AOBPreview originally published online on March 22, 2004
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Annals of Botany 93: 609-613, 2004
© 2004 Annals of Botany Company
The North-east-Brazilian Liana, Adenocalymna dichilum (Bignoniaceae) Pollinated by Bats
1 Departamento de Botânica, Universidade Federal de Pernambuco, Cidade Universitária, 50372-970 Recife-PE, Brasil and 2 Institut für Botanik der Universität Wien, Rennweg 14, A-1030 Vienna, Austria
* For correspondence. Fax 00 55 81 21268348, e-mail imachado{at}ufpe.br
Received: 10 October 2003; Returned for revision: 13 November 2003; Accepted: 22 December 2003 Published electronically: 22 March 2004
ABSTRACT
• Background and Aims Of the set of syndromes displayed by specialized (euphilic) flowers, adaptation to pollination by bats (chiropterophily) is the least known. Accumulated new evidence reveals that this pollination mode plays a considerable role in tropical communities, especially in the neotropics. One family in which bat-pollinated species are known in several genera is the Bignoniaceae. Here is reported, for the first time, bat pollination and floral ecology in Adenocalymna dichilum (tribe Bignonieae).
• Methods Floral features of this species growing in Bahia (north-east Brazil) indicated possible chiropterophily, which was subsequently confirmed by direct observation and from photographs of bat visits. Timing of anthesis and nectar parameters were monitored in the field, and floral morphology was investigated with fixed flowers.
• Key Results One to two flowers open per night on the upright, simple racemes of A. dichilum during several weeks in a ‘steady state’ mode. The bilabiate, cream-coloured corollas are functional for only a single night and wilt during the following day. A stout corolla, with a musky odour, and a large nectary disc with large quantities of watery nectar also conform to the syndrome. Glossophaga soricina (Glossophaginae) visited and pollinated the flowers in a trap-lining manner. Whilst hovering, the bats put their heads into the corolla mouth for less than 1 s to feed, thereby effecting the transfer of pollen which is deposited on their backs.
• Conclusions Adenocalymna, a New World genus comprising approx. 50 species, exhibits floral adaptive radiation including species pollinated by bees, birds and possibly moths. The discovery of chiropterophily in A. dichilum adds another facet to the array of floral syndromes represented in the genus.
Key words: Adenocalymna, Bignoniaceae, chiropterophily, Glossophaga, Campo rupestre, north-east Brazil.
INTRODUCTION
The euphilic flowers of plants in the family Bignoniaceae display a spectrum of adaptive radiations, involving different pollinator groups. Besides melittophily (adaptation to pollination by medium- to large-sized bees), which predominates, flowers pollinated by hawkmoths (Vogel, 1954; van Steenis, 1977; Gentry, 1990a), birds (Porsch, 1929; Weber and Vogel, 1984), bats (van der Pijl, 1936/37, 1956; Gould, 1978) and lemurs (Sussman and Tattersall, 1976; Zihra, 1998) also occur in the family.
In the neotropics, where Bignoniaceae represent one of the largest families of woody plants, Gentry (1974a, b, 1976, 1979, 1980, 1990a, b), Amaral (1992) and Stevens (1994) have documented considerable diversity in the reproductive biology of this plant group, and have accumulated the most comprehensive information on floral ecology in these regions.
Bat pollination of bignons (reviewed by Dobat and Peickert-Holle, 1985) has been known of for a long time and has a wide distribution, occurring in diverse genera and species in the Old and New World tropics. Since these taxa are not closely related, the syndrome must have evolved independently in the two hemispheres. All known paleotropical representatives, pollinated by Megachirop tera, are arborescent, corresponding to the fact that, generally, herbaceous chiropterophiles appear to be absent in the Old World (Baker, 1973; Vogel, 1998), except for the tree-like Musa.
Most paleotropical, bat-pollinated Bignoniaceae have inflorescences or single flowers projecting above the canopy (pin-cushion type; species of Markhamia, Oroxylum, Pajanelia and Haplophragma), rarely inflorescences on long, pendent peduncles (flagelliflory, Kigelia) or cauliflory (Madagascan Coleeae). Among neotropical types, cauliflory (Crescentia, Amphitecna and Parmentiera) and ramiflorous emergent single flowers (Enallagma inclusive Dendrosicus and Parmentiera) prevail.
Most of the floral features generally considered as typical for bat-pollination (van der Pijl, 1936/37; Vogel, 1969; Dobat and Peikert-Holle, 1985) are present in neotropical bignons, namely relatively stout petals, nocturnal anthesis often restricted to one night, white to yellowish-green perianths, copious dilute nectar, musty or cabbage-like odours, and broadly campanulate or gullet-like flower shapes.
With the exception of the widely cultivated calabas tree (Crescentia cujete), where visiting bats have been observed directly (Porsch, 1931; Carvalho, 1960; Janzen, 1983; Lemke, 1984), New World representatives of the Bignoniaceae are classed as chiropterophilous, as far as we know based only on circumstantial evidence.
In this paper we report for the first time bat pollination in Adenocalymna dichilum of the tribe Bignonieae, a north-east Brazilian species.
MATERIALS AND METHODS
Fieldwork was carried out in March 2002 on a natural population of Adenocalymna dichilum A.H. Gentry on the slopes of Pai Inácio (700 m a.s.l.), a small table mountain in the Chapada Diamantina (state of Bahia, 11°30'S, 42°10'W). The mountains show a relief with extensive outcropping of Precambrian, acidic rocks. The vegetation is a complex mosaic of types characteristic of the ‘campo rupestre’ zone (Giulietti and Pirani, 1988; Harley, 1995). The great diversity of plants in the formation is due to local variation in soil conditions, topography, slope inclination and resultant microclimates (Harley, 1995).
Adenocalymna dichilum is one of three bignoniaceous species described from Pai Inácio (Guedes and Orge, 1998). There were at least three other presumably bat-pollinated plants at the site, namely Wunderlichia crulsiana (Compositae), Calliandra spp. (Mimosaceae) and Passi flora recurva (Passifloraceae).
Flower size, scent, colour, anthesis period and nectar availability were recorded in the field. The floral morphology was analysed using a stereomicroscope with camera lucida from flowers fixed in 70 % alcohol. The volume of nectar per flower at a given time was measured from six flowers on three different plants at intervals of 1–4 h (1800 h–2200 h) using micro-syringes. The sugar concentration of the nectar was measured using a hand-held, temperature compensated refractometer (Atago). Vouchers of Adenocalymna denocalymna dichilum are deposited in the herbaria of the Universidade Federal de Pernambuco (UFP) Recife, no. 31.762 and of the University of Vienna (WU), no. Vo 2002/34.
Glossophaga soricina was identified from the examination of several photographs taken during the visits. In the field, their flower-visiting behaviour was observed on two nights. Records were made of the frequency, time and duration of the visits. Areas of the bats bodies which came into contact with pollen and stigmas were documented.
RESULTS
The study plants were basally woody, non-climbing individuals of A. dichilum growing in open, grassy areas beside a road. The plants, including their inflorescences, grew to a height of only 1·5 m. Since Gentry (1993) described this species as ‘frutex scandens’, and simple tendrils were present between the two leaflets of our plants, it was presumed they were either juveniles or, more likely, prevented from developing their normal growth form of a woody vine by the absence of supporting trees. We estimate the flowering period of the plants at the study area to be from mid-January to the end of March. The numerous abscission scars on the racemes indicated that the plants had been in bloom for several weeks. However, flowering specimens have also been collected in April (Barro Alto, Morro do Chapéu e Paramirim—BA; Herbarium Feira de Santana), May (Piaui; Gentry, 1993), July (Morro do Chapéu; L. Lohmann, pers. comm.) and December (Jussiape—BA; Herbarium Feira de Santana).
The flowers
Each individual plant had a single inflorescence, which extended above the foliage, in the form of a simple, terminal, vertically orientated, many-flowered raceme on a long, bracteose peduncle. The inflorescence structure, with only one or two flowers open at a given time (in the latter case on the same node), indicates continuous flowering over at least several weeks, thus displaying a ‘steady state’ pattern (Gentry, 1974). The flowers, on a stout pedicel (20 mm long), have a 5-dentate tubular calyx. The calyx, the subtending bracts and the two prophylls bear groups of extrafloral nectaries (single peltate trichomes). These were foraged by large, blackish ants day and night. The cream-coloured corolla, measuring 70 mm in length, has a 28-mm long and 4-mm-wide basal tube that widens rather abruptly into a campanulate limb. The limb is distally divided into two straight upper and three reflexed lower segments (Fig. 1A and B). Both the corolla and calyx are fairly rigid and tomentose externally. The four fertile stamens, and one small, median staminode, are inserted between the bell-shaped and the tubular sections, where a girdle of long hairs has developed as nectar cover. Stamens are didynamous, but the yellow anthers occur close together, with their divergent thecae spreading to the outside (Figs 1A and 2A). They lean against, and are sheltered by, the upper lip of the corolla. The style, with a narrow bifid stigma, extends above the anthers by 5 mm. The hypogynous, 5-lobed nectariferous disc considerably exceeds the ovary in volume (Fig. 2B).
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Anthesis
Anthesis began at 1745 h, a short time before sunset. Flower opening started by basal splitting of the limb segments. At this time pollen was already available, and a weak, fruity odour was detectable. Nectar production commenced at 1800 h, with an initial mean sugar concentration of 12 %. Subsequently (at approx. 2000 h), the concentration increased up to 22·0 % (mean = 19·3 %). Nectar standing crop averaged 23·8 µl (range 15–30 µl; n = 6).
Bat visits
Observations took place in clear weather and ended at midnight, prior to moonrise. Visits to the flowers by a Phyllostomatidae (Glossophaga soricina), possibly a single individual, occurred at regular intervals of approx. 1 h apart, starting around 1900 h in full darkness. This behaviour indicates a trapline pattern, which accords with a ‘steady state’ flowering strategy (sensu Gentry, 1974a). The bat always approached from one direction, visited one flower only at a time and always departed in a different direction. Visits were whilst hovering and lasted less than 1 s. Even flowers close to the ground (50 cm) were visited. Photographs (Fig. 1C) revealed a stereotypic feeding position with the bat’s snout inserted deeply into the flower’s throat. This resulted in the bat being dusted nototribically on its neck or shoulders. As the stigma must be touched first, cross-pollination is thus favoured. Flowers started to wilt the next morning and corollas were shed during the course of the day. Fruiting was not observed.
DISCUSSION AND CONCLUDING REMARKS
Although Adenocalymna is the second largest genus in the tribe Bignonieae, comprising approx. 50 species in tropical America, data on its floral biology are scarce. According to Gentry (1993) it is predominantly melittophilous. Bee pollination has been recorded in A. bracteatum by Brantjes (1979) and by Amaral (1992), and in A. marginatum by Amaral (1992). According to Amaral (1992), nectary disc size in these two bee-pollinated species is only moderate (hardly exceeding the size of the ovary) and the mean nectar concentration was typically higher than that recorded by us in A. dichilum (30·6 and 29·8 %, respectively). Porsch (1929) regarded A. comosum as bird-adapted, and A. grandifolium, a liana with orange-red, entirely tubular corolla, may also be added (personal observation by S.V. near Domingos Martins, Espirito Santo). For A. gracielzae, Gentry (1993) reports ‘. . . incipient (adaptation) to hawkmoth pollination’.
Chiropterophily has not been reported previously in the genus. The floral features of A. dichilum conform to this syndrome very well, although the floral scent is weak to humans and the tubular part of the corolla is longer than that usually found in bat-pollinated species. However, bats manage to reach the bottom of the nectar chamber with their tongues, which are extensible to 45 mm (von Helversen and von Helversen, 1975), and can thus extract the nectar exhaustively. Adenocalymna dichilum is the first neotropical member of the tribe Bignonieae and the first liana within New World Bignoniaceae so far to be confirmed as being chiropterophilous. Gentry (1993) considered the flower shape of A. dichilum to be uncommon within the genus and noted ‘. . . curiously, several quite unrelated species of Bignoniaceae share this unusual floral morphology in northeastern Brazil . . .’ These are ‘. . . Arrabidaea tynanthoides A. Gentry and A. crassa Sprague and, to a lesser extent, Mansoa ventricosa Gentry’. It would be interesting to investigate whether these shared floral features are also related to bat-pollination in these species.
ACKNOWLEDGEMENTS
We are indebted to Dr Lucia Lohmann (St Louis) for identifying A. dichilum. To Drs Eduardo Borba and Ligia Funch [Universidade Estadual de Feira de Santana (UEFS)] who were most helpful with the logistics; to Viviane and Eric Smith (UEFS) without whose company and hospitality at Lençóis-BA our project would not have been possible; and to Dr Luciano Paganucci (UEFS) for the phenological data of A. dichilum deposited in the Herbarium of the University of Feira de Santana/BA. We are also grateful to Mary Janice Santos [Universidade Federal de Pernambuco (UFPE)] for assistance in the field; to Dr Peter Gibbs (University of St Andrews), who kindly helped us to improve our English. Finally, to Drs Rogerio Gribel (INPA) and Marco Tschapka (University of Erlangen) who made important suggestions regarding the draft version of this paper. CNPq and UFPE (Recife) granted financial support to I.C.M., as did the Akademie der Wissenschaften und der Literatur (Mainz) to S.V.
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