Thorn and hook ontogeny in Artabotrys hexapetalus (Annonaceae)

Artabotrys hexapetalus is widely planted in the tropics and is known as "climbing ylang-ylang," an ornamental liana or woody climber. New natural sprouts, or water shoots, and those induced by the damage of Hurricane Andrew (24 August 1992) were collected and fixed in formalin/acidic acid/alcohol. Seeds from these plants were planted and grown in a greenhouse where seedling morphology was observed and young material collected and fixed. The development of lateral plagiotropic and orthotropic shoots was studied using both epi-illumination light microscopy and scanning electron microscopy. A series of buds develops in the axils of leaves on the orthotropic shoot. At the lateral margins of the axillary shelf, plagiotropic shoots form that will develop into either vegetative shoots, or thorns, or sympodial shoots that bear hooks and flowers. In between the two marginal buds, a series of median vertical buds develop that either remain dormant or grow out as renewal orthotropic shoots. Previous work that suggested that the plagiotropic shoot buds were displaced out of the median vertical series of supernumerary buds is not supported. The sympodial development of plagiotropic branches as inflorescence hooks is documented.     

The evolution of key functional floral traits in the early divergent angiosperm family Annonaceae

Potential key functional floral traits are assessed in the species‐rich early divergent angiosperm family Annonaceae. Pollinators (generally beetles) are attracted by various cues (particularly visual, olfactory, and thermogenic), with pollinators rewarded by nectar (generally as stigmatic exudate), heat, and protection within the partially enclosed floral chamber. Petals sometimes function as pollinator brood sites, although this could be deceptive. Annonaceae species are self‐compatible, with outcrossing promoted by a combination of protogyny, herkogamy, floral synchrony, and dicliny. Pollination efficiency is enhanced by pollen aggregation, changes in anthesis duration, and pollinator trapping involving a close alignment between petal movements and the circadian rhythms of pollinators. Most Annonaceae flowers are apocarpous, with syncarpy restricted to very few lineages; fertilization is therefore optimized by intercarpellary growth of pollen tubes, either by stigmatic exudate (suprastylar extragynoecial compitum) or possibly the floral receptacle (infrastylar extragynoecial compitum). Although Annonaceae lack a distinct style, the stigmas in several lineages are elongated to form “pseudostyles” that are hypothesized to function as sites for pollen competition. Flowers can be regarded as immature fruits in which the ovules are yet to be fertilized, with floral traits that may have little selective advantage during anthesis theoretically promoting fruit and seed dispersal. The plesiomorphic apocarpous trait may have been perpetuated in Annonaceae flowers as it promotes the independent dispersal of fruit monocarps (derived from separate carpels), thereby maximizing the spatial/temporal distance between seedlings. This might compensate for the lack of genetic diversity among seeds within fruits arising from the limited diversity of pollen donors.     

Correlated evolution of diaspore traits and potential frugivore-mediated selection in a fleshy-fruited tropical lineage (Artabotrys,Annonaceae)

Dispersal syndromes are often defined by reference to fruit traits that are associated with distinct frugivore guilds. Studies rarely examine the relationship between seed traits and frugivores or test the alternative hypothesis that traits are shaped by climatic variables. We assess whether the evolution of seed size and physical defense are correlated with dispersal-related traits and climatic variables in Artabotrys, a fleshy-fruited tropical lineage. Diaspore traits and WorldClim bioclimatic variables were compiled for 43 species. Correlated evolution was evaluated using phylogenetic regression and model-fitting approaches. The best-fitting multioptima Ornstein-Uhlenbeck model suggests that lineages with smooth testa and thin pericarp (SP) have evolved toward smaller seeds with a thinner testa, whereas lineages with rough testa and/or thick pericarp have evolved toward larger seeds with a thicker testa. A smooth testa facilitates spitting and/or swallowing of intact seeds while fruits with thin pericarp may be preferentially consumed by frugivores with less destructive oral processing, enabling lower investment in seed physical defense in SP lineages. Moreover, small seeds are more likely to be swallowed intact with a food bolus. The effect of climate on seed size and physical defense is equivocal and warrants further investigation.     

Convergent evolution of floral shape tied to pollinator shifts in Iochrominae (Solanaceae)*

Flower form is one of many floral features thought to be shaped by pollinator‐mediated selection. Although the drivers of variation in flower shape have often been examined in microevolutionary studies, relatively few have tested the relationship between shape evolution and shifts in pollination system across clades. In the present study, we use morphometric approaches to quantify shape variation across the Andean clade Iochrominae and estimate the relationship between changes in shape and shifts in pollination system using phylogenetic comparative methods. We infer multiple shifts from an ancestral state of narrow, tubular flowers toward open, bowl‐shaped, or campanulate flowers as well as one reversal to the tubular form. These transitions in flower shape are significantly correlated with changes in pollination system. Specifically, tubular forms tend to be hummingbird‐pollinated and the open forms tend to be insect‐pollinated, a pattern consistent with experimental work as well as classical floral syndromes. Nonetheless, our study provides one of the few empirical demonstrations of the relationship between flower shape and pollination system at a macroevolutionary scale.     

Contrasting pollination ecology of Disepalum species (Annonaceae): evolutionary loss of the floral chamber and partial breakdown of protogyny associated with a shift in pollination system

Disepalum comprises two monophyletic sister subgenera, Enicosanthellum and Disepalum, with strikingly different floral morphologies: the former has two whorls of unfused sepals, forming a partially enclosed floral chamber, whereas the latter possesses a single whorl of congenitally fused petals and lacks a floral chamber. The pollination ecologies of representative species are reported, including assessments of floral phenology, pollinators and floral thermogenesis. Disepalum pulchrum (subgenus Enicosanthellum) has hermaphroditic flowers with a pollination chamber and is protogynous with prolonged anthesis; it is pollinated by nitidulid beetles and drosophilid flies. Disepalum anomalum (subgenus Disepalum) is also hermaphroditic with prolonged anthesis, but has incomplete protogyny due to overlapping pistillate and staminate phases; it is pollinated by meliponine bees, which are attracted by the pollen, but which are only able to transfer pollen to receptive stigmas during the overlap phase. Alternative evolutionary hypotheses are evaluated, including the possibility that the ancestor of the subgenus Disepalum lineage may have experienced a profound genetic mutation, possibly involving genes responsible for organ merism and fusion, resulting in the loss of the pollination chamber and hence favouring different floral visitors. The breakdown in protogyny required for effective pollination is likely to have had significant ramifications on population genetic diversity.     

Pollination of strawberry by the stingless bee,Trigona minangkabau,and the honey bee,Apis mellifera: An experimental study of fertilization efficiency

To know basic information about the stingless bee, Trigona minangkabau, and the European honey bee, Apis mellifera, as pollinator of strawberry, we set three greenhouse areas: the honey bee introduced area, the stingless bee introduced area and the control area. Foraging and pollination efficiencies of the two bee species were studied comparatively. During the experimental period (10 days), the stingless bee foraged well and the nest weight did not change, though the honey bee often foraged inefficiently and the nest weight decreased by 2 kg. The average nectar volume of a flower was lower in the honey bee area (0.02 μl) and nearly the same in the other two areas (0.1 μl). We make a numerical model to describe pollination and fertilization process. This model shows that one visit of the honey bee pollinated 11% of achenes and one visit of the stingless bee did 4.7% on average and that 11 visits of the honey bee or 30 visits of the stingless bee are required per flower to attain normal berry (fertilization rate, 87%). In this study, the rate of deformed berries in the stingless bee area (73%) was lower than that of the control area (90%), but higher than that of the honey bee area (51%). From our numerical model, we conclude the stingless bee could pollinate strawberry as well as the honey bee if we introduced 1.8 times of bees used in this experiment.     

A new species of Annona (Annonaceae) from the northeastern Guayana Shield

Annona prevostiae, a new species from the northeastern margin of the Guayana Shield, is described and illustrated.     

Floral ontogeny of Annonaceae: evidence for high variability in floral form

Background and Aims

Annonaceae are one of the largest families of Magnoliales. This study investigates the comparative floral development of 15 species to understand the basis for evolutionary changes in the perianth, androecium and carpels and to provide additional characters for phylogenetic investigation.

Methods

Floral ontogeny of 15 species from 12 genera is examined and described using scanning electron microscopy.

Key Results

Initiation of the three perianth whorls is either helical or unidirectional. Merism is mostly trimerous, occasionally tetramerous and the members of the inner perianth whorl may be missing or are in double position. The androecium and the gynoecium were found to be variable in organ numbers (from highly polymerous to a fixed number, six in the androecium and one or two in the gynoecium). Initiation of the androecium starts invariably with three pairs of stamen primordia along the sides of the hexagonal floral apex. Although inner staminodes were not observed, they were reported in other genera and other families of Magnoliales, except Magnoliaceae and Myristicaceae. Initiation of further organs is centripetal. Androecia with relatively low stamen numbers have a whorled phyllotaxis throughout, while phyllotaxis becomes irregular with higher stamen numbers. The limits between stamens and carpels are unstable and carpels continue the sequence of stamens with a similar variability.

Conclusions

It was found that merism of flowers is often variable in some species with fluctuations between trimery and tetramery. Doubling of inner perianth parts is caused by (unequal) splitting of primordia, contrary to the androecium, and is independent of changes of merism. Derived features, such as a variable merism, absence of the inner perianth and inner staminodes, fixed numbers of stamen and carpels, and capitate or elongate styles are distributed in different clades and evolved independently. The evolution of the androecium is discussed in the context of basal angiosperms: paired outer stamens are the consequence of the transition between the larger perianth parts and much smaller stamens, and not the result of splitting. An increase in stamen number is correlated with their smaller size at initiation, while limits between stamens and carpels are unclear with easy transitions of one organ type into another in some genera, or the complete replacement of carpels by stamens in unisexual flowers.     

Impact of the introduced honey bee (Apis mellifera) (Hymenoptera: Apidae) on native bees: A review

Abstract Interspecific competition for a limited resource can result in the reduction of survival, growth and/or reproduction in one of the species involved. The introduced honey bee (Apis mellifera Linnaeus) is an example of a species that can compete with native bees for floral resources. Often, research into honey bee/native bee competition has focused on floral resource overlap, visitation rates or resource harvesting, and any negative interaction has been interpreted as a negative impact. Although this research can be valuable in indicating the potential for competition between honey bees and native bees, to determine if the long‐term survival of a native bee species is threatened, fecundity, survival or population density needs to be assessed. The present review evaluates research that has investigated all these measurements of honey bee/native bee competition and finds that many studies have problems with sample size, confounding factors or data interpretation. Guidelines for future research include increasing replication and using long‐term studies to investigate the impact of both commercial and feral honey bees.     

ent-Kaurane diterpenes from the stem bark of Annona vepretorum (Annonaceae) and cytotoxic evaluation

This work describes a novel ent-kaurane diterpene, ent-3β-hydroxy-kaur-16-en-19-al along with five known ent-kaurane diterpenes, ent-3β,19-dihydroxy-kaur-16-eno, ent-3β-hydroxy-kaur-16-eno, ent-3β-acetoxy-kaur-16-eno, ent-3β-hydroxy-kaurenoic acid and kaurenoic acid, as well as caryophyllene oxide, humulene epoxide II, β-sitosterol, stigmasterol and campesterol from the stem bark of Annona vepretorum Mart. (Annonaceae). Cytotoxic activities towards tumor B16-F10, HepG2, K562 and HL60 and non-tumor PBMC cell lines were evaluated for ent-kaurane diterpenes. Among them, ent-3β-hydroxy-kaur-16-en-19-al was the most active compound with higher cytotoxic effect over K562 cell line (IC₅₀ of 2.49 μg/mL) and lower over B16-F10 cell line (IC₅₀ of 21.02 μg/mL).     

Cockroach pollination and breeding system of Uvaria elmeri (Annonaceae) in a lowland mixed-dipterocarp forest in Sarawak

Tropical forest plants are known to be pollinated by a diverse array of animals. Here we report on the pollination of a woody climber species, Uvaria elmeri (Annonaceae), by cockroaches in a lowland mixed-dipterocarp forest in Sarawak, Malaysia. To the best of our knowledge, this is the first report of pollination by cockroaches. The cauliflorous flowers in the understory are protogynous and bloomed for 50 h. An odor similar to decayed wood or a mushroom was secreted by flowers and was stronger during the male stage. Pollinators were cockroaches (Blattellidae) and drosophilid flies (Drosophilidae). Cockroaches, the main pollinators, visited flowers during both female and male stages at night, feeding on stigmatic exudate and pollen. Drosophilids, the secondary pollinators. mainly visited female-stage flowers during daytime, fed on stigmatic exudate. and laid eggs on stigmas. Neither autogamy nor self-compatibility was observed. Fruit production appeared to be pollen-limited. The fruit set, which was 2% of flowers in natural condition, was significantly lower than the 30% fruit set obtained by artificial cross-pollination. We discuss the traits of cockroaches as pollinators and the breeding system of U. elmeri.     

A two-pollinator model for the evolution of floral complexity

For a new, more complex floral form to become established in a population it must overcome the problem of frequency-dependent constancy to successfully attract pollinators. This may be achieved by complex floral forms offering absolute greater rewards than the simpler forms, or by complex flowers offering a higher probability of being rewarding because fewer pollinators are able to visit them. In this paper we examine the effect of three pollinator foraging strategies on the ratio of flights within and between floral morphs and hence on the probability of a new morph establishing in a population without offering a greater reward. We incorporate pollinator behaviour based around observations of two pollinator species systems into three models of competition for pollinators. In the first model the constancy of the pollinator of the new floral morph is a function only of the foraging strategy of the existing pollinator of the original floral morph. In the next model the constancy of the second pollinator is determined by the number of rewarding flowers of each floral morph left by the original pollinator and in the third model it is determined by the ratio of rewarding flowers of each morph left by the original pollinator. The results demonstrate that under conditions of intense competition for pollinators, new, more complex floral forms are indeed able to attract high levels of constant pollinators without offering intrinsically higher rewards. However, for this to occur constancy in one of the pollinators must be a function of the ratio of rewarding to non-rewarding flowers of both floral forms. One prediction from our results is that sympatric speciation of floral complexity based on a higher probability of reward is more likely to occur in flowers offering rewards of pollen rather than nectar. This is because the cost of visiting non-rewarding flowers is usually higher where the reward is pollen rather than nectar. We also predict that complex flowers occurring at low frequency, which offer rewards of nectar, may need intrinsically greater rewards if they are to successfully attract pollinators.     

Isoquinoline alkaloids from the leaves of Xylopia laevigata (Annonaceae)

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Relationships between floral morphology and pollinator fauna in insular and main island populations of Hosta longipes (Liliaceae)

We compared the floral morphologies and pollinator fauna and morphologies of Hosta longipes var. longipes on the main Japanese island of Honshu and var. latifolia on the Izu Islands to examine the differentiation processes of H. longipes in the island system. The corolla length was shorter on the southern Izu Islands than on the main island and northern Izu Islands. However, the size of other flower parts of H. longipes did not simply decrease across main island Honshu and the Izu Islands, unlike other Izu endemic plant species studied previously. Instead, the floral morphology showed a complicated variation pattern. Pollinator fauna of H. longipes on the Izu Islands varied more widely than those on the main island. The diverse pollinator fauna may have influenced the morphological differentiation of H. longipes on these islands.     

Nesting biology of three Megachile (Hymenoptera: Megachilidae) species from Eastern Amazonia,Brazil

Megachile Latreille is a conspicuous genus of solitary bees distributed worldwide. However, the biology of tropical species is still little known. We present data on biology of Megachile brasiliensis Data Torre, Megachile sejuncta Cockerell and Megachile stilbonotaspis Moure found in two remnants of eastern Amazonian forest in northeastern Brazil. The study was conducted using the trap-nest methodology in two different areas during four periods. We collected a total of 24 nests of M. brasiliensis, 26 of M. sejuncta and 28 of M. stilbonotaspis. The differential abundance of collected nests may reflect the population size in each sampled place. The nesting activity was concentrated mainly between July and January and species presented a multivoltine pattern, except for M. sejuncta, which was partly univoltine. Assessed pollen use showed a predominant use of Attalea sp. (Arecaceae) and, for M. stilbonotaspis, Tylesia sp. and Lepidaploa sp. (Asteraceae). Babassu is a very common palm in the studied areas and the studied species seem to have a strong link with it. We also reported change of pollen use by M. sejuncta, probably due to competition with M. brasiliensis, which may have influenced the biased sex ratio observed in M. sejuncta toward males. Parasites reported here were also recorded for other Megachile species, such as Coelioxys, Brachymeria, Meloidae and Pyralidae species. Mites were observed in association with M. stilbonotaspis. The data presented here set up a background that encourages new studies on the ecology of these three Amazonian species, providing tools for proper biodiversity management and conservation.     

Effects of nectar robbing on pollinator behavior and plant reproductive success of Pitcairnia angustifolia (Bromeliaceae)

Nectar robbers may have direct and indirect effects on plant reproductive success but the presence of nectar robbing is not proof of negative fitness effects. We combined census data and field experiments to disentangle the complex effects of nectar robbing on nectar production rates, pollinator behavior, pollen export, and female reproductive success of Pitcairnia angustifolia. Under natural conditions flowers were visited by four different animal species including a robber‐like pollinator and a secondary robber. Natural levels of nectar robbing ranged from 40 to 100%. Natural variation in nectar robbing was not associated with fruit set in any year whereas seed set was weakly positively associated for 1 year only. Artificial nectar robbing did not increase nectar production or concentration, did not affect the behavior of long‐billed hummingbirds, and when faced with artificially robbed flowers, these visitors behaved as secondary nectar robbers. The number of stigmas within a patch that received pollen dye analogs and the average distance traveled by these analogs were not significantly different between robbing treatments (robbed flowers versus unrobbed flowers), but the maximum distance traveled by these pollen analogs was higher when nectar robbing was not prevented. Overall, the proportion of robbed flowers on an inflorescence had a neutral effect to a weak positive effect on the reproduction of individual plants (i.e. positive association between nectar robbing and fruit set in 2002) even when it clearly changed the behavior of its most efficient pollinator potentially increasing the frequency of nectar robbing within a plant.     

Studies in Annonaceae. XXVIII. Macromorphological variation of recent invaders in northern Central America: the case of Malmea (Annonaceae)

Cluster analysis is used to reveal patterns of macromorphological variation in a species complex of Malmea (Annonaceae) distributed in eastern Mexico, Guatemala, Belize, and Honduras. Of 53 characters, 24 are important for the clustering of 238 herbarium specimens into 12 clusters. No cluster is exclusively specified by any character or combination of characters. Neither can any geographical pattern be detected, except for the clustering of specimens from Los Tuxtlas Tropical Biological Station, Veracruz. A new subspecies from this area, M. depressa subsp. abscondita, is described. Malmea gaumeri and M. leiophylla are brought into synonymy with M. depressa. Distribution patterns of Mexican and Central American taxa of Malmea are largely concordant with those of South American taxa, which spread into Cental America after the Pliocene closure of the Isthmus of Panama. A phytogeographical novelty is presented, however, as the distribution of M. depressa subsp. abscondita within the Sierra de los Tuxtlas shows an hitherto unknown pattern: the new subspecies is distributed only on the northeastern slopes of this mountain range, and is geographically separated from M. depressa subsp. depressa, which occurs only on the southwestern slopes.