No abstract

A major challenge in evolutionary ecology is to understand how co-evolutionary processes shape patterns of interactions between species at community level. Pollination of flowers with long corolla tubes by long-tongued hawkmoths has been invoked as a showcase model of co-evolution. Recently, optimal foraging models have predicted that there might be a close association between mouthparts' length and the corolla depth of the visited flowers, thus favouring trait convergence and specialization at community level. Here, we assessed whether hawkmoths more frequently pollinate plants with floral tube lengths similar to their proboscis lengths (morphological match hypothesis) against abundance-based processes (neutral hypothesis) and ecological trait mismatches constraints (forbidden links hypothesis), and how these processes structure hawkmoth-plant mutualistic networks from five communities in four biogeographical regions of South America. We found convergence in morphological traits across the five communities and that the distribution of morphological differences between hawkmoths and plants is consistent with expectations under the morphological match hypothesis in three of the five communities. In the two remaining communities, which are ecotones between two distinct biogeographical areas, interactions are better predicted by the neutral hypothesis. Our findings are consistent with the idea that diffuse co-evolution drives the evolution of extremely long proboscises and flower tubes, and highlight the importance of morphological traits, beyond the forbidden links hypothesis, in structuring interactions between mutualistic partners, revealing that the role of niche-based processes can be much more complex than previously known.

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 biogeographicconnected 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 Malpiguiaceae species studied are pollinator-dependent, as spontaneous self-pollination is limited by herkogamy, protogyny and the stigmatic cuticle. Both the oil- and pollen-collecting behaviours of the pollinators favour the rupture of the stigmatic cuticle and the deposition of pollen on or inside the stigmas. As fruit-set rates in natural conditions are low, population fragmentation may have limited the sexual reproduction of these species.

The pollination biology of Aechmea pectinata (Bromeliaceae) was studied in a submontane rainforest in south-eastern Brazil. This species has a mainly clumped distribution and its aggregated individuals are likely to be clones. From October to January, during the flowering period, the distal third of its leaves becomes red. The inflorescence produces 1-15 flowers per day over a period of 20-25 d. The flowers are inconspicuous, greenish-white coloured, tubular shaped with a narrow opening, and the stigma is situated just above the anthers. Anthesis begins at 0400 h and flowers last for about 13 h. The highest nectar volume and sugar concentration occur between 0600 and 1000 h, and decrease throughout the day. Aechmea pectinata is self-incompatible and therefore pollinator-dependent. Hummingbirds are its main pollinators (about 90 % of the visits), visiting flowers mainly in the morning. There is a positive correlation between the number of hummingbird visits per inflorescence and the production of nectar, suggesting that the availability of this resource is important in attracting and maintaining visitors. The arrangement of the floral structures favours pollen deposition on the bill of the hummingbirds. Flowers in clumps promote hummingbird territoriality, and a consequence is self-pollination in a broader sense (geitonogamy) as individuals in assemblages are genetically close. However, trap-lining and intruding hummingbirds promote cross-pollination. These observations suggest that successful fruit set of A. pectinata depends on both the spatial distribution of its individuals and the interactions among hummingbirds.