AOBPreview originally published online on March 22, 2006
Annals of Botany 2006 97(6):965-974; doi:10.1093/aob/mcl056
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Bird Pollination in an Angraecoid Orchid on Reunion Island (Mascarene Archipelago, Indian Ocean)
1 UMR 53 Peuplements Végétaux et Bio-Agresseurs en Milieu Tropical, Université de La Réunion, 15 avenue René Cassin, BP 7151, 97415 Sainte Clotilde Messag Cedex 9, La Réunion, France and 2 Herbier Universitaire de La Réunion, 15 avenue René Cassin, BP 7151, 97415 Sainte Clotilde Messag Cedex 9, La Réunion, France
* For correspondence. E-mail claire.micheneau{at}univ-reunion.fr
Received: 15 July 2005 Returned for revision: 9 September 2005 Accepted: 24 January 2006 Published electronically: 22 March 2006
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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• Background and Aims Although numerous angraecoid orchids in Madagascar display typical sphingophilous syndrome (i.e. white, nectariferous, long-spurred flowers, producing a strong scent at the crepuscule that is attractive to moths), three species of Angraecum in Reunion, belonging to the endemic section Hadrangis, have atypical unscented and short-spurred flowers. The aim of the study was to investigate the implication of plant–pollinator interaction on the evolution of floral morphology of these peculiar island floral forms.
• Methods The flower morphology of A. striatum (one of the three section Hadrangis species) was investigated by performing a set of floral measures, and the reproductive biology was investigated by a set of hand pollination experiments. Natural pollinators were observed by means of a digital video camera. Pollinator efficiency (pollen removal and deposition) and reproductive success (fruit set) were quantified once a week in natural field conditions during the 2005 flowering season (i.e. from January to March).
• Key Results The orchid is self-compatible but requires a pollinator to achieve fruit set. Only one pollinator was observed, the endemic white-eye Zosterops borbonicus (Zosteropidae). These birds perched on inflorescences, and probed most fresh-looking flowers on each plant for nectar. Nectar was both abundant (averaging 7·7 µL) and dilute (averaging 9·7 % sugar in sucrose equivalents). Birds were mostly active between 0830 and 0930 h. Visits to plants were extremely short, lasting from 9 to 27 s. At the study site, 60·9 % of flowers had pollen removed, and 46·4 % had pollinia deposited on stigmas. The proportion of flowers that initiated a fruit averaged 20·6 % in natural conditions.
• Conclusions For the first time, a bird-pollinated orchid is described from a sub-tribe that is mainly specialized for moth pollination. This study documents a morphological shift in flowers in response to pollinator adaptations in the insular context of the Mascarene Archipelago.
Key words: Angraecum striatum, bird pollination, Mascarenes, oceanic islands, Orchidaceae, Reunion, white-eyes, Zosteropidae
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Establishment of plant–pollinator interactions is one of the most intriguing investigations of evolutionary ecology. The study of bird pollination systems has provided powerful models for understanding the consequences of pollinator shifts on floral trait evolution (i.e. floral morphology, colour, fragrance and reward properties) (Stiles, 1981
; Bradshaw and Schemske, 2003; Fenster et al., 2004), mainly because these cases are mostly derived from various forms of insect pollination (Stiles, 1981; Grant, 1993, 1994; Bradshaw and Schemske, 2003; Dupont et al., 2004; Manning and Goldblatt, 2005). Bird pollination is poorly represented in Orchidaceae (van der Pijl and Dodson, 1966; van der Cingel, 2001), which are predominantly insect pollinated (Darwin, 1862; van der Pijl and Dodson, 1966; Dressler, 1981; Nilsson, 1992; van der Cingel, 2001). The rare examples of orchid-pollinating birds are found exclusively in the nectarivores, belonging mainly to the hummingbirds (Trochilidae) in the New World (Dodson, 1962, cited in van der Pijl and Dodson, 1966; van der Pijl and Dodson, 1966; Rodríguez-Robles et al., 1992; Singer and Sazima, 2000) and sunbirds (Nectariniidae) in South Africa (Johnson, 1996; Johnson and Brown, 2004). Bird-pollinated orchids show the usual convergent adaptations observed in other families of bird-pollinated flowering plants (i.e. multiflowered inflorescences of reddish, unscented and short-spurred fleshy flowers) (van der Pijl and Dodson, 1966; van der Cingel, 2001). Most flowers have a narrow opening, restricted by a strong fold on the lip that forces a bird to push its beak against the column to reach the nectar in the spur. Unlike most angiosperms where the powder-like pollen is dispersed through a bird's feathers, in Orchidaceae, smooth surfaces such as the beak (Catling, 1987; Rodríguez-Robles et al., 1992; Johnson, 1996; Singer and Sazima, 2000) or even the foot of a bird (Johnson and Brown, 2004) are the most suitable places for pollinarium attachment. These surfaces allow firm fixation of the large, strongly adhesive plate-like viscidia (Johnson, 1996; Singer in Sazima, 2000) typically found in ornithophilous orchids. In Orchidaceae, bird pollination is particularly common in the high elevation Andean regions, where insects are rare and hummingbirds reach their greatest diversity (van der Pijl and Dodson, 1966; Dressler, 1971). Birds have been suggested to supplant insect pollinators where insect density is low, for example in high elevation ecosystems (van der Pijl and Dodson, 1966; Cruden, 1972; Hargreaves et al., 2004), in cases of winter blooming species (Castro and Roberston, 1997; Anderson, 2003; Kunitake et al., 2004) and on islands (Feinsinger et al., 1982; Anderson et al., 2001; Bernardello et al., 2004; Dupont et al., 2004) where the insect fauna is depauperate (Carlquist, 1974; Woodell, 1979; McMullen, 1987; Barrett, 1996; Anderson et al., 2001).
Oceanic islands provide natural opportunities for studying the combined process of species dispersal, establishment, maintenance and speciation, not only because insular ecosystems are often simplified (less diverse biotic communities) compared with the mainland, but also because species evolve in closed, isolated and reduced areas whose recent geological age is often known. Insular plants are frequently morphologically divergent from their continental relatives, showing a high level of speciation and spectacular adaptations (e.g. Carlquist, 1974; Baldwin, 1998; Oleson et al., 1998; Lindqvist and Albert, 2002), including shifts in breeding systems (e.g. Baker, 1955; Carlquist, 1974; Barrett and Shore, 1987; McMullen, 1987; Barrett et al., 1989; Barrett, 1996; Schultz and Ganders, 1996) and/or pollination systems (e.g. Carlquist, 1974; Weller et al., 1995; Oleson and Valido, 2003). Given that available pollinator assemblages during both colonization and consecutive establishment are considered the major driving force in plant mating system evolution (e.g. Carlquist, 1974; McMullen, 1987; Barrett, 1996; Anderson et al., 2001), morphological shifts in response to pollinator adaptations have been poorly investigated so far on the Mascarene Islands (Reunion, Mauritius and Rodrigues). Reunion is the youngest island of the archipelago, having emerged approximately 3 million years ago (McDougall and Chamalaun, 1969). Among indigenous vascular plants, Orchidaceae represent the largest family, including approx. 130 species (du Petit Thouars, 1822; Cordemoy, 1895; Roberts, 2001; see also Jacquemyn et al., 2005). Angraecum (Vandeae, Angraecinae) is one of the most important genera, represented by 25 species, of which 12 are endemic.
Angraecum is famed for the Malagasy star A. sesquipedale, which has a spur length of approx. 30 cm, and was predicted by Darwin in 1862 to be pollinated by an unknown long-tongued hawkmoth. Although the predicted pollinator (Xanthopan morganii var. praedicta) was found 41 years later in the primary forests of Madagascar (Rothschild and Jordan, 1903), effective pollination was only demonstrated 135 years after Darwin's prediction (Wasserthal, 1997). Since the time of Darwin, angraecoid orchids have been associated with a sphinglophilous pollination syndrome (i.e. white flowers with long spurs, producing a strong scent at dusk attractive to moths) (van der Pijl and Dodson, 1966). Despite the great number of species belonging to Angraecum (approx. 200 species, occurring mainly in Madagascar) (Garay, 1973; du Puy et al., 1999), few pollination studies have been reported. The rare investigations that have been conducted on Malagasy orchids (Nilsson et al., 1985, 1987; Wasserthal, 1997) have focused exclusively on long-spurred Angraecum species, which exhibit a typical sphingophilous syndrome. Floral morphology is nevertheless diverse within the genus, suggesting varying pollination systems. Three species (A. striatum, A. bracteosum and A. cadetii) endemic to the Mascarene Islands are particularly interesting since their flowers are unscented and display short wide spurs. These features are sufficiently uncommon for white flowers in the genus to have prompted Bosser (1987) to revise the section Hadrangis to comprise only these three species. We therefore proposed that the atypical flower morphology of section Hadrangis species resulted from specific adaptations to the local pollinator fauna, linked to the oceanic island context of the Mascarene Archipelago.
The main objectives of this study were to (a) describe the flower morphology and breeding system of A. striatum, a representative species of section Hadrangis; (b) identify its natural pollinators; and (c) quantify pollinator efficiency (pollen removal and deposition) and reproductive success (fruit set) in natural conditions.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Study site
Reunion Island is located 800 km to the east of Madagascar (55°39'E; 21°00'S). It is a small island (approx. 2500 km2) dominated by two volcanic massifs, one of which is still active (Piton de La Fournaise, 2619 m). The other (Piton des Neiges) rises to 3070 m and is the highest point in the Indian Ocean. Reunion presents a highly diverse ecosystem in terms of topography and climatic gradients. Since first settlement (approx. 450 years ago), littoral and lowland habitats have been destroyed through human activities, but mountain vegetation has persisted in the rugged interior of the island. Today, 30 % of the original vegetation still remains on Reunion (Strasberg et al., 2005
), whereas <1 % has been preserved on Mauritius (Strahm, 1993). Our study site was located at 1150 m in the Bébour Massif, a cloud forest preserved in the centre of Reunion. This evergreen forest is characterized by a high diversity of native tree ferns and hardwood species, harbouring many mosses, ferns and epiphytic orchids.
Study species
Our study was conducted within the 2005 flowering season on the endemic A. striatum, a monopodial epiphytic orchid relatively common in primary cloud forests, from 600 to 1600 m altitude. Flowering lasted about 2 months from the beginning of January to the end of February, with a flowering peak around January 20. Plants usually produced 1–4 erect racemes of 1–10 white unscented flowers, fleshy in texture. Unpollinated flower lifespan is about 20 d. The spur is conical in shape, short (1 cm) and wide at the entrance (0·4 cm), and contains a large amount of visible nectar. The pollinarium consists of two hard, pale yellow pollinia attached to a single viscidium by two distinct stipes. Pollinia removal and deposition are easily observable to the naked eye.
Floral measurements and nectar properties
In 2003, 16 inflorescences, each from distinct plants, were collected and preserved in 70 % ethanol for morphological measurements. Three fully opened flowers were randomly chosen per sampled inflorescence and dissected for floral measurements. A total of 14 morphological characters were measured, of which four were inflorescence traits and ten were floral features (Fig. 1) (see Table 1 for sample size). Measurements were made to the nearest 0·01 mm, using a Leica MZII stereomicroscope with a digital caliper.
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Nectar properties were recorded on 47 unvisited flowers from 13 plants. For each flower, we measured nectar column height in the spur (distance between the tip of the spur and the level of nectar) to the nearest 0·01 mm using a digital caliper. We quantified nectar volume using calibrated 5 µL capillary tubes. Nectar was then directly transferred to a hand refractometer (R5000, Atago, USA, Inc.), from which the sugar concentration (g of sucrose equivalents 100 g–1 of solution) was determined using sucrose equivalent tables.
Breeding system
Hand pollination experiments were set up both in situ and ex situ to investigate the breeding system of A. striatum. In situ experiments were carried out on 23 inflorescences, each on distinct plants situated at the study site. Prior to flower anthesis, plants were first enclosed by fine-mesh nylon bags to exclude pollinators. Three treatments were performed: (a) no pollination, to detect this species' ability to set fruit in the absence of pollinators (autonomous self-pollination) (13 inflorescences; 38 flowers); (b) self-pollinations to quantify self-compatibility (six inflorescences; 24 flowers); and (c) cross-pollinations (five inflorescences; 16 flowers). Self-pollinations were carried out by hand, pollinating flowers with their own two pollinia. Cross-pollinations were performed by hand, pollinating flowers with two pollinia from a distinct conspecific plant (at least 2 m distant). The bags were left in place till the end of the fruiting period to prevent predation.
The same sets of experiments were performed ex situ on seven plants (ten inflorescences; 52 flowers) cultivated in a greenhouse, as follows: 25 flowers (ten inflorescences) were unmanipulated, seven flowers (seven inflorescences) were self-pollinated and six flowers (five inflorescences) were cross-pollinated.
In situ, one treatment was assigned to the whole inflorescence (i.e. all flowers of the inflorescence were either self-pollinated, cross-pollinated or unmanipulated). Ex situ however, the three different treatments were randomly assigned to the flowers of the same inflorescence (i.e. each inflorescence received the three treatments). Fruit set for each treatment was recorded 4 weeks after pollination, when capsules reached their maximum size. Comparisons between self- and cross-pollination were performed using Fisher's exact tests with no prior alternative using R software (version 1. 10) for MacOSX (Iacus and Urbanek, 2005). Comparison between in situ and ex situ treatments was not performed since bias would be introduced by (a) resource allocation (the number of pollinated flowers per inflorescence was not equal in situ or ex situ); and (b) the fact that fruit development may be alter in the bagged plants (reduction of photosynthetic light).
Pollinator observations
Pollinator observations were performed using a digital video camera (Sony DCR-TRV16E camcorder with night shot option) fixed on a tripod, with power supplied by a generator situated at least 4 m from the study site to avoid noise disturbance. Observations were recorded on 1 h Fuji DVM60 tapes, replaced each hour, for intervals of 3–13 h (depending on the weather) over six days and four nights. The camcorder was hidden in the forest, 5 m from a patch of six individuals separated by <2 m, and focused on 1–5 individuals each time (hereafter termed target individuals). Before and after each videotape session, each flower of the target individuals was examined for pollen removal and/or deposition. Dates, durations and sample size of each session are shown in Table 2.
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Pollination success and fruit set at the population level
Once a week from January 5 to March 2, 2005 (i.e. nine census dates), 38 additional individuals (n = 422 flowers) were examined for the purpose of determining male and female pollination success (pollen removal and deposition, respectively). Fruit set in natural conditions was calculated by the proportion of tagged flowers that develop fruit.
Bird-pollinated orchids: literature background
With the purpose of comparing morphological convergences in ornithopilous orchids, previous studies on bird-pollinated orchids were examined for information about orchid taxonomy (sub-family, tribe and sub-tribe), habit (epiphytic or terrestrial), locality (tropical or temperate), odour production, numbers of flowers per inflorescence, flower colour, spur length, nectar properties (volume and sugar concentration), pollen movement (pollinaria removal and deposition) and fruit set in natural conditions.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Floral measurements and nectar properties
Inflorescences displayed on average 5·1 flowers (s.d. = 1·5; n = 16). Floral parts (excluding the lip) showed little variation (Table 1). Nectar volume averaged 7·7 µL per flower (s.d. = 3·4; n = 47) with a concentration of 9·7 % sugar in sucrose equivalents (s.d. = 1·3; n = 47).
Breeding system
None of the flowers tested for autonomous self-pollination produced fruit, either in situ or ex situ, suggesting that A. striatum requires a pollinating agent to set fruit (Table 3). However, the species is self-compatible (Table 3) and there was no significant difference in fruit set between self- and cross-pollination treatments (P = 0·3295 in situ; P = 1 ex situ).
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Pollinator observations
The only species recorded visiting A. striatum were Zosterops borbonicus (white-eye, Zosteropidae) (Fig. 2) during the day and some unidentified cockroach species at night. However, pollen movement was only recorded after bird visits. We observed Z. borbonicus on three consecutive days during the flowering peak of the population. On these occasions, pollen transfer by birds (i.e. pollinarium removal and deposition) was clearly observed. At the end of the first day, four previously intact flowers had pollinaria removed; on the second day, no pollen removal was observed although one flower was pollinated (Table 2).
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The daily activity of the birds was regular, taking place only in the morning between 0830 and 0930 h. with an additional visit on the second day at 1330 h (Fig. 3). Six visits in total were recorded (Table 2). The duration of a visit to a plant varied from 9 to 27 s (x = 15·3; s.d. = 6·7; n = 6). White-eyes typically landed on a leaf or inflorescence and probed all ‘fresh-looking’ flowers within reach, often starting from lower flowers, and moving around the inflorescence rachis if necessary. During a visit, 2–10 flowers were probed (x = 6·3; s.d. = 2·7; n = 6), which represented 40–100 % of opened flowers per plant. Birds rarely probed the same flower twice. They fed on nectar by inserting their beak into the large entrance of the spur (Fig. 2A). At the same time, they accumulated a large number of pollinaria on both the upper and lower base of the beak (Fig. 2B). On one occasion, we observed an individual Z. borbonicus cleaning its beak on tree fern stipes to remove pollinaria.
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Pollination and reproductive success at the population level
The rate of pollinarium removal was 60·9 % (257/422 flowers) for the whole population (38 individuals), and that of pollen deposition was 46·4 % (196/422 flowers). Pollination efficiency (deposition/removal) was high (76·2 %). In natural conditions, the proportion of tagged flowers that set a fruit averaged 20·6 % (87 initiated fruits/422 flowers).
Bird-pollinated orchids: literature background
The principal studies to date about bird-pollinated orchids, including this study, are summarized in Table 4. Within bird-pollinated orchids, morphological shifts in relation to functional interactions with birds are convergent, regardless of bird type (hummingbirds, sunbirds or white-eyes), orchid sub-family (Epidendroideae or Orchidoideae, the latter including Spiranthoideae; Chase et al., 2003), habit (epiphytic or terrestrial) and distribution (tropical or temperate). All bird-pollinated orchids show multiflowered inflorescences of short-spurred flowers (<2·5 cm long) lacking a detectable odour (see Table 4). The majority of bird-pollinated orchids also display vividly coloured flowers, but the flowers of A. striatum are pure white.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Floral morphology and nectar properties
Except for the colour flower segments (pure white), the flower morphology of A. striatum matches orchid bird pollination syndrome. According to Johnson and Steiner (2000)
, convergences in floral features are limited by phylogenetic constraints. Many examples have also shown that flower colour is not necessarily correlated with pollination syndrome (e.g. Waser et al., 1996; Momose et al., 1998; Ollerton, 1998; Johnson and Steiner, 2000). Flower colour within Angraecinae may be a conservative character. In contrast, spur length and fragrance production have evolved quickly with pollinator pressure. In Orchidaceae, the spur is reported to be under pollinator directional selection (Inoue, 1986; Nilsson, 1988; Johnson and Steiner, 1997; Johnson et al., 1998; Ellis and Johnson, 1999; Tremblay et al., 2005), although this is not always the case (see Maad, 2000; Luyt and Johnson, 2001). The value of spur length as a character for discriminating section or species (as has historically been the case within Angraecum; Perrier de la Bâthie, 1941; Garay, 1973) reaches its taxonomic limit in this study. Although there is no heavy callus on the lip of A. striatum, beak and spur morphologies appear to have a narrow optimum for efficient pollination. The bills of Z. borbonicus match the flower entrance diameter perfectly and are suitable for both extracting nectar and performing pollination (bill: 3·7 mm in basal diameter, 11·6 mm in length) (Gill, 1971; M. Lecorre, Université de la Réunion, France, unpubl. res.).
Nectar of bird-pollinated flowers is typically abundant and dilute compared with the nectar of insect-pollinated species (Baker, 1975; Bolten and Feinsinger, 1978; Pyke and Waser, 1981; Proctor et al., 1996; Nicolson, 2002; Dupont et al., 2004; Manning and Goldblatt, 2005). Nectar volume and concentration average (and range), respectively, 5·4 µL (2·7–11·7) and 20·3 % (9·9–31·2) sugar in sucrose equivalents. The nectar of A. striatum was both more abundant and more dilute than the average volume and concentration for ornithophilous orchids. Recent studies (e.g. Nicolson, 2002) have shown that nectar dilution differs between flowers visited by hummingbirds and those visited by other passerine flower-feeding birds. Dilution seems to be closely correlated with nectar sugar constituents due to sugar osmotic properties: composite sugars (i.e. sucrose) are predominant in low-dilution nectar, whereas simple hexose sugars are found in high-dilution nectar. Differences in nectar sugar chemistry are strongly correlated with physiological properties inherent in each pollinator group (Baker and Baker, 1983; Baker et al., 1998; Nicolson, 2002; Nicolson and Fleming, 2003; Dupont et al., 2004). Thus, insects and hummingbirds are able to digest complex sugars such as sucrose, whereas generalist passerine birds are only able to digest simple hexose sugar (see, for example, Martinez del Rio et al., 1992). Dupont et al. (2004) also found a correlation between nectar composition and pollination system (entomophily vs. ornithophily), but contrary to the traditional view that nectar composition is a conservative trait, it was evolutionarily labile among Canarian bird-pollinated flowers. We did not investigate the components making up the sugar of A. striatum, but it would be worthwhile for further studies to compare nectar composition between bird- and insect-pollinated species of Angraecum in the Mascarenes. The nectar of the sphingophilous A. sesquipedale was, however, more concentrated (16·5 % sugar in sucrose equivalents; Wasserthal, 1997) than the nectar of A. striatum (9·7 % sugar in sucrose equivalents), suggesting differences in sugar composition.
Bird–orchid interactions
Although around 50 bird families have been reported as flower visitors (Proctor et al., 1996), three major avian radiations are involved independently in a specialized nectar diet: hummingbirds (Trochilideae) in the New World, sunbirds (Nectaridiinae) in the Old World (primarily Africa) and honeyeaters (Meliphagidae) in Australasia (van der Pijl and Dodson, 1966; Wolf et al., 1975; Stiles, 1981; Proctor et al., 1996; Anderson, 2003). Although hummingbirds and sunbirds have been reported definitively as orchid pollinators (e.g. van der Pijl and Dodson, 1966; Rodríguez-Robles et al., 1992; Singer and Sazima, 1994; Johnson, 1996; Johnson and Brown, 2004), reports of pollination by honeyeaters are mostly anecdotal (see van der Pijl and Dodson, 1966; van der Cingel, 2001). In this study, a bird species outside these three main nectarivorous groups (Z. borbonicus) has been unambiguously observed. The family Zosteropidae (white-eyes) includes around 100 species of small arboreal songbirds (Gill, 1971; Slikas et al., 2000) with a widespread distribution throughout the Old World tropics and sub-tropics. White-eyes have colonized more oceanic islands than any other passerine family (Moreau, 1964, cited in Gill, 1971). Although some species of white-eyes play an important role in plant pollination (Gill, 1971; Proctor et al., 1996; Kunitake et al., 2004), white-eyes have a generalist diet which includes fruit, insects and nectar (Gill, 1971).
Zosterops borbonicus is endemic to the Mascarenes (two sub-species are reported, Z. b. mauritianus in Mauritius, and Z. b. borbonicus in Reunion,). On Reunion, it is one of the most common passerine birds (465 000 individuals were estimated in 1983; Barau et al., 2005), occuring over the whole island from sea level to 2300 m, with a large habitat range including both primary forests and inhabited disturbed human zones. Zosterops borbonicus has a generalist diet, including nectar, seeds, fruits and insects. However it has been reported visiting the flowers of >40 species of indigenous and introduced species (see Table 5). Angraecum striatum in turn seems to have only one pollinator. Orchids are known for their high pollinator specificity (Tremblay, 1992; Johnson and Steiner, 2000; Tremblay et al., 2005), and about 60 % of species have only one recorded pollinator (Tremblay, 1992). This specialization maximizes the efficiency of pollination (Nilsson, 1992), but results in reproduction often being strongly limited by pollinators (Tremblay et al., 2005), making orchids more dependent on their pollinators than the reverse (Nilsson, 1992; Roberts, 2003). Pollinator limits seem to have played an important role in the extraordinary diversification of the family (see Tremblay et al., 2005). In long-tongued hawkmoth-pollinated Angraecum, such an asymmetric pollination system is evident. For example, Angraecum arachnites was exclusively pollinated by Panogena lingens (Sphingidae), even through many potential pollinators were abundant in the vicinity of the orchid. This hawkmoth in turn was an effective pollinator of several long-spurred orchid species (Nilsson et al., 1985).
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Orchids reported as bird pollinated, however, generally share several species of the local avifauna. Stenorrhynchos lanceolatus, for example is pollinated by three different hummingbirds in southern Brazil (Singer and Sazima, 2000
), and Satyrium species are often pollinated by two or more sunbirds in South Africa (Johnson, 1996). Zosterops borbonicus was the only observed pollinator of A. striatum, although another species of endemic white-eye, Z. oliveaceus, is present in Reunion. The almost exclusively nectar diet of Z. oliveaceus (Gill, 1971) makes it a good candidate pollinator of A. striatum or the two others species of Angraecum section Hadrangis, which display the same ornithophilous flower characteristics. We did not observe Z. oliveaceus on A. striatum; however, this species is less abundant than Z. borbonicus (Gill, 1971).
Zosterops borbonicus behaviour
Birds were mainly active in the morning, between 0830 and 0930 h, which agrees with most previous reports of bird-pollinated orchids (e.g. Johnson, 1996: visits occurred between 0900 and 1000 h; Johnson and Brown, 2004: visits mainly occurred from 0700 to 0930 h; but Singer and Sazima, 2000: visits occurred between 1000 and 1635 h). Similarly to hummingbirds (Singer and Sazima, 2000) and sunbirds (Johnson, 1996; Johnson and Brown, 2004), white-eyes probed the majority of fresh-looking flowers on plants when foraging. As A. striatum is self-compatible, self-pollination (sensu stricto or through geitonogamy) could be expected to result from the bird's behaviour on the inflorescences. According to Singer and Sazima (2000), although self-pollinations may occur in S. lanceolatus, the chances of cross-pollination are enhanced by the granular texture of the pollinaria (from one pollinaria removal, many pollination events may follow) and the fact that birds visit several inflorescences. Moreover, they estimated that pollinaria may remain for up to 6·5 h on the bird's bill. Similarly, Johnson (1996) highlighted the firm attachment of Satyrium pollinaria on a birds' bill due to specific properties of these large and firmly adhesive viscidia. Firm fixation was thought to prevent pollinarium removal by birds when grooming. It is also possible that strong adherence would at the same time reduce self-pollination. Long periods of pollinarium attachment facilitated by strongly adherent viscidia seem to occur in A. striatum. Even if we failed to detect significant consequences of either self- or cross-pollinations on fruit set, it would be worthwhile to quantify the degree of geitonogamy among the population.
In our study, visits to plants by birds were extremely brief, as has also been observed in the hummingbird-pollinated S. lanceolatus (Singer and Sazima, 2000). van der Pijl and Dodson (1966) highlighted the difficulties of observing bird pollination due to their furtive behaviour. In this context, bird pollination of orchids may be under-estimated due to the brevity of their visits and the difficulty involved in making observations. During the last 3 years, we have repeated intensive field observations but did not observe any visitors to orchid flowers. Videotape observations offer a method of observing visits to flowers without the presence of humans altering bird behaviour.
Pollination and fruiting success
Within the 2005 flowering season, 60·9 % of flowers experienced pollen removal, and 46·4 % had pollinia deposited on their stigma. For comparison, removal (and deposition) rates ranged from 28·1 % (22·3 %) (Rodríguez-Robles et al., 1992) to 74·7 % (94·1 %) (Singer and Sazima, 2000) in hummingbird-pollinated orchids and averaged 38 % (25·9 %) in sunbird-pollinated orchids (Ellis and Johnson, 1999) (Table 4). Although the pollination rate was high, the proportion of flowers that initiated fruit was only 20·6 %, suggesting a high failure rate in fruit development. If reproductive success is strongly pollen limited in Orchidaceae (see Tremblay et al., 2005 for further references), resource limitation should also be considered (Sabat and Ackerman, 1996), especially over the lifetime of a species (e.g. Zimmerman and Aide, 1989; Ackerman and Montalvo, 1990; Mélendez-Ackerman et al., 2000). During our study, we noted a spectacular rate of flower abortion, which reached 45·7 % in the population. As reproduction limits were not the subject of this study, we are unable to discuss fruit and flower abortions. More studies, focusing precisely on predation and resource allocation, are needed.
Fruit production (20·6 %) was however close to the general mean reported recently for tropical orchids (17 %) (Tremblay et al., 2005). Compared with other bird-pollinated orchids, fruit set was however inferior (20·6 vs. 59·6 %), but close to the hummingbird-pollinated Comparettia falcata (18·1 %), which shares both the epiphytic habit and a tropical distribution (Rodríguez-Robles et al., 1992).
During our study, birds were active within the whole population of A. striatum; 84 % of the sampled individuals had at least one flower with its pollinarium removed, while 87 % had at least one flower pollinated. However, 47 % of the individuals in the population failed to set fruit, which is close to the range of 50–60 % reported by Tremblay et al. (2005) for tropical orchids.
Evolution from sphingophily to ornithophily?
The extraordinary number and diversity of long-spurred Angraecinae in Madagascar have been explained by their long-term evolution with long-tongued Sphingidae fauna, archaic relationships that have persisted in the relatively stable environment of the isolated island (Nilsson et al., 1985). In most cases, islands are colonized from mainland areas, even if rare examples of the reverse are known (e.g. Nilcholson et al., 2005). The flora of Reunion has been reported to originate primarily (>80 % of native taxa) from Madagascar and Africa (Cadet, 1977). Ongoing phylogenetic investigations, inferred from plastid DNA sequences (C. Micheneau, Université de la Réunion, France; M. Fay, RBG Kew, UK; M. Chase, RBG Kew, UK; B. Carlsward, University of Florida, USA; T. Pailler, Université de la Réunion, France, unpubl. res.) show that section Hadrangis has its closest relatives in section Humblotiangraecum (Madagascar and Comoros), whose flowers exhibit the sphingophilous syndrome. Following the hypothesis of colonization from Madagascar, section Hadrangis would have had a sphingophilous-like form when it colonized the Mascarenes. Today, some long-spurred Angraecinae are present on Reunion. However, all endemic species that exhibit flowers with spurs longer than 9 cm have become totally independent of pollinators, and are capable of autonomous self-pollination, indicating that the interactions with sphingids has been lost in these long-spurred angraecoids (T. Pailler and C. Micheneau, Université de la Réunion, France, unpubl. res.; see Jacquemyn et al., 2005 for a discussion about autogamy in orchids from Reunion).
Bird pollination is considered to be a widespread phenomenon among insular plants (e.g. Anderson et al., 2001; Anderson, 2003). To compensate for the general scarcity of island insects, insect-feeding vertebrates often include nectar and fruits in their diet (Olesen and Valido, 2003; Dupont et al., 2004). According to Dupont et al. (2004), ‘insular flowers may have evolved directionally in response to opportunist flower-visiting birds even though these pollinators are not thought to drive evolution in mainland flora’. On Reunion, if Z. borbonicus is an opportunist, the presence of the nectar-specialized Z. oliveaceus may have played a precursor role in the establishment of Zosterops–Angraecum interactions. According to Gill (1971), Z. oliveaceus is believed to have colonized the Mascarene Archipelago before Z. borbonicus. We could then hypothesize that specialization through nectar feeding of Z. oliveaceus co-evolved with section Hadrangis adaptation to ornithophily. We thus expect to observe Z. oliveaceus as a pollinator of at least one species of section Hadrangis. More studies are needed to test this hypothesis. Nevertheless, the original case of bird-pollinated Angraecum developed in this study illustrates once again both the singularity of insular ecosystems and the fascinating ability of orchids to adapt to different pollinators.
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We thank Mark W. Chase, as well as two anonymous referees for useful comments on preliminary versions of the manuscript, and Alain Brondeau (Office National des Forêts) for material support. This work was support by the Ministère Francais de l'Ecologie et du Délevoppement Durable (Écosystèmes Tropicaux) and the Région Réunion.
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