Plant-pollinator Communities Research Articles

Disentangling the role of floral sensory stimuli in pollination networks

Despite progress in understanding pollination network structure, the functional roles of floral sensory stimuli (visual, olfactory) have never been addressed comprehensively in a community context, even though such traits are known to mediate plant–pollinator interactions. Here, we use a comprehensive dataset of floral traits and a novel dynamic data-pooling methodology to explore the impacts of floral sensory diversity on the structure of a pollination network in a Mediterranean scrubland. Our approach tracks transitions in the network behaviour of each plant species throughout its flowering period and, despite dynamism in visitor composition, reveals significant links to floral scent, and/or colour as perceived by pollinators. Having accounted for floral phenology, abundance and phylogeny, the persistent association between floral sensory traits and visitor guilds supports a deeper role for sensory bias and diffuse coevolution in structuring plant–pollinator networks. This knowledge of floral sensory diversity, by identifying the most influential phenotypes, could help prioritize efforts for plant–pollinator community restoration.

Competition, trait–mediated facilitation, and the structure of plant–pollinator communities

Competition, trait–mediated facilitation, and the structure of plant–pollinator communities

Competition, trait–mediated facilitation, and the structure of plant–pollinator communities

In plant–pollinator communities many pollinators are potential generalists and their preferences for certain plants can change quickly in response to changes in plant and pollinator densities. These changes in preferences affect coexistence within pollinator guilds as well as within plant guilds. Using a mathematical model, we study how adaptations of pollinator preferences influence population dynamics of a two-plant–two-pollinator community interaction module. Adaptation leads to coexistence between generalist and specialist pollinators, and produces complex plant population dynamics, involving alternative stable states and discrete transitions in the plant community. Pollinator adaptation also leads to plant–plant apparent facilitation that is mediated by changes in pollinator preferences. We show that adaptive pollinator behavior reduces niche overlap and leads to coexistence by specialization on different plants. Thus, this article documents how adaptive pollinator preferences for plants change the structure and coexistence of plant–pollinator communities.

Opportunistic attachment assembles plant–pollinator networks

Species and interactions are being lost at alarming rates and it is imperative to understand how communities assemble if we have to prevent their collapse and restore lost interactions. Using an 8-year dataset comprising nearly 20000 pollinator visitation records, we explore the assembly of plant-pollinator communities at native plant restoration sites in an agricultural landscape. We find that species occupy highly dynamic network positions through time, causing the assembly process to be punctuated by major network reorganisations. The most persistent pollinator species are also the most variable in their network positions, contrary to what preferential attachment - the most widely studied theory of ecological network assembly - predicts. Instead, we suggest assembly occurs via an opportunistic attachment process. Our results contribute to our understanding of how communities assembly and how species interactions change through time while helping to inform efforts to reassemble robust communities.

Plant sex affects the structure of plant-pollinator networks in a subtropical forest.

Although it has long been recognized that the diversified sexual systems of plants could influence community patterns and pollination specialization, plant sex is not usually incorporated to quantify plant-pollinator networks. In this study, we observed 1776 visitations corresponding to 84 pollinator species and 28 plant species (19 sexually monomorphic plants and 9 dioecious plants) in a subtropical forest, China. We constructed three networks by, respectively, combining visitations to dioecious female and male plants at the species level, separating them, and retaining the shared visitations between them. When the shared visitations between male and female plants were considered, the modularity was increased and the nestedness was decreased with a significantly low robustness for the plant community. Only in this network, most dioecious and hermaphroditic plants were associated with different pollinator groups and separated to different modules. The results also showed that dioecious plants were more generalized and more likely to be module hubs in sex-combined network and sex-separated network but not in sex-shared network. Only in the sex-separated network, pollinators in dioecious modules were less selective than in hermaphroditic modules. Our study shows incorporating the different visitations between plant sexes could affect the analysis of key network structure properties and the description of pollination niche. To better understand niche partitioning and stability of plant-pollinator communities, it is necessary to compare pollination networks considering plant sexual diversity.

Artificial light at night as a new threat to pollination.

Pollinators are declining worldwide and this has raised concerns for a parallel decline in the essential pollination service they provide to both crops and wild plants. Anthropogenic drivers linked to this decline include habitat changes, intensive agriculture, pesticides, invasive alien species, spread of pathogens and climate change. Recently, the rapid global increase in artificial light at night has been proposed to be a new threat to terrestrial ecosystems; the consequences of this increase for ecosystem function are mostly unknown. Here we show that artificial light at night disrupts nocturnal pollination networks and has negative consequences for plant reproductive success. In artificially illuminated plant-pollinator communities, nocturnal visits to plants were reduced by 62% compared to dark areas. Notably, this resulted in an overall 13% reduction in fruit set of a focal plant even though the plant also received numerous visits by diurnal pollinators. Furthermore, by merging diurnal and nocturnal pollination sub-networks, we show that the structure of these combined networks tends to facilitate the spread of the negative consequences of disrupted nocturnal pollination to daytime pollinator communities. Our findings demonstrate that artificial light at night is a threat to pollination and that the negative effects of artificial light at night on nocturnal pollination are predicted to propagate to the diurnal community, thereby aggravating the decline of the diurnal community. We provide perspectives on the functioning of plant-pollinator communities, showing that nocturnal pollinators are not redundant to diurnal communities and increasing our understanding of the human-induced decline in pollinators and their ecosystem service.

Network analysis of phenological units to detect important species in plant-pollinator assemblages: can it inform conservation strategies?

Conservation of species is often focused either only on those that are endangered, or on maximising the number recorded on species lists. However, species share space and time with others, thus interacting and building frameworks of relationships that can be unravelled by community-level network analysis. It is these relationships that ultimately drive ecosystem function via the transfer of energy and nutrients. However interactions are rarely considered in conservation planning. Network analysis can be used to detect key species (“hubs”) that play an important role in cohesiveness of networks. We applied this approach to plant-pollinator communities on two montane Northern Apennine grasslands, paying special attention to the modules and the identity of hubs. We performed season-wide sampling and then focused the network analyses on time units consistent with plant phenology. After testing for significance of modules, only some modules were found to be significantly segregated from others. Thus, networks were organized around a structured core of modules with a set of companion species that were not organized into compartments. Using a network approach we obtained a list of important plant and pollinator species, including three Network Hubs of utmost importance, and other hubs of particular biogeographical interest. By having a lot of links and high partner diversity, hubs should convey stability to networks. Due to their role in the networks, taking into account such key species when considering the management of sites could help to preserve the greatest number of interactions and thus support many other species.

Ecological intensification to mitigate impacts of conventional intensive land use on pollinators and pollination.

Worldwide, human appropriation of ecosystems is disrupting plant–pollinator communities and pollination function through habitat conversion and landscape homogenisation. Conversion to agriculture is destroying and degrading semi‐natural ecosystems while conventional land‐use intensification (e.g. industrial management of large‐scale monocultures with high chemical inputs) homogenises landscape structure and quality. Together, these anthropogenic processes reduce the connectivity of populations and erode floral and nesting resources to undermine pollinator abundance and diversity, and ultimately pollination services. Ecological intensification of agriculture represents a strategic alternative to ameliorate these drivers of pollinator decline while supporting sustainable food production, by promoting biodiversity beneficial to agricultural production through management practices such as intercropping, crop rotations, farm‐level diversification and reduced agrochemical use. We critically evaluate its potential to address and reverse the land use and management trends currently degrading pollinator communities and potentially causing widespread pollination deficits. We find that many of the practices that constitute ecological intensification can contribute to mitigating the drivers of pollinator decline. Our findings support ecological intensification as a solution to pollinator declines, and we discuss ways to promote it in agricultural policy and practice.

Influence of plant–pollinator interactions on the assembly of plant and hummingbird communities

Summary Understanding how ecological processes structure species assemblages is a central issue in community ecology. While the influence of plant–pollinator interactions on each other's evolution is well recognized, their role in the assembly of interdependent communities of plants and pollinators is still unclear. Using data from seven communities of hummingbirds and plants that they pollinate from two tropical rain forest types (lowland and montane), we evaluated phylogenetic relationships and signal of functional traits, over space and time, to test predictions on the main processes (environmental filtering, facilitation or competition) that are driving these hummingbird–plant assemblages. Our findings suggest that the main processes driving these assemblages varied between hummingbirds and plants and between habitats, and even among communities at the same habitat. The non‐conserved floral trait and the phylogenetic patterns (even or random) give support to the hypothesis of facilitation or competition as processes regulating the composition of plant assemblages. Moreover, the positive relationship between fitness and flowering synchrony suggests facilitation as the most important mechanism for montane plant communities. Distinctively, for lowland plant communities, the combination of non‐conserved traits and clustered phylogenetic patterns may be a result of either adaptive radiation or biotic filtering driven by a particular pollinator species that plays a main role as plant community organizer. Lastly, evidence of trait conservatism, together with clustered or even phylogenetic patterns, suggests that facilitation or competition may drive the assembly of montane hummingbird communities, despite the predominance of random phylogenetic patterns. Synthesis. Overall, we present a pathway to identify central ecological processes that may drive the assembly of plant–pollinator communities. We show that different processes related with pollination that vary in space and time may contribute to the assembly of the interdependent tropical communities of plants and pollinators. These findings highlight the importance of considering ecological interactions when evaluating community assembly processes.

Changing odour landscapes: the effect of anthropogenic volatile pollutants on plant–pollinator olfactory communication

Summary Olfactory signals, often in synergy with visual signals, mediate the interactions between plants and animals. However, urbanization and agricultural practices are both sources of volatile organic compounds (VOCs) and reactive oxygen species (ROS) that have the potential to interfere with plant–animal communication and to disrupt mutualistic interactions. In this review, we explore how anthropogenic airborne pollutants may disrupt chemical information transfer between flowering plants and flower visitors. The emission of anthropogenic volatile pollutants (AVPs) including VOCs and formation of ROS, for example from traffic or industries, and non‐natural biogenic VOCs, for example from introduced crops, may have a number of effects: (i) changes in plant signalling as a consequence of plants experiencing physiological stress; (ii) chemical interference (chemical degradation/transformation of infochemicals); (iii) increased levels of background noise impeding signal detection; and (iv) changes in pollinator signal perception and behaviour. All of the above in turn could have consequences for the biological fitness of plants and animals that rely on olfactory information as pivotal functional signals. The study of anthropogenic airborne pollutants and their effects on plant signalling is just emerging and the impacts of this aspect of anthropogenic emissions are barely understood. Volatiles emitted from anthropogenically changed landscapes could, however, have far‐reaching consequences for ecosystem functioning in adjacent natural zones, particularly in fragmented landscapes. In response to the wide gap in our knowledge on the mechanisms that govern interference of anthropogenic VOCs with olfactory information, future research directions are proposed with the aim to inspire research to help elucidate the risks of anthropogenic VOCs for plant–pollinator communities and improve risk assessment strategies. A lay summary is available for this article.

Deliberately increased network connectance in a plant-pollinator community experiment

Deliberately increased network connectance in a plant-pollinator community experiment

Top-down network analysis characterizes hidden termite-termite interactions.

The analysis of ecological networks is generally bottom‐up, where networks are established by observing interactions between individuals. Emergent network properties have been indicated to reflect the dominant mode of interactions in communities that might be mutualistic (e.g., pollination) or antagonistic (e.g., host–parasitoid communities). Many ecological communities, however, comprise species interactions that are difficult to observe directly. Here, we propose that a comparison of the emergent properties from detail‐rich reference communities with known modes of interaction can inform our understanding of detail‐sparse focal communities. With this top‐down approach, we consider patterns of coexistence between termite species that live as guests in mounds built by other host termite species as a case in point. Termite societies are extremely sensitive to perturbations, which precludes determining the nature of their interactions through direct observations. We perform a literature review to construct two networks representing termite mound cohabitation in a Brazilian savanna and in the tropical forest of Cameroon. We contrast the properties of these cohabitation networks with a total of 197 geographically diverse mutualistic plant–pollinator and antagonistic host–parasitoid networks. We analyze network properties for the networks, perform a principal components analysis (PCA), and compute the Mahalanobis distance of the termite networks to the cloud of mutualistic and antagonistic networks to assess the extent to which the termite networks overlap with the properties of the reference networks. Both termite networks overlap more closely with the mutualistic plant–pollinator communities than the antagonistic host–parasitoid communities, although the Brazilian community overlap with mutualistic communities is stronger. The analysis raises the hypothesis that termite–termite cohabitation networks may be overall mutualistic. More broadly, this work provides support for the argument that cryptic communities may be analyzed via comparison to well‐characterized communities.

Species roles in plant–pollinator communities are conserved across native and alien ranges

AbstractAimAlien species alter interaction networks by disrupting existing interactions, for example between plants and pollinators, and by engaging in new interactions. Predicting the effects of an incoming invader can be difficult, although recent work suggests species roles in interaction networks may be conserved across locations. We test whether species roles in plant–pollinator networks differ between their native and alien ranges and whether the former can be used to predict the latter.LocationWorld‐wide.MethodsWe used 64 plant–pollinator networks to search for species occurring in at least one network in its native range and one network in its alien range. We found 17 species meeting these criteria, distributed in 48 plant–pollinator networks. We characterized each species’ role by estimating species‐level network indices: normalized degree, closeness centrality, betweenness centrality and two measures of contribution to modularity (c‐andz‐scores). Linear mixed models and linear regression models were used to test for differences in species role between native and alien ranges and to predict those roles from the native to the alien range, respectively.ResultsSpecies roles varied considerably across species. Nevertheless, although species lost their native mutualists and gained novel interactions in the alien community, their role did not differ significantly between ranges. Consequently, closeness centrality and normalized degree in the alien range were highly predictable from the native range networks.Main conclusionsSpecies with high degree and centrality define the core of nested networks. Our results suggest that core species are likely to establish interactions and be core species in the alien range, whilst species with few interactions in their native range will behave similarly in their alien range. Our results provide new insights into species role conservatism and could help ecologists to predict alien species impact at the community level.

Habitat type plays a greater role than livestock grazing in structuring shrubsteppe plant–pollinator communities

Livestock grazing is a widespread grassland disturbance and can negatively impact biodiversity. Pollinators constitute a vital component of grassland ecosystems, but the impact of grazing on pollinator diversity has seldom been evaluated in North America. We assessed vegetation structure, and pollinator and flowering plant abundance, richness, diversity, and community composition in four pairs of spring-grazed/ungrazed sites in south-central British Columbia, Canada. We also investigated whether pollinator or floral communities differed between the two threatened shrubsteppe habitat types we sampled—antelope-brush and big sagebrush shrubsteppe. Pan-trapping surveys captured 5907 bees, flies, beetles, wasps and butterflies constituting 253 species. We found that the percent cover of shrubs and bare soil increased with grazing, while the height of grasses and forbs decreased. In contrast, pollinator and flowering plant abundance, richness, diversity, and community composition were not significantly affected by grazing. Flowering plant and pollinator community composition did differ significantly between shrubsteppe habitats. Our results indicate that grasslands in North America, when managed responsibly, can maintain pollinator and flowering plant diversity under grazing pressure. The continued effort of land managers to balance ecological integrity and economic viability will be important for the conservation of grassland pollination systems.

Exotic Plant Infestation Is Associated with Decreased Modularity and Increased Numbers of Connectors in Mixed-Grass Prairie Pollination Networks.

The majority of pollinating insects are generalists whose lifetimes overlap flowering periods of many potentially suitable plant species. Such generality is instrumental in allowing exotic plant species to invade pollination networks. The particulars of how existing networks change in response to an invasive plant over the course of its phenology are not well characterized, but may shed light on the probability of long-term effects on plant-pollinator interactions and the stability of network structure. Here we describe changes in network topology and modular structure of infested and non-infested networks during the flowering season of the generalist non-native flowering plant, Cirsium arvense in mixed-grass prairie at Badlands National Park, South Dakota, USA. Objectives were to compare network-level effects of infestation as they propagate over the season in infested and non-infested (with respect to C. arvense) networks. We characterized plant-pollinator networks on 5 non-infested and 7 infested 1-ha plots during 4 sample periods that collectively covered the length of C. arvense flowering period. Two other abundantly-flowering invasive plants were present during this time: Melilotus officinalis had highly variable floral abundance in both C. arvense-infested and non-infested plots and Convolvulus arvensis, which occurred almost exclusively in infested plots and peaked early in the season. Modularity, including roles of individual species, and network topology were assessed for each sample period as well as in pooled infested and non-infested networks. Differences in modularity and network metrics between infested and non-infested networks were limited to the third and fourth sample periods, during flower senescence of C. arvense and the other invasive species; generality of pollinators rose concurrently, suggesting rewiring of the network and a lag effect of earlier floral abundance. Modularity was lower and number of connectors higher in infested networks, whether they were assessed in individual sample periods or pooled into infested and non-infested networks over the entire blooming period of C. arvense. Connectors typically did not reside within the same modules as C. arvense, suggesting that effects of the other invasive plants may also influence the modularity results, and that effects of infestation extend to co-flowering native plants. We conclude that the presence of abundantly flowering invasive species is associated with greater network stability due to decreased modularity, but whether this is advantageous for the associated native plant-pollinator communities depends on the nature of perturbations they experience.

Pyrodiversity begets plant-pollinator community diversity.

Fire has a major impact on the structure and function of many ecosystems globally. Pyrodiversity, the diversity of fires within a region (where diversity is based on fire characteristics such as extent, severity, and frequency), has been hypothesized to promote biodiversity, but changing climate and land management practices have eroded pyrodiversity. To assess whether changes in pyrodiversity will have impacts on ecological communities, we must first understand the mechanisms that might enable pyrodiversity to sustain biodiversity, and how such changes might interact with other disturbances such as drought. Focusing on plant-pollinator communities in mixed-conifer forest with frequent fire in Yosemite National Park, California, we examine how pyrodiversity, combined with drought intensity, influences those communities. We find that pyrodiversity is positively related to the richness of the pollinators, flowering plants, and plant-pollinator interactions. On average, a 5% increase in pyrodiversity led to the gain of approximately one pollinator and one flowering plant species and nearly two interactions. We also find that a diversity of fire characteristics contributes to the spatial heterogeneity (β-diversity) of plant and pollinator communities. Lastly, we find evidence that fire diversity buffers pollinator communities against the effects of drought-induced floral resource scarcity. Fire diversity is thus important for the maintenance of flowering plant and pollinator diversity and predicted shifts in fire regimes to include less pyrodiversity compounded with increasing drought occurrence will negatively influence the richness of these communities in this and other forested ecosystems. In addition, lower heterogeneity of fire severity may act to reduce spatial turnover of plant-pollinator communities. The heterogeneity of community composition is a primary determinant of the total species diversity present in a landscape, and thus, lower pyrodiversity may negatively affect the richness of plant-pollinator communities across large spatial scales.

Low flower-size variation in bilaterally symmetrical flowers: Support for the pollination precision hypothesis.

The evolutionary shift from radial to bilateral symmetry in flowers is generally associated with the evolution of low flower-size variation. This phenomenon supports the hypothesis that the lower size variation in bilateral flowers can be attributed to low pollinator diversity. In this study, we propose two other hypotheses to explain low flower-size variation in bilateral symmetrical flowers. To test the three hypotheses, we examined the relative importance of pollinator diversity, composition, and bilateral symmetry itself as selective forces on low flower-size variation. We examined pollinator diversity and composition and flower-size variation for 36 species in a seminatural ecosystem with high bee richness and frequent lepidopteran visitation. Bilateral flowers were more frequently visited than radial flowers by larger bees, but functional-group diversity of the pollinators did not differ between symmetry types. Although bilateral flowers had significantly lower flower-size variation than radial flowers, flower-size variation did not vary with pollinator diversity and composition but was instead related to bilateral symmetry. Our results suggest that the lower size variation in bilateral flowers might have evolved under selection favoring the control of pollinator behavior on flowers to enhance the accurate placement of pollen on the body of the pollinator, independent of pollinator type. Because of the limited research on this issue, future work should be conducted in various types of plant-pollinator communities worldwide to further clarify the issue.

Exploring the nature of ecological specialization in a coral reef fish community: morphology, diet and foraging microhabitat use.

Patterns of ecological specialization offer invaluable information about ecosystems. Yet, specialization is rarely quantified across several ecological niche axes and variables beyond the link between morphological and dietary specialization have received little attention. Here, we provide a quantitative evaluation of ecological specialization in a coral reef fish assemblage (f. Acanthuridae) along one fundamental and two realized niche axes. Specifically, we examined ecological specialization in 10 surgeonfish species with regards to morphology and two realized niche axes associated with diet and foraging microhabitat utilization using a recently developed multidimensional framework. We then investigated the potential relationships between morphological and behavioural specialization. These relationships differed markedly from the traditional ecomorphological paradigm. While morphological specialization showed no relationship with dietary specialization, it exhibited a strong relationship with foraging microhabitat specialization. However, this relationship was inverted: species with specialized morphologies were microhabitat generalists, whereas generalized morphotypes were microhabitat specialists. Interestingly, this mirrors relationships found in plant-pollinator communities and may also be applicable to other ecosystems, highlighting the potential importance of including niche axes beyond dietary specialization into ecomorphological frameworks. On coral reefs, it appears that morphotypes commonly perceived as most generalized may, in fact, be specialized in exploiting flat and easily accessible microhabitats.

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 was lower for the visitation network than the PE network, which was in turn lower than 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.

How do fynbos plant–pollinator communities respond to the loss of birds?

How do fynbos plant–pollinator communities respond to the loss of birds?