Plant diversity increases spatio‐temporal niche complementarity in plant‐pollinator interactions

Ongoing biodiversity decline impairs ecosystem processes, including pollination. Flower visitation, an important indicator of pollination services, is influenced by plant species richness. However, the spatio‐temporal responses of different pollinator groups to plant species richness have not yet been analyzed experimentally. Here, we used an experimental plant species richness gradient to analyze plant–pollinator interactions with an unprecedented spatio‐temporal resolution. We observed four pollinator functional groups (honeybees, bumblebees, solitary bees, and hoverflies) in experimental plots at three different vegetation strata between sunrise and sunset. Visits were modified by plant species richness interacting with time and space. Furthermore, the complementarity of pollinator functional groups in space and time was stronger in species‐rich mixtures. We conclude that high plant diversity should ensure stable pollination services, mediated via spatio‐temporal niche complementarity in flower visitation.     

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.     

Foraging efficiency and size matching in a plant–pollinator community: the importance of sugar content and tongue length

A long‐standing question in ecology is how species interactions are structured within communities. Although evolutionary theory predicts close size matching between floral nectar tube depth and pollinator proboscis length of interacting species, such size matching has seldom been shown and explained in multispecies assemblages. Here, we investigated the degree of size matching among Asteraceae and their pollinators and its relationship with foraging efficiency. The majority of pollinators, especially Hymenoptera, choose plant species on which they had high foraging efficiencies. When proboscides were shorter than nectar tubes, foraging efficiency rapidly decreased because of increased handling time. When proboscides were longer than nectar tubes, a decreased nectar reward rather than an increased handling time made shallow flowers more inefficient to visit. Altogether, this led to close size matching. Overall, our results show the importance of nectar reward and handling time as drivers of plant–pollinator network structure.     

Non‐linear relationship between intensity of plant–animal interactions and selection strength

The shape of the relationship between intensity of biotic interactions and strength of selection is important for spatial variation in selection, but is little explored. We quantified interactions and selection in 69 populations of the short‐lived herb Primula farinosa. As predicted because of saturation and depletion effects, the strength of selection on a discrete and on a continuously varying floral display trait were in several cases significantly non‐linearly related to the mean intensity of mutualistic and antagonistic interactions. Strength of selection was strongest at low levels of fruit initiation and at high intensities of seed predation. Seed predation varied more among populations than did fruit initiation and could explain a larger proportion of the among‐population variation in strength of selection. Our results support the contention that interaction intensity affects selection strength, and suggests that for mutualistic and antagonistic interactions that can be saturated or depleted, this relationship is sometimes non‐linear.     

Interaction rewiring and the rapid turnover of plant–pollinator networks

Whether species interactions are static or change over time has wide‐reaching ecological and evolutionary consequences. However, species interaction networks are typically constructed from temporally aggregated interaction data, thereby implicitly assuming that interactions are fixed. This approach has advanced our understanding of communities, but it obscures the timescale at which interactions form (or dissolve) and the drivers and consequences of such dynamics. We address this knowledge gap by quantifying the within‐season turnover of plant–pollinator interactions from weekly censuses across 3 years in a subalpine ecosystem. Week‐to‐week turnover of interactions (1) was high, (2) followed a consistent seasonal progression in all years of study and (3) was dominated by interaction rewiring (the reassembly of interactions among species). Simulation models revealed that species’ phenologies and relative abundances constrained both total interaction turnover and rewiring. Our findings reveal the diversity of species interactions that may be missed when the temporal dynamics of networks are ignored.     

Pollination in Lilium sargentiae (Liliaceae) and the first confirmation of long‐tongued hawkmoths as a pollinator niche in Asia

The geographical distribution of pollinators is an important factor determining the biogeographical pattern of floral evolution and diversification. In Africa, a guild of plant species has converged in a floral syndrome for pollination by long‐tongued hawkmoths (predominantly Agrius convolvuli). It is hypothesized that such floral convergence could track the geographical distribution of long‐tongued hawkmoths, so it may not be confined to Africa. We investigated the pollination biology of Lilium sargentiae E. H. Wilson, which is endemic to China and exhibits traits suggestive of long‐tongued hawkmoth pollination. Lilium sargentiae was visited by A. convolvuli as well as small beetles (Nitidulidae) but pollination was mostly or totally effected by the moth. It was consistent with other hawkmoth‐pollinated plants in terms of floral tube length, nectar traits, tepal reflectance, and scent composition. We present the first experimental evidence for the hypothesis proposed above and for hawkmoth pollination in the widespread and ornamentally and economically important genus Lilium L. in a natural habitat. Our findings imply that long‐tongued hawkmoths (especially the extremely widespread A. convolvuli) as a distinctive pollinator niche may have underlain the evolution of long‐tubed (>8 cm) flowers across different continents.     

Spatial variability in a plant–pollinator community across a continuous habitat: high heterogeneity in the face of apparent uniformity

Large‐scale spatial variability in plant–pollinator communities (e.g. along geographic gradients, across different landscapes) is relatively well understood. However, we know much less about how these communities vary at small scales within a uniform landscape. Plants are sessile and highly sensitive to microhabitat conditions, whereas pollinators are highly mobile and, for the most part, display generalist feeding habits. Therefore, we expect plants to show greater spatial variability than pollinators. We analysed the spatial heterogeneity of a community of flowering plants and their pollinators in 40 plots across a 40‐km² area within an uninterrupted Mediterranean scrubland. We recorded 3577 pollinator visits to 49 plant species. The pollinator community (170 species) was strongly dominated by honey bees (71.8% of the visits recorded). Flower and pollinator communities showed similar beta‐diversity, indicating that spatial variability was similar in the two groups. We used path analysis to establish the direct and indirect effects of flower community distribution and honey bee visitation rate (a measure of the use of floral resources by this species) on the spatial distribution of the pollinator community. Wild pollinator abundance was positively related to flower abundance. Wild pollinator visitation rate was negatively related to flower abundance, suggesting that floral resources were not limiting. Pollinator and flower richness were positively related. Pollinator species composition was weakly related to flower species composition, reflecting the generalist nature of flower–pollinator interactions and the opportunistic nature of pollinator flower choices. Honey bee visitation rate did not affect the distribution of the wild pollinator community. Overall, we show that, in spite of the apparent physiognomic uniformity, both flowers and pollinators display high levels of heterogeneity, resulting in a mosaic of idiosyncratic local communities. Our results provide a measure of the background of intrinsic heterogeneity within a uniform habitat, with potential consequences on low‐scale ecosystem function and microevolutionary patterns.     

Patterns of spatio‐temporal distribution,abundance, and diversity in a mosquito community from the eastern Smoky Hills of Kansas

Nearly 30% of emerging infectious disease events are caused by vector‐borne pathogens with wildlife origins. Their transmission involves a complex interplay among pathogens, arthropod vectors, the environment and host species, and they pose a risk for public health, livestock and wildlife species. Examining habitat associations of vector species known to transmit infectious diseases, and quantifying spatio‐temporal dynamics of mosquito vector communities is one aspect of the holistic One Health approach that is necessary to develop effective control measures. A survey was conducted from May to August, 2010 of the abundance and diversity of mosquito species occurring in the mixed‐grass prairie habitat of the Smoky Hills of Kansas. This region is an important breeding ground for North America's grassland nesting birds and, as such, it could represent an important habitat for the enzootic amplification cycle of avian malaria and infectious encephalitides, as well as spill‐over events to humans and livestock. A total of 11 species, belonging to the three genera Aedes, Anopheles, and Culex, was collected during this study. Aedes nigromaculis, Ae. sollicitans, Ae. taeniorhynchus, Culex salinarius, and Cx. tarsalis accounted for 98% of the collected species. Multiple linear regression models suggested that mosquito abundances in the grasslands of the central Great Plains were explained by meteorological and environmental variables. Temporal dynamics in mosquito abundances were well supported by models that included maximum and minimum temperature indices (adjusted R²= 0.73). Spatial dynamics of mosquito abundances were best explained by a model containing the following environmental variables (adjusted R²=0.37): ground curvature, topographic wetness index, distance to woodland, and distance to road. The mosquito species we detected are known vectors for infectious encephalitides, including West Nile virus. Understanding the microhabitat characteristics of these mosquito species in a grassland ecosystem will aid in the control and management of these disease vectors.     

Host specificity,phenotype matching and the evolution of reproductive isolation in a coevolved plant–pollinator mutualism

Coevolutionary interactions between plants and their associated pollinators and seed dispersers are thought to have promoted the diversification of flowering plants ( Raven 1977 ; Regal 1977 ; Stebbins 1981 ). The actual mechanisms by which pollinators could drive species diversification in plants are not fully understood. However, it is thought that pollinator host specialization can influence the evolution of reproductive isolation among plant populations because the pollinator’s choice of host is what determines patterns of gene flow in its host plant, and host choice may also have important consequences on pollinator and host fitness ( Grant 1949 ; Bawa 1992 ). In this issue of Molecular Ecology, Smith et al. (2009) present a very interesting study that addresses how host specialization affects pollinator fitness and patterns of gene flow in a plant host. Several aspects of this study match elements of a seminal mathematical model of plant–pollinator codivergence ( Kiester et al. 1984 ) suggesting that reciprocal selection for matched plant and pollinator reproductive traits may lead to speciation in the host and its pollinator when there is strong host specialization and a pattern of geographic subdivision. Smith et al.’s study represents an important step to fill the gap in our understanding of how reciprocal selection may lead to speciation in coevolved plant–pollinator mutualisms.     

Intraspecific variation in herbivore‐induced plant volatiles influences the spatial range of plant–parasitoid interactions

Chemical information influences the behaviour of many animals, thus affecting species interactions. Many animals forage for resources that are heterogeneously distributed in space and time, and have evolved foraging behaviour that utilizes information related to these resources. Herbivore‐induced plant volatiles (HIPVs), emitted by plants upon herbivore attack, provide information on herbivory to various animal species, including parasitoids. Little is known about the spatial scale at which plants attract parasitoids via HIPVs under field conditions and how intraspecific variation in HIPV emission affects this spatial scale. Here, we investigated the spatial scale of parasitoid attraction to two cabbage accessions that differ in relative preference of the parasitoid Cotesia glomerata when plants were damaged by Pieris brassicae caterpillars. Parasitoids were released in a field experiment with plants at distances of up to 60 m from the release site using intervals between plants of 10 or 20 m to assess parasitism rates over time and distance. Additionally, we observed host‐location behaviour of parasitoids in detail in a semi‐field tent experiment with plant spacing up to 8 m. Plant accession strongly affected successful host location in field set‐ups with 10 or 20 m intervals between plants. In the semi‐field set‐up, plant finding success by parasitoids decreased with increasing plant spacing, differed between plant accessions, and was higher for host‐infested plants than for uninfested plants. We demonstrate that parasitoids can be attracted to herbivore‐infested plants over large distances (10 m or 20 m) in the field, and that stronger plant attractiveness via HIPVs increases this distance (up to at least 20 m). Our study indicates that variation in plant traits can affect attraction distance, movement patterns of parasitoids, and ultimately spatial patterns of plant–insect interactions. It is therefore important to consider plant‐trait variation in HIPVs when studying animal foraging behaviour and multi‐trophic interactions in a spatial context.     

High‐throughput physiological phenotyping and screening system for the characterization of plant–environment interactions

We present a simple and effective high‐throughput experimental platform for simultaneous and continuous monitoring of water relations in the soil–plant–atmosphere continuum of numerous plants under dynamic environmental conditions. This system provides a simultaneously measured, detailed physiological response profile for each plant in the array, over time periods ranging from a few minutes to the entire growing season, under normal, stress and recovery conditions and at any phenological stage. Three probes for each pot in the array and a specially designed algorithm enable detailed water‐relations characterization of whole‐plant transpiration, biomass gain, stomatal conductance and root flux. They also enable quantitative calculation of the whole plant water‐use efficiency and relative water content at high resolution under dynamic soil and atmospheric conditions. The system has no moving parts and can fit into many growing environments. A screening of 65 introgression lines of a wild tomato species (Solanum pennellii) crossed with cultivated tomato (S. lycopersicum), using our system and conventional gas‐exchange tools, confirmed the accuracy of the system as well as its diagnostic capabilities. The use of this high‐throughput diagnostic screening method is discussed in light of the gaps in our understanding of the genetic regulation of whole‐plant performance, particularly under abiotic stress.     

Habitat variation,mutualism and predation shape the spatio‐temporal dynamics of tansy aphids

1. Spatially distributed resources can lead to the formation of metapopulations, where individual subpopulations are often small and can experience frequent local extinction events followed by recolonisation. An example of terrestrial metapopulations are specialised phytophagous insects on their patchily distributed host plants. 2. The present study investigated the population dynamics of a specialised aphid (Metopeurum fuscoviride) on its patchily distributed host plant (Tanacetum vulgare) and associated community of mutualistic ants and predators in a small‐scale field site. Furthermore, aphid habitat differences (plant size, C/N ratio, location and surrounding vegetation) were quantified, and seasonal timing and precipitation were considered. 3. Seasonal timing and precipitation both had effects on aphid colonisation, extinction events and aphid colony persistence. Towards the end of the season, and after higher precipitation, aphid colonisation events decreased and extinction events increased. Plant size and location as well as aphid within‐field dispersal determined the spatio‐temporal distribution of aphid colonies. 4. Mutualistic ants (Lasius niger and Myrmica rubra) increased the chance of establishment of aphid colonies. However, when M. rubra was tending, aphid colony persistence was reduced. Aphid persistence and extinction were dependent on aphid abundance, as a higher colony size reduced the probability of extinction by predation. 5. The results emphasise the importance of dispersal limitation, population growth and the presence of mutualists when studying the spatio‐temporal dynamics of tansy aphids, particularly in a small‐scale field site.     

Relative importance of drought,soil quality,and plant species in determining the strength of plant–herbivore interactions

1. Although studies on plant–herbivore interactions comparing different plant species are common, little is known about the importance of environmental conditions in determining variation in herbivory within single plant species. 2. This study assessed the effects of experimentally manipulated nutrient and water availability on plant palatability, and compared these differences with differences among species. The extent to which these patterns can be explained by leaf toughness and specific leaf area was also investigated. Six plant species from the subfamily Carduoideae and four free‐living leaf chewing invertebrates were used in the study. 3. Herbivore preferences were significantly affected by soil nutrients and water regime and varied among plant as well as herbivore species. Generally, herbivores preferred watered plants and plants from nutrient‐poor soil. The effects of soil nutrients and water regime differed between the plant and herbivore species. The differences between the plant species were greater than those between the environmental treatments. Differences at both levels could be partly explained by leaf toughness and specific leaf area. Leaf toughness, in particular, turned to be an important predictor indicating that herbivores preferred species with softer leaves, and species from wetter conditions with reduced leaf toughness. 4. The environmental conditions in which plants are growing have significant effects on plant palatability. Between‐species comparisons thus need to pay attention to this variation. Future studies may consider how the effects of current conditions interact with conditions of plant origin to predict possible effects of changes in environmental conditions on the intensity of plant–herbivore interactions.     

Anthropogenic disturbance and rainfall variation threaten the stability of plant–ant interactions in the Brazilian Caatinga

Climate change is projected to exacerbate the effects of anthropogenic disturbance, with negative impacts on ecosystem stability and functioning. We evaluate the additive and combined effects of chronic anthropogenic disturbance (CAD) and rainfall variation on the temporal stability of mutualistic EFN‐bearing plant–ant networks in a Caatinga dry forest. We evaluated whether changes in the stability of these interactions are driven by changes in the stability of the communities of partners involved and/or in ant behavior. We sampled EFN‐bearing plant–ant networks in sixteen 20 × 20 m plots distributed across CAD and rainfall gradients. The stability of EFN‐bearing plant and attendant–ant communities were measured as the inverse of temporal differences in their community structure and composition. We also computed the stability of EFN‐bearing plant–ant networks by measuring the inverse of temporal differences in network specialization metrics. We found that, in general, the structure and composition of plant and ant interacting communities were similarly stable along both environmental gradients. Only CAD and its interaction with rainfall affected the temporal stability of EFN‐bearing plant diversity, which declined as CAD increased, with a more pronounced relationship in wetter areas. However, variation in levels of CAD and, to a lesser extent, rainfall greatly modulated the stability of EFN‐bearing plant–ant network specialization. CAD reduced the stability of network generality (specialization at the ant level), an effect that was much stronger in wetter areas. Meanwhile, the stability in network vulnerability (specialization at the plant level) decreased with the increase of CAD and the decrease of rainfall levels. Finally, there was a trend of decreasing stability in specialization of the overall network with increasing CAD. Our results suggest that changes in the structure of interaction networks are mainly driven by a switch in ant behavior rather than by changes in the structure and composition of plant and ant communities between years.     

Diverse visitors with various pollinator importance and temporal change in the important pollinators of <Emphasis Type="Italic">Geranium thunbergii</Emphasis> (Geraniaceae)

Assessing pollinator importance of each floral visitor to a plant species is a key to understanding plant–pollinator interaction. The present study examined visitation frequency, pollination efficiency, and pollinator importance of the full range of floral visitors to Geranium thunbergii natural population, by measuring seed-set. During 2 years of observations, the flowers were visited by at least 45 insect species belonging to four orders. Among the main 22 visitor species, 11 species belonging to three orders (Hymenoptera, Diptera, and Lepidoptera) acted as the efficient pollinators. In both years, Hymenoptera, especially bees, was the most important pollinator to G.thunbergii. Thus, the flowers could be considered as bee-pollinated. However, the most important species were not constant between years. The study also documented that the efficient pollinators have larger body sizes. The dish-shaped floral morphology, taxonomically diverse pollinators, and temporal change in the most important pollinators indicate that G.thunbergii–pollinator interaction is a rather generalized system. The results suggest that casual observations of visitation, or even precise measurement of pollinator importance in a single season is insufficient to identify important pollinators.