Harpochilus neesianus and other novel cases of chiropterophily in

53 (1) • February 2004: 55–60
Vogel & al. • Novel cases of chiropterophily in Acanthaceae
P O L L I N AT I O N E C O LO G Y
Harpochilus neesianus and other novel cases of chiropterophily in neotropical Acanthaceae
Stefan Vogel1 , Isabel Cristina Machado2 & Ariadna Valentina Lopes2
1 Institut für Botanik der Universität Wien, Rennweg 14, A-1030 Vienna, Austria. [email protected]
(author for correspondence)
2 Departamento de Botânica, Universidade Federal de Pernambuco, 50.372-970 Recife, Pernambuco, Brazil.
imachado@ ufpe.br; [email protected]
Floral adaptation to pollination by bats is rare in Acanthaceae and only known from neotropical species. Two
novel cases are described in detail from field observations. Harpochilus neesianus, a shrub endemic in NE
Brazil, with long emergent thyrses, was seen being regularly visited by hovering glossophagine bats
(Glossophaga soricina). Its large, pale lemon-green corollas are strongly bilabiate, a shape uncomm on in the
syndrome. The lower lip segments are recurved and the upper lip is reduced to a narrow, arcuate, tubular organ
serving to support stamens and style. A sour, cabbage-like odour is released, and copious nectar is secreted by
a voluminous disk. Pollen is transferred by the bat’s upper, rear surface. Anthesis is confined to a single night.
Chiropterophily in Ruellia eurycodon is deduced from the floral syndrome. The flowers of this shrub, studied
in Goyás, Central Brazil, share the same features as Harpochilus except for the corolla shape, which conforms
to the “short bell type” frequent in neotropical bat flowers. Based on literature sources, bat pollination is also
predicted for Ruellia malaca and R. exostemma from Venezuela. The occurrence of this floral type in other
genera of the family is briefly surveyed.
KEYWORDS: Acanthaceae, bat pollination, chiropterophily, Glossophaga, Harpochilus, Ruellia
INTRODUCTION
In Acanthaceae, adaptation to pollination by chiropterans is only known from a small number of neotropical species. Most of them share the characteristic syndrome of floral features (cf. Van der Pijl, 1936; Vogel,
1958, 1968, 1969a, b; Faegri & Van der Pijl, 1979; Dobat
& Peikert-Holle, 1985) and were thus classified on this
basis as being adapted to bat pollination. They still
deserve a direct observation and documentation of regular bat visits, a task that seldom succeeds without adequate logistics, equipment and patience. As far as we
know, in the Acanthaceae this confirmation has apparently been accomplished only in Trichanthera gigantea
(Steiner, 1981; George, 1987). In the present paper, we
provide a new direct record for Harpochilus neesianus
and predict chiropterophily in Ruellia eurycodon. Two
further species of Ruellia are included based on indirect
evidence from the literature, and a brief overview of this
pollination mode in the family is presented.
MATERIAL AND METHODS
Study sites and species. — Harpochilus
neesianus was investigated in the valley of Catimbau (8º
67’ S, 37º 01’ W), a Brazilian National Park located in the
municipality of Buique, in the countryside of
Pernambuco State, northeastern Brazil, 285 km from the
coast. The vegetation of this valley is of an unusual
Caatinga type, with many plant species not found in
other Caatinga areas (including H. neesianus), some of
them normally found in open vegetation such as
“Campos rupestres” (Rodal & al., 1998). The altitude of
the area varies from 800 to 1000 m, and the mean annual precipitation is 1095.9 mm, with a rainy period
between January and June, raining mostly from April to
June; the mean temperature is 25ºC (Sudene, 1990).
Vouchers are deposited in the herbaria UFP, Nº. 15601,
and WU (Vo 1996-57).
Ruellia eurycodon was found and studied on a single
occasion by S.V. in the Sanctuario Vagafogo on the
foothills of the Serra dos Pireneus near Pirenopolis (780
m) , 15º51’ S, 48º57’ W, State of Goyás, Brazil, in August
1998; vouchers in WU (Vo 1998-29).
Floral and pollination ecology of Harpochilus neesianus. — On a first joint trip in October
1996, when we predicted chiropterophily, our attempt to
document bat visits was unsuccessful. Three years later,
C.M. and A.L. made field observations on the floral and
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53 (1) • February 2004: 55–60
pollination ecology and were able to provide photographs of the bat visits. Diurnal and nocturnal observations totalling ca. 100 h were carried out on flower visitors/pollinators. Flowers were observed with respect to
the timing and sequence of anthesis, odour emission and
flower orientation (with a compass). Nectar volume and
sugar concentration were checked on the day following
anthesis at 13:30 in previously bagged flowers, by using
microsyringes (Microliter ® 5, 10 and 25 µl) and a handheld temperature compensated refractometer (Atago®
0–50%), respectively. S.V. examined structural details
including SEM of the pollen at the Institute of Botany of
the University of Vienna.
Phenology and natural fruit set of
Harpochilus neesianus. — In order to determine the
flowering period, 20 patches of Harpochilus neesianus
individuals were observed monthly for bud and flower
production between1999 and 2000. Natural fructification
was also monitored by marking seven inflorescences
(with 22 to 42 flowers; x = 27, total of flowers = 189) and
observing fruit set.
reduced narrow “quiver” with connivent, finely undulate
margins. The lip envelopes and supports the style and the
two stamens for most of their lengths (Fig. 1A, B, 2A).
The flowers are possibly slightly protandrous. Both stamens and style surpass the lip, setting forth its curvature;
the 12 cm long style, with a punctiform stigma, finally
overtops the versatile, 6 mm large anthers for 5–6 mm.
However, some flowers of the same inflorescence and
stage of anthesis had styles equalling the stamens in
length until they abscised. An extensive globular disk
surrounds the ovary, exceeding the latter by far in volume (Fig. 2B). Mostly 1 (–3) flower(s) per inflorescence
are in anthesis at a time, distributed along the thyrse.
Irrespective of their insertion, they tend to face northeast
(Fig. 1A, B).
Anthesis. — The flowers are nocturnal and last
only a single night. The strongly incurved bud starts to
unfold at (13:00) 15:00–15:30; at that time, anthers are
still closed. Around 18:00, anthers split and a rather
unpleasant, sour, cabbage-like odour starts to be produced; at the same time, the basal tube becomes filled
with nectar. Nectar volume and sugar concentration averaged 60.33 µl and 27.25% (varying between 46–72 µl,
and 26–29%, N = 6), respectively. The sugar concentration, being higher than typical in the syndrome, may
have been raised by evaporation, since they were taken at
13:30 from previously bagged flowers. Corolla and stamens are shed during the same day, while the withered
style persists for several days.
Fruit production. — The natural fruit set was
12.17%. The fruits are four-seeded capsules. This low
fecundity suggests the occurrence of allogamy and selfincompatibility.
Pollination by bats. — Harpochilus was observed being visited and pollinated by glossophagine bats
(Glossophaga soricina) on several occasions during four
stays at the same locality in October and November
1999. Visits were observed in full moon and moon-less
nights, but in higher frequencies in moon-less nights.
They started at ca. 19:00 and the intervals between each
visit to a plant (when bats visited 1–2 flowers) varied
from ca. 24 to 40 min, at moon-less nights and full-moon
nights, respectively. All our observations ended at ca.
02:00.
The bats extracted nectar during less than one second
while on the wing. After one first visit to a previously
untouched flower, only 6 µl of nectar was left (from a
mean total of 60.33 µl). During the bat’s hovering
approach, the fertile organs hit nototribically the rear of
its back, as is shown in the photograph (Fig. 1C), or may
even touch the membrane (uropatagium) extended
between the hind legs. Thus, eventual cross pollen is
deposited on the stigma first, and the flower’s own pollen
taken up immediately thereafter. The process was also
OBSERVATIONS ON HARPOCHILUS
NEESIANUS MART.
Habit, inflorescence and flowering phenology. — A full description and illustration of the plant was
given by Nees (1847). It is a robust shrub up to 3 m high,
with soft, ovate leaves. Endemic in the States of
Pernambuco and Bahia, it grows scattered in large, but
locally restricted stands in the Caatinga formation (Sales
et al., 1998). Blooming occurs throughout the year, but
only sparsely from May to July. Plants flower intermittently and at individually variable periods. Its leafy flowering shoots, produced by plants at least 50 cm high, terminate in a 17–38 cm long spiciform thyrse. Axillary
thyrses may also be formed. Each of the leafy, petiolate
bracts (19–22 mm long) subtends two each three-flowered, congested cymes in a serial position. Inflorescences
are often slightly overarching and emerge well above the
vegetative periphery, on average 1.70 (0.5–3) m above
ground.
The flower. — The calyx, on a short pedicel, has
almost free, linear, subequal segments that stand off the
corolla tube, but are incurved. The large, pale, greenishyellow, inconspicuous corolla stands out by its strongly
bilabiate shape and narrow segments, uncommon in batpollinated plants. The tube is cylindrical, c. 14 ´ 3 mm,
with the base somewhat inflated and forming a nectar
chamber. The three abaxial segments of the limb are separate, revolute and irregularly curled. The arcuate, linear
upper lip is 6–7 cm long and only 2 mm in diameter. It is
composed of the two connate adaxial lobes, that form a
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53 (1) • February 2004: 55–60
Vogel & al. • Novel cases of chiropterophily in Acanthaceae
Fig. 1. A–C, Harpochilus neesianus. A, flower; B, flower visited by Glossophaga soricina; C, pollen grain, apertural and
polar views; D–F, Ruellia eurycodon. D, E, flower in side and frontal view; F, synflorescence. Bar: 20 µm.
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53 (1) • February 2004: 55–60
simulated by posing a captured bat in front of the flower,
with the snout advanced to the tube’s entrance.
Size relations, type of colour and scent, and dimensions of the nectariferous gland clearly indicate the presence of the chiropterophilous syndrome.
Throughout the observation period for visitors, only
one sphingid moth visited a single flower; thus the contribution of sphingids to pollen transfer seems not to be
relevant in this species.
Carpenter bees, Xylocopa grisescens, exploited the
nectar between 16:30 and 18:00 (at nightfall) by burglaring. To this end, they alighted in an oblique position and
pierced ripe buds or open flowers basally from outside
without touching the reproductive organs.
Porsch (1929), relying on the plate of Nees (1847),
had interpreted our plant as ornithophilous. We observed
hummingbirds only foraging illegitimately in the early
mornings (up to ca. 08:00) and at dusk by introducing
their beaks laterally into the corolla throat, and never
contacting stigma and anthers. Species observed were
Chlorostilbon aureoventris, Amazilia versicolor (pers.
observ.) and (?) Chrysolampis mosquitus (Santos, pers.
comm.).
morphological concept of the whole system is complicated and needs to be analyzed. Each branch produces up
to 10 buds/flowers from scaly, caducous bracts; 1–3
flowers are open at a time.
The flowers are 3.5 cm long; the calyx, immediately
preceded by two scaly prophylls, is deeply split into five
subequal segments. The calyx and the tubular, proximal
part of the cream corolla are 3 mm wide and orthotropic,
while the limb with its 18 mm long distal free lobes
curves forward and widens to an indistinctly bilabiate
bell that is gaping (25 mm wide) at the mouth (Fig. 1D,
E). The curvature develops during only one day before
anthesis. When open, the flowers face the periphery of
the bunch. The four stamens (6 mm) and the style lean
against the upper wall of the corolla with the large
anthers barely extending beyond the limb. Anthers are
arranged side by side, forming a nototribic complex. The
style extends 4 mm beyond the upper lip; the stigma is
split into two minute, inequal lobes, the larger one tilting
downward. A very large nectariferous disk forms a sort
of pedestal below the ovary (Fig. 2C).
When the plants were encountered at 17:00, no
flower was open. The fast unfolding of mature flowers
occurred between 17:30 and 18:00. As circumstances did
not allow night observations at the site, flowering shoots
were cut and carried indoors in a vial, where they kept
fresh. A strong gourd- or cucumber-like odour was produced at night, and nectar rose up in the tube. The corollas dropped the following day around 10:00, while buds
begun to enlarge to open the next night.
Habitual adaptation to bats is indicated by: anthesis
confined to a single night, a typical odour and colour hue,
the short, campanulate limb, a large disk and copious
nectar, big anthers, and a pronounced exposition of the
flowering bunch. The flower conforms to the “short bell
type”, dominant among neotropical bat flowers (Vogel,
1969b). Nectar data and species of visiting bats remain to
be established.
Ruellia eurycodon represents a novel case of this floral style in the Afro-American genus which is remarkable
for its broad spectrum of adaptive radiation into bee,
moth, butterfly, bird and bat flowers (Ezcurra, 1993). The
occurrence of the bat syndrome is already known from
Mexican species. Chavez (1974) mentioned R. bourgaei
as a candidate, without citing the source. According to
Ramamoorthy (1988, 1991), an apparently natural group
of taxa comprising R. bourgaei, R. conzattii, R. jaliscana,
R. palmeri, R. petiolaris, R. pulcherrima and R. sarukhaniana have the bat syndrome in common. The author
proposes to separate this assembly as a new section
Chiropterophila. Previously, Lindau (1897b) aligned
those known to him in section Dipteracanthus.
All of these species are perennial herbs or shrubs 1–3
m tall (except arborescent R. jaliscana that may grow 10
ADDITIONAL REMARKS
Harpochilus, a generally little-known genus with
three similar species in NE Brazil, was initially placed in
the tribe Odontonemeae (Lindau, 1897a, b). Molecular
sequence data now induced McDade & al. (2000) to
assign the taxon to their “New World Justicioids”, taking
a basal position in this monophyletic clade, also including American Justicia and the genera Megascepasma and
Poikilacanthus. The ornamentation of the tricolpate,
reticulate pollen of Harpochilus (Fig. 3) resembles that
of Justicia species, but also of Himantochilus, an
ornithophilous African justicioid genus (S.V., pers.
observ.), which possesses a similarly curled lower corolla lip. The bizarre blossom of Harpochilus, whose shape
is uncommon for bat-pollinated plants, may have
evolved from ornithophilous ancestors bearing strongly
bilabiate corollas with a mechanically nonfunctional
lower lip, such as found in species of Justicia and
Jacobinia.
Ruellia eurycodon Lindau and other cases
of chiropterophily in Ruellia. — A poorly
branched shrub up to 2.5 m high, Ruellia eurycodon
inhabits forest edges and clearings of the Cerradão formation. The large terminal paniculate synflorescence is
composed of 3–5 upright, elongate floriferous branches
with 12–15 cm long peduncles in the axils of the 2–3
uppermost foliage leaf pairs (Fig. 1F). Because accessory serial enrichment flowering branches also occur, the
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Vogel & al. • Novel cases of chiropterophily in Acanthaceae
Fig. 2. A–B, Harpochilus neesianus. A, cross-section of upper lip; B, basal portion of the flower in longisection, showing the large disk; C, Ruellia eurycodon, as in B. st = style, s = stamen, r = rugula, d = disk, c = calyx, co = corolla.
m tall), whose projecting inflorescences bear large, pale
lemon or greenish-white, obliquely bell-shaped (in R.
bourgaei ventrally deeply saccate) corollas. The disk is
huge and fleshy. The nototribic pollination organs are
included in the throat, except for R. bourgaei and R.
palmeri, which have them long exserted. Most species of
the section Chiropterophila exhibit vicariant distributions and probably evolved in Mexico from a putative
ancestor by geographical fragmentation (Ramamoorthy,
1991).
No South and Central American Ruellias were
known to display the bat syndrome. However, a new
member occurring in this realm (native to Goiás and
Mato Grosso) has come to our attention since Ezcurra &
Zappi (1996) merged the monotypic Eurychanes verbasciformis into Ruellia section Dipteracanthus. The status
of its flowers had long been evident to us from the table
and description by Nees (1847). After rediscovery of this
rare cerrado plant by Ratter in 1994 (cit. by Ezcurra &
Zappi, 1996), this assignment was substantiated by field
observations. Following Ratter, the corollas are “…large,
pale lemon-green and relatively wide…, anthesis occurs
at night”. They display a “…strong fermented scent
(resembling Cobaea scandens)”. The illustration of Nees
(1847) shows a huge, terminal, bracteose raceme with
more than one flower in anthesis. The long-exserted stamens and the style are overarching and nototribic.
Here we add two more species of Ruellia, from
Venezuela, to which adaptation to bats can be assigned
with confidence. The first author concluded this from
colour photographs shown, among other plant portraits,
in a poster by Llamozas (2002) in connection with a
floristic survey of the family in that country. Both species
share a curved corolla tube and extremely long, exserted,
nototribic pollination organs. The flower of R. malaca is
pale lemon, bell-shaped with short free segments.
According to Leonard’s diagnosis (1961), the plant is a
subshrub up to 2 m high and has long-pedunculate, condensed panicles. Leonard regards the taxon, “… although
not closely related”, as recalling R. bourgaei, one of the
Mexican chiropterophiles. After Lindau (1897a), R.
exostemma is also arbustive, with axillary, solitary flowers. These are greenish-white; their oblique, well-developed limb gapes 25 mm at the mouth.
Potentially closer relationships between these
species and R. eurycodon, as well as between both South
American groups and section Chiropterophila have yet
to be clarified. We agree with Ezcurra & Zappi (1996) by
assuming that chiropterophily has originated independently in different lineages of the genus.
Occurrence of chiropterophily in the
Acanthaceae. — As mentioned above, chiropterophily in this family is restricted to the neotropical realm (cf.
Dobat & Peikert-Holle, 1985). Within the subfamily
Acanthoideae it occurs—besides in Ruellieae and Justicieae—in the tribes Trichanthereae and Louteridieae, and
possibly in the subfam. Mendoncieae (Mendoncia).
Trichanthera gigantea, from Central and northern South
America, has been described as presumably bat-pollinated by Vogel (1969a); this was confirmed by Steiner
(1981) from observations in Panama. George (1987)
presents a photograph, taken by M. D. Tuttle, of a glossophagine bat pollinating the flower. The monotypic
Trichanthera presents inflorescences emerging from the
crown of the huge tree, with dark-red, tubular corollas
and exserted, nototribic style and anthers. Following
McDade (1983), anthesis lasts less than one day, starting
at early to mid-afternoon, with the corollas falling from
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Vogel & al. • Novel cases of chiropterophily in Acanthaceae
the plants overnight. Vogel (1969a) also predicted
Louteridium donnell-smithii to be chiropterophilous
based on the syndrome, a condition which possibly holds
true for the whole genus, which occurs in Mexico and
Guatemala with ca. 11 spp.; Louteridium has longpedunculate, much elongated, thyrses bearing large palegreenish, broadly saccate corollas with protruding,
nototribic fertile organs. Floral adaptation to bats in two
Panamanian species of Mendoncia was surmised by
Croat (1978), but without further comments.
The relative rareness of this pollination mode (and of
moth pollination) in Acanthaceae compared to
Bignoniaceae and Gesneriaceae, for example, may
reflect the poor capability of this family to produce floral
scents. On the other hand, such a handicap has furthered
the evolution of many bird-pollinated species. This
makes it all the more remarkable that a few members
have managed to achieve, and so perfectly, the floral
transformation adequate for bat-pollination.
ACKNOWLEDGEMENTS
We are indebted to Dr. Raymond Harley (Kew) and Dr.
Cecilia Ezcurra (Bariloche) for their help in identification of
Acanthaceae and their general expertise. We thank Dr. Heidemarie
Halbritter (Vienna) who skillfully took the SEM-pictures. Mag.
Susanne Pamperl and Susanne Gockner-Mayer (Vienna) helped
solve computer problems. Mary Janice Santos lent us her pleasant
company and helped during field work in the valley of Catimbau.
C.M and A.L. want to acknowledge financial support by CAPES
and the University of Pernambuco (Recife). S.V. received support
from the Akademie der Wissenschaften und Literatur (Germany).
Two Viennese colleagues, Prof. Anton Weber and Dr. Michael
Stachowitsch, critically read the manuscript and improved the
English.
LITERATURE CITED
Chavez, P. R. 1974. Observations en el polen de plantas com
probable polinization quiropterofila. Ann. Escuela
Nacional de Ciencias Biologicas 21: 115–143.
Croat, T. B. 1978. Flora of Barro Colorado Island. Stanford
Univ. Press, Stanford.
Dobat, K. & Peikert-Holle, T. 1985. Blüten und Fledermäuse.
Waldemar Kramer, Frankfurt.
Ezcurra, C. 1993. Systematics of Ruellia (Acanthaceae) in
southern South America. Ann. Bot. Missouri Bot. Gard.
80: 787–845.
Ezcurra, C. & Zappi, D. 1996. Ruellia verbasciformis, a new
combination in the genus Ruellia (Acanthaceae). Kew
Bull. 51: 819–820.
Faegri, K. & Van der Pijl, L. 1979. The Principles of
Pollination Ecology, ed. 3. Pergamon Press, Oxford.
George, U. 1987. Inseln in der Zeit, ed. 2. Gruner & Jahr,
60
53 (1) • February 2004: 55–60
Hamburg.
Leonard, E. C. 1961. (Ruellia malaca) in: Maguire, B. &
Wurdack, J. J. (eds.), The botany of the Guayana highlands IV-2. Mem. New York Bot. Gard. 10 (4): 1–87.
Lindau, G. 1897a. Acanthaceae Americanae et Asiaticae novae
vel minus cognitae. Bull. Herb. Boissier 5: 643–681.
Lindau, G. 1897b. Acanthaceae. Pp. 274–354 in: Engler, A. &
Prantl, K. (eds.), Die natürlichen Pflanzenfamilien, vol. IV
3b. Engelmann, Leipzig.
Llamozas, S. S. 2002. Familia Acanthaceae en Venezuela:
Diversidad, Distribución y Conservación. Resúmenes
VIII. Congresso Latinoamericano de Botánica. Univ. Nac.
Colombia, Cartagena de las Indias, Colombia.
McDade, L. A. 1983. Pollination intensity and seed set in
Trichanthera gigantea (Acanthaceae). Biotropica 15:
122–124.
McDade, L. A., Daniel, T. E., Masta, S. E. & Riley, K. M.
2000. Phylogenetic relationships within the tribe
Justicieae (Acanthaceae). Evidence from molecular
sequences, morphology, and cytology. Ann. Missouri Bot.
Gard. 87: 435–458.
Nees, T. F. 1847. Acanthaceae. Pp. 1–164 in: Martius, C. v.
(ed.), Flora Brasiliensis IX. Beck, Vienna and Fleischer,
Leipzig.
Van der Pijl, L. 1936. Fledermäuse und Blumen. Flora 131:
1–40.
Porsch, O. 1929. Vogelblumenstudien II. Jb. Wiss. Bot. 70:
181–277.
Ramamoorthy, T. P. 1988. A new species of Ruellia
(Acanthaceae) from western Mexico. Ann. Missouri Bot.
Gard. 75: 1664–1665.
Ramamoorthy, T. P. 1991. Ruellia sect. Chiropterophila
(Acanthaceae), a novelty from Mexico. Bot. J. Linn. Soc.
107: 79–88.
Rodal, M. J. N., Andrade, K. V. A., Sales, M. F. & Gomes,
A. P. S. 1998. Fitossociologia do componente lenhoso de
um refúgio vegetacional no Município de Buíque,
Pernambuco. Rev. Bras. Biol. 58: 517–526.
Sales, M. F. de, Mayo, S. & Nogueira, M. J. 1998. Plantas
Vasculares das Florestas Serranas de Pernambuco. Univ.
Federal Rural de Pernambuco, Imprensa Universitaria,
Recife.
Steiner, K. E. 1981. Nectarivory and potential pollination by a
neotropical marsupial. Ann. Missouri Bot. Gard. 68:
505–513.
SUDENE (Superintendência do desenvolvimento do Nordeste)
1990. Dados pluviométricos do Nordeste - Estado de
Pernambuco. Sêrie pluviométrica 6. Recife.
Vogel, S. 1958. Fledermausblumen in Südamerika. - Ein
Beitrag zur Kenntnis des chiropterophilen Stiltypus.
Österr. Bot. Z. 104: 491–530.
Vogel, S. 1968. Chiropterophilie in der neotropischen Flora I.
Flora, B: 157: 562–602.
Vogel, S. 1969a. Chiropterophilie in der neotropischen Flora II.
Flora, B: 158: 185– 222.
Vogel, S. 1969b. Chiropterophilie in der neotropischen Flora
III. Flora, B: 158: 289–323.