Manipulation of soil mycorrhizal fungi influences floral traits.

Most plants form root hyphal relationships with mycorrhizal fungi, especially arbuscular mycorrhizal fungi (AMF). These associations are known to positively impact plant biomass and competitive ability. However, less is known about how mycorrhizas impact other ecological interactions, such as those mediated by pollinators. We performed a meta-regression of studies that manipulated AMF and measured traits related to pollination, including floral display size, rewards, visitation, and reproduction, extracting 63 studies with 423 effects. On average, the presence of mycorrhizas was associated with positive effects on floral traits. Specifically, we found impacts of AMF on floral display size, pollinator visitation and reproduction, and a positive but nonsignificant impact on rewards. Studies manipulating mycorrhizas with fungicide tended to report contrasting results, possibly because fungicide destroys both beneficial and pathogenic microbes. Our study highlights the potential for relationships with mycorrhizal fungi to play an important, yet underrecognized role in plant-pollinator interactions. With heightened awareness of the need for a more sustainable agricultural industry, mycorrhizal fungi may offer the opportunity to reduce reliance on inorganic fertilizers. At the same time, fungicides are now ubiquitous in agricultural systems. Our study demonstrates indirect ways in which plant-belowground fungal partnerships could manifest in plant-pollinator interactions.

New Evidence Suggests No Sex Bias in Herbivory or Plant Defense.

AbstractDioecious plants can exhibit sexual dimorphism across a suite of plant traits, including susceptibility to herbivory and secondary chemistry. One hypothesis is that because of greater costs of reproduction in females, males should grow faster and invest less in defense, resulting in male-biased herbivory. Indeed, a series of articles and a prominent meta-analysis have established male-biased herbivory as a rule. However, more recent reviews have raised questions about how general the pattern is, citing the low breadth of taxon sampling. The literature on this topic has not been formally quantified by meta-analysis in over 15 years. Here, we report the results of a meta-analysis of studies that measured sex bias in either herbivory and/or secondary defense in 71 dioecious plant species. We added 58 observations of herbivory and 41 of secondary chemistry to the original. We control for nonindependence of effects from the same study and taxonomic group to address critiques of earlier studies. For secondary chemistry, we found no support for any consistent difference between male and female plants. For herbivory, results are directionally similar to earlier reports, although not statistically significant once we accounted for taxonomic group and study. We also found that earlier studies reported stronger male bias than more recent studies. We discuss our results in light of the decline effect, where the magnitude of a described effect declines as the number of observations increases, and consider whether the data sets exhibit signs of evidence of the type(s) of biases that can result in declining effect sizes over time.

Spring wildflower phenology and pollinator activity respond similarly to climatic variation in an eastern hardwood forest.

Climate warming could disrupt species interactions if organisms' phenologies respond to climate change at different rates. Phenologies of plants and insects can be sensitive to temperature and timing of snowmelt; however, many important pollinators including ground-nesting bees have been little studied in this context. Without knowledge of the environmental cues affecting phenologies of co-occurring species, we have little ability to predict how species assemblages, and species interactions, will be affected by climate change. Here, we studied a hardwood forest understory over six years, to determine how spring temperatures, snowmelt timing, and photoperiod influence the phenology of two spring wildflowers (Anemone spp. and Trillium grandiflorum), activity of ground-nesting bees, and their temporal overlap. Surface degree-day accumulation was a better predictor of phenology for Anemone spp. (plant) and Nomada (bees) than were day of year (a proxy for photoperiod) or snowmelt date, whereas Trillium flowering appeared most sensitive to photoperiodic cues. Activity periods of Andrena and Lasioglossum bees were equally well described by degree-day accumulation and day of year. No taxon's phenology was best predicted by snowmelt date. Despite these differences among taxa in their phenological responses, timing of bee activity and flowering responded similarly to variation in snowmelt date and early spring temperatures. Furthermore, temporal overlap between flowering and bee activity was similar over the years of this study and was unaffected by variability in snowmelt date or temperature. Nevertheless, the differences among some taxa in their phenological responses suggests that diverging temporal shifts are a possibility for the future.

No consistent pollinator-mediated impacts of alien plants on natives.

The introduction of an alien plant is widely assumed to have negative consequences for the pollinator-mediated fitness of nearby natives. Indeed, a number of studies, including a highly cited meta-analysis, have concluded that the trend for such interactions is competitive. Here we provide evidence that publication bias and study design have obscured our ability to assess the pollinator-mediated impacts of alien plants. In a meta-analysis of 76 studies, we demonstrate that alien/native status does not predict the outcome of pollinator-mediated interactions among plants. Moreover, we found no evidence that similarity in floral traits or phylogenetic distance between species pairs influences the outcome of pollinator-mediated interactions. Instead, we report that aspects of study design, such as distance between the control and nearest neighbour, and/or the arrangement of study plants better predict the impact of a neighbour than does alien/native status. Our study sheds new light on the role that publication bias and experimental design play in the evaluation of key patterns in ecology. We conclude that, due to the absence of clear, generalisable pollinator-mediated impacts of alien species, management schemes should base decisions on community-wide assessments of the impacts of individual alien plant species, and not solely on alien/native status itself.

Global biogeography of mating system variation in seed plants.

Latitudinal gradients in biotic interactions have been suggested as causes of global patterns of biodiversity and phenotypic variation. Plant biologists have long speculated that outcrossing mating systems are more common at low than high latitudes owing to a greater predictability of plant-pollinator interactions in the tropics; however, these ideas have not previously been tested. Here, we present the first global biogeographic analysis of plant mating systems based on 624 published studies from 492 taxa. We found a weak decline in outcrossing rate towards higher latitudes and among some biomes, but no biogeographic patterns in the frequency of self-incompatibility. Incorporating life history and growth form into biogeographic analyses reduced or eliminated the importance of latitude and biome in predicting outcrossing or self-incompatibility. Our results suggest that biogeographic patterns in mating system are more likely a reflection of the frequency of life forms across latitudes rather than the strength of plant-pollinator interactions.

Evidence that a herbivore tolerance response affects selection on floral traits and inflorescence architecture in purple loosestrife (Lythrum salicaria).

Background and Aims: The study of the evolution of floral traits has generally focused on pollination as the primary driver of selection. However, herbivores can also impose selection on floral traits through a variety of mechanisms, including florivory and parasitism. Less well understood is whether floral and inflorescence architecture traits that influence a plant's tolerance to herbivory, such as compensatory regrowth, alter pollinator-mediated selection. Methods: Because herbivore damage to Lythrum salicaria meristems typically leads to an increase in the number of inflorescences and the size of the floral display, an experiment was conducted to test whether simulated herbivory (i.e. clipping the developing meristem) could alter the magnitude or direction of pollinator-mediated selection on a suite of floral and inflorescence architecture traits. Using a pollen supplementation protocol, pollen limitation was compared in the presence and absence of meristem damage in order to quantify any interaction between pollinator and herbivore-mediated selection on floral traits. Key Results: Surprisingly, in spite of an obvious impact on floral display and architecture, with clipped plants producing more inflorescences and more flowers, there was no difference in pollen limitation between clipped and unclipped plants. Correspondingly, there was no evidence that imposing herbivore damage altered pollinator-mediated selection in this system. Rather, the herbivory treatment alone was found to alter direct selection on floral display, with clipped plants experiencing greater selection for earlier flowering and weaker selection for number of inflorescences when compared with unclipped plants. Conclusions: These findings imply that herbivory on its own can drive selection on plant floral traits and inflorescence architecture in this species, even more so than pollinators. Specifically, herbivory can impose selection on floral traits if such traits influence a plant's tolerance to herbivory, such as through the timing of flowering and/or the compensatory regrowth response.

Indirect effects of herbivory on plant-pollinator interactions in invasive Lythrum salicaria.

PREMISE OF THE STUDY: Herbivory can affect a plant's fitness in a variety of ways, including modifying the biotic interactions of the plant. In particular, when herbivory influences floral display, we hypothesize that pollinator visitation will be altered accordingly. Here we studied the indirect effects of feeding by two beetles, Neogalerucella calmariensis and N. pusilla, released as a biological control, on plant-pollinator interactions and fitness in the invasive plant, purple loosestrife (Lythrum salicaria). METHODS: Two herbivory treatments (ambient and simulated) were applied to plants in a naturally occurring population of purple loosestrife. During flowering, traits of plants in the treatment and control groups were recorded. Data on pollinator visitation behavior was then collected after intense larval herbivory had ended. KEY RESULTS: Plants exposed to herbivory treatments produced more flowers and inflorescences but flowered significantly later than those in the control group. Moreover, we found a significant, positive association of herbivory with the number of flowers probed by bumblebees and with the number of times a foraging pollinator moved among inflorescences on a single plant. No differences in female fitness (fruit or seed production) were detected. CONCLUSIONS: We conclude that herbivore-mediated differences in floral display traits impacted pollinator visitation behavior. However, as we discuss, differences in pollinator visitation did not translate into detectable differences in female reproductive success. We postulate that herbivory could influence other unmeasured aspects of fitness, such as seed quality or the number of seeds sired.

Evidence for pollen limitation of a native plant in invaded communities.

Animal-pollinated invasive species have frequently been demonstrated to outcompete native species for pollinator attention, which can have detrimental effects on the reproductive success and population dynamics of native species. Many animal-pollinated invasive species exhibit showy flowers and provide substantial rewards, allowing them to act as pollinator 'magnets', which, at a large scale, can attract more pollinators to an area, but, at a smaller scale, may reduce compatible pollen flow to local native species, possibly explaining why most studies detect competition. By performing pollen limitation experiments of populations in both invaded and uninvaded sites, we demonstrate that the invasive plant Lythrum salicaria appears to facilitate, rather than hinder, the reproductive success of native confamilial Decodon verticillatus, even at a small scale, in a wetland habitat in southeastern Ontario. We found no evidence for a magnet species effect on pollinator attraction to invaded sites. Germination experiments confirmed that seeds from invaded sites had similar germination rates to those from uninvaded sites, making it unlikely that a difference in inbreeding was masking competitive effects. We describe several explanations for our findings. Notably, there were no differences in seed set among populations at invaded and uninvaded sites. Our results underscore the inherent complexity of studying the ecological impacts of invasive species on natives.

Common pesticides disrupt critical ecological interactions.

Critical ecological interactions can be disrupted by pesticides, leading to serious ecosystem and economic harm. For the most part, however, the extent and magnitude of these impacts are unknown. We argue for increased investigation of ecosystem impacts of common pesticides by scientists and scrutiny by regulators.

Effect of local community phylogenetic structure on pollen limitation in an obligately insect-pollinated plant.

PREMISE OF THE STUDY: Pollination is a key aspect of ecosystem function in the majority of land plant communities. It is well established that many animal-pollinated plants suffer lower seed set than they are capable of, likely because of competition for pollinators. Previously, competition for pollinator services has been shown to be most intense in communities with the greatest plant diversity. In spite of the fact that community evolutionary relations have a demonstrated impact on many ecological processes, their role in competition for pollinator services has rarely been examined. METHODS: In this study, we explore relations among several aspects of the surrounding plant community, including species richness, phylodiversity, evolutionary distance from a focal species, and pollen limitation in an annual insect-pollinated plant. KEY RESULTS: We did not find a significant effect of species richness on competition for pollination. However, consistent with a greater role for facilitation than competition, we found that a focal species occurring in communities composed of species of close relatives, especially other members of the Asteraceae, was less pollen limited than when it occurred in communities composed of more distant relatives. CONCLUSIONS: Our results demonstrate that community phylodiversity is an important correlate of pollen limitation in this system and that it has greater explanatory power than species richness alone.

Trait correlates and functional significance of heteranthery in flowering plants.

• Flowering plants display extraordinary diversity in the morphology of male sexual organs, yet the functional significance of this variation is not well understood. Here, we conducted a comparative analysis of floral correlates of heteranthery - the morphological and functional differentiation of anthers within flowers - among angiosperm families to identify traits associated with this condition. • We performed a phylogenetic analysis of correlated evolution between heteranthery and several floral traits commonly reported from heterantherous taxa. In addition, we quantified the effect of phylogenetic uncertainty in the observed patterns of correlated evolution by comparing trees in which polytomous branches were randomly resolved. • Heteranthery is reported from 12 angiosperm orders and is phylogenetically associated with the absence of floral nectaries, buzz-pollination and enantiostyly (mirror-image flowers). These associations are robust to particularities of the underlying phylogenetic hypothesis. • Heteranthery has probably evolved as a result of pollinator-mediated selection and appears to function to reduce the conflict of relying on pollen both as food to attract pollinators and as the agent of male gamete transfer. The relative scarcity of heteranthery among angiosperm families suggests that the conditions permitting its evolution are not easily met despite the abundance of pollen-collecting bees and nectarless flowers.

Correlated evolution of mating system and floral display traits in flowering plants and its implications for the distribution of mating system variation.

Reduced allocation to structures for pollinator attraction is predicted in selfing species. We explored the association between outcrossing and floral display in a broad sample of angiosperms. We used the demonstrated relationship to test for bias against selfing species in the outcrossing rate distribution, the shape of which has relevance for the stability of mixed mating. Relationships between outcrossing rate, flower size, flower number and floral display, measured as the product of flower size and number, were examined using phylogenetically independent contrasts. The distribution of floral displays among species in the outcrossing rate database was compared with that of a random sample of the same flora. The outcrossing rate was positively associated with the product of flower size and number; individually, components of display were less strongly related to outcrossing. Compared with a random sample, species in the outcrossing rate database showed a deficit of small floral display sizes. We found broad support for reduced allocation to attraction in selfing species. We suggest that covariation between mating systems and total allocation to attraction can explain the deviation from expected trade-offs between flower size and number. Our results suggest a bias against estimating outcrossing rates in the lower half of the distribution, but not specifically against highly selfing species.

Linking floral symmetry genes to breeding system evolution.

Understanding the genetic basis of ecologically important traits is a major focus of evolutionary research. Recent advances in molecular genetic techniques should significantly increase our understanding of how regulatory genes function. By contrast, our understanding of the broader macro-evolutionary implications of developmental gene function lags behind. Here we review published data on the floral symmetry gene network (FSGN), and conduct phylogenetic analyses that provide evidence of a link between floral symmetry and breeding systems in angiosperms via dichogamy. Our results suggest that known genes in the FSGN and those yet to be described underlie this association. We posit that the integration of floral symmetry and the roles of other regulatory genes in plant breeding system evolution will provide new insights about macro-evolutionary patterns and processes in flowering plants.

A model of the evolution of dichogamy incorporating sex-ratio selection, anther-stigma interference, and inbreeding depression.

Historically, explanations for the evolution of floral traits that reduce self-fertilization have tended to focus on selection to avoid inbreeding depression. However, there is growing support for the hypothesis that such traits also play a role in promoting efficient pollen dispersal by reducing anther-stigma interference. The relative importance of these two selective pressures is currently a popular topic of investigation. To date, there has been no theoretical exploration of the relative contributions of selection to avoid the genetic costs of self-fertilization and selection to promote efficient pollen dispersal on the evolution of floral traits. We developed a population genetic model to examine the influence of these factors on the evolution of dichogamy: the temporal separation of anther maturation and stigma receptivity. Our analysis indicates that anther-stigma interference can favor dichogamy even in the absence of in-breeding depression. Although anther-stigma interference and inbreeding depression are the key forces driving the initial evolution of dichogamy, selection to match the timing of pollen dispersal to the availability of ovules at the population level becomes a more potent force opposing the further evolution of dichogamy as the extent of temporal separation increases. This result may help to explain otherwise puzzling phenomena such as why dichogamy is rarely complete in nature and why dichogamy tends to be associated with asynchronous flower presentation.

The role of local species abundance in the evolution of pollinator attraction in flowering plants.

We present a population genetic model that incorporates aspects of pollinator efficiency and abundance to examine the effect of the local plant community on the evolution of floral trait specialization. Our model predicts that plant species evolve to be pollinator specialists on the most effective and common pollinators when their abundance is low relative to other plant species in the community (i.e., conspecific pollen is relatively rare) and evolve to be pollinator generalists when they are numerically dominant (i.e., conspecific pollen is abundant). Strong flower constancy also favors generalist floral traits. Furthermore, generalist species are predicted to differentiate when there is a concave trade-off in attracting pollinator species with different floral trait preferences. This result implies that populations that evolve toward a generalist strategy may be more prone to speciation. Ours is the first theoretical model to include local species abundance explicitly, despite the fact that it has been previously identified as an important factor in the evolution of plant specialization. Our results add a layer of ecological complexity to previous models of floral evolution and therefore have the potential to improve our power to predict circumstances under which specialized and generalized plant-pollinator interactions should evolve.

Floral symmetry affects speciation rates in angiosperms.

Despite much recent activity in the field of pollination biology, the extent to which animal pollinators drive the formation of new angiosperm species remains unresolved. One problem has been identifying floral adaptations that promote reproductive isolation. The evolution of a bilaterally symmetrical corolla restricts the direction of approach and movement of pollinators on and between flowers. Restricting pollinators to approaching a flower from a single direction facilitates specific placement of pollen on the pollinator. When coupled with pollinator constancy, precise pollen placement can increase the probability that pollen grains reach a compatible stigma. This has the potential to generate reproductive isolation between species, because mutations that cause changes in the placement of pollen on the pollinator may decrease gene flow between incipient species. I predict that animal-pollinated lineages that possess bilaterally symmetrical flowers should have higher speciation rates than lineages possessing radially symmetrical flowers. Using sister-group comparisons I demonstrate that bilaterally symmetric lineages tend to be more species rich than their radially symmetrical sister lineages. This study supports an important role for pollinator-mediated speciation and demonstrates that floral morphology plays a key role in angiosperm speciation.

Analysis of inbreeding depression in mixed-mating plants provides evidence for selective interference and stable mixed mating.

Hermaphroditic individuals can produce both selfed and outcrossed progeny, termed mixed mating. General theory predicts that mixed-mating populations should evolve quickly toward high rates of selfing, driven by rapid purging of genetic load and loss of inbreeding depression (ID), but the substantial number of mixed-mating species observed in nature calls this prediction into question. Lower average ID reported for selfing than for outcrossing populations is consistent with purging and suggests that mixed-mating taxa in evolutionary transition will have intermediate ID. We compared the magnitude of ID from published estimates for highly selfing (r > 0.8), mixed-mating (0.2 ≤ r ≥ 0.8), and highly outcrossing (r < 0.2) plant populations across 58 species. We found that mixed-mating and outcrossing taxa have equally high average lifetime ID (δ= 0.58 and 0.54, respectively) and similar ID at each of four life-cycle stages. These results are not consistent with evolution toward selfing in most mixed-mating taxa. We suggest that prevention of purging by selective interference could explain stable mixed mating in many natural populations. We identify critical gaps in the empirical data on ID and outline key approaches to filling them.

Plant mating systems in a changing world.

There is increasing evidence that human disturbance can negatively impact plant-pollinator interactions such as outcross pollination. We present a meta-analysis of 22 studies involving 27 plant species showing a significant reduction in the proportion of seeds outcrossed in response to anthropogenic habitat modifications. We discuss the evolutionary consequences of disturbance on plant mating systems, and in particular whether reproductive assurance through selfing effectively compensates for reduced outcrossing. The extent to which disturbance reduces pollinator versus mate availability could generate diverse selective forces on reproductive traits. Investigating how anthropogenic change influences plant mating will lead to new opportunities for better understanding of how mating systems evolve, as well as of the ecological and evolutionary consequences of human activities and how to mitigate them.

Plant-pollinator interactions and the assembly of plant communities.

Most studies of plant community assembly have focused on how the abiotic aspects of a habitat (e.g. soil moisture or mineral composition) or direct interactions among plants in a community (e.g. competition for space or nutrients) influence which species establish and persist, but they have tended to neglect indirect interactions such as those mediated by pollinators. We address three types of plant-pollinator interactions--filtering, facilitation and competitive exclusion--and their predicted impacts on communities. The few available studies that address how pollinator-mediated interactions limit or promote plant species establishment and persistence provide support for many of these predictions. An integrated framework for understanding plant community assembly needs to incorporate abiotic and biotic interactions, including plant-pollinator and other plant-animal interactions.