Predicting plant-pollinator interactions: concepts, methods, and challenges.

Plant-pollinator interactions are ecologically and economically important, and, as a result, their prediction is a crucial theoretical and applied goal for ecologists. Although various analytical methods are available, we still have a limited ability to predict plant-pollinator interactions. The predictive ability of different plant-pollinator interaction models depends on the specific definitions used to conceptualize and quantify species attributes (e.g., morphological traits), sampling effects (e.g., detection probabilities), and data resolution and availability. Progress in the study of plant-pollinator interactions requires conceptual and methodological advances concerning the mechanisms and species attributes governing interactions as well as improved modeling approaches to predict interactions. Current methods to predict plant-pollinator interactions present ample opportunities for improvement and spark new horizons for basic and applied research.

Predictions and test of multiple climate-species richness hypotheses to explain the spatial distribution of tenebrionid beetles in mountain environments.

Few studies have evaluated how climate is mechanistically related to species richness in mountain environments. We used path analysis to evaluate predictions of several mechanistic hypotheses based on their hypothesized mechanism relating climate with richness of darkling beetles (Coleoptera: Tenebrionidae). We modeled the influence of spatial covariation on climatic variables and tenebrionid richness. Results showed that richness peaks at mid elevations, chiefly influenced by precipitation and temperature, both directly and indirectly through geographic range sizes. The best fitting model explains 84% of the variance of tenebrionid richness. We suggest this pattern is induced by a water-energy balance along the altitudinal gradient. At low elevations, energy availability is high but water deficit may limit species richness; in contrast, at high elevations water availability is high, but energy deficit may limit species richness. These results suggest high susceptibility of the study region to future global climate change.

Invasive species modulate the structure and stability of a multilayer mutualistic network.

Species interactions are critical for maintaining community structure and dynamics, but the effects of invasive species on multitrophic networks remain poorly understood. We leveraged an ongoing invasion scenario in Patagonia, Argentina, to explore how non-native ungulates affect multitrophic networks. Ungulates disrupt a hummingbird-mistletoe-marsupial keystone interaction, which alters community composition. We sampled pollination and seed dispersal interactions in intact and invaded sites. We constructed pollination and seed dispersal networks for each site, which we connected via shared plants. We calculated pollination-seed dispersal connectivity, identified clusters of highly connected species, and quantified species' roles in connecting species clusters. To link structural variation to stability, we quantified network tolerance to single random species removal (disturbance propagation) and sequential species removal (robustness) using a stochastic coextinction model. Ungulates reduced the connectivity between pollination and seed dispersal and produced fewer clusters with a skewed size distribution. Moreover, species shifted their structural role, fragmenting the network by reducing the 'bridges' among species clusters. These structural changes altered the dynamics of cascading effects, increasing disturbance propagation and reducing network robustness. Our results highlight invasive species' role in altering community structure and subsequent stability in multitrophic communities.

Electromagnetic fields disrupt the pollination service by honeybees.

We assessed the effect that electromagnetic field (EMF) exerts on honeybees' pollination efficiency using field and laboratory experiments. First, we measured levels of gene and protein expression in metabolic pathways involved in stress and behavioral responses elicited by EMF. Second, we assessed the effect of EMF on honeybee behavior and seed production by the honeybee-pollinated California poppy and, lastly, by measuring the consequences of pollination failure on plants' community richness and abundance. EMF exposure exerted strong physiological stress on honeybees as shown by the enhanced expression of heat-shock proteins and genes involved in antioxidant activity and affected the expression levels of behavior-related genes. Moreover, California poppy individuals growing near EMF received fewer honeybee visits and produced fewer seeds than plants growing far from EMF. Last, we found a hump-shaped relationship between EMF and plant species richness and plant abundance. Our study provides conclusive evidence of detrimental impacts of EMF on honeybee's pollination behavior, leading to negative effects on plant community.

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.

Plant-frugivore network simplification under habitat fragmentation leaves a small core of interacting generalists.

Habitat fragmentation impacts seed dispersal processes that are important in maintaining biodiversity and ecosystem functioning. However, it is still unclear how habitat fragmentation affects frugivorous interactions due to the lack of high-quality data on plant-frugivore networks. Here we recorded 10,117 plant-frugivore interactions from 22 reservoir islands and six nearby mainland sites using the technology of arboreal camera trapping to assess the effects of island area and isolation on the diversity, structure, and stability of plant-frugivore networks. We found that network simplification under habitat fragmentation reduces the number of interactions involving specialized species and large-bodied frugivores. Small islands had more connected, less modular, and more nested networks that consisted mainly of small-bodied birds and abundant plants, as well as showed evidence of interaction release (i.e., dietary expansion of frugivores). Our results reveal the importance of preserving large forest remnants to support plant-frugivore interaction diversity and forest functionality.

Quantitative Prediction of Interactions in Bipartite Networks Based on Traits, Abundances, and Phylogeny.

AbstractEcological interactions link species in networks. Loss of species from or introduction of new species into an existing network may have substantial effects for interaction patterns. Predicting changes in interaction frequency while allowing for rewiring of existing interactions-and hence estimating the consequences of community compositional changes-is thus a central challenge for network ecology. Interactions between species groups, such as pollinators and flowers or parasitoids and hosts, are moderated by matching morphological traits or sensory clues, most of which are unknown to us. If these traits are phylogenetically conserved, however, we can use phylogenetic distances to construct latent, surrogate traits and try to match those across groups, in addition to observed traits. Understanding how important traits and trait matching are, relative to abundances and chance, is crucial to estimating the fundamental predictability of network interactions. Here, we present a statistically sound approach ("tapnet") to fitting abundances, traits, and phylogeny to observed network data to predict interaction frequencies. We thereby expand existing approaches to quantitative bipartite networks, which so far have failed to correctly represent the nonindependence of network interactions. Furthermore, we use simulations and cross validation on independent data to evaluate the predictive power of the fit. Our results show that tapnet is on a par with abundance-only, matching centrality, and machine learning approaches. This approach also allows us to evaluate how well current concepts of trait matching work. On the basis of our results, we expect that interactions in well-sampled networks can be well predicted if traits and abundances are the main driver of interaction frequency.

Ecological network complexity scales with area.

Larger geographical areas contain more species-an observation raised to a law in ecology. Less explored is whether biodiversity changes are accompanied by a modification of interaction networks. We use data from 32 spatial interaction networks from different ecosystems to analyse how network structure changes with area. We find that basic community structure descriptors (number of species, links and links per species) increase with area following a power law. Yet, the distribution of links per species varies little with area, indicating that the fundamental organization of interactions within networks is conserved. Our null model analyses suggest that the spatial scaling of network structure is determined by factors beyond species richness and the number of links. We demonstrate that biodiversity-area relationships can be extended from species counts to higher levels of network complexity. Therefore, the consequences of anthropogenic habitat destruction may extend from species loss to wider simplification of natural communities.

A keystone mutualism promotes resistance to invasion.

It is not uncommon for one or a few species, and their interactions, to have disproportionate effects on other species in ecological communities. Such keystone interactions might affect how communities respond to the invasion of non-native species by preventing or inhibiting the establishment, spread or impact of non-native species. We explore whether a keystone mutualism among a hummingbird-mistletoe-marsupial promotes ecological resistance to an invasive pollinator, the bumblebee Bombus terrestris, by comparing data collected at sites prior to bumblebee invasion to data collected 11 years after the invasion in sites with and without the keystone mutualism. We built pollination networks and focused on network motifs, regarded as building blocks of networks, to identify the central pollinators and estimate the change in their interactions after invasion of B. terrestris. We also estimated the interaction rewiring across the season in post-invasion networks and tested it as a possible mechanism explaining how the keystone mutualism increased ecological resistance to invasion. We found two times more species in post-invasion sites with the keystone mutualism than in post-invasion sites without the keystone mutualism. Moreover, we found that invasive bumblebee reduced the strength and interaction niche of the five central pollinator species while increasing its own strength and interaction niche, suggesting a replacement of interactions. Also, we found that the keystone mutualism promoted resistance to B. terrestris invasion by reducing its negative impacts on central species. In the presence of the keystone mutualism, central species had three times more direct interactions than in sites without this keystone mutualism. The higher interaction rewiring, after invasion of B. terrestris, in sites with the keystone mutualism indicates greater chances of central pollinators to form new interactions and reduces their competence for resources with the non-native bumblebee. Our results demonstrate that a keystone mutualism can enhance community resistance against the impacts of a non-native invasive pollinator by increasing species diversity and promoting interaction rewiring in the community. This study suggests that the conservation of mutualisms, especially those considered keystone, could be essential for long-term preservation of natural communities under current and future impacts of global change.

Es común que una o unas pocas especies y sus interacciones tengan efectos desproporcionado sobre otras especies en las comunidades. Estas especies y sus interacciones claves podrían afectar el modo en que las comunidades responden a la invasión de especies no nativas al prevenir o disminuir su establecimiento, su propagación o el impacto de las mismas. En este estudio evaluamos si un mutualismo clave entre un colibrí, un muérdago y un marsupial promueve la resistencia de la comunidad frente a un polinizador invasor, el abejorro Bombus terrestris, mediante la comparación de datos colectados en sitios previos a la invasión del abejorro y datos colectados 11 años después de su invasión, en sitios con y sin el mutualismo clave. Construimos redes ecológicas planta-polinizador y nos centramos en los modos de interacción ("interaction motifs"), los cuales son usados como bloques en la construcción de las redes, para identificar los polinizadores centrales y estimar el cambio en sus interacciones después de la invasión de B. terrestris. Además, en las redes posteriores a la invasión estimamos la reconexión de interacciones a lo largo de la temporada y la evaluamos como un posible mecanismo mediante la cual el mutualismo clave aumentó la resistencia a la invasión. En sitios posteriores a la invasión con el mutualismo clave encontramos dos veces más especies que en sitios posteriores a la invasión ausentes de éste. Además, en los sitios ausentes del mutualismo clave, encontramos que el abejorro invasor redujo la fuerza y el nicho de interacción de los cinco polinizadores centrales mientras incrementó su propia fuerza y nicho de interacciones, sugiriendo un reemplazo de interacciones. Asimismo, encontramos que el mutualismo clave promovió la resistencia de la comunidad a la invasión de B. terrestris al reducir sus impactos negativos sobre las especies centrales. En presencia del mutualismo clave, las especies centrales presentaron tres veces más interacciones directas que en sitios ausentes de esta interacción. La gran reconexión de interacciones encontrada en sitios posteriores a la invasión con el mutualismo clave indica mayores probabilidades de que los polinizadores centrales formen nuevas interacciones y reduzcan la competencia por recursos con el abejorro no nativo. Nuestros resultados demuestran que un mutualismo clave puede mejorar la resistencia de la comunidad frente a los impactos de especies invasoras al incrementar la diversidad de especies y promover la reconexión de interacciones en la comunidad. Este estudio sugiere que la conservación de las interacciones mutualistas, principalmente aquellas consideradas claves, podría ser esencial para preservar las comunidades naturales frente a los impactos del cambio global.

The disruption of a keystone interaction erodes pollination and seed dispersal networks.

Understanding the impacts of global change on ecological communities is a major challenge in modern ecology. The gain or loss of particular species and the disruption of key interactions are both consequences and drivers of global change that can lead to the disassembly of ecological networks. We examined whether the disruption of a hummingbird-mistletoe-marsupial mutualism by the invasion of non-native species can have cascading effects on both pollination and seed dispersal networks in the temperate forest of Patagonia, Argentina. We focused on network motifs, subnetworks composed of a small number of species exhibiting particular patterns of interaction, to examine the structure and diversity of mutualistic networks. We found that the hummingbird-mistletoe-marsupial mutualism plays a critical role in the community by increasing the complexity of pollination and seed dispersal networks through supporting a high diversity of interactions. Moreover, we found that the disruption of this tripartite mutualism by non-native ungulates resulted in diverse indirect effects that led to less complex pollination and seed dispersal networks. Our results demonstrate that the gains and losses of particular species and the alteration of key interactions can lead to cascading effects in the community through the disassembly of mutualistic networks.

Within-day dynamics of plant-pollinator networks are dominated by early flower closure: an experimental test of network plasticity.

Temporal variability of plant-pollinator interactions is important for fully understanding the structure, function, and stability of plant-pollinator networks, but most network studies so far have ignored within-day dynamics. Strong diel dynamics (e.g., a regular daily cycle) were found for networks with Cichorieae, which typically close their flowers around noon. Here, we experimentally prevented early flower closure to test whether these dynamics are driven by the temporally limited availability of Cichorieae, or by timing of pollinator activity. We further tested if the dynamics involving Cichorieae and their pollinators also affect the dynamics on other plants in the network. Finally, we explored the structure of such manipulated networks (with Cichorieae available in the morning and afternoon) compared to unmanipulated controls (Cichorieae available only in the morning). We found that flower closure of Cichorieae is indeed an important driver of diel network dynamics, while other drivers of pollinator timing appeared less important. If Cichorieae flowers were available in the afternoon, they were visited by generalist and specialist pollinators, which overall decreased link turnover between morning and afternoon. Effects of afternoon availability of Cichorieae on other plants in the network were inconclusive: pollinator switching to and from Cichorieae tended to increase. On the level of the aggregated (full-day) network, the treatment resulted in increased dominance of Cichorieae, reducing modularity and increasing plant generality. These results highlight that network dynamics can be predicted by knowledge of diel or seasonal phenology, and that fixed species timing assumptions will misrepresent the expected dynamics.

Plant-plant co-occurrences under a complex land-use gradient in a temperate forest.

Land-use generates multiple stress factors, and we need to understand their effects on plant-plant interactions to predict the consequences of land-use intensification. The stress-gradient hypothesis predicts that the relative strength of positive and negative interactions changes inversely under increasing environmental stress. However, the outcome of interactions also depends on stress factor's complexity, the scale of analysis, and the role of functional traits in structuring the community. We evaluated plant-plant co-occurrences in a temperate forest, aiming to identify changes in pairwise and network metrics under increasing silvopastoral use intensity. Proportionally, positive co-occurrences were more frequent under high than low use, while negative co-occurrences were more frequent under low than high. Networks of negative co-occurrences showed higher centralization under low use, while networks of positive co-occurrences showed lower modularity and higher centralization under high use. We found a partial relationship between co-occurrences and key functional traits expected to mediate facilitation and competition processes. Our results shows that the stress-gradient hypothesis predicts changes in spatial co-occurrences even when two stress factors interact in a complex way. Networks of negative co-occurrences showed a hierarchical effect of dominant species under low use intensity. But positive co-occurrence network structure partially presented the characteristics expected if the facilitation was an important mechanism characterizing the community under high disturbance intensity. The partial relationship between functional traits and co-occurrences may indicate that other factors besides biotic interactions may be structuring the observed negative spatial associations in temperate Patagonian forests.

Plant-pollinator interactions between generalists persist over time and space.

Generalist species are the linchpins of networks, as they are important for maintaining network structure and function. Previous studies have shown that interactions between generalists tend to occur consistently across years and sites. However, the link between temporal and spatial interaction persistence across scales remains unclear. To address this gap, we collected data on plant-pollinator interactions throughout the flowering period for 5 yr across six plots in a subalpine meadow in the Rocky Mountains. We found that interactions between generalists tended to persist more in time and space such that interactions near the network core were more frequently recorded across years, within seasons, and among plots. We posit that species' tolerance of environmental variation across time and space plays a key role in generalization by regulating spatiotemporal overlap with interaction partners. Our results imply a role of spatiotemporal environmental variation in organizing species interactions, marrying niche concepts that emphasize species environmental constraints and their community role.

Seeing through the static: the temporal dimension of plant-animal mutualistic interactions.

Most studies of plant-animal mutualistic networks have come from a temporally static perspective. This approach has revealed general patterns in network structure, but limits our ability to understand the ecological and evolutionary processes that shape these networks and to predict the consequences of natural and human-driven disturbance on species interactions. We review the growing literature on temporal dynamics of plant-animal mutualistic networks including pollination, seed dispersal and ant defence mutualisms. We then discuss potential mechanisms underlying such variation in interactions, ranging from behavioural and physiological processes at the finest temporal scales to ecological and evolutionary processes at the broadest. We find that at the finest temporal scales (days, weeks, months) mutualistic interactions are highly dynamic, with considerable variation in network structure. At intermediate scales (years, decades), networks still exhibit high levels of temporal variation, but such variation appears to influence network properties only weakly. At the broadest temporal scales (many decades, centuries and beyond), continued shifts in interactions appear to reshape network structure, leading to dramatic community changes, including loss of species and function. Our review highlights the importance of considering the temporal dimension for understanding the ecology and evolution of complex webs of mutualistic interactions.

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.

Strength of niche processes for species interactions is lower for generalists and exotic species.

Niche and neutral processes jointly influence species interactions. Predictions of interactions based on these processes assume that they operate similarly across all species. However, species characteristics could systematically create differences in the strength of niche or neutral processes for each interspecific interaction. We used national-level records of plant-frugivore interactions, species traits, biogeographic status (native vs. exotic), phylogenies and species range sizes to test the hypothesis that the strength of niche processes in species interactions changes in predictable ways depending on trophic generalism and biogeographic status of the interacting species. The strength of niche processes (measured as trait matching) decreased when the generalism of the interacting partners increased. Furthermore, the slope of this negative relationship between trait matching and generalism of the interacting partners was steeper (more negative) for interactions between exotic species than those between native species. These results remained significant after accounting for the potential effects of neutral processes (estimated by species range size). These observed changes in the strength of niche processes in generating species interactions, after accounting for effects of neutral processes, could improve predictions of ecological networks from species trait data. Specifically, due to their shorter co-evolutionary history, exotic species tend to interact with native species even when lower trait matching occurs than in interactions among native species. Likewise, interactions between generalist bird species and generalist plant species should be expected to occur despite low trait matching between species, whereas interactions between specialist species involve higher trait matching.

Trait matching and phenological overlap increase the spatio-temporal stability and functionality of plant-pollinator interactions.

Morphology and phenology influence plant-pollinator network structure, but whether they generate more stable pairwise interactions with higher pollination success remains unknown. Here we evaluate the importance of morphological trait matching, phenological overlap and specialisation for the spatio-temporal stability (measured as variability) of plant-pollinator interactions and for pollination success, while controlling for species' abundance. To this end, we combined a 6-year plant-pollinator interaction dataset, with information on species traits, phenologies, specialisation, abundance and pollination success, into structural equation models. Interactions among abundant plants and pollinators with well-matched traits and phenologies formed the stable and functional backbone of the pollination network, whereas poorly matched interactions were variable in time and had lower pollination success. We conclude that phenological overlap could be more useful for predicting changes in species interactions than species abundances, and that non-random extinction of species with well-matched traits could decrease the stability of interactions within communities and reduce their functioning.

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.

Landscape connectivity explains interaction network patterns at multiple scales.

Under a metacommunity framework, the spatial configuration of habitat fragments could determine local community structure. Yet, quantifying fragment connectivity is challenging, as it depends on multiple variables at several geographical scales. We assessed the extent to which fragment connectivity and area explain patterns in interaction structure among four herbivore guilds and their host plants in a metacommunity. We propose an integrative connectivity metric including geographic distance, neighboring fragment area and similarity in resource composition as an extension of Hanski's classic metric. We then used nonlinear models to assess whether fragment connectivity and area predicted link richness and similarity in link composition. We found that link richness was always negatively related to connectivity but at different geographic scales depending on the herbivore guild. In contrast, while link composition was also related to connectivity, the direction and strength of this relationship varied among herbivore guilds and type of link composition (qualitative or quantitative). Furthermore, focal fragment area was not an important determinant of interaction diversity in local communities. Our findings emphasize resource similarity as a novel dimension of fragment connectivity relevant in explaining interaction diversity patterns in natural trophic networks.

Phenology determines the robustness of plant-pollinator networks.

Plant-pollinator systems are essential for ecosystem functioning, which calls for an understanding of the determinants of their robustness to environmental threats. Previous studies considering such robustness have focused mostly on species' connectivity properties, particularly their degree. We hypothesized that species' phenological attributes are at least as important as degree as determinants of network robustness. To test this, we combined dynamic modeling, computer simulation and analysis of data from 12 plant-pollinator networks with detailed information of topology of interactions as well as species' phenology of plant flowering and pollinator emergence. We found that phenological attributes are strong determinants of network robustness, a result consistent across the networks studied. Plant species persistence was most sensitive to increased larval mortality of pollinators that start earlier or finish later in the season. Pollinator persistence was especially sensitive to decreased visitation rates and increased larval mortality of specialists. Our findings suggest that seasonality of climatic events and anthropic impacts such as the release of pollutants is critical for the future integrity of terrestrial biodiversity.