Intensive pasture management alters the composition and structure of plant-pollinator interactions in Sibiu, Romania.

Background: Land management change towards intensive grazing has been shown to alter plant and pollinator communities and the structure of plant-pollinator interactions in different ways across the world. Land-use intensification in Eastern Europe is shifting highly diverse, traditionally managed hay meadows towards intensive pastures, but few studies have examined how this influences plant-pollinator networks. We hypothesized that the effects of intensive grazing on networks will depend on how plant communities and their floral traits change. Methods: We investigated plant and pollinator diversity and composition and the structure of plant-pollinator interactions near Sibiu, Romania at sites that were traditionally managed as hay meadows or intensive pastures. We quantified the identity and abundance of flowering plants, and used transect walks to observe pollinator genera interacting with flowering plant species. We evaluated the effects of management on diversity, composition and several indices of network structure. Results: Pollinator but not plant diversity declined in pastures and both plant and pollinator taxonomic composition shifted. Functional diversity and composition remained unchanged, with rather specialized flowers having been found to dominate in both hay meadows and pastures. Apis mellifera was found to be the most abundant pollinator. Its foraging preferences played a crucial role in shaping plant-pollinator network structure. Apis mellifera thus preferred the highly abundant Dorycnium herbaceum in hay meadows, leading to hay meadows networks with lower Shannon diversity and interaction evenness. In pastures, however, it preferred less abundant and more generalized flower resources. With pollinators being overall less abundant and more generalized in pastures, we found that niche overlap between plants was higher. Discussion: With both hay meadows and pastures being dominated by plant species with similar floral traits, shifts in pollinator preferences seem to have driven the observed changes in plant-pollinator interaction networks. We thus conclude that the effects of grazing on pollinators and their interactions are likely to depend on the traits of plant species present in different management types as well as on the effects of grazing on plant community composition. We thereby highlight the need for better understanding how floral abundance shapes pollinator visitation rates and how floral traits may influence this relationship.

The myriad of complex demographic responses of terrestrial mammals to climate change and gaps of knowledge: A global analysis.

Approximately 25% of mammals are currently threatened with extinction, a risk that is amplified under climate change. Species persistence under climate change is determined by the combined effects of climatic factors on multiple demographic rates (survival, development and reproduction), and hence, population dynamics. Thus, to quantify which species and regions on Earth are most vulnerable to climate-driven extinction, a global understanding of how different demographic rates respond to climate is urgently needed. Here, we perform a systematic review of literature on demographic responses to climate, focusing on terrestrial mammals, for which extensive demographic data are available. To assess the full spectrum of responses, we synthesize information from studies that quantitatively link climate to multiple demographic rates. We find only 106 such studies, corresponding to 87 mammal species. These 87 species constitute <1% of all terrestrial mammals. Our synthesis reveals a strong mismatch between the locations of demographic studies and the regions and taxa currently recognized as most vulnerable to climate change. Surprisingly, for most mammals and regions sensitive to climate change, holistic demographic responses to climate remain unknown. At the same time, we reveal that filling this knowledge gap is critical as the effects of climate change will operate via complex demographic mechanisms: a vast majority of mammal populations display projected increases in some demographic rates but declines in others, often depending on the specific environmental context, complicating simple projections of population fates. Assessments of population viability under climate change are in critical need to gather data that account for multiple demographic responses, and coordinated actions to assess demography holistically should be prioritized for mammals and other taxa.

Pollen analysis using multispectral imaging flow cytometry and deep learning.

Pollen identification and quantification are crucial but challenging tasks in addressing a variety of evolutionary and ecological questions (pollination, paleobotany), but also for other fields of research (e.g. allergology, honey analysis or forensics). Researchers are exploring alternative methods to automate these tasks but, for several reasons, manual microscopy is still the gold standard. In this study, we present a new method for pollen analysis using multispectral imaging flow cytometry in combination with deep learning. We demonstrate that our method allows fast measurement while delivering high accuracy pollen identification. A dataset of 426 876 images depicting pollen from 35 plant species was used to train a convolutional neural network classifier. We found the best-performing classifier to yield a species-averaged accuracy of 96%. Even species that are difficult to differentiate using microscopy could be clearly separated. Our approach also allows a detailed determination of morphological pollen traits, such as size, symmetry or structure. Our phylogenetic analyses suggest phylogenetic conservatism in some of these traits. Given a comprehensive pollen reference database, we provide a powerful tool to be used in any pollen study with a need for rapid and accurate species identification, pollen grain quantification and trait extraction of recent pollen.

Land use and pollinator dependency drives global patterns of pollen limitation in the Anthropocene.

Land use change, by disrupting the co-evolved interactions between plants and their pollinators, could be causing plant reproduction to be limited by pollen supply. Using a phylogenetically controlled meta-analysis on over 2200 experimental studies and more than 1200 wild plants, we ask if land use intensification is causing plant reproduction to be pollen limited at global scales. Here we report that plants reliant on pollinators in urban settings are more pollen limited than similarly pollinator-reliant plants in other landscapes. Plants functionally specialized on bee pollinators are more pollen limited in natural than managed vegetation, but the reverse is true for plants pollinated exclusively by a non-bee functional group or those pollinated by multiple functional groups. Plants ecologically specialized on a single pollinator taxon were extremely pollen limited across land use types. These results suggest that while urbanization intensifies pollen limitation, ecologically and functionally specialized plants are at risk of pollen limitation across land use categories.

Global geographic patterns of heterospecific pollen receipt help uncover potential ecological and evolutionary impacts across plant communities worldwide.

Species interactions are known to be key in driving patterns of biodiversity across the globe. Plant-plant interactions through heterospecific pollen (HP) transfer by their shared pollinators is common and has consequences for plant reproductive success and floral evolution, and thus has the potential to influence global patterns of biodiversity and plant community assembly. The literature on HP transfer is growing and it is therefore timely to review patterns and causes of among-species variation in HP receipt at a global scale, thus uncovering its potential contribution to global patterns of biodiversity. Here we analyzed published data on 245 species distributed across five continents to evaluate latitudinal and altitudinal patterns of HP receipt. We further analyzed the role of floral symmetry and evolutionary history in mediating patterns of HP receipt. Latitude and elevation affected the likelihood and intensity of HP receipt indicating that HP transfer increases in species-rich communities and in areas with high abundance of vertebrate pollinators. Floral symmetry and evolutionary history determined HP load size across plant communities worldwide. Overall, our results suggest that HP receipt may have the potential to contribute to global geographic patterns of plant diversity by imposing strong selective pressures in species-rich areas across the globe.

Plant traits moderate pollen limitation of introduced and native plants: a phylogenetic meta-analysis of global scale.

The role of pollination in the success of invasive plants needs to be understood because invasives have substantial effects on species interactions and ecosystem functions. Previous research has shown both that reproduction of invasive plants is often pollen limited and that invasive plants can have high seed production, motivating the questions: How do invasive populations maintain reproductive success in spite of pollen limitation? What species traits moderate pollen limitation for invaders? We conducted a phylogenetic meta-analysis with 68 invasive, 50 introduced noninvasive and 1931 native plant populations, across 1249 species. We found that invasive populations with generalist pollination or pollinator dependence were less pollen limited than natives, but invasives and introduced noninvasives did not differ. Invasive species produced 3× fewer ovules/flower and >250× more flowers per plant, compared with their native relatives. While these traits were negatively correlated, consistent with a tradeoff, this did not differ with invasion status. Invasive plants that produce many flowers and have floral generalisation are able to compensate for or avoid pollen limitation, potentially helping to explain the invaders' reproductive successes.

Exotic plant species receive adequate pollinator service despite variable integration into plant-pollinator networks.

Both exotic and native plant species rely on insect pollinators for reproductive success, and yet few studies have evaluated whether and how exotic plant species receive services from native pollinators for successful reproduction in their introduced range. Plant species are expected to successfully reproduce in their exotic range if they have low reliance on animal pollinators or if they successfully integrate themselves into resident plant-pollinator networks. Here, we quantify the breeding system, network integration, and pollen limitation for ten focal exotic plant species in North America. Most exotic plant species relied on animal pollinators for reproduction, and these species varied in their network integration. However, plant reproduction was limited by pollen receipt for only one plant species. Our results demonstrate that even poorly integrated exotic plant species can still have high pollination service and high reproductive success. The comprehensive framework considered here provides a method to consider the contribution of plant breeding systems and the pollinator community to pollen limitation, and can be applied to future studies to provide a more synthetic understanding of the factors that determine reproductive success of exotic plant species.

Interactive effects of harvest and deer herbivory on the population dynamics of American ginseng.

Few demographic models for any species consider the role of multiple, interacting ecological threats. Many forest herbs are heavily browsed by white-tailed deer (Odocoileus virginianus) and a number of these are also harvested for the medicinal, floral, or horticultural trades. Previous studies of the viability of American ginseng (Panax quinquefolius) have separately examined the effects of harvesting and deer herbivory. We followed individually marked ginseng plants in 6 populations for 8 years and documented deer browse levels, conducted helicopter surveys to estimate the deer herd size, and documented 2 ginseng harvests. We used this long-term data set to develop a stochastic demographic model that quantified the separate and interactive role of these threats to ginseng viability. Although harvesting and deer herbivory negatively affected ginseng population growth, their effects were not additive. Deer herbivory negatively affected population growth in the absence but not in the presence of harvesting. Life table response experiments revealed that in the presence of harvesting, deer herbivory had some positive effects on vital rates because browsed plants were less apparent to harvesters. Ginseng populations that were harvested responsibly (i.e., planting seeds from harvested individuals) had higher growth rates than those that were harvested irresponsibly. We concluded that both deer populations and harvesting must be managed to ensure sustainable populations of American ginseng. Our findings underscore the importance of long-term monitoring to assess threats to viability and the need for a broad ecological understanding of the complexity of ecosystem management.

Pollination decays in biodiversity hotspots.

As pollinators decline globally, competition for their services is expected to intensify, and this antagonism may be most severe where the number of plant species is the greatest. Using meta-analysis and comparative phylogenetic analysis, we provide a global-scale test of whether reproduction becomes more limited by pollen receipt (pollen limitation) as the number of coexisting plant species increases. As predicted, we find a significant positive relationship between pollen limitation and species richness. In addition, this pattern is particularly strong for species that are obligately outcrossing and for trees relative to herbs or shrubs. We suggest that plants occurring in species-rich communities may be more prone to pollen limitation because of interspecific competition for pollinators. As a consequence, plants in biodiversity hotspots may have a higher risk of extinction and/or experience increased selection pressure to specialize on certain pollinators or diversify into different phenological niches. The combination of higher pollen limitation and habitat destruction represents a dual risk to tropical plant species that has not been previously identified.

Trophic cascades across ecosystems.

Predation can be intense, creating strong direct and indirect effects throughout food webs. In addition, ecologists increasingly recognize that fluxes of organisms across ecosystem boundaries can have major consequences for community dynamics. Species with complex life histories often shift habitats during their life cycles and provide potent conduits coupling ecosystems. Thus, local interactions that affect predator abundance in one ecosystem (for example a larval habitat) may have reverberating effects in another (for example an adult habitat). Here we show that fish indirectly facilitate terrestrial plant reproduction through cascading trophic interactions across ecosystem boundaries. Fish reduce larval dragonfly abundances in ponds, leading to fewer adult dragonflies nearby. Adult dragonflies consume insect pollinators and alter their foraging behaviour. As a result, plants near ponds with fish receive more pollinator visits and are less pollen limited than plants near fish-free ponds. Our results confirm that strong species interactions can reverberate across ecosystems, and emphasize the importance of landscape-level processes in driving local species interactions.

Plant population dynamics, pollinator foraging, and the selection of self-fertilization.

Many flowering plants rely on pollinators, self-fertilization, or both for reproduction. We model the consequences of these features for plant population dynamics and mating system evolution. Our mating systems-based population dynamics model includes an Allee effect. This often leads to an extinction threshold, defined as a density below which population densities decrease. Reliance on generalist pollinators who primarily visit higher density plant species increases the extinction threshold, whereas autonomous modes of selfing decrease and can eliminate the threshold. Generalist pollinators visiting higher density plant species coupled with autonomous selfing may introduce an effect where populations decreasing in density below the extinction threshold may nonetheless persist through selfing. The extinction threshold and selfing at low density result in populations where individuals adopting a single reproductive strategy exhibit mating systems that depend on population density. The ecological and evolutionary analyses provide a mechanism where prior selfing evolves even though inbreeding depression is greater than one-half. Simultaneous consideration of ecological and evolutionary dynamics confirms unusual features (e.g., evolution into extinction or abrupt increases in population density) implicit in our separate consideration of ecological and evolutionary scenarios. Our analysis has consequences for understanding pollen limitation, reproductive assurance, and the evolution of mating systems.

Floral density, pollen limitation, and reproductive success in Trillium grandiflorum.

Decreases in floral density can disrupt mutualistic interactions between plants and their pollinators, and decrease reproductive success. I addressed the relationship between floral density and plant reproductive success using two experimental approaches: a pollen supplementation experiment in 12 populations of Trillium grandiflorum that naturally varied in floral density, and a transplant experiment in which floral density was manipulated in plots at four experimental sites. In the pollen supplementation experiments, the degree of pollen limitation, in terms of fruit set and seed set, decreased with floral density. Further, in the experimental sites, plant reproductive success increased asymptotically with floral density. These results demonstrate the value of simultaneously conducting experiments in both experimental sites and natural populations to understand how population density influences plant reproductive success. Factors that reduce the density of this perennial herb, such as habitat fragmentation and herbivory by white-tailed deer ( Odocoileus virginianus), should be expected to limit its reproduction.