Phenotypic selection patterns in a hybrid zone between two Calceolaria species with contrasting pollinators: insights from field surveys and fitness assessments.

Hybrid zones provide natural experimental settings to test hypotheses about species divergence. We concentrated on a hybrid swarm in which oil-collecting bees and flower-pecking birds act as pollinators of two Calceolaria species. We asked whether both pollinators contributed to flower divergence by differentially promoting prezygotic fitness at the phenotypic extremes that represent parentals. We studied pollinator-mediated selection on phenotypic traits critical in plant-pollinator mechanical interaction, namely plant height, reward-to-stigma distance, and flower shape. We utilised the quantity and quality of pollen deposited as fitness measures and distinguished between the contribution of the two pollinator types. Results showed uni- and bivariate disruptive selection for most traits through pollen grains deposited by both pollinators. Bird-mediated fitness favoured low plants with a long reward-to-stigma distance and a straight corolla, while bee-mediated fitness favoured tall plants with a short reward-to-stigma distance and curved corolla. In addition, stabilising selection at one end of the phenotypic range showed a bird-mediated reproductive asymmetry within the swarm. The disruptive pattern was countered, albeit weakly, by hybrids receiving higher-quality pollen on the stigmas. Results suggest that pollinator-mediated selection promotes divergence of integrated flower phenotypes mechanically adjusted either to bees or birds underscoring the importance of pollinator specialisation in diversification.

Darwin's inflorescence syndrome is indeed associated with bee pollination.

KEY MESSAGE: A relationship between vertical acropetal inflorescences with protandrous flowers and bee pollination was hypothesized by Darwin back in 1877. Here we provide empirical evidence supporting this association across the angiosperms. Plant reproduction is not only determined by flower traits but also by the arrangement of flowers within inflorescences. Based on his observations of the orchid Spiranthes autumnalis, Darwin proposed in 1877 that bee-pollinated plants presenting protandrous flowers on vertical acropetal inflorescences, where proximal flowers open first, can exploit the stereotypical foraging behavior of their pollinators (i.e., upward movement through the inflorescence) to promote pollen exportation and reduce self-pollination. In these inflorescences, male-phase flowers lie spatially above female-phase flowers. To examine this untested hypothesis, we compiled literature information from 718 angiosperms species and evaluated the association between vertical acropetal inflorescences with protandrous flowers and bee pollination within a phylogenetic comparative framework. Results reveal that this type of inflorescence is indeed more common in species pollinated by bees. Moreover, this association does not seem to be weakened by the presence of alternative self-pollination avoidance mechanisms, like self-incompatibility, suggesting that this inflorescence type benefits mainly male rather than female fitness. Other inflorescence types placing male-phase flowers above female-phase flowers, e.g., vertical basipetal inflorescences with protogynous flowers, do not provide strong evidence of a differential association with pollination by bees. Female-biased nectar production in vertical acropetal inflorescences with protandrous flowers may reinforce the behavior of bees to fly upwards, rendering Darwin's configuration more adaptive than other inflorescence configurations.

Osmophores and petal surface traits in Bignonieae species.

This study characterizes the osmophores and corolla traits in 18 species of Bignonieae Dumort., a Bignoniaceae tribe occurring in the Cerrado, a neotropical savanna in Brazil. To detect osmophore distribution, whole, newly opened flowers were immersed in Neutral Red Solution. Samples from the corolla tube and lobes were also fixed and analyzed micromorphologically, anatomically, and histochemically. The osmophores showed six markedly different distribution patterns that were not clearly associated with histological features. In most species, osmophores comprised papillose secretory epidermises and a few layers of subepidermal parenchyma. Starch grains, lipid droplets, and terpenes were detected in osmophores. An ornamented cuticle, cuticular folds, glandular and non-glandular trichomes, raised stomata and epicuticular wax granules are common traits in the species studied and may be useful in determining the taxonomy of the group. We found that 94% of the species visited by bees had papillose epidermises while the single hummingbird-pollinated species presented a flattened epidermis. Variations in osmophore pattern among species visited by bees, including variations within the same plant genus, are novel finding. Additionally, the Bignonieae species visited by bees presented a textured corolla surface, which has been reported as facilitating bee attachment and movement towards the floral resource. Future studies with a greater number of Bignonieae species and more detailed pollinator behavioral assays may help in the interpretation of the variations in corolla traits and functional relationships between flowers and pollinators.

To each their own! Nectar plasticity within a flower mediates distinct ecological interactions.

Nuptial and extranuptial nectaries are involved in interactions with different animal functional groups. Nectar traits involved in pollination mutualisms are well known. However, we know little about those traits involved in other mutualisms, such as ant-plant interactions, especially when both types of nectaries are in the same plant organ, the flower. Here we investigated if when two types of nectaries are exploited by distinct functional groups of floral visitors, even being within the same plant organ, the nectar secreted presents distinct features that fit animal requirements. We compared nectar secretion dynamics, floral visitors and nectar chemical composition of both nuptial and extranuptial nectaries in natural populations of the liana Amphilophium mansoanum (Bignoniaceae). For that we characterized nectar sugar, amino acid and specialized metabolite composition by high-performance liquid chromatography. Nuptial nectaries were visited by three medium- and large-sized bee species and extranuptial nectaries were visited mainly by ants, but also by cockroaches, wasps and flies. Nuptial and extranuptial nectar differed regarding volume, concentration, milligrams of sugars per flower and secretion dynamics. Nuptial nectar was sucrose-dominated, with high amounts of γ-aminobutyric acid and ß-aminobutyric acid and with theophylline-like alkaloid, which were all exclusive of nuptial nectar. Whereas extranuptial nectar was hexose-rich, had a richer and less variable amino acid chemical profile, with high amounts of serine and alanine amino acids and with higher amounts of the specialized metabolite tyramine. The nectar traits from nuptial and extranuptial nectaries differ in energy amount and nutritional value, as well as in neuroactive specialized metabolites. These differences seem to match floral visitors' requirements, since they exclusively consume one of the two nectar types and may be exerting selective pressures on the composition of the respective resources of interest.

Evolutionary lability in floral ontogeny affects pollination biology in Trimezieae.

PREMISE: There is little direct evidence linking floral development and pollination biology in plants. We characterize both aspects in plain and ornamented flowers of Trimezieae (Iridaceae) to investigate how changes in floral ontogeny may affect their interactions with pollinators through time. METHODS: We examined floral ontogeny in 11 species and documented pollination biology in five species displaying a wide range of floral morphologies. We coded and reconstructed ancestral states of flower types over the tribal phylogeny to estimate the frequency of transition between different floral types. RESULTS: All Trimezieae flowers are similar in early floral development, but ornamented flowers have additional ontogenetic steps compared with plain flowers, indicating heterochrony. Ornamented flowers have a hinge pollination mechanism (newly described here) and attract more pollinator guilds, while plain flowers offer less variety of resources for a shorter time. Although the ornamented condition is plesiomorphic in this clade, shifts to plain flowers have occurred frequently and abruptly during the past 5 million years, with some subsequent reversals. CONCLUSIONS: Heterochrony has resulted in labile morphological changes during flower evolution in Trimezieae. Counterintuitively, species with plain flowers, which are endemic to the campo rupestre, are derived within the tribe and show a higher specialization than the ornamented species, with the former being visited by pollen-collecting bees only.

Economic Valuation of Bee Pollination Services for Passion Fruit (Malpighiales: Passifloraceae) Cultivation on Smallholding Farms in São Paulo, Brazil, Using the Avoided Cost Method.

This paper estimates the economic value of ecosystem services provided by Brazilian native bee, Xylocopa spp. Latreille (Hymenoptera: Apidae), pollination on a scale relevant to individual smallholder farmers that produce yellow passion fruit (Passiflora edulis Sims). The study areas are located in the vicinity of Pedro de Toledo and Itariri (Sao Paulo State-Brazil), in the Atlantic Forest region. The local economy is based on family farms, small stores, and ecotourism. The value was obtained using the ecological economics Avoided Cost Method, also known as replacement cost. Farms from this region informally hire temporary day laborers to supplement natural pollination with manual pollination of passion fruit flowers, so the cost of contracting temporary laborers was used to estimate the economic value of bee pollination. The value of pollination services was estimated at US$ 2,583.00 per hectare over 2 yr of P. edulis farming. Our estimates based on passion fruit farmer surveys and ecological valuation over 2 yr suggest that manual pollination accounts for 44-48% of production costs and results in a loss of ~58% of profits when wild bee pollination services are not available and manual pollination is required. We suggest that smallholder farmers follow the suggestions of previous studies and conserve adequate forest habitat for bee nesting and foraging, plan pesticide use around flowering and pollination, and supplement bee populations to maximize the benefit of the pollination ecosystem service and profits.

Reproduction, pollination and seed predation of Senna multijuga (Fabaceae) in two protected areas in the Brazilian Atlantic forest

One important subject is to determine the effectiveness of conservation areas, where different management categories are being applied, to maintain effective sexual reproduction in plants and their interactions with animal groups. To evaluate this issue, we compared the phenology, reproductive success, pollination and pre-dispersal seed predation of the legume tree Senna multijuga in two differently managed protected areas in Southeastern Brazil: the Itatiaia National Park and the Environmental Protection Area of Serrinha do Alambari, from December 2007 to December 2008. Vegetative and reproductive phenodinamycs were registered monthly in 80 individuals; other evaluations included 104 observation hours for pollination (March-May 2008) in 51 inflorescences; besides, fruit counts, fecundity and seed predation. Sexual reproduction of S. multijuga depends on the transfer of pollen by large bees (Bombus, Centris, Epicharis and Xylocopa), as the species is self-incompatible. Bruchidae species of the genus Acanthoscelides and Sennius predate seeds. Vegetative and reproductive phenodynamics differed among sites. Our results indicated that ecological interactions were lower at the protected area, but the reproductive processes in S. multijuga were not ruptured or critically degraded. This reinforces the idea that landscape areas with intermediate levels of protection, such as environmental protection areas, are suitable as buffer zones, and thus, relevant to the conservation of ecological processes when associated with more strictly protected areas. Rev. Biol. Trop. 59 (4): 1939-1948. Epub 2011 December 01.

Es importante determinar la eficacia de las áreas de conservación cuando se están implementando diferentes categorías de manejo, y una forma de hacerlo es conociendo si se mantiene una reproducción sexual efectiva en las especies de plantas y sus interacciones con grupos de animales. Para evaluar esta cuestión, se comparó la fenología, el éxito reproductivo, la polinización y la pre-dispersión de semillas depredadas de la leguminosa Senna multijuga en dos áreas protegidas sometidas a diferente tipos de manejo en el sureste de Brasil: el Parque Nacional de Itatiaia y el Área de Protección Ambiental de Serrinha de Alambari, de diciembre 2007 a diciembre 2008. La fenodinámica vegetativa y reproductiva fue registrada mensualmente en 80 individuos; otras evaluaciones incluyeron 104 horas de observación de la polinización (marzo-mayo 2008) en 51 inflorescencias, además del conteo de frutos, fecundidad y depredación de semillas. S. multijuga tiene una reproducción sexual que depende de la polinización de abejas grandes (Bombus, Centris, Epicharis y Xylocopa) y se considera una especie auto-incompatible. Las semillas son depredadas por especies de Bruchidae de los géneros Acanthoscelides y Sennius. La fenodinámica vegetativa y reproductiva difirió entre sitios. Nuestros resultados indican que las interacciones ecológicas fueron menores en el área protegida, pero los procesos reproductivos de S. multijuga no se vieron interrumpidos ni degradados de manera crítica. Esto refuerza la idea de que las zonas de paisaje con niveles intermedios de protección, tales como las áreas de protección ambiental, son adecuadas como zonas de amortiguamiento, y por lo tanto, relevantes para la conservación de los procesos ecológicos cuando se asocian con áreas en las que se da una protección más estricta.