 (inner whorl 5 and outer whorl 5); female lobes when fully open (30–)60° to 90° from the vertical plane through the floral centre; male lobes when fully open 0° to 30(–45)° from the vertical plane through the floral centre; outer lobes ovate, length (F) 38–57 × width (E) 39–58 mm, red with white warts adaxially, with white dots abaxially, glabrous; inner lobes spathulate, 38–51 × 31–38 mm, with white warts adaxially, with white dots abaxially, glabrous. Diaphragm 51–61 mm in diameter (H); 14–21 mm across aperture (J); collar width (I) 16–24 mm; basal band (IB) white with pink radial stripes, turning red then purple-black with age; ramenta band (IM) 9–15 mm wide, reddish black, turning purple-black with age, ramenta (K) mostly bi- or multilobed in females and occasionally in males, mostly crateriform in males and occasionally in females, 5–9 mm long, wine-red at base, turning dark orange to dark red towards their apex, blackening with age; distal band (ID) 4–7 mm wide, dark red turning black with age. Perigone tube circumference (D) around lobe bases 254–265 mm, height (L) 31–38 mm. Central column (Q) dimorphic between sexes: female column 16–20 mm high, 14–15 mm in diameter at narrowest point, disk bowl-shaped, upper surface whitish cream, margin reddish, crest of disk (T) 35–39 mm in diameter, depth of disk (U) 5–6 mm, height of disk (S) to just above vestigial anthers 10–11 mm, stigmatic fascia (WF) 13.5–15 mm wide, sparsely bristly; male column 16–19 mm high, c. 8 mm in diameter at narrowest point, disk bowl-shaped, upper surface wine-red, margin dark red, crest of disk (T) 23–33 mm in diameter, depth of disk (U) 6–8 mm, height of disk to just above anthers 8–10 mm, longitudinal strip of tissue bearing anther (WM) 12–13 mm long, hairy. Anthers (Z) 20, set in a ring, each 2.5 mm wide, filaments 2.0–2.3 mm long. Ovary (P) inferior, 36–38 × 14–20 mm, cavities irregular and bearing many ovules.
Additional features of sexual dimorphism from the Lang Biang observations
Bänziger and Hansen (1997) have summarised the distinction between females and males by differences mainly in the column (stalk and disk) form and structure, the colour of the upper disk surface, the form and dimensions of radial ridges on the inner surface of the perigone tube, and the occurrence of ovarial chambers in an expanded base below the column in the female. The Sapria himalayana f. albovinosa populations in our study area also conformed in these characteristics.
Additionally, we have observed several more attributes that help in the distinction between the sexes in Sapria himalayana f. albovinosa. For the Lang Biang populations examined, all males consistently had more steeply held perigone lobes (spreading 0–45° from the vertical) than females, in which the lobes were more spread out at wider angles (spreading 30–90° from the vertical) in fully open flowers (Figs. 3c, 4c, Table 1). Male flowers that were past anthesis and beginning to appear discoloured were also examined, and were found to have similarly steeply held perigone lobes, indicating that this was indeed the full extent of floral opening in males (Fig. 5e, f). We remain uncertain if biomechanical reasons linked to structural variation have caused these differences.
The basal cupules of male and female flowers were also different. Males have a much lower cupule (2–6 mm high) than females (10–16.6 mm high) (see Table 1, Fig. 5). This difference appears to be a significant and easy character for quick determination of the sex even when the flower is in the advanced bud stage, i.e., when the bud begins to reveal the apex of the paler colored developing perigone lobes (and before the other main characters can be assessed), and so might be of potential importance in field investigations that require special preparations for sampling or observation of the different sexes.
Some natural history aspects
The host plant (Fig. 6) was identified as the liana Tetrastigma laoticum Gagnep. (Vitaceae). Although the host plant populations at the Lang Biang Plateau sites were dense, we were unsure of their genetic variation and relationships, as lianas often drape onto the forest floor and can vegetatively generate new individuals. More detailed studies of the host vine relationships of Rafflesia by Pelser et al. (2016) have demonstrated that the more common species of Rafflesia can have multiple host vines, so that host-parasite specificity is not as great as previously supposed. In other words, the potentially clonal nature of neighbouring host lianas was uncertain. It was also not known if the phenological behaviour of the host lianas, e.g., if a state of flowering had any possible effects on their predisposition to infection by and establishment of the parasite. From our observations, male and female flowers can be mixed together in the same cluster from one individual liana. Flowers are red when open, turning black as they senesce. We have not specially studied the pollinators but were able to note that flies belonging to the Calliphoridae and Stratiomyidae families visited open flowers (Fig. 7c, d). The pollination biology of Sapria is similar to that of Rafflesia in that pollen from the anther is deposited on the visiting flies, which is then carried to other flowers (Heide-Jørgensen 2008).
There is currently a dearth of information on seed development, seed dispersal, germination, as well as ecology in terms of infection and establishment for Sapria species. Better observations of these aspects will only be possible where a good number of populations are present, allowing comparative work, within secure sites where disturbance is likely to be absent or minimal, such as at the presently known Vietnamese sites. Also, the security and commonness of the parasite on site would enable possibilities for tagging and longer-term observations to be carried out, such as phenology and other ecological attributes, and plans are being formed by our research group for suitable studies on Sapria himalayana f. albovinosa.
Conservation management
Both known Sapria sites on the Lang Biang Plateau are within relatively undisturbed broadleaf evergreen montane forest with Acer (Aceraceae), Fagaceae trees and Tetrastigma (Vitaceae) lianas commonly occurring. Recent studies of genetic populations of Rafflesiaceae have indicated that loss of a single infected host vine could result in large genetic losses of the parasite (Barkman et al. 2017), thus conservation activities should also focus on the conservation of host vine populations.
Whereas the Nam Ban site is itself a protection forest, the Tuyền Lâm site is within the Lâm Viên Protection Forest where only light tourism activities (e.g., forest trekking and interpretation) are permitted.
Following our investigations, the Southern Institute of Ecology has alerted authorities of the Lâm Đồng Province, under which jurisdiction the sites are administered, for the sites to be specially demarcated as Protected Research Reserves. This special status will no doubt enhance further careful use of designated parts of the Tuyền Lâm site for nature tourism, as well as maintain the integrity of the other strictly protected parts that will, among other things, contribute to the conduct of our longer-term studies.