Anthropogenic land-use change decreases pollination and male and female fitness in terrestrial flowering plants.

BACKGROUND AND AIMS: The majority of the earth's land area is currently occupied by humans. Measuring how terrestrial plants reproduce in these pervasive environments is essential for understanding their long-term viability and their ability to adapt to changing environments. METHODS: We conducted hierarchical and phylogenetically-independent meta-analyses to assess the overall effects of anthropogenic land-use changes on pollination, and male and female fitness in terrestrial plants. KEY RESULTS: We found negative global effects of land use change (i.e., mainly habitat loss and fragmentation) on pollination and on female and male fitness of terrestrial flowering plants. Negative effects were stronger in plants with self-incompatibility (SI) systems and pollinated by invertebrates, regardless of life form and sexual expression. Pollination and female fitness of pollination generalist and specialist plants were similarly negatively affected by land-use change, whereas male fitness of specialist plants showed no effects. CONCLUSIONS: Our findings indicate that angiosperm populations remaining in fragmented habitats negatively affect pollination, and female and male fitness, which will likely decrease the recruitment, survival, and long-term viability of plant populations remaining in fragmented landscapes. We underline the main current gaps of knowledge for future research agendas and call out not only for a decrease in the current rates of land-use changes across the world but also to embark on active restoration efforts to increase the area and connectivity of remaining natural habitats.

Exotic and native plants play equally important roles in supporting and structuring plant-hummingbird networks within urban green spaces.

Background: Urban gardens, despite their transformed nature, serve as invaluable microcosms for a quantitative examination of floral resource provision to urban pollinators, considering the plant's origin. Thus, knowledge has increased, emphasizing the importance of these green areas for hosting and conserving pollinator communities. However, there is a significant knowledge gap concerning the changing availability of these native and exotic floral resources over time and their impact on structuring interaction networks with specific pollinators. Methods: Over a year-long period, monthly surveys were conducted to record both native and exotic plant species visited by hummingbirds in an urban garden at Tlaxcala, Mexico. Flower visits were recorded, and the total flowers on each plant visited were tallied. Additionally, all observed hummingbirds were recorded during the transect walks, regardless of plant visits, to determine hummingbird abundance. The interactions were summarized using matrices, and network descriptors like connectance, specializacion, nestedness, and modularity were computed. Plant and hummingbird species in the core and periphery of the network were also identified. Lastly, simulations were performed to assess the network's resilience to the extinction of highly connected native and exotic plant species, including those previously situated in the network's core. Results: We recorded 4,674 interactions between 28 plant species, and eight hummingbird species. The majority of plants showed an ornithophilic syndrome, with 20 species considered exotic. Despite asynchronous flowering, there was overlap observed across different plant species throughout the year. Exotic plants like Jacaranda mimosifolia and Nicotiana glauca produced more flowers annually than native species. The abundance of hummingbirds varied throughout the study, with Saucerottia berillyna being the most abundant species. The plant-hummingbird network displayed high connectance, indicating generalization in their interaction. Significant nestedness was observed, mainly influenced by exotic plant species. The core of the network was enriched with exotic plants, while Basilinna leucotis and Cynanthus latirostris played central roles among hummingbirds. Network resilience to species extinction remained generally high. Conclusions: Our findings provide valuable insights into the dynamics and structure of plant-hummingbird interactions in urban gardens, emphasizing the influence of exotic plant species and the network's resilience to perturbations. Understanding and managing the impact of exotic plants on such networks is crucial for the conservation and sustainable functioning of urban ecosystems.

Floral Visitation, Phytochemical and Biological Activities of Bioproducts from Tetragonisca angustula (Hymenoptera, Apidae, Meliponini): A Review.

Tetragonisca angustula (Latreille, 1811) is an indigenous neotropical stingless bee, popularly known as "Jataí", with a wide distribution in the Brazilian territory. T. angustula produces other derivatives such as propolis, geopropolis, fermented (saburá pollen), cerumen and resins, which are important in folk medicine. In this review, the objective was to gather research on the main plant species visited by T. angustula, as well as studies that verified the chemical composition and biological properties of T. angustula bioproducts. The bibliographic review was performed by searching the Scopus, Web of Science, ScienceDirect, and PubMed databases for publications from 2003 to February 2023. We found 78 studies that analyzed the interactions between T. angustula and floral species, with species from the botanical families Fabaceae, Asteraceae, Malvaceae, Bignoniaceae, Solanaceae, Myrtaceae and Lamiaceae being the most reported as the main food sources for this species. The presence of compounds belonging to the class of flavonoids, phenolic acids, terpenoids and alkaloids has been identified by studying the chemical composition of honey, propolis, geopropolis and fermented pollen (saburá) in 21 studies. The data collected in the literature emphasize that these T. angustula products have remarkable biological properties, especially their antibacterial and antioxidant activities.

Phenological mismatches and the demography of solitary bees.

Species respond idiosyncratically to environmental variation, which may generate phenological mismatches. We assess the consequences of such mismatches for solitary bees. During 9 years, we studied flowering phenology and nesting phenology and demography of five wood-nesting solitary bee species representing a broad gradient of specialization/generalization in the use of floral resources. We found that the reproductive performance and population growth rate of bees tended to be lower with increasing nesting-flowering mismatches, except for the most generalized bee species. Our findings help elucidate the role of phenological mismatches for the demography of wild pollinators, which perform key ecosystem functions and provide important services for humanity. Furthermore, if climate change increases phenological mismatches in this system, we expect negative consequences of climate change for specialist bees.

Latitudinal gradients in biotic interactions: Are cacti pollination systems more specialized in the tropics?

Biotic interactions are said to be more specialized in the tropics, and this was also proposed for the pollination systems of columnar cacti from North America. However, this has not yet been tested for a wider set of cactus species. Here, we use the available information about pollination in the Cactaceae to explore the geographic patterns of this mutualistic interaction, and test if there is a latitudinal gradient in its degree of specialization. We performed a bibliographic search of all publications on the pollination of cacti species and summarized the information to build a database. We used generalized linear models to evaluate if the degree of specialization in cacti pollination systems is affected by latitude, using two different measures: the number of pollinator guilds (functional specialization) and the number of pollinator species (ecological specialization). Our database contained information about the pollination of 148 species. The most frequent pollinator guilds were bees, birds, moths and bats. There was no apparent effect of latitude on the number of guilds that pollinate a cactus species. However, latitude had a small but significant effect on the number of pollinator species that service a given cactus species. Bees are found as pollinators of most cactus species, along a wide latitudinal gradient. Bat and bird pollination is more common in the tropics than in the extra-tropics. The available information suggests that cacti pollination systems are slightly more ecologically specialized in the tropics, but it does not support any trend with regard to functional specialization.

A sophisticated case of division of labour in the trimorphic stamens of the Cassia fistula (Leguminosae) flower.

Buzz-pollinated pollen flowers have pollen as the primary resource for pollinators and must deal with a conflict between the exploitation of pollen grains by bees and pollination success. It has been hypothesized that heterostemony allows division of labour between stamens as a solution to the pollen dilemma. To test the division of labour hypothesis, we chose Cassia fistula, which has a trimorphic androecium and analysed androecium development, pollen grain release mechanisms and visitor behaviour. We explored the reflectance of floral organs and carried out an exclusion experiment to test the attractiveness of each stamen morph to the bee species. Finally, we explored the structural, ultrastructural and functional variation between the pollen grains, including pollen viability across stamen morphs. The differences among the three stamen morphs, which is developed from two whorls of the stamen, are the first evidence of the division of labour in our study system. Large Bombus and Xylocopa bees actively and exclusively exploited the pollen grains from the central poricidal anthers generating pollen deposition on their bodies. The reflectance pattern of floral organs indicated a targeting of these large bees to the central anthers, corroborated by the anther manipulative experiment where only the exclusion of the anthers positioned in the flower centre, especially the intermediate stamens, reduced bee visits. Both results revealed a division of labour, in which the intermediate stamen morph was responsible for both floral attractiveness and pollen resources. Only the largest stamen morph produced germinable pollen grains, highlighting their role as pollinating stamens. The smallest stamen morph has a less clear function, likely representing an economy in pollen production for feeding function. Our findings suggest that the evolution of the trimorphic androecium is associated with division of labour in large pollen flowers and can represent a strong strategy for circumventing the pollen dilemma, optimizing the feeding function by reducing pollen grain investment from central anthers.

Color signals of bee-pollinated flowers: the significance of natural leaf background.

PREMISE: Flower color is a primary pollinator attractant and generally adjusted to the cognitive system of the pollinators. The perception of flower color depends on the visual system of pollinators and also on environmental factors such as light conditions and the background against which flowers are displayed. METHODS: Using bee-pollinated Fabaceae species as a model, we analyzed flower color diversity and compared flower color signals considering both the standard green and the natural leaf background of two tropical seasonally dry vegetations-a mountain rupestrian grassland (campo rupestre) and a woody savanna (cerrado)-compared to a nontropical Mediterranean shrubland. RESULTS: By using natural background, bees discriminated color for 58% of the flowers in the campo rupestre and for only 43% in cerrado. Both vegetations were surpassed by 75% of bee color discrimination in Mediterranean vegetation. Chromatic contrast and purity were similar among the three vegetation types. Green contrast and brightness were similar between the tropical vegetations but differed from the Mediterranean shrubland. Green contrast differences were lost when using a standard green background, and most variables (purity, green contrast, and brightness) differed according to the background (natural or standard green) in all vegetations. CONCLUSIONS: The natural background influenced bee perception of flower color regardless of vegetation. The background of the campo rupestre promoted green contrast for flowers, ensuring flower detection by pollinators and, along with bees, may also act as a selective pressure driving the diversity of flower colors in Fabaceae species. We highlight the importance of considering the natural background coloration when analyzing flower color signals.

Plant-centred sampling estimates higher beta diversity of interactions than pollinator-based sampling across habitats.

When describing plant-animal interaction networks, sampling can be performed using plant- or animal-centred approaches. Despite known effects of sampling on network structure, how samplings affect the estimates of interaction ß-diversity across networks is still unresolved. We investigated how the sampling method affects the assessment of ß-diversity of interactions, turnover and rewiring. We contrasted plant- and animal-centred sampling methods applied to pollination networks across habitats in a heterogeneous tropical landscape, the Pantanal Wetlands. We also asked whether plant traits influence the difference in interaction specialization according to sampling. Plant-centred networks resulted in higher ß-diversity of interactions in space than animal-centred networks. Turnover explained most of the ß-diversity in both methods, but rewiring was proportionately more important when using the animal-centred method. While the plant-centred method indicated lower network modularity and specialization, floral traits modulated the effects of the sampling method on species-level network metrics. Combining animal- and plant-centred approaches returned intermediate values for ß-diversity of interactions and network metrics. Distinct methods may also be better suited for answering questions at different scales. Our results point out that the method choice, or combination of methods, should always reflect the appropriate scale of the factors determining the interactions being investigated.

Drivers of the structure of plant-hummingbird interaction networks at multiple temporal scales.

In semi-arid environments, the marked contrast in temperature and precipitation over the year strongly shapes ecological communities. The composition of species and their ecological interactions within a community may vary greatly over time. Although intra-annual variations are often studied, empirical information on how plant-bird relationships are structured within and among years, and how their drivers may change over time are still limited. In this study, we analyzed the temporal dynamics of the structure of plant-hummingbird interaction networks by evaluating changes in species richness, diversity of interactions, modularity, network specialization, nestedness, and ß-diversity of interactions throughout four years in a Mexican xeric shrubland landscape. We also evaluated if the relative importance of abundance, phenology, morphology, and nectar sugar content consistently explains the frequency of pairwise interactions between plants and hummingbirds across different years. We found that species richness, diversity of interactions, nestedness, and network specialization did vary within and among years. We also observed that the ß-diversity of interactions was high among years and was mostly associated with species turnover (i.e., changes in species composition), with a minor contribution of interaction rewiring (i.e., shifting partner species at different times). Finally, the temporal co-occurrence of hummingbird and plant species among months was the best predictor of the frequency of pairwise interactions, and this pattern was consistent within and among years. Our study underscores the importance of considering the temporal scale to understand how changes in species phenologies, and the resulting temporal co-occurrences influence the structure of interaction networks.

Core-periphery dynamics in a plant-pollinator network.

Mutualistic networks are highly dynamic, characterized by high temporal turnover of species and interactions. Yet, we have a limited understanding of how the internal structure of these networks and the roles species play in them vary through time. We used 6 years of observation data and a novel statistical method (dynamic stochastic block models) to assess how network structure and species' structural position within the network change throughout subseasons of the flowering season and across years in a quantitative plant-pollinator network from a dryland ecosystem in Argentina. Our analyses revealed a core-periphery structure persistent through subseasons and years. Yet, species structural position as core or peripheral was highly dynamic: virtually all species that were at the core in some subseasons were also peripheral in other subseasons, while many other species always remained peripheral. Our results illuminate our understanding of the dynamics of mutualistic networks and have important implications for ecosystem management and conservation.

Precipitation and predation risk alter the diversity and behavior of pollinators and reduce plant fitness.

Biotic and abiotic factors may individually or interactively disrupt plant-pollinator interactions, influencing plant fitness. Although variations in temperature and precipitation are expected to modify the overall impact of predators on plant-pollinator interactions, few empirical studies have assessed if these weather conditions influence anti-predator behaviors and how this context-dependent response may cascade down to plant fitness. To answer this question, we manipulated predation risk (using artificial spiders) in different years to investigate how natural variation in temperature and precipitation may affect diversity (richness and composition) and behavioral (visitation) responses of flower-visiting insects to predation risk, and how these effects influence plant fitness. Our findings indicate that predation risk and an increase in precipitation independently reduced plant fitness (i.e., seed set) by decreasing flower visitation. Predation risk reduced pollinator visitation and richness, and altered species composition of pollinators. Additionally, an increase in precipitation was associated with lower flower visitation and pollinator richness but did not alter pollinator species composition. However, maximum daily temperature did not affect any component of the pollinator assemblage or plant fitness. Our results indicate that biotic and abiotic drivers have different impacts on pollinator behavior and diversity with consequences for plant fitness components. Even small variation in precipitation conditions promotes complex and substantial cascading effects on plants by affecting both pollinator communities and the outcome of plant-pollinator interactions. Tropical communities are expected to be highly susceptible to climatic changes, and these changes may have drastic consequences for biotic interactions in the tropics.

Phenotypic selection mosaic for flower length influenced by geographically varying hawkmoth pollinator proboscis length and abiotic environment.

Biotic and abiotic context may affect the intensity of interspecific interactions and subsequently drive locally particular phenotypic selection patterns on interacting traits. We evaluated the geographical variation of matching traits of the brush-type flowers of Caesalpinia gilliesii and of the proboscis length of its guild of hawkmoth pollinators, as well as their relationship with environmental variables. We assessed the geographical variation of interacting traits (style and filament vs mean proboscis length of the guild of hawkmoths) across seven populations and estimated phenotypic selection on the plant side. Interacting traits showed similar relationships with environmental variables. Phenotypic selection on the plant side was influenced by proboscis length and by environmental conditions. Mean proboscis length of the guild was shorter than previously recorded for the same study area, thus probably shifting the selective optima of flower length. We observed two presumptive coevolutionary cold spots where one-sided negative directional selection is acting on style length. The lack of selection on the pollinator side should be further confirmed. We provided joint evidence, mostly lacking, about the geographical variation of selective pressures on the plant side associated with both proboscis length and abiotic conditions. We suggest that recent environmental change may be shifting floral length optima.

Spatio-temporal effects of climate change on the geographical distribution and flowering phenology of hummingbird-pollinated plants.

BACKGROUNDS AND AIMS: Tropical plant species are already suffering the effects of climate change and projections warn of even greater changes in the following decades. Of particular concern are alterations in flowering phenology, given that it is considered a fitness trait, part of plant species ecological niche, with potential cascade effects in plant-pollinator interactions. The aim of the study was to assess the potential impacts of climate change on the geographical distribution and flowering phenology of hummingbird-pollinated plants. METHODS: We implemented ecological niche modelling (ENM) to investigate the potential impacts of different climate change scenarios on the geographical distribution and flowering phenology of 62 hummingbird-pollinated plant species in the Brazilian Atlantic Forest. KEY RESULTS: Distribution models indicate future changes in the climatic suitability of their current habitats, suggesting a tendency towards discontinuity, reduction and spatial displacement. Flowering models indicate that climate can influence species phenology in different ways: some species may experience increased flowering suitability whereas others may suffer decreased suitability. CONCLUSIONS: Our results suggest that hummingbird-pollinated species are prone to changes in their geographical distribution and flowering under different climate scenarios. Such variation may impact the community structure of ecological networks and reproductive success of tropical plants in the near future.

Relative effectiveness of insects versus hummingbirds as pollinators of Rubiaceae plants across elevation in Dominica, Caribbean.

Most angiosperms rely on animal pollination for reproduction, but the dependence on specific pollinator groups varies greatly between species and localities. Notably, such dependence may be influenced by both floral traits and environmental conditions. Despite its importance, their joint contribution has rarely been studied at the assemblage level. At two elevations on the Caribbean island of Dominica, we measured the floral traits and the relative contributions of insects versus hummingbirds as pollinators of plants in the Rubiaceae family. Pollinator importance was measured as visitation rate (VR) and single visit pollen deposition (SVD), which were combined to assess overall pollinator effectiveness (PE). In the wet and cool Dominican highland, we found that hummingbirds were relatively more frequent and effective pollinators than insects, whereas insects and hummingbirds were equally frequent and effective pollinators at the warmer and less rainy midelevation. Furthermore, floral traits correlated independently of environment with the relative importance of pollinators, hummingbirds being more important in plant species having flowers with long and wide corollas producing higher volumes of dilute nectar. Our findings show that both environmental conditions and floral traits influence whether insects or hummingbirds are the most important pollinators of plants in the Rubiaceae family, highlighting the complexity of plant-pollinator systems.

Nectar Replaced by Volatile Secretion: A Potential New Role for Nectarless Flowers in a Bee-Pollinated Plant Species.

The presence of nectarless flowers in nectariferous plants is a widespread phenomenon in angiosperms. However, the frequency and distribution of nectarless flowers in natural populations, and the transition from nectariferous to nectarless flowers are poorly known. Variation in nectar production may affect mutualism stability, since energetic resource availability influences pollinators' foraging behavior. Here, we described the spatial and temporal nectar production patterns of Jacaranda oxyphylla, a bee-pollinated species that naturally presents nectarless flowers. Additionally, we compared nectariferous and nectarless floral disks in order to identify histological, subcellular and chemical changes that accompanied the loss of nectar production ability. For that we used standard methods for light and transmission electron microscopy, and gas chromatography coupled to mass spectrometry for chemical analyses. We verified that 47% of flowers did not produce nectar during the whole flower lifespan (nectarless flowers). We also observed remarkable inter-plant variation, with individuals having only nectarless flowers, others only nectariferous ones and most of them showing different proportions of both flower types, with variable nectar volumes (3-21 µl). Additionally, among nectariferous flowers, we registered two distinct rhythms of nectar production. 'Early' flowers produced nectar from 0 to 24 h, and 'late' flowers produced nectar from 24 to 48 h of anthesis. Although disks from nectariferous and nectarless flowers displayed similar histological organization, they differed strongly at subcellular level. Nectariferous ('early' and 'late') flowers exhibited a cellular apparatus typical of nectar secretion, while nectarless flowers exhibited osmophoric features. We found three aliphatic and one aromatic compound(s) that were detected in both the headspace of flowers and the disks of nectarless flowers, but not the disks of nectariferous flowers Although the remarkable variation in nectar availability may discourage pollinator visits, nectarless flowers might compensate it by producing volatile compounds that can be part of floral scent, acting as chemical attractants. Thus, nectarless flowers may be helping to maintain pollination in this scenario of trophic resource supply scarcity. We suggest that J. oxyphylla can be transitioning from a nectar-based pollination system to another resource-based or even to a deceit mechanism of pollination.

Pollination in the Chilean Mediterranean-type ecosystem: a review of current advances and pending tasks.

We conducted a systematic review of the scientific literature published on plant-pollinator interactions, from both the plant and pollinator perspective, in the Chilean Mediterranean-type ecosystem (MTE hereafter). Our search identified 69 published papers on 235 native plant species from 62 families. Less than 7.9% of the flowering species inhabiting the Chilean Mediterranean have been studied, and most studies were restricted to only one locality and one reproductive season. The geographic location of the studies differed from a random pattern, showing two well-defined areas where most studies were conducted. Likewise, most studies in the Andes Range were performed above 2000 m a.s.l. The number of species of flower visitor per plant species was low (4.25 ± 0.22), which probably results from the historical and biogeographic isolation of Chile. This literature survey shows that studies relating floral traits with pollinator attraction and plant reproduction are the most frequent topics of research, reaching 37.6% of studies, followed by studies that examine pollination in relation to human impact (16.1%), micro- and macroevolution (14.0%), relationships between pollination and other ecological interactions (10.8%), community and network assessments (11.8%), and effects of abiotic variables on pollination interactions (9.7%). Our review highlights a lack of research on the effects of pollination for anthropogenic land use especially as agricultural practice is one of the most salient features of the Chilean MTE. Future directions to increase our understanding of the role of plant-pollinator relationships for biodiversity maintenance should include: to extend the taxonomic and geographic scope of research, to increase the number of spatial and temporal replicates, to increase the number of studies on pollination networks as they provide estimates of community complexity and putative stability, to develop studies that estimate the importance of pollination for plant demographic parameters and conservation, and to conduct studies that estimate the ecological service provided by Chilean native pollinators for crop yield and sustainable agriculture.

Evolutionary consequences of ecological factors: pollinator reliability predicts mating-system traits of a perennial plant.

The reproductive-assurance hypothesis predicts that mating-system traits will evolve towards increased autonomous self-pollination in plant populations experiencing unreliable pollinator service. We tested this long-standing hypothesis by assessing geographic covariation among pollinator reliability, outcrossing rates, heterozygosity and relevant floral traits across populations of Dalechampia scandens in Costa Rica. Mean outcrossing rates ranged from 0.16 to 0.49 across four populations, and covaried with the average rates of pollen arrival on stigmas, a measure of pollinator reliability. Across populations, genetically based differences in herkogamy (anther-stigma distance) were associated with variation in stigmatic pollen loads, outcrossing rates and heterozygosity. These observations are consistent with the hypothesis that, when pollinators are unreliable, floral traits promoting autonomous selfing evolve as a mechanism of reproductive assurance. Extensive covariation between floral traits and mating system among closely related populations further suggests that floral traits influencing mating systems track variation in adaptive optima generated by variation in pollinator reliability.