Atypical Flowers Can Be as Profitable as Typical Hummingbird Flowers.

In western North America, hummingbirds can be observed systematically visiting flowers that lack the typical reddish color, tubular morphology, and dilute nectar of "hummingbird flowers." Curious about this behavior, we asked whether these atypical flowers are energetically profitable for hummingbirds. Our field measurements of nectar content and hummingbird foraging speeds, taken over four decades at multiple localities, show that atypical flowers can be as profitable as typical ones and suggest that the profit can support 24-h metabolic requirements of the birds. Thus, atypical flowers may contribute to successful migration of hummingbirds, enhance their population densities, and allow them to occupy areas seemingly depauperate in suitable resources. These results illustrate what can be gained by attending to the unexpected.

Comment on "Cognition-mediated evolution of low-quality floral nectars".

Nachev et al (Reports, 6 January 2017, p. 75) present dilute nectar in bat-pollinated plants as "paradoxical" because bats prefer concentrated nectar, but paradox disappears with realistic assumptions about nectar evolution. We argue that they make unrealistic assumptions about the cognitive abilities of bat pollinators, invoke Weber's law inappropriately, and cannot predict observed nectar concentrations of bat flowers or negative correlations between pollinator body size and average concentration.

Is Plant Fitness Proportional to Seed Set? An Experiment and a Spatial Model.

Individual differences in fecundity often serve as proxies for differences in overall fitness, especially when it is difficult to track the fate of an individual's offspring to reproductive maturity. Using fecundity may be biased, however, if density-dependent interactions between siblings affect survival and reproduction of offspring from high- and low-fecundity parents differently. To test for such density-dependent effects in plants, we sowed seeds of the wildflower Ipomopsis aggregata (scarlet gilia) to mimic partially overlapping seed shadows of pairs of plants, one of which produced twice as many seeds. We tested for differences in offspring success using a genetic marker to track offspring to flowering multiple years later. Without density dependence, the high-fecundity parent should produce twice as many surviving offspring. We also developed a model that considered the geometry of seed shadows and assumed limited survivors so that the number of juvenile recruits is proportional to the area. Rather than a ratio of 2∶1 offspring success from high- versus low-fecundity parents, our model predicted a ratio of 1.42∶1, which would translate into weaker selection. Empirical ratios of juvenile offspring and of flowers produced conformed well to the model's prediction. Extending the model shows how spatial relationships of parents and seed dispersal patterns modify inferences about relative fitness based solely on fecundity.

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.

Drought, pollen and nectar availability, and pollination success.

Pollination success of animal-pollinated flowers depends on rate of pollinator visits and on pollen deposition per visit, both of which should vary with the pollen and nectar "neighborhoods" of a plant, i.e., with pollen and nectar availability in nearby plants. One determinant of these neighborhoods is per-flower production of pollen and nectar, which is likely to respond to environmental influences. In this study, we explored environmental effects on pollen and nectar production and on pollination success in order to follow up a surprising result from a previous study: flowers of Ipomopsis aggregata received less pollen in years of high visitation by their hummingbird pollinators. A new analysis of the earlier data indicated that high bird visitation corresponded to drought years. We hypothesized that drought might contribute to the enigmatic prior result if it decreases both nectar and pollen production: in dry years, low nectar availability could cause hummingbirds to visit flowers at a higher rate, and low pollen availability could cause them to deposit less pollen per visit. A greenhouse experiment demonstrated that drought does reduce both pollen and nectar production by I. aggregata flowers. This result was corroborated across 6 yr of variable precipitation and soil moisture in four unmanipulated field populations. In addition, experimental removal of pollen from flowers reduced the pollen received by nearby flowers. We conclude that there is much to learn about how abiotic and biotic environmental drivers jointly affect pollen and nectar production and availability, and how this contributes to pollen and nectar neighborhoods and thus influences pollination success.

Responses of high-altitude graminoids and soil fungi to 20 years of experimental warming.

High-elevation ecosystems are expected to be particularly sensitive to climate warming because cold temperatures constrain biological processes. Deeper understanding of the consequences of climate change will come from studies that consider not only the direct effects of temperature on individual species, but also the indirect effects of altered species interactions. Here we show that 20 years of experimental warming has changed the species composition of graminoid (grass and sedge) assemblages in a subalpine meadow of the Rocky Mountains, USA, by increasing the frequency of sedges and reducing the frequency of grasses. Because sedges typically have weak interactions with mycorrhizal fungi relative to grasses, lowered abundances of arbuscular mycorrhizal (AM) fungi or other root-inhabiting fungi could underlie warming-induced shifts in plant species composition. However, warming increased root colonization by AM fungi for two grass species, possibly because AM fungi can enhance plant water uptake when soils are dried by experimental warming. Warming had no effect on AM fungal colonization of three other graminoids. Increased AM fungal colonization of the dominant shrub Artemisia tridentata provided further grounds for rejecting the hypothesis that reduced AM fungi caused the shift from grasses to sedges. Non-AM fungi (including dark septate endophytes) also showed general increases with warming. Our results demonstrate that lumping grasses and sedges when characterizing plant community responses can mask significant shifts in the responses of primary producers, and their symbiotic fungi, to climate change.

Coyotes, deer, and wildflowers: diverse evidence points to a trophic cascade.

Spatial gradients in human activity, coyote activity, deer activity, and deer herbivory provide an unusual type of evidence for a trophic cascade. Activity of coyotes, which eat young mule deer (fawns), decreased with proximity to a remote biological field station, indicating that these predators avoided an area of high human activity. In contrast, activity of adult female deer (does) and intensity of herbivory on palatable plant species both increased with proximity to the station and were positively correlated with each other. The gradient in deer activity was not explained by availabilities of preferred habitats or plant species because these did not vary with distance from the station. Does spent less time feeding when they encountered coyote urine next to a feed block, indicating that increased vigilance may contribute, along with avoidance of areas with coyotes, to lower herbivory away from the station. Judging from two palatable wildflower species whose seed crop and seedling recruitment were greatly reduced near the field station, the coyote-deer-wildflower trophic cascade has the potential to influence plant community composition. Our study illustrates the value of a case-history approach, in which different forms of ecological data about a single system are used to develop conceptual models of complex ecological phenomena. Such an iterative model-building process is a common, but underappreciated, way of understanding how ecological systems work.

Asynchronous changes in phenology of migrating Broad-tailed Hummingbirds and their early-season nectar resources.

Phenological advancements driven by climate change are especially pronounced at higher latitudes, so that migrants from lower latitudes may increasingly arrive at breeding grounds after the appearance of seasonal resources. To explore this possibility, we compared dates of first arrival of Broad-tailed Hummingbirds (Selasphorus platycercus) to dates of flowering of plants they visit for nectar. Near the southern limit of the breeding range, neither hummingbird arrival nor first flowering dates have changed significantly over the past few decades. At a nearby migration stopover site, first flowering of a major food plant has advanced, but peak flowering has not. Near the northern limit of the breeding range, first and peak flowering of early-season food plants have shifted to earlier dates, resulting in a shorter interval between appearance of first hummingbirds and first flowers. If phenological shifts continue at current rates, hummingbirds will eventually arrive at northern breeding grounds after flowering begins, which could reduce their nesting success. These results support the prediction that migratory species may experience the greatest phenological mismatches at the poleward limits of their migration. A novel hypothesis based on these results posits that the poleward limit for some species may contract toward lower latitudes under continued warming.

Effects of floral neighborhood on seed set and degree of outbreeding in a high-alpine cushion plant.

Plants flowering together may influence each other's pollination and fecundity over a range of physical distances. Their effects on one another can be competitive, neutral, or facilitative. We manipulated the floral neighborhood of the high-alpine cushion plant Eritrichium nanum in the Swiss Alps and measured the effects of co-flowering neighbors on both the number of seeds produced and the degree of inbreeding and outbreeding in the offspring, as deduced from nuclear microsatellite markers. Seed set of E. nanum did not vary significantly with the presence or absence of two Saxifraga species growing as near neighbors, but it was higher in E. nanum cushions growing at low conspecific density than in those growing at high density. In addition, floral neighborhood had no detectable effect on the degree of selfing of E. nanum, but seeds from cushions growing at low conspecific density were more highly outbred than seeds from cushions at high density. Thus, there was no evidence of either competition or facilitation between E. nanum and Saxifraga spp. as mediated by pollinators at the spatial scale of our experimental manipulation. In contrast, the greater fecundity of E. nanum cushions at low density was consistent with reduced intraspecific competition for pollinators and might also represent a beneficial effect of highly outbred seeds as brought about by more long-distance pollinator flights under low-density conditions.

New frontiers in competition for pollination.

BACKGROUND: Co-flowering plant species frequently share pollinators. Pollinator sharing is often detrimental to one or more of these species, leading to competition for pollination. Perhaps because it offers an intriguing juxtaposition of ecological opposites - mutualism and competition - within one relatively tractable system, competition for pollination has captured the interest of ecologists for over a century. SCOPE: Our intent is to contemplate exciting areas for further work on competition for pollination, rather than to exhaustively review past studies. After a brief historical summary, we present a conceptual framework that incorporates many aspects of competition for pollination, involving both the quantity and quality of pollination services, and both female and male sex functions of flowers. Using this framework, we contemplate a relatively subtle mechanism of competition involving pollen loss, and consider how competition might affect plant mating systems, overall reproductive success and multi-species interactions. We next consider how competition for pollination might be altered by several emerging consequences of a changing planet, including the spread of alien species, climate change and pollinator declines. Most of these topics represent new frontiers whose exploration has just begun. CONCLUSIONS: Competition for pollination has served as a model for the integration of ecological and evolutionary perspectives in the study of species interactions. Its study has elucidated both obvious and more subtle mechanisms, and has documented a range of outcomes. However, the potential for this interaction to inform our understanding of both pure and applied aspects of pollination biology has only begun to be realized.

A global test of the pollination syndrome hypothesis.

BACKGROUND AND AIMS: 'Pollination syndromes' are suites of phenotypic traits hypothesized to reflect convergent adaptations of flowers for pollination by specific types of animals. They were first developed in the 1870s and honed during the mid 20th Century. In spite of this long history and their central role in organizing research on plant-pollinator interactions, the pollination syndromes have rarely been subjected to test. The syndromes were tested here by asking whether they successfully capture patterns of covariance of floral traits and predict the most common pollinators of flowers. METHODS: Flowers in six communities from three continents were scored for expression of floral traits used in published descriptions of the pollination syndromes, and simultaneously the pollinators of as many species as possible were characterized. KEY RESULTS: Ordination of flowers in a multivariate 'phenotype space' defined by the syndromes showed that almost no plant species fall within the discrete syndrome clusters. Furthermore, in approximately two-thirds of plant species, the most common pollinator could not be successfully predicted by assuming that each plant species belongs to the syndrome closest to it in phenotype space. CONCLUSIONS: The pollination syndrome hypothesis as usually articulated does not successfully describe the diversity of floral phenotypes or predict the pollinators of most plant species. Caution is suggested when using pollination syndromes for organizing floral diversity, or for inferring agents of floral adaptation. A fresh look at how traits of flowers and pollinators relate to visitation and pollen transfer is recommended, in order to determine whether axes can be identified that describe floral functional diversity more successfully than the traditional syndromes.

Size-specific interaction patterns and size matching in a plant-pollinator interaction web.

BACKGROUND AND AIMS: Many recent studies show that plant-pollinator interaction webs exhibit consistent structural features such as long-tailed distributions of the degree of generalization, nestedness of interactions and asymmetric interaction dependencies. Recognition of these shared features has led to a variety of mechanistic attempts at explanation. Here it is hypothesized that beside size thresholds and species abundances, the frequency distribution of sizes (nectar depths and proboscis lengths) will play a key role in determining observed interaction patterns. METHODS: To test the influence of size distributions, a new network parameter is introduced: the degree of size matching between nectar depth and proboscis length. The observed degree of size matching in a Spanish plant-pollinator web was compared with the expected degree based on joint probability distributions, integrating size thresholds and abundance, and taking the sampling method into account. KEY RESULTS: Nectar depths and proboscis lengths both exhibited right-skewed frequency distributions across species and individuals. Species-based size matching was equally close for plants, independent of nectar depth, but differed significantly for pollinators of dissimilar proboscis length. The observed patterns were predicted well by a model considering size distributions across species. Observed size matching was closer when relative abundances of species were included, especially for flowers with openly accessible nectar and pollinators with long proboscises, but was predicted somewhat less successfully by the model that included abundances. CONCLUSIONS: The results suggest that in addition to size thresholds and species abundances, size distributions are important for understanding interaction patterns in plant-pollinator webs. It is likely that the understanding will be improved further by characterizing for entire communities how nectar production of flowers and energetic requirements of pollinators covary with size, and how sampling methods influence the observed interaction patterns.

Lifetime fitness in two generations of Ipomopsis hybrids.

Various models purporting to explain natural hybrid zones make different assumptions about the fitness of hybrids. One class of models assumes that hybrids have intrinsically low fitness due to genetic incompatibilities, whereas other models allow hybrid fitness to vary across natural environments. We used the intrinsic rate of increase to assess lifetime fitness of hybrids between two species of montane plants Ipomopsis aggregata and Ipomopsis tenuituba planted as seed into multiple field environments. Because fitness is predicted to depend upon genetic composition of the hybrids, we included F1 hybrids, F2 hybrids, and backcrosses in our field tests. The F2 hybrids had female fitness as high, or higher, than expected under an additive model of fitness. These results run counter to any model of hybrid zone dynamics that relies solely on intrinsic nuclear genetic incompatibilities. Instead, we found that selection was environmentally dependent. In this hybrid zone, cytoplasmic effects and genotype-by-environment interactions appear more important in lowering hybrid fitness than do intrinsic genomic incompatibilities between nuclear genes.

Bridging the generation gap in plants: pollination, parental fecundity, and offspring demography.

Despite extensive study of pollination and plant reproduction on the one hand, and of plant demography on the other, we know remarkably little about links between seed production in successive generations, and hence about long-term population consequences of variation in pollination success. We bridged this "generation gap" in Ipomopsis aggregata, a long-lived semelparous wildflower that is pollinator limited, by adding varying densities of seeds to natural populations and following resulting plants through their entire life histories. To determine whether pollen limitation of seed production constrains rate of population growth in this species, we sowed seeds into replicated plots at a density that mimics typical pollination success and spacing of flowering plants in nature, and at twice that density to mimic full pollination. Per capita offspring survival, flower production, and contribution to population increase (lambda) did not decline with sowing density in this experiment, suggesting that typical I. aggregata populations freed from pollen limitation will grow over the short term. In a second experiment we addressed whether density dependence would eventually erase the growth benefits of full pollination, by sowing a 10-fold range of seed densities that falls within extremes estimated for the natural "seed rain" that reaches the soil surface. Per capita survival to flowering and age at flowering were again unaffected by sowing density, but offspring size, per capita flower production, and lambda declined with density. Such density dependence complicates efforts to predict population dynamics over the longer term, because it changes components of the life history (in this case fecundity) as a population grows. A complete understanding of how constraints on seed production affect long-term population growth will hinge on following offspring fates at least through flowering of the first offspring generation, and doing so for a realistic range of population densities.

Global warming and the disruption of plant-pollinator interactions.

Anthropogenic climate change is widely expected to drive species extinct by hampering individual survival and reproduction, by reducing the amount and accessibility of suitable habitat, or by eliminating other organisms that are essential to the species in question. Less well appreciated is the likelihood that climate change will directly disrupt or eliminate mutually beneficial (mutualistic) ecological interactions between species even before extinctions occur. We explored the potential disruption of a ubiquitous mutualistic interaction of terrestrial habitats, that between plants and their animal pollinators, via climate change. We used a highly resolved empirical network of interactions between 1420 pollinator and 429 plant species to simulate consequences of the phenological shifts that can be expected with a doubling of atmospheric CO(2). Depending on model assumptions, phenological shifts reduced the floral resources available to 17-50% of all pollinator species, causing as much as half of the ancestral activity period of the animals to fall at times when no food plants were available. Reduced overlap between plants and pollinators also decreased diet breadth of the pollinators. The predicted result of these disruptions is the extinction of pollinators, plants and their crucial interactions.

Evolutionary dynamics of an Ipomopsis hybrid zone: confronting models with lifetime fitness data.

Interspecific hybridization is a recurring aspect of the evolution of many plant and animal groups. The temporal dynamics of hybrid zones and the evolutionary consequences of hybridization should depend on fitness of parental and hybrid individuals expressed in different environments. We measured lifetime fitness, including survival and reproduction, of plants of Ipomopsis aggregata, Ipomopsis tenuituba, and their F1 hybrids, in experimental plantings in a natural hybrid zone. Fitness, measured as the finite rate of increase ( lambda ), depended strongly on environment. Each parental species performed well in its home locale and poorly in the locale of the other species. Hybrids performed as well as parents overall but enjoyed their highest fitness in the hybrid site. Furthermore, F1 hybrids with I. tenuituba as maternal parent survived well only at the hybrid site, suggesting a cytonuclearxenvironment interaction. These results support an "environmental cline" model of hybrid zone dynamics, with complexities in the fitness of hybrids consistent also with an "evolutionary novelty" model. Combined with those of earlier studies of pollination, our results suggest that both vegetative adaptation to physical environment and floral adaptation to pollinators contribute to observed patterns of phenotypic expression in this hybrid zone and to persistence of the hybrid zone.

Self-sterility in Ipomopsis aggregata (Polemoniaceae) is due to prezygotic ovule degeneration.

Based on previous studies, extreme (>99%) self-sterility in scarlet gilia (Ipomopsis aggregata) appears to be involved in late-acting ovarian self-incompatibility (OSI). Here, we confirm this suggestion by comparing structural events that follow from cross- vs. self-pollinations of I. aggregata. Growth of cross- and self-pollen tubes in the style at 11 h and growth in the ovary at 24 h was equivalent. Nonetheless, by 24 h, cross-pollen effected a significantly higher percentage of both ovule penetration and fertilization. Ovules in self-pollinated flowers showed pronounced changes, including an absence of embryo sac expansion and reduced starch in the integument, by 11 h post-pollination, well before pollen tube entry into the ovary. In addition, the integumentary tapetum and adjacent 1-3 cell layers exhibited abnormal cell division, pronounced deposition of thick, pectin-rich cell walls, and cellular collapse. Ovules and embryo sacs from cross-pollinated flowers rarely showed such features. Developmental changes in ovules from self-pollinated flowers eventually resulted in integument and embryo sac collapse, a process not observed in ovules of unpollinated flowers. We suggest that OSI involves long-distance signaling between self-pollen or self-pollen tubes and carpel tissue that reduces availability of receptive ovules for fertilization before pollen tubes arrive in the ovary.

Tolerance of pollination networks to species extinctions.

Mutually beneficial interactions between flowering plants and animal pollinators represent a critical 'ecosystem service' under threat of anthropogenic extinction. We explored probable patterns of extinction in two large networks of plants and flower visitors by simulating the removal of pollinators and consequent loss of the plants that depend upon them for reproduction. For each network, we removed pollinators at random, systematically from least-linked (most specialized) to most-linked (most generalized), and systematically from most- to least-linked. Plant species diversity declined most rapidly with preferential removal of the most-linked pollinators, but declines were no worse than linear. This relative tolerance to extinction derives from redundancy in pollinators per plant and from nested topology of the networks. Tolerance in pollination networks contrasts with catastrophic declines reported from standard food webs. The discrepancy may be a result of the method used: previous studies removed species from multiple trophic levels based only on their linkage, whereas our preferential removal of pollinators reflects their greater risk of extinction relative to that of plants. In both pollination networks, the most-linked pollinators were bumble-bees and some solitary bees. These animals should receive special attention in efforts to conserve temperate pollination systems.