Botanical Journal of the Linnean Society, 2011, 167, 344–350. With 3 figures
Nocturne for an unknown pollinator: first description of
a night-flowering orchid (Bulbophyllum nocturnum)
ANDRÉ SCHUITEMAN1*, JAAP JAN VERMEULEN2, ED DE VOGEL3 and ART VOGEL4
1
Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AB, UK
Lauwerbes 8, 2318 AT Leiden, the Netherlands
3
Netherlands Centre for Biodiversity Naturalis (section NHN), Leiden University, PO Box 9514, 2300
RA Leiden, the Netherlands
4
Hortus Botanicus, Leiden University, PO Box 9516, 2300 RA Leiden, the Netherlands
2
Received 26 January 2011; revised 26 January 2011; accepted for publication 15 August 2011
Bulbophyllum nocturnum, a species of section Epicrianthes from New Britain, is described and illustrated. It is
the first known example of an orchid species in which the flowers open after dark and close in the morning. The
poorly understood pollination biology of section Epicrianthes, a clade with highly unusual flowers, is discussed.
Attention is drawn to the close resemblance between the petal appendages of some species and the fruiting bodies
of certain Myxogastria. © 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011,
167, 344–350.
ADDITIONAL KEYWORDS: Myxogastria – New Britain – Orchidacaeae – Papua New Guinea – pollination.
INTRODUCTION
A few plant species have flowers that open after dark
and close before or shortly after sunrise. Examples
include the queen of the night [Selenicereus grandiflorus (L.) Britt. & Rose; Cactaceae], the midnight
horror (Oroxylum indicum Vent.; Bignoniaceae) and
the night blooming jasmine (Cestrum nocturnum L.;
Solanaceae), but no night-flowering orchid species
have been reported, even though Orchidaceae is
the largest plant family, with more than 25 000
species (Hassler, 2001). Orchids display a wide range
of phenologies and pollination syndromes (van der
Pijl & Dodson, 1966; van der Cingel, 2001; Jersáková,
Johnson & Kindlmann, 2006). Many orchid species
are pollinated by nocturnal Lepidoptera. A wellknown example is Angraecum sesquipedale Thouars
from Madagascar, for which Darwin correctly predicted that the pollinating moth species would
have a 30-cm-long proboscis to match the spur of
the flower (Darwin, 1862; Micheneau, Johnson &
Fay, 2009). Moth-pollinated orchids may time their
*Corresponding author. E-mail: a.schuiteman@kew.org
344
fragrance emissions to attract nocturnal insects, but
all have flowers that remain open during the day. We
describe the first example of a truly nocturnal orchid,
Bulbophyllum nocturnum J.J.Verm., de Vogel, Schuit.
& A.Vogel, sp. nov., which was recently discovered
in New Britain, Papua New Guinea. It has flowers
opening at around 22:00 h and closing at around
10:00 h, lasting only a single night. This was observed
in cultivation in the Netherlands in winter, which
implies that the flowers closed a few hours after
sunrise. We also draw attention to the remarkable
and largely unexplained floral morphology of this
species and others in Bulbophyllum Thouars section
Epicrianthes (Blume) Hook.f.
PHENOLOGY AND POLLINATION BIOLOGY
The pantropical genus Bulbophyllum contains about
2000 known species, which makes it by far the largest
genus of Orchidaceae. The greatest diversity in terms
of number of species occurs in South-East Asia and
Australasia, in particular in New Guinea, where more
than 600 species are found (Schuiteman, Vermeulen
& de Vogel, 2010). Members of this genus are
© 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 167, 344–350
BULBOPHYLLUM NOCTURNUM
© 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 167, 344–350
345
Figure 1. Six species of Bulbophyllum section Epicrianthes: B. johannuli J.J.Verm. (top left; flower, photograph P. Jongejan); B. macneiceae Schuit. & de Vogel
(top centre; flower, photograph P. Jongejan); B. tarantula Schuit. & de Vogel (top right; flower, photograph E.d.V.); B. xanthomelanon J.J.Verm. & P.O’Byrne
(bottom left; centre of flower, photograph A.S.); B. macrorhopalon Schltr. (bottom centre; centre of flower, photograph A.S.); B. cimicinum J.J.Verm. (bottom right;
centre of flower, photograph A.S.).
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A. SCHUITEMAN ET AL.
Figure 2. Bulbophyllum nocturnum J.J.Verm., de Vogel, Schuit. & A.Vogel: A, habit; B, flower; C, dorsal sepal, petal,
lip and lateral sepal; D, lip; E, column and lip; F, pollinia; G, anther. All after Hortus Botanicus Leiden cult. 20080300
(drawing J.J.V.).
䉴
typically myophilous, but at the same time display
a great variety of pollination strategies. We have
observed blowflies visiting and detaching pollinia
from the foetid flowers of B. lasianthum Lindl. and
B. wakoi Howcroft in the Hortus Botanicus Leiden,
and other diptera, including fruit-flies and midges,
have been reported as pollinators of Bulbophyllum
(Jones & Gray, 1976; Bartareau, 1994; Borba &
Semir, 1998; Tan & Nishida, 2007). Most Bulbophyllum spp. probably have deceptive flowers (Jersáková
et al., 2006), offering no reward, but some offer nectar,
for example B. longiflorum Thouars (Jones & Gray,
1976). One of us (A.S.) observed a satyroid butterfly
visiting the inflorescence of B. macrocoleum Seidenf.
in Laos, probing each lip with its proboscis, but the
detachment of pollinia did not occur and the butterfly
was probably not a pollinator.
As many Bulbophyllum spp. flower only for a short
period, they are rarely seen in flower during field
work. As a result, they are under-represented in
herbarium collections. Hundreds of species are only
known from the type specimen. Ex situ cultivation of
plants until flowering, at which time specimens can
be preserved (as described by Schuiteman & de Vogel,
2003), has added much to our knowledge of the genus.
Recent botanical exploration in the island of New
Britain (Papua New Guinea) by one of us (E.d.V.)
yielded many orchid plants now cultivated at the
Hortus Botanicus Leiden. Among these was a Bulbophyllum sp. which soon produced flower buds, but
these all seemingly aborted the night before they
were expected to open. Only a close watch one night
revealed its nocturnal flowering habit. We established
for several subsequently observed flowers that they
all opened at around 22:00 h and closed at around
10:00 h.
The plant proved to represent an undescribed
species of Bulbophyllum section Epicrianthes, a clade
with 38 species, 18 of which are endemic to New
Guinea. The flowers in these orchids, although small,
are noteworthy for their bizarre morphology (Fig. 1).
They are short lived, usually not lasting more than
1 day. Collectively, the authors have observed 23
species of section Epicrianthes flowering in glasshouse conditions and/or in the field. All, except B. nocturnum described below, were seen with open flowers
in the middle of the day or during the afternoon.
The petals carry intricate appendages that probably
serve to attract pollinators; these appendages are
often suspended by extremely fine, thread-like stalks
(clearly visible in Fig. 1, bottom centre), so that they
are capable of moving about in the slightest air
current. In only a few species are the appendages
rigidly attached (e.g. B. cheiropetalum Ridl. and
B. macneiceae Schuit. & de Vogel). The petal appendages of several species rather closely resemble in
shape and size the fruiting bodies of slime moulds
(Myxogastria). Those of B. cimicinum J.J.Verm.
(Fig. 1, bottom right), for example, resemble the fruiting bodies of Arcyria spp.; those of B. xanthomelanon
J.J.Verm. & P.O’Byrne (Fig. 1, bottom left) resemble
Stemonitis spp. As yet, we do not know whether this
resemblance is more than coincidental. Other visual
stimuli may include light effects caused by the
glistening vesicles (enlarged cells) on the lip. A
fungus-like scent has been reported for B. epicrianthes Hook.f. (Carr, 1928), but has not been noticed by
us in the species that we observed.
Field studies are difficult because members of this
section usually occur sporadically in remote areas
and flower briefly and intermittently. It is uncommon
to find more than one or two specimens growing in
close proximity. However, B. hexarhopalon Schltr. is
reported to be common in New Caledonia (Société
Néo-Calédonienne d’Orchidophilie, 1995). We are
aware of only one published report of ‘tiny flies’ visiting the flowers of B. epicrianthes, in Peninsular
Malaysia (Carr, 1928). Photographs by T. M. Reeve
(reproduced in Schuiteman et al., 2010), taken in
Papua New Guinea, show a flower of B. macrorhopalon Schltr. being visited by two small, midge-like,
black flies, about 4 mm long, similar to those reported
by Carr. These two independent observations of small
flies as potential pollinators, and their behaviour as
described by Carr (1928), contradict the hypothesis
that the flowers are pollinated by pseudocopulation,
like many other orchids with insect-like flowers, or
that they mimic prey animals. The zoomorphic
appearance of these flowers is likely to be coincidental, and mycomyophily would appear to be the most
probable pollination syndrome in this group of
orchids.
The floral morphology of B. nocturnum is similar to
that of several other diurnal species, but the species
is unusual for having its flowers open during the dark
for most of their lifetime. This suggests that nocturnal insects, most likely small diptera, are among
its potential pollinators, but, in the absence of field
studies, this must remain speculation. It also remains
to be investigated whether the timing of the opening
and closing of the flowers relative to sunset and
sunrise would be different in the wild.
© 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 167, 344–350
BULBOPHYLLUM NOCTURNUM
A
B
C
G
D
E
F
© 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 167, 344–350
347
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A. SCHUITEMAN ET AL.
Figure 3. Flower of Bulbophyllum nocturnum J.J.Verm., de Vogel, Schuit. & A.Vogel, Hortus Botanicus Leiden cult.
20080300 (photograph J.J.V.).
© 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 167, 344–350
BULBOPHYLLUM NOCTURNUM
TAXONOMY
BULBOPHYLLUM NOCTURNUM J.J.VERM., DE
VOGEL, SCHUIT. & A.VOGEL, SP. NOV., FIGS. 2 & 3
Bulbophyllo corrugato et B. hexarhopalo appendicibus
generum duorum (crassioribus et tenuioribus) in
margine apicali petalorum distributis simile, sed a
B. corrugato appendicibus crassioribus pluribus (7,
non 4) multo angustioribus et ad apicem acutum
attenuatis (non obtusis), a B. hexarhopalo appendicibus tenuioribus quam appendicibus crassioribus
minus (non magis) quam dimidio brevioribus et foliis
abaxialiter corrugatis (non laevibus), a speciebus
ambabus labelli superficie adaxiali verrucosa, differt;
flores noctu aperti.
Type: Papua New Guinea, West New Britain Province, Asengseng logging area, Upper Agulo River,
Hortus Botanicus Leiden cult. 20080300 (holotype
LAE, isotypes K, L).
Description: Rhizome patent to pendulous, up to
15 cm long, 3–4 mm in diameter, sections between
pseudobulbs 2.4–3 cm long, cataphylls persistent.
Pseudobulbs 1.0–1.5 ¥ 0.4–0.5 cm, distant, ellipsoidcylindrical. Leaves subsessile, 5.3–6.2 ¥ 2.1–3.2 cm,
index (length/width) 1.8–2.5, elliptic to ovate, acute,
abaxial surface corrugated. Inflorescence c. 2 cm
long, one-flowered; peduncle porrect, c. 0.5 cm long;
peduncle scales two, the longest c. 4 mm long; floral
bract c. 6 mm long, tubular, acute. Flowers opening
widely, without noticeable smell, lasting about 12 h,
largely nocturnal, opening from 22:00 h to 10:00 h
in cultivation. Pedicel with ovary c. 10 mm long,
basal node on a c. 4-mm-long stump. Dorsal sepal c.
14 ¥ 4 mm, index c. 3.5, spreading, ovate, acute,
margins entire, base broadly attached, thick, surface
glabrous. Lateral sepals c. 15 ¥ 4 mm, index 3.7–3.8,
free, triangular, otherwise as the dorsal sepal. Petals
c. 1 ¥ 2 mm, index c. 0.5, porrect, forming a narrow
seam along the base of the column, entire (excluding
the appendages), surface glabrous; with two types of
stalked, papillose appendages along the apical
margin; the first type thick, widest near the base and
gradually tapering distally, 5.5–8.0 ¥ 0.2–0.3 mm,
acute, abruptly narrowed into a thread-like stalk c.
2 mm long, the second type much thinner, subulate,
3.0–3.5 mm long, gradually passing into a 1.5–2.0 mm
thread-like stalk; these appendages divided into three
groups: three and four of the first type at the upper
and lower edge of the petal respectively, three of the
second type in between. Lip c. 3.3 ¥ 1.3 mm, index
2.5–2.6, straight, three-lobed with patent, triangular,
acute lobes attached to the proximal 1/4–1/5 of the
length of the lip, midlobe obovate, acuminate, thick;
adaxial surface constricted to a narrow, deeply
349
furrowed, irregularly verrucose strip with irregular
edges; abaxial surface inflated, somewhat furrowed,
increasingly papillose with elongated papillae
towards the tip. Column c. 2.4 mm long; foot slightly
widened distally; stelidia c. 0.7 mm long, triangular,
obtuse, upper margin erose, lower with a patent,
deltoid, subacute tooth with a much smaller tooth on
its front margin; anther cap abaxially with a narrow
crest, surface glabrous, front margin drawn out into a
retuse beak; pollinia four, inner ones about half as
long as the outer.
Colours: Plant green, not flushed with purple. Sepals
yellowish green, somewhat tinged red proximally.
Petals with greyish appendages. Lip dark red.
Column yellow tinged red.
Ecology: Epiphyte in rainforest; altitude 240–300 m.
Notes: In the distribution of the two types of appendage (thin and thick) on the petals, B. nocturnum
resembles B. hexarhopalon and B. corrugatum
J.J.Verm. From the first it differs by the abaxially
corrugated leaves (smooth in B. hexarhopalon) and by
the thin petal appendages being more than half as
long as the thick ones (less than half as long as the
thick ones in B. hexarhopalon). From the second it
differs by the larger number of thick petal appendages (seven versus four), these in addition being much
thinner and gradually tapering into an acute tip
(obtuse in B. corrugatum). It differs from both by the
verrucose adaxial surface of the lip. Finally, it may be
worth noting that Schlechter originally spelt the
epithet of B. hexarhopalon as hexarhopalos. However,
he undoubtedly intended to use a classical Greek
word for club, ‘rhopalon’, which refers to the
club-shaped appendages of the petals, not the name
Rhopalos of a mythological figure. Therefore, hexarhopalon is the correct spelling. Schlechter later
described several related species with epithets ending
in -rhopalon, which supports this correction.
ACKNOWLEDGEMENTS
E.d.V. wishes to thank the Department of Environment and Conservation, Papua New Guinea, for permission to collect and export the specimen described
here, and Rimbunan Hijau PNG for logistic support
in their logging area. We thank Philip Oswald for
improving the Latin diagnosis.
REFERENCES
Bartareau T. 1994. Pollination of Bulbophyllum macphersonii Rupp by a midge fly (Forcipomyia sauteri). Orchadian
11: 255–258.
© 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 167, 344–350
350
A. SCHUITEMAN ET AL.
Borba EL, Semir J. 1998. Wind-assisted fly pollination in
three Bulbophyllum (Orchidaceae) species occurring in the
Brazilian Campos Rupestres. Lindleyana 13: 203–218.
Carr CE. 1928. Orchid pollination notes. Journal of the
Malayan Branch of the Royal Asiatic Society 6: 49–72.
van der Cingel NA. 2001. An atlas of orchid pollination:
America, Africa, Asia and Australia. Rotterdam: A.A.
Balkema.
Darwin C. 1862. On the various contrivances by which
British and foreign orchids are fertilised by insects, and on
the good effects of intercrossing. London: J. Murray.
Hassler M. 2001. Statistischer Überblick über die Familie
Orchidaceae und eine weltweite Checkliste der Orchideen.
In: Schlechter R, ed. Die orchideen, Vol. 1/C. Berlin: Parey
Buchverlag, 2826–2891.
Jersáková J, Johnson SD, Kindlmann P. 2006. Mechanisms and evolution of deceptive pollination in orchids.
Biological Reviews 81: 219–235.
Jones DL, Gray B. 1976. The pollination of Bulbophyllum
longiflorum Thouars. American Orchid Society Bulletin 45:
15–17.
Micheneau C, Johnson SD, Fay MF. 2009. Orchid pollination: from Darwin to the present day. Botanical Journal of
the Linnean Society 161: 1–19.
van der Pijl L, Dodson CH. 1966. Orchid flowers: their
pollination and evolution. Coral Gables, FL: University of
Miami Press.
Schuiteman A, Vermeulen JJ, de Vogel EF. 2010. Flora
Malesiana: orchids of New Guinea, vol. VI; genus Bulbophyllum. (CD-ROM). Amsterdam: ETI/Leiden: Nationaal
Herbarium Nederland.
Schuiteman A, de Vogel EF. 2003. Taxonomy for conservation. In: Dixon KW, Kell SP, Barrett RL, Cribb PJ, eds.
Orchid conservation. Kota Kinabalu: Natural History Publications (Borneo), 55–68.
Société
Néo-Calédonienne
d’Orchidophilie.
1995.
Orchidées indigènes de Nouvelle-Calédonie. Nouméa: Société
Néo-Calédonienne d’Orchidophilie.
Tan KH, Nishida R. 2007. Zingerone in the floral synomone
of Bulbophyllum baileyi (Orchidaceae) attracts Bactrocera
fruit flies during pollination. Biochemical Systematics and
Ecology 35: 334–341.
© 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 167, 344–350