Marlies Sazima

Specialization in Plant-Hummingbird Networks Is Associated with Species Richness, Contemporary Precipitation and Quaternary Climate-Change Velocity

Large-scale geographical patterns of biotic specialization and the underlying drivers are poorly understood, but it is widely believed that climate plays an important role in determining specialization. As climate-driven range dynamics should diminish local adaptations and favor generalization, one hypothesis is that contemporary biotic specialization is determined by the degree of past climatic instability, primarily Quaternary climate-change velocity. Other prominent hypotheses predict that either contemporary climate or species richness affect biotic specialization. To gain insight into geographical patterns of contemporary biotic specialization and its drivers, we use network analysis to determine the degree of specialization in plant-hummingbird mutualistic networks sampled at 31 localities, spanning a wide range of climate regimes across the Americas. We found greater biotic specialization at lower latitudes, with latitude explaining 20–22% of the spatial variation in plant-hummingbird specialization. Potential drivers of specialization - contemporary climate, Quaternary climate-change velocity, and species richness - had superior explanatory power, together explaining 53–64% of the variation in specialization. Notably, our data provides empirical evidence for the hypothesized roles of species richness, contemporary precipitation and Quaternary climate-change velocity as key predictors of biotic specialization, whereas contemporary temperature and seasonality seem unimportant in determining specialization. These results suggest that both ecological and evolutionary processes at Quaternary time scales can be important in driving large-scale geographical patterns of contemporary biotic specialization, at least for co-evolved systems such as plant-hummingbird networks.

Bat Pollination of the Passion Flower, Passiflora mucronata, in Southeastern Brazil

The pollination by bats of the passion flower, Passiflora mucronata, has been studied in southeastern Brazil. Experiments indicate that the flowers are self-incompatible. They are typically chiropterophilous being white, long-stalked, and exserted from the foliage canopy, opening after dark, and producing nectar throughout the night. The flower opens in less than 15 seconds and shows subsequent movements of the anthers and stigmas which results in a zygomorphic flower, an uncommon condition in Passiflora. The grouping of anthers and stigmas increases the deposition of pollen on the head of the visiting bat and offers the greatest stigmatic surface to be brushed with pollen already deposited on the bats head. Two species of phyllostomid bats, Glossophaga soticina (long-tongued) and Caorollia perspici iata (short-tongued), were observed pollinating the flowers. Other nocturnal visitors were sphingid and noctuid moths, and wasps, but all were ineffectual pollinators. The flowers of P. mucronata remain open until mid-morning and are visited by diurnal bees, wasps, butterflies, and hummingbirds, but it seems that only honeybees effect pollination, and their active foraging for pollen may prevent much of the potontial pollination by hummingbirds.

Processes entangling interactions in communities: forbidden links are more important than abundance in a hummingbird -plant network

Understanding the relative importance of multiple processes on structuring species interactions within communities is one of the major challenges in ecology. Here, we evaluated the relative importance of species abundance and forbidden links in structuring a hummingbird–plant interaction network from the Atlantic rainforest in Brazil. Our results show that models incorporating phenological overlapping and morphological matches were more accurate in predicting the observed interactions than models considering species abundance. This means that forbidden links, by imposing constraints on species interactions, play a greater role than species abundance in structuring the ecological network. We also show that using the frequency of interaction as a proxy for species abundance and network metrics to describe the detailed network structure might lead to biased conclusions regarding mechanisms generating network structure. Together, our findings suggest that species abundance can be a less important driver of species interactions in communities than previously thought.

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 bats 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.

The Saw-billed HermitRamphodon naevius and its flowers in southeastern Brazil

The large Saw-billed HermitRamphodon naevius and its foraging behaviour on a variety of ornithophilous flowers were studied at one site in the Atlantic rainforest in southeastern Brazil. The flower assemblage visited by this endemic hermit throughout the year is composed mainly by epiphytes and herbs, Bromeliaceae and Heliconiaceae being the staple foodplants. Most of the plant species present steady-state, long-tubed and high-reward flowers, and bloom sequentially. The Saw-billed Hermit is a year-round resident and traplining forager, behaves aggressively over its feeding routes, and excludes conspecifics and other hummingbird species from its main flower sources. This large hermit regularly visited and pollinated about 45 % of the native ornithophilous plants at the study site, thus acting as the major pollinator on this flower assemblage. Der große in Südbrasilien endemische Sägeschnabel-Schattenkolibri (Ramphodon naevius) und dessen Nahrungsverhalten an ornithophilen Blüten einer Pflanzengesellschaft des atlantischen Regenwaldes wurde untersucht. Die von ihm besuchten Blüten gehören hauptsächlich zu Kräutern und Epiphyten, wobei Bromeliaceen und Heliconiaceen die Hauptnahrungspflanzen bilden. Diese Arten haben eine lange Blühperiode und blühen konsekutiv. Die Blüten besitzen lange Kronröhren und sondern reichlich Nektar ab. Der standortstreue Kolibri hält eine bestimmte Route und einen Zeitplan bei der Nahrungsaufnahme ein; er verhält sich aggressiv sowohl gegenüber Individuen seiner eigenen Art als auch solchen anderer Kolibriarten, die er von den wichtigsten Nahrungsquellen vertreibt. Der Sägeschnabel-Schattenkolibri besuchte regelmäßig ca. 45 % der ornithophilen einheimischen Pflanzen einer bestimmten Gesellschaft. Damit ist er der wichtigste Bestäuber dieser Pflanzen.

The perfume flowers ofCyphomandra (Solanaceae): Pollination by euglossine bees, bellows mechanism, osmophores, and volatiles

The perfume syndrome and pollination by fragrance-collecting euglossine bees in the neotropic solanaceous genusCyphomandra was confirmed by field observations. In SE Brazil,C. sciadostylis was visited byEufriesea violaceae, andC. diploconos byEuglossa mandibularis; C. hartwegii was pollinated byEulaema meriana in Costa Rica. The primary attractant, fragrant droplets that ooze from the dorsally bulged connectives, is mopped up by the males with the forebasitarsi. Thereby, the poricidal thecae are inadvertently pushed causing the dry pollen to dust the bees sternum. The number and direction of the pollen jets are related to pollinator size and stigma structure. The flowers are homogamous, selfsterile, and last three days. The androecium is optically non-contrasting or has cryptic colour. Flowers ofC. sciadostylis andC. diploconos undergo a colour change and an almost three-fold increase in corolla size when scent production and visits cease. The dorsal papillar epidermis of the connective is underlain by a glandular parenchyma typical of osmophores. GC techniques revealed germacrene D as the main component in the mentholic scent ofC. sciadostylis, ipsdienol, heneicosane, and tricosane as dominant in the nutmeg-like scent ofC. diploconos, and benzyl acetate and benzyl alcohol in the sweet fragrance ofC. hartwegii. In all cases, these were accompanied by numerous minor components of heterogeneous chemical nature.—Pollen release by means of a peculiar pneumatic bellows mechanism appears as a necessary and probably ubiquitous feature ofCyphomandra. Even a slight pressure exerted upon the thin, elastic thecal walls blows pollen jets through the pores. Unusual anatomic changes accompany anther maturation. Initially voluminous parenchymatic locular intumescences (placentoids) contract completely during meiosis, then expand once more when the pollen is ripe, pushing the grains against the locular wall, and contract a second time, allowing air to enter the thecae.—Cyphomandra pinetorum was found to be exceptional in exhibiting a pollen flower syndrome, and not cryptical but optically contrasting yellow anthers, as known forSolanum.

POLLINATION BIOLOGY IN A TROPICAL HIGH-ALTITUDE GRASSLAND IN BRAZIL: INTERACTIONS AT THE COMMUNITY LEVEL1, 2

Abstract Surveys of local assemblages of plants and their pollinators are among the most useful ways to evaluate specialization in pollination and to discuss the patterns of plant-pollinator interactions among ecosystems. The high-altitude grasslands from southeastern Brazil constitute diminutive island-like formations surrounded by montane rainforests. We registered the floral traits of 124 species from the Serra da Bocaina grasslands (about 60% of the animal-pollinated species of this flora), and determined the pollinators of 106 of them. Asteraceae (40 species) and Melastomataceae (10 species) were prominent, while most families were represented by few species. The predominant floral traits were: dish or short-tubular shape; nectar as a reward; and greenish or violaceous colors. Pollinators were divided into eight functional groups (small bees, syrphids, other dipterans, etc.) and small bees, wasps, and large bees were the most important pollinators. Butterflies, beetles, and hummingbirds were poorly represented, and no bats, hawkmoths, or odor-collecting bees were detected. Plants were grouped in nine pollination systems, among which nectar-flowers pollinated by bees (28%), by wasps or wasps and flies (21%), or by several insect groups (19%) were the most representative. With regard to the degree of specialization, plant species were classified according to their number of pollinator groups. About 33% of the species were monophilous and 30% were oligophilous (i.e., pollinated by one or two functional groups, respectively). The remaining species were either polyphilous (17%) or holophilous (19%), a highly generalist system in which at least three groups act as indistinct pollinators. The general trends of the floral traits and plant-pollinator interactions at the Bocaina grasslands resemble those of biogeographic-connected ecosystems, such as the Venezuelan arbustal, and the Brazilian campo rupestre and cerrado. However, in the Bocaina grasslands, the mean number of pollinator types per plant was 2.09, one of the highest values obtained for worldwide floras. The origin of the high-altitude grasslands is linked to episodes of expansion and retraction due to glacial events. Such a situation may have favored species able to quickly occupy new habitats, including those that do not depend on a few highly specialized pollinators. The prevalence of Asteraceae may also be linked to more generalized pollination systems. Alternatively, some floral traits, such as spontaneous self-pollination and long-lived flowers, may be advantageous for species with more specialized systems in these grasslands with harsh climatic conditions and low rates of pollinator visitation.

The assemblage of flowers visited by hummingbirds in the "capões" of Southern Pantanal, Mato Grosso do Sul, Brazil

Summary Flower species visited by hummingbirds were studied over 13 months in 52 forested patches (“capoes”) in the seasonally flooded plains of Southern Pantanal, western Brazil. The size of the surveyed capoes ranged from 0.2 to 3.8 ha and the total sampled area measured 51.6 ha. We recorded 21 plant species, mainly herbs and climbers, whose flowers were visited by hummingbirds. Most of these plant species are regarded as non-ornithophilous (71.4%). The flowering peaks of the hummingbird-visited plants occurred at the end of the dry season and during the rainy season. The density of ornithophilous and non-ornithophilous flowers was higher during the rainy season and the dry season, respectively. Helicteres guazumaefolia is the most frequent ornithophilous species, bearing flowers throughout the year. Four hummingbird species were observed in the capoes. Their mean visiting rates for ornithophilous flowers (x = 0.019 ± 0.01 visits.min −1 .number of flowers −1 ) did not differ (P = 0.09, Kruskal-Wallis) from those for non-ornithophilous flowers (x = 0.025 ± 0.06 visits.min −1 .number of flowers −1 ). The most frequent visitor, Hylocharis chrysura was the only hummingbird recorded every month. It visited 20 plant species, 75% of which were non-ornithophilous, and seems to be the major pollinating bird in the capoes. The availability of H. guazumaefolia flowers throughout the year may favor the residence of this hummingbird in the study area.

Nectar by day and night:Siphocampylus sulfureus (Lobeliaceae) pollinated by hummingbirds and bats

Most species of the neotropical genusSiphocampylus are believed to be bird-pollinated. The pollination biology ofSiphocampylus sulfureus was studied in a montane region in SE Brazil. This species has features intermediate between ornithophilous and chiropterophilous syndromes: it presents a striking combination of yellowish flowers with strong odour (chiropterophilous features), and diurnal anthesis and sucrose-dominated nectar (ornithophilous features). Major pollinators were hummingbirds by day, and a phyllostomid bat by night.Siphocampylus sulfureus may be viewed as a recent derivate from the presumed ornithophilous stock within sect.Macrosiphon, and thus benefits from the activity of both diurnal and nocturnal vertebrate pollinators.

Pollination biology of two species ofKielmeyera (Guttiferae) from Brazilian cerrado vegetation

The pollination biology and breeding systems ofKielmeyera coriacea andK. speciosa, two sympatric woody species common in the cerrado vegetation of C. Brazil, were studied. Both species have similar nectarless, polystemonous “Papaver-type” flowers which are visited by a similar spectrum of insects, though they bloom in different seasons and are thus phenologically isolated. Large carpenter bees seem to be the most important pollinators and these and other bees effect “buzz pollen” retrieval despite the fact that anthers are not poricidal. Both species ofKielmeyera possess strong xenogamous breeding systems. The presence of staminate flowers and andromonoecy inK. coriacea, as well as the longevity ofK. speciosa flowers are discussed as alternative strategies to improve pollination success and reproductive efficacy.