Bat Pollination Syndromes Research Articles

Rethinking the pollination syndromes in Hymenaea (Leguminosae): the role of anthesis in the diversification.

Floral traits associated with functional groups of pollinators have been largely employed to understand mechanisms of floral diversification. Hymenaea is a monophyletic legume genus widely recognized to being bat-pollinated, with nocturnal anthesis and copious nectar. The most of species has short-paniculate inflorescences, white and robust flowers, congruent with a bat-pollination syndrome. However, other Hymenaea species show a different floral pattern (e.g., long-paniculate inflorescences and smaller flowers) which we report here as being bird pollinated. We examined the floral traits and visitors of Hymenaea oblongifolia var. latifolia and identified evolutionary shifts in floral traits associated with potential pollinators of Hymenaea species. Floral traits of H. oblongifolia var. latifolia differ from those expected for bat-pollinated flowers in species of sect. Hymenaea, and we observed hummingbirds collecting nectar legitimately. Our phylogenetic analysis did not support the monophyly of the taxonomic sections and suggests that bat pollination is ancestral in Hymenaea, with bird pollination evolving later. The transition coupling with shifts in the timing of anthesis and other floral traits. Pollinator-mediated evolutionary divergence hypothesis partially explains the Hymenaea diversification in the Neotropics. It is congruent with those species shifting from traits linked traditionally to bat pollination to hummingbird pollination.

Repeated evolution of vertebrate pollination syndromes in a recently diverged Andean plant clade.

Although specialized interactions, including those involving plants and their pollinators, are often invoked to explain high species diversity, they are rarely explored at macroevolutionary scales. We investigate the dynamic evolution of hummingbird and bat pollination syndromes in the centropogonid clade (Lobelioideae: Campanulaceae), an Andean-centered group of ∼550 angiosperm species. We demonstrate that flowers hypothesized to be adapted to different pollinators based on flower color fall into distinct regions of morphospace, and this is validated by morphology of species with known pollinators. This supports the existence of pollination syndromes in the centropogonids, an idea corroborated by ecological studies. We further demonstrate that hummingbird pollination is ancestral, and that bat pollination has evolved ∼13 times independently, with ∼11 reversals. This convergence is associated with correlated evolution of floral traits within selective regimes corresponding to pollination syndrome. Collectively, our results suggest that floral morphological diversity is extremely labile, likely resulting from selection imposed by pollinators. Finally, even though this clade's rapid diversification is partially attributed to their association with vertebrate pollinators, we detect no difference in diversification rates between hummingbird- and bat-pollinated lineages. Our study demonstrates the utility of pollination syndromes as a proxy for ecological relationships in macroevolutionary studies of certain species-rich clades.

The floral bat lure dimethyl disulphide does not attract the palaeotropical Dawn bat

In the neotropics, dimethyl disulphide (DMDS) is innately attractive to flower-visiting bats, and acts as a powerful bat lure in the scent bouquets of many bat-pollinated flowers. At first, DMDS appeared to be part of a general bat pollination syndrome. However, DMDS is absent in many bat-pollinated flowers of West Africa, and it is unclear whether palaeotropical flower-visiting bats are also attracted to it. Furthermore, DMDS was previously observed in neotropical, but not palaeotropical, populations of Ceiba pentandra (Malvaceae, Bombacoideae). We tested for an attraction to DMDS in the most common flower-visiting bat in Thailand, the dawn bat Eonycteris spelaea. We gave bats choices of Ceiba pentandra flowers, where one random flower was scented with DMDS. Rather than preferring the DMDS-treated flower, 21 of 22 bats chose an untreated flower, showing no attraction to DMDS. Alongside past evidence, this result suggests that the role of DMDS in bat pollination syndromes may result from an adaptive convergence that is limited to the neotropics. This hypothesis could be tested through comparative studies of (1) attraction across bats, (2) floral DMDS presence across bat-pollinated plants in Asia, and (3) floral DMDS measures across New and Old World populations of Ceiba pentandra.

Reproductive biology of a highly endemic species: Cipocereus laniflorus N.P. Taylor & Zappi (Cactaceae)

Cipocereus laniflorus N.P. Taylor & Zappi is an endemic species from the Serra do Caraça, State of Minas Gerais, Brazil. In order to propose conservation strategies for this species, its reproductive strategies were investigated, including reproductive phenology, floral biology, floral visitors and breeding system. The flowering and fruiting period extends from May to October. Few flowers per plant open each night, producing up to 0.4 ml nectar, but 30% of them are nectarless. Probably pollen is also offered as a resource. Fruiting efficiency of C. laniflorus (47%) is close to that found in other Cactaceae species. Pollen of this species was detected in Anoura geoffroy, Soricina glossophaga and Pygoderma bilabiatum bats. Amongst the characteristics related to bat-pollination syndrome found in C. laniflorus, the cream-white colouring of the internal part of the flower, the numerous stamens and the nocturnal anthesis of short duration can be highlighted. Flowers of C. laniflorus are also visited by Nitidulidae beetles, Trigona fulviventris bees and hummingbirds, however bats are the main pollinators of this species. Finally, as a self-sterile species, C. laniflorus needs a pollinator and is more susceptible to the risk of extinction if local disturbances affect its pollination system.

Evaluation of pollination syndromes in Antillean Gesneriaceae: evidence for bat, hummingbird and generalized flowers

Summary Current views about the predominance of generalization of pollination systems have stimulated controversy concerning the validity of pollination syndromes. In order to assess the extent to which floral characters reflect selection by the most important pollinators we evaluated pollination syndromes in a florally diverse plant group, the tribe Gesnerieae, a monophyletic plant radiation from the Antillean islands. The study species include representatives of three groups of floral phenotypes, two of which chiefly correspond to ornithophilous and chiropterophilous syndromes. The third group includes subcampanulate flowers (characterized by a corolla constriction above the nectar chamber) with combinations of traits not fitting classic pollination syndromes. Pollination systems were characterized for 19 Gesnerieae species in five Antillean islands between 2003 and 2007 and supplemented with observations of four Gesneriaceae species from Costa Rica. Pollinator visitation and frequency of contact with anthers or stigmas were used to calculate an index of pollinator importance. Eleven floral traits including morphology, phenology and rewards were used to assess clustering patterns in phenotype space. Multidimensional scaling analysis of floral traits resulted in two clusters comprising: (i) tubular, red to yellow‐flowered species with diurnal anthesis, (ii) bell‐shaped‐flowered species; two groups of floral phenotypes were evident within the latter cluster, campanulate nocturnal and subcampanulate flowers. Correlations between pollinator importance values and floral axes revealed strong associations with the expected pollinators, hummingbirds for tubular flowers, and bats for campanulate flowers; subcampanulate‐flowered species had generalized pollination systems including bats, hummingbirds and insects. Discriminant analysis of the multivariate set of floral traits correctly classified 19 out of 23 species into the predicted pollination categories. Synthesis. This study provides support for classic hummingbird and bat pollination syndromes, demonstrating the importance of pollinator‐mediated selection in the floral diversification of Antillean Gesnerieae. However, there was evidence for generalized pollination systems in species characterized by a unique morphological trait (corolla constriction), but with variable combinations of other floral traits. These findings suggests that floral phenotypes might also evolve under selection by various functional groups of pollinators, and underscores the importance of considering the presence and effectiveness of all floral visitors in pollination studies.

The pollination ecology of two species of Parkia (Mimosaceae) in southern Thailand

Abstract:Although the floral traits ofParkiaconform to the bat-pollination syndrome, many visitors other than bats have been observed at their flowers. Some chiropterophilous plants are also pollinated by other animals; the syndrome is therefore best regarded as a hypothesis for which field observations and pollination experiments are required. The present study aimed, for the first time, to determine the breeding system of the economically important canopy trees,Parkia speciosaandP. timoriana, and to identify their pollinators. Pollination experiments carried out in Trang and Songkhla Provinces, in 28 trees ofP. speciosaand fourP. timorianaindicated that they are self incompatible. Open pollination resulted in the highest fruit set (average 60–67% of inflorescences per tree) although this was not significantly different from hand-crossed pollination (48–60%). Insect pollination resulted in fruit set in only 12% ofP. speciosainflorescences. Fruit bats, mainlyEonycteris spelaea, visit flowering plants continuously from dusk till after midnight. Nocturnal and diurnal insects (moths and stingless bees respectively) visit capitula, mostly at the nectar zone. Nectarivorous bats are the most effective pollinator forP. speciosaandP. timoriana. The fact that populations ofE. spelaeaappear to be declining throughout their distribution is therefore a matter of increasing concern.

Pollination ecology and breeding systems of five Gesneria species from Puerto Rico.

The genus Gesneria diversified in the Greater Antilles giving rise to various floral designs corresponding to different pollination syndromes. The goal of this study was to characterize the pollination and breeding systems of five Puerto Rican Gesneria species. The study was conducted in Arecibo and El Yunke National Forest, Puerto Rico, between 2003 and 2007. Floral visitors were documented by human observers and video cameras. Floral longevity and nectar production were recorded for the five study species. Tests for self-compatibility and autonomous selfing were conducted through hand-pollination and bagging experiments. Floral phenology and nectar production schedules agree with nocturnal (in bell-shaped flowered G. pedunculosa and G. viridiflora subsp. sintenisii) or diurnal pollination syndromes (in tubular-flowered G. citrina, G. cuneifolia and G. reticulata). Nectar concentration is consistently low (8-13 %) across species. Gesneria citrina and G. cuneifolia are exclusively pollinated by hummingbirds, while Gesneria reticulata relies mostly on autonomous self-pollination, despite having classic ornithophilous flowers. A variety of floral visitors was recorded for the two species with bell-shaped flowers; however, not all visitors have the ability to transfer pollen. Bats are the primary pollinators of G. pedunculosa, with bananaquits probably acting as secondary pollinators. For G. viridiflora subsp. sintenisii, both bats and hummingbirds contact the flower's reproductive organs, thus, this species is considered to be a generalist despite its nocturnal floral syndrome. All species are self-compatible but only tubular-flowered Gesneria are capable of autonomous self-pollination. The visitation patterns described in this study fit the predicted hummingbird and bat pollination syndromes and support both specialization and generalization of pollination systems in Puerto Rican Gesneria. Specialization is associated with low pollinator visitation, particularly by hummingbirds, which may explain the occurrence of autonomous selfing mechanisms in tubular-flowered species.

Floral biology ofPilosocereus tuberculatus(Werderm.) Byles & Rowley: a bat pollinated cactus endemic from the “Caatinga” in northeastern Brazil

Brazil is the third major centre of diversity for the family Cactaceae, with approximately ¾ of the species found in the country being endemic, and a total of 162 native species, including around 20 belonging to Pilosocereus. This family is exclusively pollinated by animals, varying widely between beetles, bees, butterflies, moths, hummingbirds and bats. Pilosocereus tuberculatus is a tree-like cactus with candelabriform branching, with a relict distribution restricted to a few localities in the states of Pernambuco, Bahia, Sergipe and probably southern Piauí. The present work reports observations of bat-pollination in natural populations of the species in an area of dryland woody vegetation (‘caatinga’) in the municipality of Buíque, state of Pernambuco, Brazil. The slightly zygomorphic flowers have olive-green outer perianth-segments and white inner perianth-segments with purplish spots, and a straight, almost cylindric flower tube 3.5–4.0 cm long. Nocturnal anthesis, a strong smell and internally white flowers with abundant nectar (23–309µl) of relatively low sugar content (9.5–17.0%) are characteristic of the bat-pollination syndrome. Pollen is available and the stigma is functional during anthesis as a whole, from between 18:00–18:20h and 8:20–8:50h the following morning. Visits were recorded during the day by bees (Apis mellifera, Trigona spinipes and Xylocopa grisescens) and a hummingbird (Heliomaster squamosus) and during the night by bats (Glossophaga soricina and Lonchophylla mordax). The bats were observed at intervals varying between 5 seconds and 55 minutes, during 18 nights (i.e. 270 hours of observation). In P. tuberculatus spontaneous self-pollination did not produce fruits. The ratio of fruits formed by cross-pollination (69%) compared with manual self-pollination (0%) indicates that the predominant reproductive system in P. tuberculatus is allogamy, and that its reproduction depends on the efficiency of the pollen-vectors. Based on behaviour displayed during bat, bee and hummingbird visits, and the ratio of natural fruit formation, P. tuberculatus depends mostly on its nocturnal visitors for pollination. Bat-pollination, which is predominant for the genus Pilosocereus, has been interpreted as a mechanism of parallel evolution between cacti and bats, and it is possible to consider P. tuberculatus as an example of this close relationship, including a the new record of the glossophagine bat L. mordax as a cactophilic bat.

Pollination of three species of Abutilon (Malvaceae) intermediate between bat and hummingbird flower syndromes

Some species of Abutilon in southeastern Brazil overlap their flower features between hummingbird and bat pollination syndromes. We studied three such species in the montane rainforest in southeastern Brazil. Abutilon rufinerve , A. regnellii and A. aff. regnellii present the following combination of ornithophilous and chiropterophilous features: bell to bowl-shaped flowers lasting about 30 h, coloured pinkish to purplish, or yellowish, crepuscular (dusk or dawn) anthesis, and very faint cabbage odour. The flowers are visited and pollinated by a species of phyllostomid bat at night, and by several species of hummingbirds during the day. Although somewhat intermediate between ornithophily and chiropterophily, the floral features of the three species of Abutilon tend towards the bat-pollination syndrome.

Tetrastylis ovalis: A second case of bat-pollinated passionflower (Passifloraceae)

The floral biology ofTetrastylis ovalis and its pollination by bats was studied in southeastern Brazil. The flowers ofT. ovalis seem more fitted to bat-pollination than those ofPassiflora mucronata, the other known chiropterophilous passionflower. Two species of bats were observed visiting flowers ofT. ovalis: the phyllostomidsGlossophaga soricina andRhinophylla pumilio. Due to the attributes ofTetrastylis, its presumed primitiveness and a better defined bat-pollination syndrome we suggest that chiropterophily evolved independently in the former genus and inPassiflora.

Bat pollination ofEncholirium glaziovii, a terrestrial bromeliad

The many-flowered, brush-like spikes ofEncholirium glaziovii, a ground-dwelling pitcairnioid bromeliad of the “campo rupestre” formation of southeastern Brazil, was observed being pollinated by the glossophagine bat,Lonchophylla bokermanni, in the Serra do Cipo (Minas Gerais). Nectar feeding was while hovering, and the pollen was preferentially transferred by the bat's snout. The floral pattern is chiropterophilous; unlike known tillandsioid bat flowers, stamens and style are protrusive beyond a small, persistent perigon, and anthesis, apparently protogynous, extends over several nights, with gradual onset and cease. Although various other flower-visitingChiroptera are known to occur in the area and are not mechanically precluded from exploitingEncholirium glaziovii, no one seems to compete withLonchophylla bokermanni. This species, a trap-liner, habitually forages in open habitats, a possible reason for its exclusiveness.—Flower details of two other species ofEncholirium from the same locality including one with the bat pollination syndrome, are given.

"Two Bob Each Way": The Pollination and Breeding System of the Australian Rain Forest Tree Syzygium cormiflorum (Myrtaceae)

The breeding system of a cauliflorous rainforest tree Syzygium cormiflorum was examined to assess the degree of self-compatibility, the type and effectiveness of its pollinators, and the postfertilization seed loss and net seed production. The species is xenogamous, but shows a degree of self-compatibility, with successful pollination via autogamy ranging from 10 to 32 percent, via geitonogamy 16-60 percent, via intrapopulation xenogamy 58-82 percent, and via interpopulation xenogamy 80-92 percent. The difference in fertilization rates between autogamy and geitonogamy is discussed. Bats, birds, and insects were successful pollinators, with bats (and possibly large moths) being the most effective despite visiting the flowers less frequently than birds. Bats, and possibly large moths, accounted for 55.4 percent of successful pollinations, compared to 19.6 percent for birds and 25 percent for small insects. Postfertilization seed loss due to the predatory activity of a weevil was very high, up to 70 percent. The pattern of average nectar flow favors birds, but individual flowers produce nectar at varying times suitable for nocturnal or diurnal visitors or both. There is some evidence that breeding is restricted to crosses between individuals in a local population. The pollination system may be adaptive in maximizing fertilization in situations lacking the major pollinators, but the difficulty of distinguishing this from a system evolving from night to day pollination or vice versa is recognized. THE RAINFOREST TREE FLORA OF AUSTRALIA totals over 1200 species, yet there has been no quantitative study made of the pollination biology and breeding system of any of them. This is in marked contrast to the Neotropics and southeast Asia where a few studies of controlled pollination and pollinator biology have been done, resulting in a rapid reassessment of the general view of breeding systems in tropical forest trees. The earlier view (Corner 1954, Baker 1959, Fedorov 1966) was that rainforest trees were mostly self-compatible and self-pollinated, allowing maximum seed set in an environment where pollinator movements were supposedly limited. It is now held that outcrossing is the more important phenomenon encountered (e.g., Ashton 1969, Bawa 1974, Frankie & Baker 1974, Frankie et al. 1976). The Myrtaceae is an important and conspicuous element in the Australian flora and is well represented in our rainforests. The largest genus in these forests is the widely distributed Syzygium, which has over 500 species world wide with 52 in Australia of which 41 are endemic (Hyland 1983). Studies of two species of Syzygium have already been reported. Lack and Kevan (1984) examined the breeding system of Syzygium lineatum on Sulawesi, and Hopper (1980) recorded floral visitors to Syzygium tierneyanum in north Queensland. I Received 31 December 1984, revision accepted 20 April 1985. The subject of the present study, the first quantitative assessment of breeding of an Australian rainforest tree, was S. cormiflorum (F. Muell.) B. Hyland, a small subcanopy tree which commonly occurs in a variety of rainforest types between Townsville and Cooktown in north Queensland and again further north in the forests of the Mcllwraith and Iron ranges. It exists as two forms, a small (up to 60 cm DBH) cauliflorous tree or a larger (up to 100 cm DBH) ramiflorous tree; the former occurring from sea level to 1200 m altitude but commoner at higher elevations, and the latter from sea level to 900 m and commoner at lower elevations. On a small scale it appears to be patchily distributed. All further references are to the cauliflorous form. The flowers are not numerous and are borne in small cymes on cauline excrescences that increase in size with age. They are large (calyx tube 7-20 mm long x 9-16 mm diameter, filaments 15-30 mm long) and creamy white with four small white petals and numerous stamens (a shaving brush type) and have a faint unpleasant smell. The majority project downward, but in big clusters they are forced to point in all directions. There are 3050 ovules in the ovary of the cauliflorous form and 90100 in the ramiflorous form. The fruits are large (30-60 mm diameter), red or white, and fleshy. The only recorded floral visitor is the nocturnal pygmy possum (Cercatetus caudatus) (Winter 1979), but the BIOTROPICA 18(2): 115-125 1986 115 This content downloaded from 157.55.39.17 on Fri, 02 Sep 2016 05:36:59 UTC All use subject to http://about.jstor.org/terms floral attributes of this tree are those that characterize plants with a bat-pollination syndrome (Faegri & van der Pijl 1971). The aims of this study were to determine by controlled pollination the degree of self-compatibility in S. cormiflorum, to assess the effectiveness of its floral visitors as pollinators and to relate this to floral biology, and to measure postfertilization fruit loss and net seed produc-