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Korean J. Pl. Taxon > Volume 55(3); 2025 > Article
DEVKOTA and NICKRENT: Misunderstood mistletoes: The status of the genus Loranthus (Loranthaceae) from the Central Himalayas of Nepal

Abstract

Confusion currently surrounds the application of names to some mistletoes found in Nepal. As exemplified by the eFlora of India, Loranthus lambertianus and L. odoratus are both treated as species of Helixanthera. The type of the former species was first collected in Nepal in 1826 but additional collections since then are lacking. A new collection of L. lambertianus from the Tamakoshi Valley of Dolakha District, Central Himalayas of Nepal was obtained and it matches the type morphologically. A new description from this material is provided. In addition, molecular phylogenetic data place it with eight other species of Loranthus in a well-supported clade separate from Helixanthera. We acknowledge that the taxonomic history of these mistletoes is complex, however, this part of the story is now clear and should be used to update world plant taxonomic databases, checklists, and floras.

INTRODUCTION

Within the Sandalwood order (Santalales) there are nearly 1,700 hemiparasitic mistletoe species classified in five families: Amphorogynaceae, Misodendraceae, Santalaceae, Viscaceae and Loranthaceae, the latter being the largest with 76 genera and over 1,000 species (Nickrent, 2020). Seven genera of Loranthaceae have been documented for Nepal: Dendrophthoe Mart., Helixanthera Lour., Loranthus Jacq., Macrosolen (Blume) Reichb., Scurrula L., Taxillus Tiegh. and Tolypanthus Blume. The genus Loranthus consists of ca. nine Old World species distributed from eastern Asia to Europe (Nickrent et al., 2021) and two of these species occur in Nepal: L. odoratus Wall. and L. lambertianus Schult. & Schult. f. Verification of the identity of these taxa, specifically whether they are Loranthus or Helixanthera, is required for ongoing floristic projects in the region, thus the stimulus for this paper.
Loranthus odoratus was first collected in 1820 in Nepal by Nathaniel Wallich who published this name in Flora Indica (1824). This specimen was from the hills surrounding the Kathmandu Valley, Nepal. The type is extant and present at Kew (K001111169). As currently circumscribed, this species is widespread with a distributional range spanning Nepal, India, China, Myanmar, Thailand, and Indonesia. This species is quite polymorphic and possibly non-monophyletic (Nickrent et al., 2021).
Loranthus lambertianus was published in 1829 by the Austrian botanists Josef August Schultes and his son Julius Hermann Schultes in Linnaeus’ Systema Vegetabilium. They examined a specimen, collected in 1826 in Nepal that was communicated by the British botanist Aylmer Bourke Lambert. This specimen is extant and bears the original label by Schultes which says Species nova, Loranthus lambertianus si Tibi placet, dicenda. A subsequent label is attached from Herbarium Martii (Herbarium of Carl von Martius). In 1870 that collection was transferred to the Herbier du Jardin Botanique de l’Etat which later became the National Botanical Garden of Belgium. Since 2014, this is the herbarium at the Meise Botanic Garden in Bruxelles, Belgium. This sheet (BR0000021461484) has at least four shoots, one of which bears an intact inflorescence. Another specimen exists at the Herbier Museum Paris (P00756278) that bears a label from that institution reading Loranthus lambertianus Schultes type. Communiqu par Lambert Schultes, 1826 (Communiqu par l’Herbier de Bruxelles H. de Martius). This specimen consists of a single leaf and a short stem with two leaves with no reproductive material. It was annotated in September 1927 by B. H. Danser as Hyphear lambertianum (Schult.) Dans. This is possibly a fragment from the BR specimen.
The status of the genus Loranthus was recently reviewed (Nickrent et al., 2021) and particular attention was paid to the two species from Nepal. Despite this, it appears that this information has not been noticed and/or accepted by a number of projects and websites. The family Loranthaceae has not yet been treated in the Flora of Nepal (electronic version at http://www.floraofnepal.org/onlineflora). In contrast, the Annotated Checklist of the Flowering Plants of Nepal (http://www.efloras.org/) lists the correct names L. odoratus and L. lambertianus. The Flora of China (Qiu et al., 2003) includes L. lambertianus but not L. odoratus, (or as its synonym Helixanthera odorata (Wall.) Rajasek), despite there being three collections of this species from China on GBIF. World Flora Online (Kew) considers L. odoratus Wall. a valid species whereas it lists L. lambertianus as a synonym of Helixanthera lambertiana (Schult. f.) Rajasek. The eFlora of India lists Helixanthera odorata with L. odoratus as a synonym. Neither Helixanthera lambertiana nor Loranthus lambertianus is listed on this site, despite the fact that this taxon is known from India (Sikkim).
The Global Biodiversity Information Facility (GBIF) assembles data from many herbaria and websites. For Loranthus lambertianus, it indicates its source is the Catalogue of Life Checklist (COLC, https://www.gbif.org/dataset/7ddf754f-d193-4cc9-b351-99906754a03b). That checklist has L. lambertianus as the correct species name for this taxon, however, GBIF lists it as a synonym of Helixanthera lambertiana. Similarly, the Catalogue of Life website (COL https://www.catalogueoflife.org/) recognises L. odoratus as the correct name whereas GBIF has it as a synonym of Helixanthera odorata (Wall.) Rajasek. Curiously, the COL recognizes both L. lambertianus and L. odoratus as the correct names. Its dataset source derives from the World Plants website (Michael Hassler, https://www.worldplants.de/world-plants-complete-list/complete-plant-list) who recently updated the nomenclature for these two mistletoes. Overall, it appears that information is being inconsistently disseminated.
The above discussion was provided to demonstrate the varied taxonomic treatments seen on different websites for the two mistletoes found in Nepal, Loranthus lambertianus and L. odoratus. Here we review the biological and nomenclatural issues surrounding these two species and justify our decision to include them in the genus Loranthus.

MATERIALS AND METHODS

Fieldwork by the first author in the Tamakoshi valley of Bagmati Pradesh Province, Dolakha District, Nepal took place on 25 April 2015. The forests of the Godawari area were explored for one week during which time Loranthus lambertianus, in vegetative condition, was seen parasitizing stems of Quercus semecarpifolia Sm. On 20 May 2018, MPD returned to the site where samples were collected, photographs taken, morphological characteristics recorded and voucher specimens pressed. Multiple individuals of the mistletoe infecting Quercus semecarpifolia were observed. The population was located at an elevation of 2,598 m (2759′00.1″N, 8612′29.1″E) on an exposed, SE facing slope of 50°, close to the Tibetan border. The vouchers (M. Devkota 1421) are deposited in the National Herbarium and Plant Laboratories (KATH070853 and KATH070854). Digital images of the specimens can be accessed on the Herbarium Plant Database at the http://plantdatabase.kath.gov.np/plants/search. Flower samples were stored in 75% alcohol and examined in the Botany Department, Amrit Campus, Tribhuvan University. These were compared with mistletoe specimens deposited in KATH. Digital images of 23 herbarium sheets of Loranthus odoratus are present on the KATH Herbarium Plant Database, including those made by MPD (nos. 301, 1168).
All of the relevant literature associated with Loranthus and Helixanthera was assembled as well as photographs of living plants, herbarium specimens, illustrations, and written descriptions.

RESULTS AND DISCUSSION

The Loranthus lambertianus collection

This mistletoe was commonly found on the higher canopies of the host where it partially or completely defoliated the infected branches. The heavily degraded forest had Q. semecarpifolia as the dominant tree with Alnus nepalensis D. Don, Betula alnoides Buch.-Ham. ex D. Don, and Pieris formosa as associated tree species.
An initial search of the KATH herbarium showed that no mistletoes matched the collected specimen. Examination of this specimen and a thorough literature search confirmed that this was Loranthus lambertianus, a species listed in the Annotated Checklist of the Flowering Plants of Nepal; however, that website did not provide any details regarding the occurrence and distribution of the mistletoe in the country. Further, it was found that no previous checklist of the flowering plants of Nepal, including the works of Hara et al. (1982) and Press et al. (2000), included this mistletoe in their species lists. Because the Latin protologue by Schultes and Schultes (1829) was the only description of the species, the following is provided.

Description of Loranthus lambertianus

Shrubs, deciduous, erect, to 1.5 m tall, glabrous, producing large ball-like haustoria, epicortical roots absent. Stems pseudo-dichotomously branched, distinctly articulated; older branches dark brown, terete, lenticelate; younger branches dark brown, covered with brown papery caducous winter bracts, terete, smooth. Leaves alternate, simple, borne on brachyblasts, petiole 2–3 mm long; lower leaves entire, ovate, ca. 1 cm long; upper leaf blades entire, broadly to narrowly ovate, oblong, sometimes obovate, 1.7–4 cm long, thin and papery, base cuneate, apex acute or rounded, lateral veins obscure, in 3 to 4 pairs, more prominent on upper surface. Inflorescences spikes, solitary, terminal, on older branches, 3–3.5 cm long, peduncles subangular, 3 mm long. Flowers bisexual, epigynous, 10–15, sessile, arranged opposite and sub-opposite in pits (fovea) of inflorescence axis, evenly spaced, angled slightly acropetally, subtending bract minute, forming part of foveal rim, 5–6 mm wide, 6-merous; calyculus minute, entire; petals 6, free, valvate, pale yellow, lanceolate or oblong, 2.8–3 mm long, apex acute, reflexed at anthesis; stamens 6, filaments 1.3–1.5 mm long, adnate one half their length to the base of the petals; anthers 3/4 width of the petal bases, white, with two smaller basal locules and two larger terminal ones; ovaries inferior, the lower portions sunken into the pits; style 1–1.5 mm long, stout; stigma capitate, flattened, obliquely lobed with an undulate and finely papillate margin. Flowering: April–June. Fruiting: assumed June–August.
This description matches very well with the one provided by Schultes and Schultes (1829), with the exception that they indicated the flowers were 5- vs. 6-merous. Comparing the type of Loranthus lambertianus with Devkota 1421 (Fig. 1) shows the overall similarity between the two. Unfortunately, the photograph of the type does not provide sufficient resolution to confirm flower merosity (the specimen was not examined directly). It is possible that Schultes erred in the description of the flower, however, this seems unlikely since he placed this species in section “b. Flores pentandri, 2. Inflorescentia terminali. More likely is the fact that species of Loranthus show plasticity in floral merosity, e.g., 4-, 5- and 6- merous flowers can occur on the same plant. This was observed by Danser (1936) who said “Moreover the number of petals appears not to be constant in Hyphear [Loranthus] europaeum, as its flowers are in general 6-merous, but partly 5 and even 4-merous.”

Loranthus and Helixanthera: Morphological evidence

Danser (1931) proposed a new system of classification for the Old World Loranthaceae. His second of two keys concerned Hypheatinae (Loranthinae of Engler) that distinguished Hyphear from Helixanthera by the former having inflorescences as spikes and globose anther thecae and the latter having spikes or racemes and oblong anther thecae. Danser (1938) said “Hyphear is very closely related to Helixanthera, and, if it will finally appear undesirable to elevate the very different sections of the latter genus to the rank of genera (about which I still am in doubt), it will be better to consider also Hyphear as a section of Helixanthera.”
Balle et al. (1960) proposed conserving the name Loranthus Jacq. over Hyphear and this was accepted at the Edinburgh International Botanical Congress in 1964. Her main focus was upon Loranthus europaeus, but with that name transferred, other species of Hyphear by Danser (1929) were also moved (back) into Loranthus. Thus, Hyphear lambertianum (Schult. & Schult. f.) Danser became L. lambertianus Schult. & Schult. f.
Although Barlow (1997) treated Helixanthera and Loranthus as separate genera, he followed Danser by considering them closely related. Indeed, these two are the last to be distinguished in his key to genera. The couplets were “flowers hermaphrodite, anthers linear” for Helixanthera and “flowers mostly unisexual, anthers globose to subglobose” for Loranthus. Only L. odoratus is present in Flora Malesiana, and regarding flower sexuality, Barlow wrote “flowers probably functionally unisexual but often with vestigial organs of the other sex.” His description only mentions flowers with an androecium whereas the illustration shows a plant in fruit. The specimen of L. odoratus examined by coauthor MPD from Nepal had bisexual flowers, but as discussed in Nickrent et al. (2021), the sexual mode of this species requires further research. Because of doubts about the systematic value of flower merosity and sexuality, Danser (1936) suggested that only two species of Loranthus (as Hyphear) might exist.
The key to genera of Loranthaceae in Flora of China (Qiu et al., 2003) included several characters to differentiate Helixanthera from Loranthus. These were flowers sessile vs. pedicellate, flower merosity, corolla color, corolla size, and anther shape (ellipsoid in Helixanthera vs. ovoid, biglobose, or absent in Loranthus). Although flowers are generally larger in Helixanthera than in Loranthus, most character states overlap among the various species in the two genera or only apply to certain species. It appears that all Helixanthera have bisexual flowers whereas Loranthus has variable flower sexuality, including some species with bisexual flowers. Compared with Helixanthera, anther shapes in Loranthus are relatively homogeneous. But the description “globose” or “subglobose” that applies to species such as L. europaeus does not apply to others such as L. odoratus that has elliptic anthers much like those seen in various Helixanthera species.
Rajasekaran (2007) made two new combinations: Helixanthera lambertiana (Schult.) Rajasekaran and H. odorata (Wall.) Rajasekaran but provided no discussion or justification for these transfers. These concepts were carried over into the Flora of India treatment (Rajasekaran 2012) which is strongly influencing the Flora of Nepal project.

Loranthus and Helixanthera: Molecular evidence

Along with all members of Santalales, Loranthaceae has been the subject of numerous molecular phylogenetic studies. Multigene studies that sampled representatives of both Helixanthera and Loranthus include Vidal-Russell and Nickrent (2008), Su et al. (2015), Liu et al. (2018), and Nickrent et al. (2019). In all of these, the genus Loranthus is sister to Cecarria obtusifolia (Merr.) Barlow and that clade did not include Helixanthera (Fig. 2A). More recently, a detailed molecular phylogenetic and morphological cladistic study of all species of Loranthus was conducted (Nickrent et al., 2021). Whole chloroplast genome sequences and nuclear ribosomal DNA supported the monophyly of Loranthus (nine species) and the sister relationship between this genus and Cecarria (Fig. 2B). The classification of Loranthaceae proposed in Nickrent et al. (2010) placed both Loranthus and Helixanthera in tribe Lorantheae, however, they were segregated into subtribes Loranthinae and Dendrophthoinae, respectively.
In contrast to the well-supported monophyly of Loranthus, such is not case with Helixanthera (Fig. 2A). This mistletoe contains ca. 40 species distributed from Africa through southern Asia and into eastern Asia and Malesia. Five species were sampled in the molecular study by Liu et al. (2018) wherein those representatives were placed on three different clades of Lorantheae. Although modern taxonomists consider all of these congeneric, the molecular evidence strongly suggests that the assemblage is polyphyletic and separate genera should be recognized. This would fit with past views of workers who erected a number of genera to account for the wide range of morphological variability e.g., Acrostachys Tiegh., Chiridium Tiegh., Coleobotrys Tiegh., Dithecina Tiegh., Lanthorus C. Presl., Leucobotrys Tiegh., Phoenicanthemum (Blume) Blume, Strepsimela Raf., and Sycophila Welw. ex Tiegh. Despite the problems of generic circumscription surrounding Helixanthera, they do not affect the composition of Lorantheae subtribe Loranthinae.

CONCLUSION

As shown in the above discussion, the unstable taxonomic history of these mistletoes is a direct reflection of their complex morphologies and sexual systems, as well as different concepts employed by pre-molecular workers who studied these plants. In the past, monophyly was not relevant to generic circumscription because phylogenies reflecting the evolutionary history of these plants were not available. Today the results from robust phylogenetic analyses should be used to inform the taxonomic treatment of a group and the nomenclature should accommodate such information by maintaining monophyletic genera.
This and previous studies strongly support the concept that the mistletoe present in Nepal is Loranthus lambertianus, not Helixanthera lambertiana (a synonym). Previous molecular phylogenetic studies showed that all species of Loranthus are monophyletic and separate from Helixanthera. The recently collected specimens conform well to the type and description of that species by Schultes and Schultes (1829) and it was a component of the Loranthus clade in the molecular phylogenetic analysis. For these reasons, the transfer of L. lambertianus to Helixanthera lambertiana as made by Rajasekaran (2007) is not supported.

NOTES

ACKNOWLEDGEMENTS
The authors thank the Austrian Science Academy (OAW) for supporting the collection trip to Tamakoshi Valley, especially to Dr. Gerhard Glatzel who facilitated this support. Moreover, we would like to thank the staff of KATH for allowing access to their herbarium specimens.
CONFLICTS OF INTEREST
The authors declare that there are no conflicts of interest.

Fig. 1
Loranthus lambertianus Schult. & Schult. f. A. Inflorescence bearing portion of the specimen from the Meise Botanic Garden Herbarium (BR0000021461484) collected in 1826 in Nepal. B. Flowering shoot of plant collected and photographed by M. P. Devkota (1421, KATH070853) in Tamakoshi valley of Bagmati Pradesh Province, Nepal.
kjpt-55-3-165f1.jpg
Fig. 2
Loranthaceae molecular phylogenies. A. Simplified phylogenetic tree derived from Liu et al. (2018) showing the positions of Loranthus and Helixanthera within the overall Loranthaceae phylogeny. This and other studies showed that Helixanthera is not monophyletic nor closely related to Loranthus. B. Nuclear ribosomal DNA phylogenetic tree showing the monophyly of Loranthus and the position of L. lambertianus. Modified from Nickrent et al. (2021).
kjpt-55-3-165f2.jpg

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