Bat Pollination of Weberocereus tunilla, an Epiphytic Rain Forest Cactus with Functional Flagelliflory

Abstract: We studied the pollination of the epiphytic cactus Weberocereus tunilla (Weber) Britton and Rose at the La Selva Biological Station in the Atlantic lowland rain forest of Costa Rica. The large, night-blooming, unpleasantly-smelling flowers were suspended on elongated main stems that hang down as much as 2 m below canopy tree branches, resulting in a unique form of flagelliflory. The only visitors to flowers were three species of glossophagine bats: Glossophaga commissarisi, Hylonycteris underwoodi and Lichonycteris obscura. Patterns of nectar secretion and concentration were found to be typical for bat-pollinated flowers. Flowering phenology and the occurrence of pollen on bats were recorded during a 1-yr period. Preliminary observations suggest that at least two other Costa Rican species of Weberocereus, W. biolleyi and W. trichophorus and possibly other species of the tribe Hylocereeae, are also pollinated by glossophagine bats.     

Pollination Biology of Piperaceae Species in Southeastern Brazil

Phenology, floral biology and breeding system are describedfor 14 Piperaceae species at two sites covered by semi-deciduousforest in southeastern Brazil. Flowering occurred continuouslythroughout the year, with a peak during the windy months. Allspecies had minute odorous and nectarless flowers visited byinsects; five of them showed a substantial degree of self-compatibility,and one was andromonoecious. Seven species were wind pollinated,and three were exclusively pollinated by insects. Flower visitorswere mainly hoverflies and bees. Copyright 2000 Annals of BotanyCompany Piper spp., Ottonia spp., Pothomorphe umbellata, pepper family, phenology, floral biology, breeding system, ambophily, semi-deciduous forest     

Acoustic traits of bat-pollinated flowers compared to flowers of other pollination syndromes and their echo-based classification using convolutional neural networks

Bat-pollinated flowers have to attract their pollinators in absence of light and therefore some species developed specialized echoic floral parts. These parts are usually concave shaped and act like acoustic retroreflectors making the flowers acoustically conspicuous to the bats. Acoustic plant specializations only have been described for two bat-pollinated species in the Neotropics and one other bat-dependent plant in South East Asia. However, it remains unclear whether other bat-pollinated plant species also show acoustic adaptations. Moreover, acoustic traits have never been compared between bat-pollinated flowers and flowers belonging to other pollination syndromes. To investigate acoustic traits of bat-pollinated flowers we recorded a dataset of 32320 flower echoes, collected from 168 individual flowers belonging to 12 different species. 6 of these species were pollinated by bats and 6 species were pollinated by insects or hummingbirds. We analyzed the spectral target strength of the flowers and trained a convolutional neural network (CNN) on the spectrograms of the flower echoes. We found that bat-pollinated flowers have a significantly higher echo target strength, independent of their size, and differ in their morphology, specifically in the lower variance of their morphological features. We found that a good classification accuracy by our CNN (up to 84%) can be achieved with only one echo/spectrogram to classify the 12 different plant species, both bat-pollinated and otherwise, with bat-pollinated flowers being easier to classify. The higher classification performance of bat-pollinated flowers can be explained by the lower variance of their morphology.     

Dyssochroma viridiflorum (Solanaceae): a reproductively bat-dependent epiphyte from the Atlantic rainforest in Brazil

Few Neotropical plant species seem to depend on the same animal type both for pollination and seed dispersal, and the known instances refer mostly to birds as the agents in these two phases of a plant reproductive cycle. Dyssochroma viridiflorum (Solanaceae), an epiphyte endemic to the Atlantic rainforest in south-eastern Brazil, was found to be visited by phyllostomid bats for nectar as well as for fruits, with the pollination and seed dispersal of the plant ensured by these flying mammals. The greenish flowers open at night and are visited by the nectar-feeding bat Glossophaga soricina, whereas the yellowish-white fruits are consumed by two species of fruit-eating bats, Carollia perspicillata and Sturnira lilium. Only clinging visits, an uncommon behavioural pattern for glossophagine bats while feeding on flowers, were recorded. The small seeds of D. viridiflorum are swallowed along with the fruit pulp and later defecated on the bats' flying pathways. It is suggested that species of Dyssochroma and two other solanaceous bat-pollinated genera, Merinthopodium and Trianaea, form a derived and bat-dependent clade within the Juanulloeae.     

Three pollination morphs in Cimicifuga simplex; incipient speciation due to inferiority in competition

Cimicifuga simplex, a Japanese herb, has three different pollinator guilds. At high altitudes it is pollinated by bumblebees. In lowlands, Impatiens textori, a much superior nectar-producer, outcompetes it for bumblebees. In sunny lowland habitats, flowers of a second morph produce a two-component fragrance which facilitates pollination by fritillaries. In experiments, the two components separately had limited effect on alighting rate, while application of both together elevated the attractiveness of non-fragrant flowers to the same as for naturally fragrant flowers. In heavily shaded lowland habitats, a third morph with nonfragrant flowers does not blom until after I. textori, and is pollinated by occasional bumblebees. The data strongly suggest that inferiority in competition has induced incipient speciation in this plant species.     

Sulphur-containing “perfumes” attract flower-visiting bats

 We tested the attractiveness of individual scent compounds of bat-pollinated flowers to their pollinators, small flower-visiting bats of the genus Glossophaga (Phyllostomidae). Twenty compounds belonging to four different chemical substance classes were tested, both in the laboratory and in the field. In the laboratory, the bats (Glossophaga soricina) approached odour sources spontaneously and without preceding experience. Without ever receiving any reward they preferred the scent of a sulphur-containing compound, dimethyl disulphide, to several other odour components emitted by bat-pollinated flowers, and to scentless controls. In the field, at La Selva station in the tropical lowland rain forest of Costa Rica, G. commissarisi were attracted by two sulphur-containing compounds, dimethyl disulphide and 2,4-dithiapentane, to visit artificial flowers filled with sugar water. Thus, in nectarivorous bats the sense of smell obviously plays an important role in searching for and localising food sources, and even single components of the scent bouquets of bat-pollinated flowers are attractive. The preference for sulphur-containing odours seems to be innate. Accepted: 9 November 1999     

Altitudinally restricted communities of Schizophoran flies in Queensland’s Wet Tropics: vulnerability to climate change

The Australian Wet Tropics World Heritage Area (WTWHA) contains a number of highland vertebrates predicted to face extinction due to a warming climate, but little is known about risks to invertebrates, which are vital to ecosystem health. This study investigates the distribution and abundance patterns of the Dipteran sub-order Schizophora along an altitudinal transect in the Carbine Uplands of the WTWHA using Malaise traps. The season of peak abundance changed with altitude, with highland abundance peaking in October, and lowland abundance peaking in April. There was a high level of species turnover with altitude, and some evidence for distinct low-, mid-, and high-elevation assemblages, with the high-elevation assemblage containing the most restricted species. We would expect this high-elevation assemblage to be at risk of local extinction with 2–3° of warming, and the mid-elevation assemblage to be at risk with 4–5° warming. Future work should continue sampling to confirm patterns presented here and to monitor range shifts with climate change. A highland species—Helosciomyza ferruginea Hendel is suggested as a good indicator species for such monitoring.     

Enclosure of Pollinated Flowers Weakens the Gametophytic Self-Incompatibility Response in Lycopersicon peruvianum

Williams, E. G. and Webb, M. C. 1987. Enclosure of pollinatedflowers weakens the gametophytic self-incompatibility responsein Lycopersicon peruvianum.— J. exp. Bot. 38: 1756–1764. Enclosure of pollinated flowers in a restricted airspace weakensthe gametophytic self-incompatibility response in the wild tomato,Lycopersicon peruvianum (L.) Mill. This 'closed box effect'occurs both for detached flowers in a semi-vitro system, andin situ for flowers attached to the plant. Entry of self pollentubes into ovules is observed in both systems. When pedicelsare treated with IAA to prevent abscission of flowers and poorlyfilled fruits, the method can be used to obtain selfed seedfrom mature flowers on the plant. Ethylene is detectable incontainers enclosing flowers, and is considered a more likelyagent of the effect than carbon dioxide or high relative humidity. Key words: Self-incompatibility, pseudo-self-compatibility, Lycopersicon peruvianum, ethylene     

Some Effects of Light Intensity, Daylength and Temperature on Flowering and Pollen Tube Growth in the Watermelon (Citrullus lanatus)

The effects of light and temperature on flowering and pollentube growth were studied in watermelon [Citrullus lanatus(Thunb.)Matsum. and Nakai, cv. Early Yates] plants grown in controlledenvironment cabinets. All female flowers were pollinated inone group of plants; none was pollinated in the other group. Temperature increase from 25 ^°C to 35 ^°C with daylengthof 14 h and light intensity of 32 klx caused increase in flowernumber per plant, proportion of male flowers, ovary length anddiameter, ovule number per ovary, rate of pollen tube growthand percentage of penetrated ovules at 24 hand 48 h after pollination.Very few flowers were produced at 40 ^°C, but there was ahigh proportion of male flowers. Increase in daylength from14 h to 24 h at 25 ^°C with light intensity of 32 klx alsoincreased number of flowers per plant, ovary length and diameterand number of ovules per ovary but sex expression and rate ofpollen tube growth were unaffected. Reduction in daylength from14 h to 8 hat 25 °C and light intensity of 32 klx and reductionin light intensity from 32 klx to 8 klx at 25 ^°C and 14h daylength both produced an increase in the percentage of immatureovules. The presence of fruit on the vine resulted in fewerflowers per plant and in reduced ovary legnth and diameter underall conditions tested. The results are discussed in relation to the fruiting responseof the plant.     

Pollinator Specificity and Convergence in Fly-pollinated Pleurothallis(Orchidaceae) Species: A Multiple Population Approach

We studied the floral biology of 12 populations of five rupicolousPleurothallis(Orchidaceae) species occurring in campo rupestre vegetationat nine localities in Brazil. All of these species are pollinatedby flies belonging to the families Chloropidae and Phoridae.In the five Pleurothallis species studied, all conspecific populationsattracted the same pollinator species. All pollinators werefemales; they laid eggs in flowers of the two nectarless species,but never in the flowers of nectar-presenting species. The twopairs ofPleurothallis species with similar flower morphologiesand odours attracted the same pollinators: P. johannensis -P. fabiobarrosii, pollinated by Tricimba sp. (Chloropidae) andP. teres - P. ochreata pollinated by Megaselia spp. (Phoridae).There was no overlap in the distribution of thePleurothallisspecies that shared pollinators. Despite similarities in floralmorphology and odour, genetic data show that these species pairsare not each other's closest relatives. We hypothesize thatthese similarities are due to convergence in allopatric speciesthat evolved similar pollination mechanisms. Conversely, thereare reasons to believe that adaptation to different pollinationmechanisms occurred in the closely related species P. johannensisand P. teres.Copyright 2001 Annals of Botany Company Pleurothallis, Orchidaceae, floral biology, fly-pollination, Chloropidae, Phoridae, pollinator specificity, campo rupestre     

The Bizarre Inflorescence of Norantea brasiliensis (Marcgraviaceae): Visits of Hovering and Perching Birds1

The pollination biology of Norantea brasiliensis (Marcgraviaceae) was studied in the rain forest of southeastern Brazil. This plant presents bizarre, brush-type racemous inflorescences bearing numerous flowers and extrafloral cup-shaped nectaries. Flower anthesis is diurnal, nectar production is continuous and copious, and the sticky pollen is readily removed by visitors during the first morning hours. The ruby-coloured inflorescences were visited by eight species of hummingbirds (Trochilidae), and 10 species of passerine birds (three Coerebidae and seven Thraupidae). Hummingbirds hovered while probing for nectar and touched flowers occasionally, whereas passerine birds perched and made contact with flowers habitually. Due to differences in flower-visiting and general foraging behaviour, perching birds act as better pollen vectors than hovering birds. The inflorescence of Norantea brasiliensis seems well fitted for pollination by passerine birds, and the hexose-dominated nectar supports this idea. Pollination syndrome trends within Marcgraviaceae may stem from insect-pollinated, condensed and spike-like inflorescences which would give rise to bird-pollinated, brush-type inflorescences. From the same basic condensed inflorescence, bat-pollinated umbelliform inflorescence may be derived from bird-pollinated, pendulous and corymb-like inflorescences. These postulated inflorescence types are found among the extant species of Marcgraviaceae.     

Nectar Sugar Composition in Relation to Pollination Syndromes in Sinningieae (Gesneriaceae)

A putative correlation between nectar sugar composition andpollination syndrome was evaluated in the tribe Sinningieae(Neotropical Gesneriaceae). Sucrose, fructose and glucose werequantified in the nectar of 45 species using high performanceanion-exchange chromatography. Representative species of thehummingbird, bee, bat and moth pollination syndromes were sampledin relation to their numeric importance in the tribe. In hummingbirdand bee flowers, which represent 95% of the species in Sinningieae,nectar was sucrose-dominant (ratio [sucrose]/[hexose] > 1).Sugar ratios below one were only found in the nectar of threespecies with moth and bat syndromes. Sugar concentration averaged23.9 ± 10.6% (wt/total wt) in hummingbird flowers and28.7 ± 10.6% in bee flowers, whereas diluted nectar (7.1± 3.4%) was restricted to bat flowers. Similarities inthe nectar of hummingbird and bee flowers contrast with thepresence of specific morphological traits associated with thesetwo syndromes, indicating that plant-pollinator relationshipsrely on flower display rather than on nectar characteristics.By contrast, distinct nectar chemistry is correlated with thebat syndrome in which a particularly low sucrose productionis responsible for hexose dominance. Copyright 2001 Annals ofBotany Company Nectar sugar composition, pollination syndrome, Sinningia, Gesneriaceae, Brazil     

Pollination biology and floral scent chemistry of the Neotropical chiropterophilous Parkia pendula

During the past several decades, the pollination biology of Old World plant species pollinated by flying foxes and of New World plants pollinated by highly specialized nectar-feeding glossophagine bats has been studied in detail. However, little is known about Neotropical plants that are pollinated by less specialized phyllostomid bats. Therefore, we studied the pollination biology of Parkia pendula , a tree pollinated by Phyllostomus . Flowers of P. pendula are arranged in capitula, and a capitulum is composed of approximately 800 hermaphrodite flowers and 260 sterile flowers. The sterile flowers produced a total of 7.4 ml nectar per night, with a sugar concentration of 14.95%, and proline as the dominant amino acid. Nectar production is highest at dusk and ends at 03:00 h. The floral scent is dominated by monoterpenoids (97.9%), with ( E )-β-ocimene being the dominant (84.0%) compound. No sulfur compounds were detected. The capitula are heavily visited by four species of phyllostomid bats, of which Phyllostomus discolor is the most abundant (98.9%). Nectar production per capitulum is within the reported range of nectar produced by this pantropical genus (5.0–8.0 ml). This genus-wide range seems to be optimal for attracting non-specialized nectar-feeding bats and forces them to visit capitula of several trees to satisfy their dietary needs, thus increasing the probability of cross-pollination for this plant.     

Prolongation of Embryo Sac Viability in Pear (Pyrus communis) Following Pollination or Treatment with Gibberellic Acid

Embryo sac development has been investigated in unpollinated,cross pollinated and gibberellic acid (GA₂) treated flowersof Pyrus communis L. While pollination and GA₃ treatments donot alter embryo sac development, they prolong embryo sac viability.In untreated unpollinated flowers, ovules degenerate between12 and 21 d after anthesis, while in cross pollinated and GA₃treated flowers this degeneration is postponed by about 10 d.Thus, in a cross pollinated flower this extends the period overwhich a successful fertilization can take place. This increasedperiod of viability is accompanied by an elongation of the embryosac itself. Elongation takes place two weeks prior to fertilizationin cross pollinated flowers. The extension of life span of embryo sacs following pollinationand treatment with gibberellic acid indicates that a stimulusinduced by ‘pollination’ could be mediated by GA₃Whatever its mechanism of operation, the prolongation of embryosac viability by pollination represents a selective advantage,in that the period at which the ovules are receptive to fertilizationmust be significantly extended. Embryo sac, gibberellic acid, Pyrus communis, pear, pollination     

Flower Morphology and Pollination Mechanism in Three Sympatric Goodyerinae Orchids from Southeastern Brazil

The pollination biology of Aspidogyne argentea, Aspidogyne longicornuandErythrodes arietina was studied in south-eastern Brazil.The three species are self-compatible but are pollinator-dependent.These three orchid species offer nectar as a reward to pollinatorsand flower visitors. The twoAspidogyne spp. have a dorsally-adhesiveviscidium, a feature which precludes pollinators other thanbees. Erythrodes arietina flowers are protandrous and show aventrally-adhesive viscidium. Aspidogyne argentea is visitedby halictid bees (here ranked as probable pollinators) and Hesperiidaebutterflies. Aspidogyne longicornu is pollinated by femalesof Euglossa(Euglossini) and visited by the hummingbird Phaethornisruber and by the euglossine bees Eulaema seabrai(females) andEulaema cingulata(males). The pollinarium adheres to the ventralsurface of the bee labrum, a very difficult place for bees toclean. The dorsally adhesive viscidium in Aspidogyne parallelsthat of the Spiranthinae genera of the so-called ‘Pelexiaalliance’. This condition seems to be particularly adaptativeunder conditions of low-frequency pollinator visits. Erythrodesarietina is pollinated by bees of the genera Paratetrapediaand Osiris which carry the pollinarium on the dorsal surfaceof their proboscis. Occasionally, these bees remove pollinariafrom their mouthparts using their forelegs. In general, in thespecies studied, a combination of both pollinator behaviourand morphological peculiarities promotes cross-pollination.Copyright 2001 Annals of Botany Company Orchids, Goodyerinae, Aspidogyne, Erythrodes, pollination, bees, hummingbirds, butterflies, morphology, viscidium, protandry     

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 Cipó (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.     

Covariation of flower traits and bird pollinator assemblages among populations of Kniphofia linearifolia (Asphodelaceae)

Globally, bird-pollinated plants can be separated into two groups, one consisting of species pollinated by specialist nectarivores, and the other of plants pollinated by occasional nectarivores. There are marked differences in nectar properties among the two groups, implying that there has been pollinator-mediated selection on these traits. This raises the possibility that variation in bird assemblages among populations of a plant species could lead to the evolution of intraspecific variation in floral traits. We examined this hypothesis in Kniphofia linearifolia, a common and widespread plant in southern Africa. Although bees are common visitors to flowers of this species, exclusion of birds from inflorescences led to significant reductions in seed set, indicating that the species is primarily bird-pollinated. We showed that bird pollinator assemblages differ markedly between five different populations of K. linearifolia, and that variation in flower morphology and nectar properties between these populations are associated with the dominant guild of bird visitors at each population. We identified two distinct morphotypes, based on corolla length, nectar volume and nectar concentration, which reflect the bird assemblages found in each type. Further work is needed to establish if a natural geographic mosaic of bird assemblages are the ultimate cause of differentiation in floral traits in this species.     

The power requirements (Glossophaginae: Phyllostomidae) in nectar-feeding bats for clinging to flowers

Nectar-feeding bats are the heaviest pollinators exploiting flowers in a hovering foraging mode. As hovering flight is considered to be energetically costly, clinging to flowers would be beneficial from an energetic perspective. I examined the rate of oxygen consumption and carbon dioxide release during clinging flower visitation in two 10-g Glossophaga soricina (Glossophinae: Phyllostomidae) to evaluate the potential energetic benefit of clinging versus hovering. In addition, I measured the duration of flower visits of free-ranging glossophagine bats to Markea neurantha (Solanaceae), a bat-pollinated plant that allows both hovering and clinging flower visitation. After 20 s of clinging to an artificial respiratory mask, the bats respiratory exchange ratio did not significantly deviate from 1, indicating the combustion of sugar. The average oxygen uptake rate equaled 1.39 ml min^–1 (±0.38 SD, STPD) and the carbon dioxide release rate equaled 1.33 ml min^–1 (±0.20 SD, STPD) for feeder visits longer than 20 s (n=79). Converting the oxygen uptake rate into power input yielded 0.49 W, less than a third of the power requirements for hovering for a 10-g bat. Free-ranging 10-g glossophagine bats exploited flowers of M. neurantha for, on average, 0.32 s ( ±0.14 SD, n=273) during hovering and for 0.39 s (±0.18 SD, n=152) during clinging visitations. A comparison between the power requirements of flower exploitation in differently sized bats indicates that clinging would benefit larger nectar-feeding bats to a greater extent than smaller species.Communicated by G. Heldmaier     

A Geographic Mosaic of Plant–Pollinator Interactions in the Eastern Caribbean Islands

The interplay between generalized and specialized plant–animal interactions is a core concept in understanding the evolution of mutualisms. Within the Eastern Caribbean, Heliconia bihai is a dominant forest species in the southern island of St. Vincent where H. caribaea is virtually absent. Heliconia caribaea is most common on the northern island of St. Kitts where H. bihai is restricted to the tops of the highest peaks. Both species are abundant on the central island of Dominica. We compared flowering patterns, nectar characteristics, and visitation frequency of hummingbirds in the two heliconias on the three islands to determine the extent of geographic variations in this plant–pollinator mutualism. The peak flowering season of the two heliconias was observed to be in April–May on all three islands with little within‐ and between‐island variations. Nectar production significantly varied between species and between islands. Visitation patterns by the principal hummingbird pollinators also varied between the islands: (1) on Dominica, only females of a single species of hummingbird pollinated the flowers of H. bihai (sexual specialization), whereas both sexes of the same hummingbird pollinated the flowers of H. caribaea (species specialization); (2) on St. Vincent, both sexes of the same hummingbird pollinated the flowers of H. bihai (species specialization); and (3) on St. Kitts, only females pollinated the flowers of H. bihai (sexual specialization), whereas several species of hummingbird visited the flowers of H. caribaea (species generalization). We propose that the Heliconia–hummingbird interactions in the Eastern Caribbean represent a geographically variable coevolutionary mosaic of plant–pollinator interactions.     

Oxypetalum banksii subsp. banksii: a taxon of Asclepiadaceae with an extragynoecial compitum

 The floral morphology of seven Oxypetalum species and, in particular, the spatial relationship between the five stigmatic chambers and two separate ovaries of their flowers with respect to transmission of the pollen tube are studied. In all species, except O. banksii subsp. banksii, floral morphology is similar to that in other Asclepiadeae, and the flowers pollinated with one pollinium develop only one follicle, which means compitum absence. In O. banksii subsp. banksii flowers, the secretory interstaminal tissue lines the inner walls of the stigmatic chambers as in the other species studied, but it also reaches the upper part of the inner surface of the filament tube, where it surrounds the styles, an unprecedented feature for Asclepiadaceae. This tissue secretes nectar and mucilage; the latter acts as transmitting medium for the growth of pollen tubes from pollinia inserted and hydrated in stigmatic chambers (“hyperstigmas”). Mucilage also functions as an extragynoecial compitum: in flowers pollinated with one pollinium both carpels develop into a follicle. Received August 28, 2001; accepted April 9, 2002 Published online: October 14, 2002 Addresses of the authors: Milene Faria Vieira (e-mail: mfvieira@mail.ufv.br), Departamento de Biologia Vegetal, Universidade Federal de Vi?osa, 36571-000, Vi?osa, Minas Gerais, Brazil. George John Shepherd, Departamento de Botanica, Instituto de Biologia, Universidade Estadual de Campinas, C.P. 6109, 13083-970, Campinas, S?o Paulo, Brazil.