Urbanisation generates multiple trait syndromes for terrestrial animal taxa worldwide.

Cities can host significant biological diversity. Yet, urbanisation leads to the loss of habitats, species, and functional groups. Understanding how multiple taxa respond to urbanisation globally is essential to promote and conserve biodiversity in cities. Using a dataset encompassing six terrestrial faunal taxa (amphibians, bats, bees, birds, carabid beetles and reptiles) across 379 cities on 6 continents, we show that urbanisation produces taxon-specific changes in trait composition, with traits related to reproductive strategy showing the strongest response. Our findings suggest that urbanisation results in four trait syndromes (mobile generalists, site specialists, central place foragers, and mobile specialists), with resources associated with reproduction and diet likely driving patterns in traits associated with mobility and body size. Functional diversity measures showed varied responses, leading to shifts in trait space likely driven by critical resource distribution and abundance, and taxon-specific trait syndromes. Maximising opportunities to support taxa with different urban trait syndromes should be pivotal in conservation and management programmes within and among cities. This will reduce the likelihood of biotic homogenisation and helps ensure that urban environments have the capacity to respond to future challenges. These actions are critical to reframe the role of cities in global biodiversity loss.

Large herbivores transform plant-pollinator networks in an African savanna.

Pollination by animals is a key ecosystem service1,2 and interactions between plants and their pollinators are a model system for studying ecological networks,3,4 yet plant-pollinator networks are typically studied in isolation from the broader ecosystems in which they are embedded. The plants visited by pollinators also interact with other consumer guilds that eat stems, leaves, fruits, or seeds. One such guild, large mammalian herbivores, are well-known ecosystem engineers5-7 and may have substantial impacts on plant-pollinator networks. Although moderate herbivory can sometimes promote plant diversity,8 potentially benefiting pollinators, large herbivores might alternatively reduce resource availability for pollinators by consuming flowers,9 reducing plant density,10 and promoting somatic regrowth over reproduction.11 The direction and magnitude of such effects may hinge on abiotic context-in particular, rainfall, which modulates the effects of ungulates on vegetation.12 Using a long-term, large-scale experiment replicated across a rainfall gradient in central Kenya, we show that a diverse assemblage of native large herbivores, ranging from 5-kg antelopes to 4,000-kg African elephants, limited resource availability for pollinators by reducing flower abundance and diversity; this in turn resulted in fewer pollinator visits and lower pollinator diversity. Exclusion of large herbivores increased floral-resource abundance and pollinator-assemblage diversity, rendering plant-pollinator networks larger, more functionally redundant, and less vulnerable to pollinator extinction. Our results show that species extrinsic to plant-pollinator interactions can indirectly and strongly alter network structure. Forecasting the effects of environmental change on pollination services and interaction webs more broadly will require accounting for the effects of extrinsic keystone species.

Author Correction: Pollinator importance networks illustrate the crucial value of bees in a highly speciose plant community.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Pollinator size and its consequences: Robust estimates of body size in pollinating insects.

Body size is an integral functional trait that underlies pollination-related ecological processes, yet it is often impractical to measure directly. Allometric scaling laws have been used to overcome this problem. However, most existing models rely upon small sample sizes, geographically restricted sampling and have limited applicability for non-bee taxa. Allometric models that consider biogeography, phylogenetic relatedness, and intraspecific variation are urgently required to ensure greater accuracy. We measured body size as dry weight and intertegular distance (ITD) of 391 bee species (4,035 specimens) and 103 hoverfly species (399 specimens) across four biogeographic regions: Australia, Europe, North America, and South America. We updated existing models within a Bayesian mixed-model framework to test the power of ITD to predict interspecific variation in pollinator dry weight in interaction with different co-variates: phylogeny or taxonomy, sexual dimorphism, and biogeographic region. In addition, we used ordinary least squares regression to assess intraspecific dry weight ~ ITD relationships for ten bees and five hoverfly species. Including co-variates led to more robust interspecific body size predictions for both bees and hoverflies relative to models with the ITD alone. In contrast, at the intraspecific level, our results demonstrate that the ITD is an inconsistent predictor of body size for bees and hoverflies. The use of allometric scaling laws to estimate body size is more suitable for interspecific comparative analyses than assessing intraspecific variation. Collectively, these models form the basis of the dynamic R package, "pollimetry," which provides a comprehensive resource for allometric pollination research worldwide.

A systems approach reveals urban pollinator hotspots and conservation opportunities.

Urban areas are often perceived to have lower biodiversity than the wider countryside, but a few small-scale studies suggest that some urban land uses can support substantial pollinator populations. We present a large-scale, well-replicated study of floral resources and pollinators in 360 sites incorporating all major land uses in four British cities. Using a systems approach, we developed Bayesian network models integrating pollinator dispersal and resource switching to estimate city-scale effects of management interventions on plant-pollinator community robustness to species loss. We show that residential gardens and allotments (community gardens) are pollinator 'hotspots': gardens due to their extensive area, and allotments due to their high pollinator diversity and leverage on city-scale plant-pollinator community robustness. Household income was positively associated with pollinator abundance in gardens, highlighting the influence of socioeconomic factors. Our results underpin urban planning recommendations to enhance pollinator conservation, using increasing city-scale community robustness as our measure of success.

Pollinator importance networks illustrate the crucial value of bees in a highly speciose plant community.

Accurate predictions of pollination service delivery require a comprehensive understanding of the interactions between plants and flower visitors. To improve measurements of pollinator performance underlying such predictions, we surveyed visitation frequency, pollinator effectiveness (pollen deposition ability) and pollinator importance (the product of visitation frequency and effectiveness) of flower visitors in a diverse Mediterranean flower meadow. With these data we constructed the largest pollinator importance network to date and compared it with the corresponding visitation network to estimate the specialisation of the community with greater precision. Visitation frequencies at the community level were positively correlated with the amount of pollen deposited during individual visits, though rarely correlated at lower taxonomic resolution. Bees had the highest levels of pollinator effectiveness, with Apis, Andrena, Lasioglossum and Osmiini bees being the most effective visitors to a number of plant species. Bomblyiid flies were the most effective non-bee flower visitors. Predictions of community specialisation (H2') were higher in the pollinator importance network than the visitation network, mirroring previous studies. Our results increase confidence in existing measures of pollinator redundancy at the community level using visitation data, while also providing detailed information on interaction quality at the plant species level.

The city as a refuge for insect pollinators.

Research on urban insect pollinators is changing views on the biological value and ecological importance of cities. The abundance and diversity of native bee species in urban landscapes that are absent in nearby rural lands evidence the biological value and ecological importance of cities and have implications for biodiversity conservation. Lagging behind this revised image of the city are urban conservation programs that historically have invested in education and outreach rather than programs designed to achieve high-priority species conservation results. We synthesized research on urban bee species diversity and abundance to determine how urban conservation could be repositioned to better align with new views on the ecological importance of urban landscapes. Due to insect pollinators' relatively small functional requirements-habitat range, life cycle, and nesting behavior-relative to larger mammals, we argue that pollinators put high-priority and high-impact urban conservation within reach. In a rapidly urbanizing world, transforming how environmental managers view the city can improve citizen engagement and contribute to the development of more sustainable urbanization.

Molecular taxonomic analysis of the plant associations of adult pollen beetles (Nitidulidae: Meligethinae), and the population structure of Brassicogethes aeneus.

Pollen beetles (Nitidulidae: Meligethinae) are among the most abundant flower-visiting insects in Europe. While some species damage millions of hectares of crops annually, the biology of many species is little known. We assessed the utility of a 797 base pair fragment of the cytochrome oxidase 1 gene to resolve molecular operational taxonomic units (MOTUs) in 750 adult pollen beetles sampled from flowers of 63 plant species sampled across the UK and continental Europe. We used the same locus to analyse region-scale patterns in population structure and demography in an economically important pest, Brassicogethes aeneus. We identified 44 Meligethinae at ∼2% divergence, 35 of which contained published sequences. A few specimens could not be identified because the MOTUs containing them included published sequences for multiple Linnaean species, suggesting either retention of ancestral haplotype polymorphism or identification errors in published sequences. Over 90% of UK specimens were identifiable as B. aeneus. Plant associations of adult B. aeneus were found to be far wider taxonomically than for their larvae. UK B. aeneus populations showed contrasting affiliations between the north (most similar to Scandinavia and the Baltic) and south (most similar to western continental Europe), with strong signatures of population growth in the south.

A horizon scan of future threats and opportunities for pollinators and pollination.

Background. Pollinators, which provide the agriculturally and ecologically essential service of pollination, are under threat at a global scale. Habitat loss and homogenisation, pesticides, parasites and pathogens, invasive species, and climate change have been identified as past and current threats to pollinators. Actions to mitigate these threats, e.g., agri-environment schemes and pesticide-use moratoriums, exist, but have largely been applied post-hoc. However, future sustainability of pollinators and the service they provide requires anticipation of potential threats and opportunities before they occur, enabling timely implementation of policy and practice to prevent, rather than mitigate, further pollinator declines. Methods.Using a horizon scanning approach we identified issues that are likely to impact pollinators, either positively or negatively, over the coming three decades. Results.Our analysis highlights six high priority, and nine secondary issues. High priorities are: (1) corporate control of global agriculture, (2) novel systemic pesticides, (3) novel RNA viruses, (4) the development of new managed pollinators, (5) more frequent heatwaves and drought under climate change, and (6) the potential positive impact of reduced chemical use on pollinators in non-agricultural settings. Discussion. While current pollinator management approaches are largely driven by mitigating past impacts, we present opportunities for pre-emptive practice, legislation, and policy to sustainably manage pollinators for future generations.

Food for Pollinators: Quantifying the Nectar and Pollen Resources of Urban Flower Meadows.

Planted meadows are increasingly used to improve the biodiversity and aesthetic amenity value of urban areas. Although many 'pollinator-friendly' seed mixes are available, the floral resources these provide to flower-visiting insects, and how these change through time, are largely unknown. Such data are necessary to compare the resources provided by alternative meadow seed mixes to each other and to other flowering habitats. We used quantitative surveys of over 2 million flowers to estimate the nectar and pollen resources offered by two exemplar commercial seed mixes (one annual, one perennial) and associated weeds grown as 300m2 meadows across four UK cities, sampled at six time points between May and September 2013. Nectar sugar and pollen rewards per flower varied widely across 65 species surveyed, with native British weed species (including dandelion, Taraxacum agg.) contributing the top five nectar producers and two of the top ten pollen producers. Seed mix species yielding the highest rewards per flower included Leontodon hispidus, Centaurea cyanus and C. nigra for nectar, and Papaver rhoeas, Eschscholzia californica and Malva moschata for pollen. Perennial meadows produced up to 20x more nectar and up to 6x more pollen than annual meadows, which in turn produced far more than amenity grassland controls. Perennial meadows produced resources earlier in the year than annual meadows, but both seed mixes delivered very low resource levels early in the year and these were provided almost entirely by native weeds. Pollen volume per flower is well predicted statistically by floral morphology, and nectar sugar mass and pollen volume per unit area are correlated with flower counts, raising the possibility that resource levels can be estimated for species or habitats where they cannot be measured directly. Our approach does not incorporate resource quality information (for example, pollen protein or essential amino acid content), but can easily do so when suitable data exist. Our approach should inform the design of new seed mixes to ensure continuity in floral resource availability throughout the year, and to identify suitable species to fill resource gaps in established mixes.

Constructing more informative plant-pollinator networks: visitation and pollen deposition networks in a heathland plant community.

Interaction networks are widely used as tools to understand plant-pollinator communities, and to examine potential threats to plant diversity and food security if the ecosystem service provided by pollinating animals declines. However, most networks to date are based on recording visits to flowers, rather than recording clearly defined effective pollination events. Here we provide the first networks that explicitly incorporate measures of pollinator effectiveness (PE) from pollen deposition on stigmas per visit, and pollinator importance (PI) as the product of PE and visit frequency. These more informative networks, here produced for a low diversity heathland habitat, reveal that plant-pollinator interactions are more specialized than shown in most previous studies. At the studied site, the specialization index [Formula: see text] was lower for the visitation network than the PE network, which was in turn lower than [Formula: see text] for the PI network. Our study shows that collecting PE data is feasible for community-level studies in low diversity communities and that including information about PE can change the structure of interaction networks. This could have important consequences for our understanding of threats to pollination systems.

Where is the UK's pollinator biodiversity? The importance of urban areas for flower-visiting insects.

Insect pollinators provide a crucial ecosystem service, but are under threat. Urban areas could be important for pollinators, though their value relative to other habitats is poorly known. We compared pollinator communities using quantified flower-visitation networks in 36 sites (each 1 km(2)) in three landscapes: urban, farmland and nature reserves. Overall, flower-visitor abundance and species richness did not differ significantly between the three landscape types. Bee abundance did not differ between landscapes, but bee species richness was higher in urban areas than farmland. Hoverfly abundance was higher in farmland and nature reserves than urban sites, but species richness did not differ significantly. While urban pollinator assemblages were more homogeneous across space than those in farmland or nature reserves, there was no significant difference in the numbers of rarer species between the three landscapes. Network-level specialization was higher in farmland than urban sites. Relative to other habitats, urban visitors foraged from a greater number of plant species (higher generality) but also visited a lower proportion of available plant species (higher specialization), both possibly driven by higher urban plant richness. Urban areas are growing, and improving their value for pollinators should be part of any national strategy to conserve and restore pollinators.

The potential for indirect effects between co-flowering plants via shared pollinators depends on resource abundance, accessibility and relatedness.

Co-flowering plant species commonly share flower visitors, and thus have the potential to influence each other's pollination. In this study we analysed 750 quantitative plant-pollinator networks from 28 studies representing diverse biomes worldwide. We show that the potential for one plant species to influence another indirectly via shared pollinators was greater for plants whose resources were more abundant (higher floral unit number and nectar sugar content) and more accessible. The potential indirect influence was also stronger between phylogenetically closer plant species and was independent of plant geographic origin (native vs. non-native). The positive effect of nectar sugar content and phylogenetic proximity was much more accentuated for bees than for other groups. Consequently, the impact of these factors depends on the pollination mode of plants, e.g. bee or fly pollinated. Our findings may help predict which plant species have the greatest importance in the functioning of plant-pollination networks.

Daily temporal structure in African savanna flower visitation networks and consequences for network sampling.

Ecological interaction networks are a valuable approach to understanding plant-pollinator interactions at the community level. Highly structured daily activity patterns are a feature of the biology of many flower visitors, particularly provisioning female bees, which often visit different floral sources at different times. Such temporal structure implies that presence/absence and relative abundance of specific flower-visitor interactions (links) in interaction networks may be highly sensitive to the daily timing of data collection. Further, relative timing of interactions is central to their possible role in competition or facilitation of seed set among coflowering plants sharing pollinators. To date, however, no study has examined the network impacts of daily temporal variation in visitor activity at a community scale. Here we use temporally structured sampling to examine the consequences of daily activity patterns upon network properties using fully quantified flower-visitor interaction data for a Kenyan savanna habitat. Interactions were sampled at four sequential three-hour time intervals between 06:00 and 18:00, across multiple seasonal time points for two sampling sites. In all data sets the richness and relative abundance of links depended critically on when during the day visitation was observed. Permutation-based null modeling revealed significant temporal structure across daily time intervals at three of the four seasonal time points, driven primarily by patterns in bee activity. This sensitivity of network structure shows the need to consider daily time in network sampling design, both to maximize the probability of sampling links relevant to plant reproductive success and to facilitate appropriate interpretation of interspecific relationships. Our data also suggest that daily structuring at a community level could reduce indirect competitive interactions when coflowering plants share pollinators, as is commonly observed during flowering in highly seasonal habitats.