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On the Use of the Showy Mistletoe Helixanthera cylindrica (Santalales: Loranthaceae) as a Nectar Source for Butterflies in the Malay Peninsula, South-East Asia

Journal of the Lepidopterists’ Society
75(4), 2021, 297–301
Additional key words: Charana; Iolaini; Jacoona; Lycaenidae; Malaysia; Purlisa; Tajuria
There is little published information on the
interactions of pollinating insects and the flowers of
showy mistletoes. The Santalales is an important
angiosperm order comprising over 2,200 species in 160
genera, many of which are parasitic (Nickrent et al.
2010). Of these, the hemiparasitic mistletoes from the
families Loranthaceae, Viscaceae, and Amphoro-
gynaceae (sensu Nickrent et al. 2010) are of considerable
interest to lepidopterists. In Peninsular Malaysia, the
following genera of parasitic mistletoe are utilised as
larval hosts by several families of butterflies, viz:
Dendrophthoe, Dendrotrophe, Helixanthera, Loranthus,
Macrosolen, Scurrula, and Viscum (Igarashi and Fukuda,
1996, 2000; Corbet et al. 2020). Of the Malaysian
butterflies, the pierid genus Delias is solely dependent
on mistletoe as larval hosts, as are a handful of genera
from the lycaenid tribes Iolaini and Remelanini, and
several species from the nymphalid genus Euthalia. A
further number of species are facultative feeders of
mistletoe in their early stages (e.g. the lycaenids Anthene
emolus, Arhopala centaurus, Hypolycaena erylus, and
Semanga superba [Ballmer 2008, Tan & Khew 2012]).
While the role of mistletoe in the early stages of
indomalayan butterflies has been well illustrated (see
Igarashi & Fukuda 1996, 2000), their role as a nectar
resource for adult butterflies is comparatively less well
understood. Here we report on the use of Helixanthera
cylindrica as a nectar source for adult butterflies in
Peninsular Malaysia.
Between August–September 2020, the second and
last authors recorded butterfly activity on an exposed
hilltop at Genting Tea Estate, Pahang, Malaysia. The
field site is part of a 40 ha. tea estate with a mix of
secondary forested growth and old tea plantations, at an
elevation of approximately 700 m above sea level. Of
note were the stands of matured tea trees (Camellia
sinensis) heavily infested with hemiparasitic mistletoes,
in particular Dendrophthoe pentandra, Helixanthera
cylindrica, Macrosolen cochinchinensis, and Scurrula
ferruginea (all Loranthaceae). In addition to Camellia,
flowering was observed for all aforementioned species of
mistletoe during the period of observation. The stands of
tea trees were interspersed with the dipterocarp Shorea
sumatrana. Observations were made over eight non-
consecutive days, between the hours of 0945 and 1300 h.
Notes were made of any butterfly seen probing flowers
or engaging in sustained nectaring.
Across all eight days of field observation, butterfly
activity was noted to be particularly high on the flowers
of H. cylindrica. No butterfly activity was observed on
the flowers of D. pentandra, M. cochinchinensis, and S.
ferruginea. Interestingly, the showy and fragrant flowers
of Camellia that were concurrently in flower were
evidently of little interest to butterflies, with only brief
nectaring attempts by two species of hesperiid (Pithauria
marsena and Hasora vitta) observed over the span of
eight days. In total, we recorded 32 species of butterflies
from three families probing at or taking nectar from H.
cylindrica (Table 1). Of these, 24 were from the family
Lycaenidae (75% of all observations), four from the
family Papilionidae (12.5%), and four from the family
Pieridae (12.5%) (Table 1). Of the observed species of
lycaenids, 58.3% were those from the tribe Iolaini,
including the genera Charana, Dacalana, Jacoona,
Pratapa, Purlisa, Rachana, Suasa, and Tajuria. A handful
of species from these genera reported here are listed as
rare or very rare in Peninsular Malaysia (Corbet et al.,
2020), for example Charana mandarinus splendida,
Jacoona anasuja anasuja, Purlisa gigantea gigantea, and
Suasa lisides suessa. Of these, P. gigantea gigantea
occurs only at mid to high elevations. Five species were
recorded visiting the flowers of H. cylindrica with high
frequency (six days or more, i.e. 75%). These were
Appias lyncida vasava, Niphanda asialis, Dacalana
vidura azyada, Purlisa gigantea gigantea, and Tajuria
deudorix ingeni. In contrast, 14 species had only single
day observations (accounting for 12.5% of total
Among the South East Asian loranthaceous
mistletoes, birds are recorded as the major vector of
biotic pollination (Danser 1929, Docters van Leeuwen
1954, Barlow 1997). In contrast to entomophilous
species, bird-pollinated mistletoes are often showy, and
with large gamopetalous flowers (30–160 mm) that are
either red or with contrasting colours such as orange,
yellow, green, or even black (Vidal-Russell & Nickrent
2008). The red, curved shape and long corolla length of
Helixanthera cylindrica flowers suggests that
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FIG. 1. Helixanthera cylindrica parasitizing Camellia sinensis, in situ photograph showing habitus. Note bright red inflores-
cence. Individual flower shown in figure inset. Photographs by N.L. Liew.
FIG. 2. A selection of butterflies photographed at Genting Tea Estate, Pahang, Malaysia. All species were recorded feeding
on flowers of H. cylindrica. A: Delias hyparete metarete; B: Nacaduba kurava nemana; C: Purlisa gigantea gigantea;
D: Jacoona anasuja anasuja; E: Charana mandarinus splendendida; F: Dacalana vidura azyada; G: Tajuria deudorix ingeni;
H: Tajuria yajna selangorana; I: Tajuria dominus dominus; J: Tajuria isaeus verna; K: Rachana jalindra burbona; L: Suasa
lisides suessa. All photographs by N.L. Liew.
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TABLE 1. Species of butterflies observed probing flowers or engaging in sustained nectaring of Helixanthera cylindrica at Genting
Tea E sta te , P ah an g, Ma lay si a. Fr eq uen cy of o bse rv at io ns co rre sp on d t o t he to ta l n um be r o f d ay s ( ou t o f ei ght ) tha t eac h spe ci es wa s
Species Family Subfamily Tribe
larval host
(# of days
Graphium agamemnon agamemnon Papilionidae Papilioninae Leptocircini No 1
Graphium evemon eventus Papilionidae Papilioninae Leptocircini No 3
Graphium sarpedon luctatius Papilionidae Papilioninae Leptocircini No 2
Lamproptera meges virescens Papilionidae Papilioninae Leptocircini No 1
Appias lyncida vasava Pieridae Pierinae Pierini No 7
Delias hyparete metarete Pieridae Pierinae Pierini Yes (Obligate) 3
Delias pasithoe parthenope Pieridae Pierinae Pierini Yes (Obligate) 1
Eurema simulatrix tecmessa Pieridae Coliadinae Euremini No 5
Acytolepis puspa lambi Lycaenidae Polyommatinae Polyommatini No 5
Jamides talinga Lycaenidae Polyommatinae Polyommatini No 1
Nacaduba angusta kerriana Lycaenidae Polyommatinae Polyommatini No 1
Nacaduba kurava nemana Lycaenidae Polyommatinae Polyommatini No 1
Nacaduba pactolus odon Lycaenidae Polyommatinae Polyommatini No 1
Niphanda asialis Lycaenidae Polyommatinae Niphandini No 6
Arhopala centaurus nakula Lycaenidae Theclinae Arhopalini Yes (Facultative) 1
Cheritra freja frigga Lycaenidae Theclinae Cheritrini No 1
Araotes lapithis arianus Lycaenidae Theclinae Deudorigini No 1
Sithon nedymond nedymond Lycaenidae Theclinae Deudorigini No 1
Charana mandarinus splendendida Lycaenidae Theclinae Iolaini Yes (Obligate) 3
Dacalana vidura azyada Lycaenidae Theclinae Iolaini Yes (Obligate) 6
Jacoona anasuja anasuja Lycaenidae Theclinae Iolaini Yes (Obligate) 5
Pratapa deva relata Lycaenidae Theclinae Iolaini Yes (Obligate) 2
Pratapa icetoides calculis Lycaenidae Theclinae Iolaini Yes (Obligate) 1
Purlisa gigantea gigantea Lycaenidae Theclinae Iolaini Yes (Obligate) 6
Rachana jalindra burbona Lycaenidae Theclinae Iolaini Yes (Obligate) 3
Suasa lisides suessa Lycaenidae Theclinae Iolaini Yes (Obligate) 3
Tajuria deudorix ingeni Lycaenidae Theclinae Iolaini Yes (Obligate) 6
Tajuria dominus dominus Lycaenidae Theclinae Iolaini Yes (Obligate) 1
Tajuria isaeus verna Lycaenidae Theclinae Iolaini Yes (Obligate) 1
Tajuria ister tussis Lycaenidae Theclinae Iolaini Yes (Obligate) 4
Tajuria mantra mantra Lycaenidae Theclinae Iolaini Yes (Obligate) 5
Tajuria yajna selangorana Lycaenidae Theclinae Iolaini Yes (Obligate) 4
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nectarivorous birds like sunbirds (Nectariniidae) are its
main pollinators (Figure 1). Some examples of bird-
pollinated mistletoes include Macrosolen, and
Dendrophthoe (Vidal-Russell & Nickrent 2008), and in
the latter, pollination and seed dispersal has been
reported to be facilitated by flower peckers (Dicaeidae)
and other passerine birds (Start 2011).
On the other hand, reports of butterflies and other
insects acting as pollinators of Helixanthera are few. We
note that all observations reported here only detail the
feeding or nectaring of flowers, and do not necessarily
imply pollination. More detailed experimental
observations are needed to demonstrate pollination and
fruit set as a result of butterfly nectaring activity. It is
possible that at this particular locale, interest in the
flowers of H. cylindrica by butterflies is opportunistic, as
few flowering plants are expected to occur in a dedicated
intercrop of Camellia and Shorea. Consequently, flowers
produced by the hemiparasitic mistletoes act as an oasis,
providing a much-needed resource in a landscape
otherwise denuded of nectar and suitable larval hosts.
While all four species of loranthaceous mistletoes
observed at this location produced flowers, only those of
H. cylindrica were attractive to butterflies. It is possible
that the bright red flowers of H. cylindrica were simply
more attractive to butterflies, and with the larger flowers
supporting larger butterflies such as papilionids and
pierids (Table 1; Figure 2A).
Given the abundance of other loranthaceous
mistletoes at this locale, hostplant interactions could also
account for the increased butterfly activity around stands
of H. cylindrica. Of the 32 species of butterflies
observed, 17 (50%) are known to rely on mistletoe as
larval hosts. Of these, only one species (Arhopala
centaurus nakula) is facultatively reliant on Macrosolen
cochinchinensis. The remaining 16 species have
caterpillars that are obligate feeders of mistletoe, and
apart from Delias hyparete metarete and Delias pasithoe
parthenope, all are iolaine lycaenids (Figure 2).
Oviposition was observed for both Purlisa gigantea
gigantea and Charana mandarinus splendida, on H.
cylindrica and D. pentandra respectively. Inspection of
both plants disclosed the presence of several ova and
larvae, though these were not collected. It is likely that
the early stages of other ioline lycaenids were present on
these plants. We note that among the species of
butterflies observed, only Purlisa gigantea gigantea
(Ballmer, 2008; pers. obs.) and Tajur ia y ajn a selang or an a
(pers. obs.) are known to utilize H. cylindrica as a larval
host. Ballmer (2008) reported the use of H. cylindrica as
a larval host for Anthene emolus, Hypolycaena erylus,
and Tajuria cippus in south Thailand, though none of
these species were observed by us.
Additionally, the topography of this site serves an
attractive vantage point for observing several lycaenid
genera, including Niphanda, Charana, Pratapa, and
Tajuria, all of which have species with strong affinities
for exposed hill-tops. Males are most frequently seen on
lofty perches, where they intercept passing females in a
behaviour known as “hill-topping”. These sites act as a
rendezvous point for both sexes, with hill-topping males
quickly intercepting any females passing through.
Indeed, both Niphanda asialis and Tajuria deudorix
ingeni were among the most frequently observed species
at this site. Together, this combination of topography,
abundance of loranthaceous host plants, and general
scarcity of nectar could account for the increased
observations of butterflies on the flowers of H.
cylindrica, particularly in acting as a magnet for many
otherwise rare iolaine species. While there are certainly
many gaps in these brief observations, our report
provides insight into the ecology of several rare and
poorly studied Malayan butterflies. Further field
observations will undoubtedly recover more records of
other butterflies interacting with Helixanthera, though a
more in-depth study is needed to determine whether H.
cylindrica is more widely utilized as a source of nectar
outside of this locale, and whether it remains a preferred
choice in the presence of other flowering plants.
No live butterflies were collected during the course of this
study. We thank Aaron Soh for useful correspondence on
Malaysian mistletoes. Michael Braby and David Lohman pro-
vided useful comments that greatly improved the quality of this
study. We thank Laurence Kirton for discourse regarding nomen-
clature and etymology.
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YI-KAI TEA* School of Life and Environmental
Sciences, University of Sydney, Sydney, Australia;
Department of Ichthyology, Australian Museum Re-
search Institute, Australian Museum, 1 William
Street, Sydney, NSW 2010 Australia; *Correspond-
ing e-mail: NYOK-LIN
LIEW Teacher Education Institute, International
Languages Campus, Ministry of Education
Malaysia, JONATHAN WEI SOONG 829 Upper Bukit
Timah Road, #04-21, Singapore, 678187 AND
HENRY S. BARLOW PO Box 10139, 50704 Kuala
Lumpur, Malaysia
Submitted for publication 3 May 2021; revised and accepted 14
May 2021.
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ResearchGate has not been able to resolve any citations for this publication.
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The fifth edition of Corbet and Pendlebury's classic 'The Butterflies of the Malay Peninsula' is now available. The text has been updated with new information on distributions, life histories and larval food plants. The taxonomy of each species has been reviewed, and the text and relevant keys have been revised with newly published information. The text runs to 506 pages and includes an extensive bibliography and full indices. Additionally, the layout has been modernized for better readability and aesthetics while several of the figures have been redrawn for clarity. It includes a completely new set of 132 colour plates illustrating every species reliably recorded from Singapore and the Malay Peninsula, showing the upperside and underside of both males and females of most species. The immature stages of selected species, representing each butterfly subfamily, are illustrated in 6 colour plates. There are also 25 pages of genitalia drawings.
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We present here a revised classification of Santalales, an angiosperm order that contains 18 families, 160 genera, and over 2200 species. Both nonparasitic and parasitic flowering plants occur in the traditionally circumscribed family Olacaceae whereas all other families are composed entirely of parasites. The five evolutionary radiations of aerial parasitism produced mistletoes that constitute most of the generic and specific diversity seen in the order. This classification, although based primarily upon results from molecular phylogenetic investigations, brings together all currently available information that contributes to our understanding of relationships among these plants. Monophyletic groups (clades) obtained from molecular analyses were named using a Linnaean ranked system. Four new families are named that formerly resided in Santalaceae s.l.: Amphorogynaceae, Cervantesiaceae, Comandraceae, and Nanodeaceae. A new tribal and subtribal classification for Loranthaceae is presented where nine new subtribe names are proposed.
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Loranthaceae (73 genera and ca. 900 species) comprise mostly aerial hemiparasitic plants. Three monotypic genera considered relicts are root parasites. The family is diverse in tropical areas, but representatives are also found in temperate habitats. Previous classifications were based on floral and inflorescence morphology, karyological information, and biogeography. The family has been divided into three tribes: Nuytsiae, Elytrantheae (subtribes Elytranthinae and Gaiadendrinae), and Lorantheae (subtribes Loranthinae and Psittacanthinae). Nuytsiae and Elytrantheae are characterized by a base chromosome number of x = 12, whereas subtribes Loranthinae (x = 9) and Psittacanthinae (x = 8) numbers are derived via aneuploid reduction. To elucidate the phylogeny of the family, we analyzed sequences from five genes (nuclear small and large subunit rDNA and the chloroplast genes rbcL, matK, and trnL-F) representing most genera using parsimony, likelihood, and Bayesian inference. The three root parasites, Nuytsia, Atkinsonia, and Gaiadendron, are supported as successive sister taxa to the remaining genera, resulting in a monophyletic group of aerial parasites. Three major clades are resolved each corresponding to a subtribe. However, two South American genera (Tristerix and Notanthera) and the New Zealand genus Tupeia, which were previously classified in subtribe Elytranthinae, are weakly supported as part of a clade representing the South American subtribe Psittacanthinae.
A new system for the genera of Loranthaceae-Loranthoideae, with a nomenclator for the Old World species of this subfamily
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DANSER, B.H. 1933. A new system for the genera of Loranthaceae-Loranthoideae, with a nomenclator for the Old World species of this subfamily. Verhandelingen der Koninklijke Akademie van Wetenschappen te Amsterdam Afdeling Natuurkunde. 2: 1-128.
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