Selection of Floral Traits by Pollinators and Seed Predators during Sequential Life History Stages.

AbstractOrganismal traits often influence fitness via interactions with multiple species. That selection is not necessarily predictable from pairwise interactions, such as when interactions occur during different life cycle stages. Theoretically, directional selection during two sequential episodes (e.g., pollination and seed survival) can generate quadratic or correlational selection for a set of traits that passes both selective filters. We compared strength of selection during pollination versus seed predation in the field and tested whether interactions with multiple species give rise to nonlinear selection on floral traits. We planted common gardens with seeds of two species of Ipomopsis and hybrids at sites where pollination was primarily by hummingbirds or also included hawk moths. We examined selection on six floral traits, including corolla width, sepal width, color, nectar, and two scent compounds. Female fitness (seeds) was broken down into fitness during (1) pollination (seeds initiated) and (2) seed predation (proportion of seeds escaping fly predation). All traits showed evidence of selection. Directional and quadratic selection were stronger during seed initiation than during seed predation. Correlational selection occurred mostly during seed initiation rather than arising from combining species interactions at two points in the life cycle. These results underscore how multispecies interactions can combine to exert selection on trait combinations.

Earlier snow melt and reduced summer precipitation alter floral traits important to pollination.

Climate change can cause changes in expression of organismal traits that influence fitness. In flowering plants, floral traits can respond to drought, and that phenotypic plasticity has the potential to affect pollination and plant reproductive success. Global climate change is leading to earlier snow melt in snow-dominated ecosystems as well as affecting precipitation during the growing season, but the effects of snow melt timing on floral morphology and rewards remain unknown. We conducted crossed manipulations of spring snow melt timing (early vs. control) and summer monsoon precipitation (addition, control, and reduction) that mimicked recent natural variation, and examined plastic responses in floral traits of Ipomopsis aggregata over 3 years in the Rocky Mountains. We tested whether increased summer precipitation compensated for earlier snow melt, and if plasticity was associated with changes in soil moisture and/or leaf gas exchange. Lower summer precipitation decreased corolla length, style length, corolla width, sepal width, and nectar production, and increased nectar concentration. Earlier snow melt (taking into account natural and experimental variation) had the same effects on those traits and decreased inflorescence height. The effect of reduced summer precipitation was stronger in earlier snow melt years for corolla length and sepal width. Trait reductions were explained by drier soil during the flowering period, but this effect was only partially explained by how drier soils affected plant water stress, as measured by leaf gas exchange. We predicted the effects of plastic trait changes on pollinator visitation rates, pollination success, and seed production using prior studies on I. aggregata. The largest predicted effect of drier soil on relative fitness components via plasticity was a decrease in male fitness caused by reduced pollinator rewards (nectar production). Early snow melt and reduced precipitation are strong drivers of phenotypic plasticity, and both should be considered when predicting effects of climate change on plant traits in snow-dominated ecosystems.

Plant-pollinator interaction niche broadens in response to severe drought perturbations.

The composition of plant-pollinator interactions-i.e., who interacts with whom in diverse communities-is highly dynamic, and we have a very limited understanding of how interaction identities change in response to perturbations in nature. One prediction from niche and diet theory is that resource niches will broaden to compensate for resource reductions driven by perturbations, yet this has not been empirically tested in plant-pollinator systems in response to real-world perturbations in the field. Here, we use a long-term dataset of floral visitation to Ipomopsis aggregata, a montane perennial herb, to test whether the breadth of its floral visitation niche (i.e., flower visitor richness) changed in response to naturally occurring drought perturbations. Fewer floral resources are available in drought years, which could drive pollinators to expand their foraging niches, thereby expanding plants' floral visitation niches. We compared two drought years to three non-drought years to analyze changes in niche breadth and community composition of floral visitors to I. aggregata, predicting broadened niche breadth and distinct visitor community composition in drought years compared to non-drought years. We found statistically significant increases in niche breadth in drought years as compared to non-drought conditions, but no statistically distinguishable changes in community composition of flower visitors. Our findings suggest that plants' floral visitation niches may exhibit considerable plasticity in response to disturbance. This may have widespread consequences for community-level stability as well as functional consequences if increased niche overlap affects pollination services.

Experimental species removals impact the architecture of pollination networks.

Mutualistic networks are key for the creation and maintenance of biodiversity, yet are threatened by global environmental change. Most simulation models assume that network structure remains static after species losses, despite theoretical and empirical reasons to expect dynamic responses. We assessed the effects of experimental single bumblebee species removals on the structure of entire flower visitation networks. We hypothesized that network structure would change following processes linking interspecific competition with dietary niche breadth. We found that single pollinator species losses impact pollination network structure: resource complementarity decreased, while resource overlap increased. Despite marginally increased connectance, fewer plant species were visited after species removals. These changes may have negative functional impacts, as complementarity is important for maintaining biodiversity-ecological functioning relationships and visitation of rare plant species is critical for maintaining diverse plant communities.

Niche partitioning due to adaptive foraging reverses effects of nestedness and connectance on pollination network stability.

Much research debates whether properties of ecological networks such as nestedness and connectance stabilise biological communities while ignoring key behavioural aspects of organisms within these networks. Here, we computationally assess how adaptive foraging (AF) behaviour interacts with network architecture to determine the stability of plant-pollinator networks. We find that AF reverses negative effects of nestedness and positive effects of connectance on the stability of the networks by partitioning the niches among species within guilds. This behaviour enables generalist pollinators to preferentially forage on the most specialised of their plant partners which increases the pollination services to specialist plants and cedes the resources of generalist plants to specialist pollinators. We corroborate these behavioural preferences with intensive field observations of bee foraging. Our results show that incorporating key organismal behaviours with well-known biological mechanisms such as consumer-resource interactions into the analysis of ecological networks may greatly improve our understanding of complex ecosystems.

Heterospecific pollen deposition in Delphinium barbeyi: linking stigmatic pollen loads to reproductive output in the field.

BACKGROUND AND AIMS: Most pollinators are generalists and therefore are likely to transfer heterospecific pollen among co-flowering plants. Most work on the impacts of heterospecific pollen deposition on plant fecundity has utilized hand-pollination experiments in greenhouse settings, and we continue to know very little about the reproductive effects of heterospecific pollen in field settings. METHODS: We explored how patterns of naturally deposited heterospecific pollen relate to the reproductive output of Delphinium barbeyi, a common subalpine perennial herb in the Rocky Mountains (USA). We assessed a wide range of naturally occurring heterospecific pollen proportions and pollen load sizes, and linked stigmatic pollen deposition directly to seed set in individual carpels in the field. KEY RESULTS: We found that heterospecific pollen deposition in D. barbeyi is common, but typically found at low levels across stigmas collected in our sites. Neither conspecific nor heterospecific pollen deposition was related to carpel abortion. By contrast, we saw a significant positive relationship between conspecific pollen amount and viable seed production, as well as a significant negative interaction between the effects of conspecific pollen and heterospecific pollen amount, whereby the effect of conspecific pollen on viable seed production became weaker with greater heterospecific deposition on stigmas. CONCLUSIONS: To our knowledge, this is the first demonstration of a relationship between heterospecific pollen and seed production in a field setting. In addition, it is the first report of an interaction between conspecific and heterospecific pollen quantities on seed production. These findings, taken with the results from other studies, suggest that greenhouse hand-pollination studies and field studies should be more tightly integrated in future work to better understand how heterospecific pollen transfer can be detrimental for plant reproduction.

Single pollinator species losses reduce floral fidelity and plant reproductive function.

Understanding the functional impacts of pollinator species losses on plant populations is critical given ongoing pollinator declines. Simulation models of pollination networks suggest that plant communities will be resilient to losing many or even most of the pollinator species in an ecosystem. These predictions, however, have not been tested empirically and implicitly assume that pollination efficacy is unaffected by interactions with interspecific competitors. By contrast, ecological theory and data from a wide range of ecosystems show that interspecific competition can drive variation in ecological specialization over short timescales via behavioral or morphological plasticity, although the potential implications of such changes in specialization for ecosystem functioning remain unexplored. We conducted manipulative field experiments in which we temporarily removed single pollinator species from study plots in subalpine meadows, to test the hypothesis that interactions between pollinator species can shape individual species' functional roles via changes in foraging specialization. We show that loss of a single pollinator species reduces floral fidelity (short-term specialization) in the remaining pollinators, with significant implications for ecosystem functioning in terms of reduced plant reproduction, even when potentially effective pollinators remained in the system. Our results suggest that ongoing pollinator declines may have more serious negative implications for plant communities than is currently assumed. More broadly, we show that the individual functional contributions of species can be dynamic and shaped by the community of interspecific competitors, thereby documenting a distinct mechanism for how biodiversity can drive ecosystem functioning, with potential relevance to a wide range of taxa and systems.

Variation in context-dependent foraging behavior across pollinators.

Pollinator foraging behavior has direct consequences for plant reproduction and has been implicated in driving floral trait evolution. Exploring the degree to which pollinators exhibit flexibility in foraging behavior will add to a mechanistic understanding of how pollinators can impose selection on plant traits. Although plants have evolved suites of floral traits to attract pollinators, flower color is a particularly important aspect of the floral display. Some pollinators show strong innate color preference, but many pollinators display flexibility in preference due to learning associations between rewards and color, or due to variable perception of color in different environments or plant communities. This study examines the flexibility in flower color preference of two groups of native butterfly pollinators under natural field conditions. We find that pipevine swallowtails (Battus philenor) and skippers (family Hesperiidae), the predominate pollinators of the two native Texas Phlox species, Phlox cuspidata and Phlox drummondii, display distinct patterns of color preferences across different contexts. Pipevine swallowtails exhibit highly flexible color preferences and likely utilize other floral traits to make foraging decisions. In contrast, skippers have consistent color preferences and likely use flower color as a primary cue for foraging. As a result of this variation in color preference flexibility, the two pollinator groups impose concordant selection on flower color in some contexts but discordant selection in other contexts. This variability could have profound implications for how flower traits respond to pollinator-mediated selection. Our findings suggest that studying dynamics of behavior in natural field conditions is important for understanding plant-pollinator interactions.

The impact of plant enemies shows a phylogenetic signal.

The host ranges of plant pathogens and herbivores are phylogenetically constrained, so that closely related plant species are more likely to share pests and pathogens. Here we conducted a reanalysis of data from published experimental studies to test whether the severity of host-enemy interactions follows a similar phylogenetic signal. The impact of herbivores and pathogens on their host plants declined steadily with phylogenetic distance from the most severely affected focal hosts. The steepness of this phylogenetic signal was similar to that previously measured for binary-response host ranges. Enemy behavior and development showed similar, but weaker phylogenetic signal, with oviposition and growth rates declining with evolutionary distance from optimal hosts. Phylogenetic distance is an informative surrogate for estimating the likely impacts of a pest or pathogen on potential plant hosts, and may be particularly useful in early assessing risk from emergent plant pests, where critical decisions must be made with incomplete host records.