Andrea A. Cocucci

Variation of Pollinator Assemblages and Pollen Limitation in a Locally Specialized System: The Oil-producing Nierembergia linariifolia (Solanaceae)

BACKGROUND AND AIMSnFew studies have examined the dynamics of specialist plant-pollinator interactions at a geographical scale. This knowledge is crucial for a more general evolutionary and ecological understanding of specialized plant-pollinator systems. In the present study, variations in pollinator activity, assemblage composition and pollen limitation were explored in the oil-producing species Nierembergia linariifolia (Solanaceae).nnnMETHODSnPollen limitation in fruit and seed production was analysed by supplementary hand pollination in five wild populations. Pollinator activity and identity were recorded while carrying out supplementary pollination to assess the effect of pollinators on the degree of pollen limitation. In two populations, pollen limitation was discriminated into quantitative and qualitative components by comparing supplementation and hand cross-pollination in fruit set and seed set. The effect of flower number per plant on the number of flowers pollinated per visitor per visit to a plant was examined in one of these populations as a possible cause of low-quality pollination by increasing geitonogamy.nnnRESULTS AND CONCLUSIONSnAlthough pollen limitation was evident along time and space, differences in magnitude were detected among populations and years that were greatly explained by pollinator activity, which was significantly different across populations. Floral display size had a significant effect on the visitation rate per flower. Limitation by quality clearly affected one population presumably due to a high proportion of geitonogamous pollen. The great inter-population variation in plant-pollinator interaction (both in pollinator assemblages composition and pollinator activity) and fitness consequences, suggests that this system should be viewed as a mosaic of locally selective processes and locally specialized interactions.

A simple floral fragrance and unusual osmophore structure in Cyclopogon elatus (Orchidaceae)

We studied gland morphology, anatomy and the chemical composition of the floral fragrance in the sweat bee-pollinated orchid Cyclopogon elatus. This is apparently the first such analysis for any Cyclopogon species, and one of very few studies in which both odour and osmophore are characterised in a nectar-rewarding orchid. Structures responsible for floral scent production were localised with neutral red staining and histochemical assays for lipids and starch. Their morphology and anatomy were studied with scanning electron microscopy and light microscopy thin sections, respectively. Fragrance samples were collected using SPME fibres and analysed with GC-MS. Anatomical evidence suggests that two parallel oval-shaped patches of unicellular trichomes on the abaxial surface of the labellum are osmophores. These are rich in stored lipids, while the parenchyma surrounding the vascular bundles contains starch. Only freshly opened flowers produced odours, while buds and withered flowers lacked scent. The chemical composition of the odour was dominated (>99.8%) by a single compound, trans-4,8-dimethyl-nona-1,3,7-triene (DMNT). Gland anatomy and position on the outside of the perianth are unusual for scent glands in general. The presence of DMNT, a nearly ubiquitous compound in herbivore-induced vegetative emissions and one of the major floral volatiles of Yucca, is not surprising in view of hypotheses on the evolutionary origin of flower scents, suggesting that wound volatiles are utilised as kairomonal attractants by florivores whose activities result in pollination.

Flower power: its association with bee power and floral functional morphology in papilionate legumes

BACKGROUND AND AIMSnA test was made of the hypothesis that papilionate legume flowers filter pollinators according to their ability to exert strength to open flowers to access rewards. In addition, interactions with pollen vectors were expected to explain the structural complexity of the architecture of these flowers since operative flower strength may be determined by a combination of morphological traits which form part of an intrafloral functional module.nnnMETHODSnSix papilionate species were studied: Collaea argentina, Desmodium uncinatum, Galactia latisiliqua, Lathyrus odoratus, Spartium junceum and Tipuana tipu. Measurements were made of the strength needed to open keels and the strength that pollinators were capable of exerting. Morphological traits of all petals were also measured to determine which of them could be either mutually correlated or correlated with operative strength and moment of strength and participated in a functional module.nnnKEY RESULTSnIt was observed that pollinators were capable in all cases of exerting forces higher and often several times higher than that needed to access floral rewards, and no association could be detected between floral operative strength and strength exerted by the corresponding pollinators. On the other hand, strong and significant correlations were found among morphometric traits and, of these, with operative strength and moment. This was particularly evident among traits of the keel and the wings, presumably involved in the functioning of the floral moveable mechanism.nnnCONCLUSIONSnThough visitors are often many times stronger than the operative strength of the flowers they pollinate, exceptionally weak bees such as Apis mellifera cannot open the strongest flowers. On the other hand, strong correlations among certain petal morphometric traits (particularly between the keel and wings) give support to the idea that an intrafloral module is associated with the functioning of the mechanism of these legume flowers. In addition, the highly significant correlations found across petals support the view of functional phenotypic integration transcending the ontogenetic organization of flower structure.

Functional morphology and wasp pollination of two South American asclepiads (Asclepiadoideae–Apocynaceae)

UNLABELLEDnBACKGROUND AND AIMS The extreme complexity of asclepiad flowers (Asclepiadoideae-Apocynaceae) has generated particular interest in the pollination biology of this group of plants especially in the mechanisms involved in the pollination processes. This study compares two South American species, Morrenia odorata and Morrenia brachystephana, with respect to morphology and anatomy of flower structures, dynamic aspects of the pollination mechanism, diversity of visitors and effectiveness of pollinators.nnnMETHODSnFloral structure was studied with fresh and fixed flowers following classical techniques. The pollination mechanism was studied by visiting fresh flowers in the laboratory with artificial pollinator body parts created with an eyelash. Morphometric and nectar measurements were also taken. Pollen transfer efficiency in the flowers was calculated by recording the frequency of removed and inserted pollinia. Visitor activity was recorded in the field, and floral visitors were captured for subsequent analysis of pollen loads. Finally, pollinator effectiveness was calculated with an index.nnnKEY RESULTSnThe detailed structure of the flowers revealed a complex system of guide rails and chambers precisely arranged in order to achieve effective pollinaria transport. Morrenia odorata is functionally specialized for wasp pollination, and M. brachystephana for wasp and bee pollination. Pollinators transport chains of pollinaria adhered to their mouthparts.nnnCONCLUSIONSnMorrenia odorata and M. brachystephana present differences in the morphology and size of their corona, gynostegium and pollinaria, which explain the differences in details of the functioning of the general pollination mechanism. Pollination is performed by different groups of highly effective pollinators. Morrenia species are specialized for pollination mainly by several species of wasps, a specialized pollination which has been poorly studied. In particular, pompilid wasps are reported as important pollinators in other regions outside South Africa. A putative new function of nectar in asclepiads is presented, as it would be contributing to the pollination mechanism.

Evidence of rodent pollination inCajophora coronata (Loasaceae)

Vegetative and floral features ofCajophora coronata (Loasaceae) suggest adaptations to pollination by rodents: (1) mammal guard represented by a covering of stinging hairs; (2) geoflory; (3) white corolla; (4) open flowers with copious low concentration nectar; (5) abundant pollen; (6) maximum pollen and nectar presentation in the afternoon hours and in the night. Palynological analysis revealed pollen loads ofC. coronata on the nostrils and whiskers of captured rodents (Graomys griseoflavus, fam.Muridae). Pollen and anther remains were also found in faeces sampled in the surroundings. Additional evidence includes rodent footprints obtained by placing smoked plates beneath the flowers, which revealed flower visitation during the night. These observations are to our knowledge the first evidence of flower visitation by rodents in South America and the first in the New World outside the range of flower bats and bat flowers.

The buck in the milkweed: evidence of male–male interference among pollinaria on pollinators

Direct physical confrontation among conspecifics for access to mates is a form of sexual selection well known among animals, but not thought to take place in plants. Consequently, no structures are known that can be considered as weapons that evolved under such confrontation. Pollinaria of milkweeds may physically compete for access to attachment points on the pollinators body, and occasionally pollinaria may link onto pre-existing pollinaria on a pollinator resulting in concatenation. We hypothesized that concatenation may result in interference between proximal and distal pollinaria, and that features of nonconcatenating pollinaria might be attributed to prevention of concatenation. We tested this by analyzing pollen donation efficiency, experimental manipulation of the phenotype and the phylogenetic patterns of co-occurrence of traits. It is shown that concatenation was able to diminish the reproductive performance of proximal pollinaria, that horns on pollinaria prevented concatenation, and that horn acquisition was correlated with a loss of concatenation. The experimental removal of horns in species that did not concatenate caused reversion to concatenation. The present work could be the first evidence of male physical struggles and of the acquisition of weapons related to these struggles, that are analogous to those known in animals.

The long and the short of it: a global analysis of hawkmoth pollination niches and interaction networks

1. Proboscis length has been proposed as a key dimension of plant pollination niches, but this niche space has not previously been explored at regional and global scales for any pollination system. Hawkmoths are ideal organisms for exploring pollinator niches as they are important pollinators in most of the biodiverse regions of the earth and vary greatly in proboscis length, with some species having the longest proboscides of all insects. 2. Using datasets for nine biogeographical regions spanning the Old and New World, we ask whether it is possible to identify distinct hawkmoth pollination niches based on the frequency distribution of proboscis length, and whether these niches are reflected in the depths of flowers that are pollinated by hawkmoths. We also investigate the levels of specialization in hawkmoth pollination systems at the regional and community level using data from interaction network studies. 3. We found that most regional hawkmoth assemblages have bimodal or multimodal distributions of proboscis length, and that these are matched by similar distributions of floral tube lengths. Hawkmoths, particularly those with longer proboscides, are polyphagous and at the network level show foraging specialization equivalent to or less than that of bees and hummingbirds. In the case of plants, shorter-tubed flowers are usually visited by numerous hawkmoth species, while those that are longer-tubed tend to exclude shorter-proboscid hawkmoths and thus become ecologically specialized on longer-proboscid hawkmoth species. Longer-tubed flowers tend to have greater nectar rewards and this promotes short-term constancy by long-proboscid hawkmoths. 4. Our results show that pollinator proboscis length is a key niche axis for plants and can account for patterns of evolution in functional traits such as floral tube length and nectar volume. We also highlight a paradoxical trend for nectar resource niche breadth to increase according to proboscis length of pollinators, while pollinator niche breadth decreases according to the tube length of flowers.

Functional modularity in a forcible flower mechanism: relationships among morphology, biomechanical features and fitness

Flowers may be interpreted as complex combinations of organs functionally coordinated to attract pollinators and to mechanically interact with the pollinator’s body, particularly when flower mechanisms are actively handled by pollinators. Thus, a functional modularity of traits in keel flowers (Fabaceae) was expected because of a compartmentalization between attraction and mechanical functions. To test this hypothesis, we used Collaea argentina, a Fabaceae that exhibits typical keel flowers. The force needed to open keels, the keel displacement angle and floral morphometric traits in 100 plants from a natural population were measured to detect floral characters correlated with the biomechanical variables. Furthermore, we examined the relationships among this functional module, biomechanical variables and female reproductive success to explore whether these traits are the targets of pollinator–mediated phenotypic selection, and used path analysis to examine the causal relationship among these variables. A functional module formed by two morphometric traits of the petals directly involved in the floral mechanism (keel and wings) was found, but no flag trait was involved in this module. Even though the functional module had a positive effect on force and there were significant relationships between the displacement angle and fruit set, no significant effect of force on female reproductive success was detected. These results question whether selection currently plays a role favouring the integration of this module, but this may be consistent with a past stabilizing selection on the force needed to open the keel.

Does hardness make flower love less promiscuous? Effect of biomechanical floral traits on visitation rates and pollination assemblages

Visitation rates and assemblage composition of pollinators have often been related to environmental, ecological and phenotypic variables. However, the interaction between flowers and pollinators has not been evaluated in a biomechanical context. Floral rewards in keel flowers (Fabaceae, Faboideae) are concealed behind four joined petals, the keel-wing unit, and are accessible only if pollinators open this unit by exerting force on it. Force needed to open the flower is expected to affect the interaction with pollinators because pollinators must invest time and energy to open the keels. Consequently, plants with stiff flowers should be expected to experience diminished visitation frequency, particularly by weak visitors. To test this expectation of diminished visitation rates and of assemblage composition biased by pollinator strength, we measured the force needed to open the keel flowers of five co-occurring legume species and, using a canonical correspondence analysis (CCA), we tested their association with pollinator visitation rates and assemblage composition. We additionally included a size flag variable in CCA to test the effect of attractiveness on pollinator visits. There was no association between flower stiffness and visitation frequency. According to the CCA, pollinator assemblage compositions were associated with the force needed to open the keel and not flag size. As a general pattern, weak flowers are pollinated by an uneven assemblage of weak bees while the stiffest flowers are pollinated by an even assemblage of large and strong bees. These results supports the idea that force has an effect in controlling pollinator assemblage composition.

The diversity and evolution of pollination systems in large plant clades: Apocynaceae as a case study

Abstract Background and Aims Large clades of angiosperms are often characterized by diverse interactions with pollinators, but how these pollination systems are structured phylogenetically and biogeographically is still uncertain for most families. Apocynaceae is a clade of >5300 species with a worldwide distribution. A database representing >10 % of species in the family was used to explore the diversity of pollinators and evolutionary shifts in pollination systems across major clades and regions. Methods The database was compiled from published and unpublished reports. Plants were categorized into broad pollination systems and then subdivided to include bimodal systems. These were mapped against the five major divisions of the family, and against the smaller clades. Finally, pollination systems were mapped onto a phylogenetic reconstruction that included those species for which sequence data are available, and transition rates between pollination systems were calculated. Key Results Most Apocynaceae are insect pollinated with few records of bird pollination. Almost three-quarters of species are pollinated by a single higher taxon (e.g. flies or moths); 7 % have bimodal pollination systems, whilst the remaining approx. 20 % are insect generalists. The less phenotypically specialized flowers of the Rauvolfioids are pollinated by a more restricted set of pollinators than are more complex flowers within the Apocynoids + Periplocoideae + Secamonoideae + Asclepiadoideae (APSA) clade. Certain combinations of bimodal pollination systems are more common than others. Some pollination systems are missing from particular regions, whilst others are over-represented. Conclusions Within Apocynaceae, interactions with pollinators are highly structured both phylogenetically and biogeographically. Variation in transition rates between pollination systems suggest constraints on their evolution, whereas regional differences point to environmental effects such as filtering of certain pollinators from habitats. This is the most extensive analysis of its type so far attempted and gives important insights into the diversity and evolution of pollination systems in large clades.