The authors introduce the term facultative vivipary for the first time in gingers and elaborate on this reproductive strategy. Four new observations of facultative vivipary are reported in the genus Hedychium which were discovered during botanical explorations by the authors in Northeast India (NE India) over the past three years. The viviparous taxa are H. marginatum C.B.Clarke, H. speciosum var. gardnerianum (Ker Gawl.) Sanoj & M.Sabu (previously, H. gardnerianum Sheppard ex Ker Gawl.), H. thyrsiforme Buch.-Ham. ex Sm. and H. urophyllum G.Lodd. The authors also attempt to summarise the occurrence of vivipary in the family Zingiberaceae from published reports and to clarify a taxonomic misidentification in a previously known report of vivipary in Hedychium elatum.

Facultative vivipary, gingers, Meghalaya, Nagaland, phenology, pseudovivipary, recalcitrant seeds

Vivipary in plants is a heterogeneous term that describes a unique and rare reproductive strategy where seedlings are precociously produced while still on the maternal parent (Goebel 1905). With the discovery of several examples of germination on the parent plant in various angiosperm families, vivipary has become a biologically complex term because it now accommodates both sexual (true vivipary and cryptovivipary, see Elmqvist and Cox 1996) as well as asexual reproductive (pseudovivipary) strategies in plants (Farnsworth 2000).

True vivipary refers to vivipary sensu stricto and it is defined as penetration of a sexually reproduced embryo through the fruit pericarp and the resultant dispersal of this seedling (Cota-Sánchez 2004). Contrastingly, cryptovivipary is defined as vivipary wherein the seedling does not penetrate the fruit pericarp (Cota-Sánchez and Abreu 2007), while pseudovivipary is defined as production of apomictic or asexual propagules (like bulbils) on the parent plant (Law et al. 1983, Ofir and Kigel 2014). Thus sexually reproduced progeny (seed) is an integral part of the definition of vivipary and should not be confused with pseudovivipary which refers to production of apomictic or asexual plantlets or bulbils (Poulsen and Nordal 2005).

Within the family Zingiberaceae, vivipary is rarely discussed as an important reproductive strategy, except in Hedychium elatum R.Br. by Bhadra et al. (2013) (taxonomic misidentification discussed later). However, vivipary has been recorded in taxonomic descriptions such as in Camptandra latifolia Ridl. (Ridley 1899), in natural history observations (Hedychium gardnerianum Sheppard ex Ker Gawl.; Djeddour et al. 2012) and in pollination studies (Alpinia mutica Roxb.; Aswani and Sabu 2015). In contrast, pseudovivipary is very common in the form of bulbils and it has been recorded in at least six genera within Zingiberaceae: Alpinia Roxb., Boesenbergia Kuntze, Globba L., Hedychium J.Koenig, Larsenianthus W.J.Kress & Mood and Zingiber Mill. (Table 1). Interestingly, pseudovivipary (bulbil formation) was one of the key characters used to distinguish section Globba into two series by Schumann (1904) during the revision of Zingiberaceae, although recent molecular studies have not addressed the role of bulbil as an important character defining clades (see Williams et al. 2004).

The genus Hedychium (more than 80 species, see Sanoj 2011) is native to the Indian subcontinent, China, Southeast Asia (mainland and maritime) and Madagascar (Kress et al. 2002, Newman et al. 2004, Newman and Pullan 2007, Sanoj et al. 2013, WCSP 2018). The highly speciose regions are identified to be NE India (Arunachal Pradesh, Manipur, Meghalaya, Mizoram, Nagaland and Sikkim), Southwest China (Yunnan), Myanmar, Thailand, Borneo and Java (Holttum 1950, Sirirugsa and Larsen 1995, Gao et al. 2008, Sarangthem et al. 2013). The plant habit ranges from terrestrial to epiphytic as well as lithophytic and each plant has a perennial rhizome which bears new ramets annually. Each ramet gives rise to a terminal inflorescence (known as thyrse) which consists of primary inflorescence bracts that hold flowers in cincinni (Kirchoff 1997). Two main types of inflorescence bracts are identified in Hedychium- imbricate (where bracts are broad and overlapping, hiding the rachis) and folded (where bracts are narrow and fold partially or completely to enclose the flowers, leaving rachis visible, Holttum 1950). The flowers are hermaphroditic, characterised by reduced petals and petaloid staminodes. The fruit is a septifragal capsule, light to dark green when young and changes to yellow with age (Fig. 1A). It splits open into three fleshy lobes, deep yellow or orange internally, with seeds arranged as in axile placentation. Mature seed is brown or black, covered by an aril which is either deep red or bluish-violet (in H. hookeri Baker, Srivastava 1984; fig. 1B). Frugivorous birds (Orchard 1973, Larsen et al. 1998) and rodents (Ridley 1899, Shiels 2011) are major dispersers of Hedychium seeds.

Figure 1. 

Septifragal capsule of Hedychium. A Unripe fruit of H. marginatum B Ripe fruit of H. spicatum (seeds can be seen covered by aril). Photographed by A. Ashokan.

Although the name Hedychium is more than 230 years old (Koenig 1783), the report of vivipary in this genus is very recent (Djeddour et al. 2012, Bhadra et al. 2013). The first vivipary in Hedychium was detailed by Bhadra et al. (2013) in H. elatum from Kalimpong, on the way to Darjeeling (West Bengal, India) although it had already been reported in Djeddour et al. (2012). Here, four new observations are reported of facultative vivipary in the genus Hedychium: H. marginatum, H. speciosum var. gardnerianum, H. thyrsiforme and H. urophyllum. The taxonomic misidentification in Bhadra et al. 2013 is also reported and it is suggested that vivipary was not observed by them in H. elatum but the plant observed by them could likely be H. speciosum var. gardnerianum. Since voucher information is not available from Bhadra et al. (2013), their published images were used to assign an identity to the plant identified by them as H. elatum. Based on a published image (figure 1A in Bhadra et al. 2013) and the characters listed here in Table 2, it is clear that the species they reported cannot be H. elatum. Since voucher specimens or high resolution images are critical in species-level identification in Hedychium, it is suggested that the two likely species illustrated by Bhadra et al. in their figure 1A are either H. gracile Roxb. or H. griffithianum Wall. (Wallich 1853) based on the inflorescence shape and delicate nature of the inflorescence bracts and flowers, which are characteristics to these species (Table 2). Further, the plant shown in figures 1B–H of Bhadra et al. is identified as H. speciosum var. gardnerianum (Ker Gawl.) Sanoj & M.Sabu. Therefore, the plant image shown with vivipary (figures 1B–H in Bhadra et al. 2013) is identified as H. speciosum var. gardnerianum because of the taxonomic description given by Bhadra et al. as “leaves white pulverulent beneath” which is characteristic of H. speciosum var. gardnerianum (Baker 1894).

For taxonomic clarity, the key morphological and ecological characters of the Hedychium taxa) are listed below where facultative vivipary has been observed. Voucher information is provided below as: collector name, voucher number, herbarium deposited.

1. Hedychium marginatum C.B.Clarke (Figs 2A–B, 3A; V. Gowda, VG-NL1899, BHPL)

Plant terrestrial, up to 1.5 m tall. Inflorescence conical; bracts imbricate; cincinni 3–6 flowers. Flowers orange-yellow, fragrant. Capsule elliptic, green and minutely hairy. Seeds many; aril red. The viviparous individual (bearing at least 10 seedlings on its dried infructescence) was observed along the Mokokchung-Tuensang Road, Mokokchung, Nagaland (26°19'59"N; 94°32'50"E) in August 2017 (Fig. 4).

Figure 2. 

Facultative vivipary in Hedychium. A–B Hedychium marginatum C–DH. speciosum var. gardnerianum, E&F. H. thyrsiforme, G&H. H. urophyllum. Photographed by A. Ashokan & N.S. Prasanna (E&F).

It is very common in the Indian states of Manipur and Nagaland (Clarke 1890, Baker 1894, Sanoj 2011).

Flowering period: August to October; fruiting from September to November.

2. Hedychium speciosum var. gardnerianum (Ker Gawl.) Sanoj & M.Sabu (Figs 2C, D, 3B; A. Ashokan, VG-ML1660, BHPL)

Plant terrestrial, up to 2.5 m tall. Inflorescence cylindrical; bracts folded, folding supervolute; cincinni 2 flowers. Flowers lemon-yellow with bright red stamen, highly fragrant. Capsule oblong, green and glabrous. Seeds many; aril red. The viviparous individuals were found growing along the Shillong-Dawki Road in the East Khasi Hills district, Meghalaya (25°22'25"N; 91°52'37"E) in August 2016 and 2017 (Fig. 4).

It has a wide distribution range covering Eastern Himalaya and NE India, especially the Indian states of Arunachal Pradesh and Meghalaya (Edwards 1823, Roscoe 1828).

Flowering period: July to October; fruiting from September to November.

3. Hedychium thyrsiforme Buch.-Ham. ex Sm. (Figs 2E–F, 3C; N.S.Prasanna, VG-MZ2201, BHPL)

Plant terrestrial, up to 1.5 m tall. Inflorescence pyramidal; bracts folded, folding supervolute; cincinni 3–8 flowers. Flowers white, mildly fragrant. Capsule oblong, green and glabrous. Seeds many; aril red. The viviparous individual (bearing one seedling on its dried infructescence) was observed in Aizawl, Mizoram (23°43'48"N; 92°43'52"E) in July 2017 (Fig. 4).

It grows very commonly in the Indian state of Mizoram. It was originally described from Nepal (Smith 1811).

Flowering period: August to October; fruiting from September to November.

Figure 3. 

Inflorescence. A Hedychium marginatum BH. speciosum var. gardnerianumC H. thyrsiforme D H. urophyllum. Photographed by A. Ashokan.

4. Hedychium urophyllum G.Lodd. (Figs 2G–H, 3D; A. Ashokan, VG-ML1612 & 1725, BHPL)

Plant terrestrial, up to 2.2 m tall. Inflorescence conical; bracts imbricate; bracts are found to retain water; cincinni 2–4 flowers. Flowers bright yellow, highly fragrant. Capsule elliptic, dark green and glabrous. Seeds many; aril red. The viviparous H. urophyllum was growing in a mixed pine forest at Sanmer along the Shillong-Elephant Falls Road, East Khasi Hills district, Meghalaya (25°32'47"N; 91°50'16"E) in June 2015 and August 2016 (Fig. 4).

Figure 4. 

Distribution records for facultative vivipary in Hedychium in NE India.

It is endemic to Meghalaya (Loddiges 1831, Sanoj 2011).

Flowering period: July to September; fruiting from September to November.

During the three year study in NE India, four different Hedychium taxa showing vivipary have been identified: H. marginatum, H. speciosum var. gardnerianum, H. thyrsiforme and H. urophyllum. However, current observations of vivipary in Hedychium cannot be strictly identified as true vivipary or cryptovivipary (Elmqvist and Cox 1996, Cota-Sánchez 2004) since the fruit of Hedychium (septifragal capsule) dehisces before seed maturation while true vivipary requires the embryo to penetrate the fruit pericarp during germination. This makes the viviparous seed germination in Hedychium or gingers a case of “facultative vivipary”, which is introduced for the first time in gingers. The term “facultative vivipary” is proposed for the reproductive strategy observed in Hedychium since it represents the facultative nature of this reproductive strategy (occurs only when seeds are retained by bracts) as well as the viviparous nature of the germinating seed (seedling borne on the parent plant).

The factors leading to the incidence of facultative vivipary can be identified as a combination of climatic, ecological and physiological variables (Lee and Harmer 1980, Cox and Humphries 1993). In most Hedychium, flowering and fruiting coincide with the rainy season (an ecological trait shared amongst almost all Hedychium). The morphology of bracts in many Hedychium is such that the bracts can hold water. Thus the bracts provide a platform for the germination of the recalcitrant seeds by holding water which favours their germination. Further, these bracts are retained even after maturity of seeds thus facilitating their continued growth as seedlings. Thus, facultative vivipary may be a result of ‘failure to disperse’ either due to the structural hindrance imparted by the bracts or due to the absence of a disperser. The importance of facultative vivipary was not discounted as an important reproductive strategy that may facilitate seed germination under unpredictable climatic conditions, but this remains to be tested.

This multi-year observation of facultative vivipary in four Hedychium taxa suggests that facultative vivipary may be a more common reproductive strategy than that which is known so far. The immediate germination of seeds on the parent plant in at least four taxa also implies that recalcitrance of seeds (i.e. absence of dormancy) may be common in Hedychium (also true for other gingers, Leong-Škorničková, pers. com.). Recalcitrance has been suggested to be a common characteristic of plants growing in wet habitats (Farnsworth 2000), which is true for most Hedychium. Further, morphologically, it has been shown that Hedychium and other gingers have a thin seed coat (Benedict et al. 2015), which may also facilitate recalcitrance. Thus, it is predicted that facultative vivipary may be more common in Hedychium because of the physiology of the seed, i.e. its recalcitrant nature.

The authors’ efforts to summarise vivipary sensu lato across Zingiberaceae from published literature showed that vivipary sensu stricto is absent and that all reported cases of vivipary in other gingers can also only be identified as “facultative vivipary” or pseudovivipary, as in the case of Hedychium. Other genera that display facultative vivipary (except in A. mutica) also show similar characters as observed in Hedychium that favour this reproductive strategy, such as persistent bracts, bract structure that may retain the seeds, and recalcitrant seeds. It was found that both facultative vivipary and pseudovivipary are common amongst gingers with pseudovivipary being more frequent only in Globba (Table 1). Finally, in the genus Hedychium, pseudovivipary is only reported in H. greenii (Fig. 5).

Figure 5. 

Pseudovivipary (Bulbil formation). A Hedychium greenii (the inset in the upper right is an inflorescence) B Alpinia purpurata C Globba multiflora D Larsenianthus careyanus. Photographed by A. Ashokan & Preeti (A).

To understand if vivipary sensu lato is a convergent character in Hedychium, different types of vivipary were mapped on a preliminary molecular phylogenetic tree (modified from nrDNA ITS tree of Wood et al. 2000, with the addition of H. marginatum and H. speciosum var. gardnerianum). It was found that both facultative vivipary and pseudovivipary are currently restricted only to a few members within the Clade IV (as defined in Wood et al. 2000). To understand the relevance of facultative vivipary and pseudovivipary as important reproductive strategies in gingers, it is suggested that future studies should treat different types of vivipary as an important morphological character along with seed characteristics (i.e. presence or absence of dormancy).

The authors thank the Ministry of Human Resources and Development (MHRD), the National Geographic Society for research funds to V. Gowda, IISER-Bhopal for the infrastructure, the Council for Scientific and Industrial Research (CSIR) for the senior research fellowship to A. Ashokan and the Heliconia Society International (HSI) for the field research grant to A. Ashokan. We also thank State Forest Departments of Arunachal Pradesh, Manipur, Meghalaya, Mizoram and Nagaland for research permits, Dr. Mark Newman (Royal Botanic Garden Edinburgh) for drawing our attention to the taxonomic error in the identity of H. elatum that appeared in the previous report and Dr. Jana Leong-Škorničková (Singapore Botanic Gardens) and Dr. Neeta Sarangthem for research inputs. We also appreciate the suggestions and advice from two reviewers and the subject editor Dr. Yasen Mutafchiev that has helped us improve the manuscript.