@article{hamon_youngsteadt_irwin_sorenson_2024, title={As prey and pollinators, insects increase reproduction and allow for outcrossing in the carnivorous plant <i>Dionaea muscipula}, ISSN={0002-9122 1537-2197}, url={http://dx.doi.org/10.1002/ajb2.16279}, DOI={10.1002/ajb2.16279}, abstractNote={AbstractPremiseUnderstanding the factors that limit reproductive success is a key component of plant biology. Carnivorous plants rely on insects as both nutrient sources and pollinators, providing a unique system for studying the effects of both resource and pollen limitation on plant reproduction.MethodsWe conducted a field experiment using wild‐growing Dionaea muscipula J. Ellis (Droseraceae) in which we manipulated prey and pollen in a factorial design and measured flower production, number of fruits, and number of seeds. Because understanding reproduction requires knowledge of a plant species' reproductive and pollination biology, we also examined the pollination system, per‐visit pollinator effectiveness, and pollen‐ovule (P/O) ratio of D. muscipula.ResultsPlants that received supplemental prey produced more flowers than control plants. They also had a higher overall fitness estimate (number of flowers × fruit set (total fruits/total flowers) × seeds per fruit), although this benefit was significant only when prey supplementation occurred in the previous growing season. Neither pollen supplementation nor the interaction between pollen and prey supplementation significantly affected overall plant fitness.ConclusionsThis study reinforces the reliance of D. muscipula on adequate prey capture for flower, fruit, and seed production and a mobile pollen vector for reproduction, indicating the importance of considering insects as part of an effective conservation management plan for this species.}, journal={American Journal of Botany}, publisher={Wiley}, author={Hamon, Laura E. and Youngsteadt, Elsa and Irwin, Rebecca E. and Sorenson, Clyde E.}, year={2024}, month={Jan} }
 @book{armstead_carper_davidson_blanchard_hopwood_larcom_black_briles_irwin_jolma_et al._2024, place={Denver, Colorado}, title={Colorado Native Pollinating Insects Health Study}, institution={Colorado Department of Natural Resources}, author={Armstead, S. and Carper, A. and Davidson, D. and Blanchard, M. and Hopwood, J. and Larcom, R. and Black, S. and Briles, C. and Irwin, R. and Jolma, G. and et al.}, year={2024} }
 @article{bronstein_davidowitz_lichtenberg_irwin_2024, title={The Hole Truth: Why Do Bumble Bees Rob Flowers More Than Once?}, volume={13}, ISSN={["2223-7747"]}, DOI={10.3390/plants13172507}, abstractNote={Primary nectar-robbers feed through holes they make in flowers, often bypassing the plant’s reproductive organs in the process. In many robbed plants, multiple holes are made in a single flower. Why a flower should be robbed repeatedly is difficult to understand: a hole signals that a nectar forager has already fed, which would seem likely to predict low rewards. We tested three explanations for this pattern in Corydalis caseana (Fumariaceae), a bumble bee pollinated and robbed plant: (1) multiple holes appear only after all flowers have been robbed once; (2) individual foragers make multiple holes during single visits; and (3) it is more profitable for bees to rob older flowers, even if they have already been robbed. We tested these hypotheses from 2014 to 2016 in a Colorado, USA population using data on robbing rates over time, floral longevity, nectar accumulation in visited and unvisited flowers, and the accumulation of robbing holes across the life of flowers. Multiple holes were already appearing when two-thirds of flowers still lacked a single hole, allowing us to reject the first hypothesis. The second hypothesis cannot offer a full explanation for multiple robbing holes because 35% of additional holes appeared in flowers one or more days after the first hole was made. Repeated sampling of bagged and exposed inflorescences revealed that flowers filled at a constant rate and refilled completely after being drained. Consequently, young flowers are of consistently low value to foragers compared to older flowers even if they had previously been robbed, consistent with the third hypothesis. While further studies are needed, these results offer a simple explanation for the paradoxical clustering of nectar-robbing damage in this and possibly other plant species.}, number={17}, journal={PLANTS-BASEL}, author={Bronstein, Judith L. and Davidowitz, Goggy and Lichtenberg, Elinor M. and Irwin, Rebecca E.}, year={2024}, month={Sep} }
 @article{ruzi_youngsteadt_cherveny_kettenbach_levenson_carley_collazo_irwin_2023, title={Bee species richness through time in an urbanizing landscape of the southeastern <scp>United States}, volume={30}, ISSN={1354-1013 1365-2486}, url={http://dx.doi.org/10.1111/gcb.17060}, DOI={10.1111/gcb.17060}, abstractNote={AbstractCompared to non‐urban environments, cities host ecological communities with altered taxonomic diversity and functional trait composition. However, we know little about how these urban changes take shape over time. Using historical bee (Apoidea: Anthophila) museum specimens supplemented with online repositories and researcher collections, we investigated whether bee species richness tracked urban and human population growth over the past 118 years. We also determined which species were no longer collected, whether those species shared certain traits, and if collector behavior changed over time. We focused on Wake County, North Carolina, United States where human population size has increased over 16 times over the last century along with the urban area within its largest city, Raleigh, which has increased over four times. We estimated bee species richness with occupancy models, and rarefaction and extrapolation curves to account for imperfect detection and sample coverage. To determine if bee traits correlated with when species were collected, we compiled information on native status, nesting habits, diet breadth, and sociality. We used non‐metric multidimensional scaling to determine if individual collectors contributed different bee assemblages over time. In total, there were 328 species collected in Wake County. We found that although bee species richness varied, there was no clear trend in bee species richness over time. However, recent collections (since 2003) were missing 195 species, and there was a shift in trait composition, particularly lost species were below‐ground nesters. The top collectors in the dataset differed in how often they collected bee species, but this was not consistent between historic and contemporary time periods; some contemporary collectors grouped closer together than others, potentially due to focusing on urban habitats. Use of historical collections and complimentary analyses can fill knowledge gaps to help understand temporal patterns of species richness in taxonomic groups that may not have planned long‐term data.}, number={1}, journal={Global Change Biology}, publisher={Wiley}, author={Ruzi, Selina A. and Youngsteadt, Elsa and Cherveny, April Hamblin and Kettenbach, Jessica and Levenson, Hannah K. and Carley, Danesha Seth and Collazo, Jaime A. and Irwin, Rebecca E.}, year={2023}, month={Dec} }
 @article{strange_tripodi_huntzinger_knoblett_klinger_herndon_vuong_mcfrederick_irwin_evans_et al._2023, title={Comparative analysis of 3 pollen sterilization methods for feeding bumble bees}, volume={116}, ISSN={0022-0493 1938-291X}, url={http://dx.doi.org/10.1093/jee/toad036}, DOI={10.1093/jee/toad036}, abstractNote={Abstract
               Pollen is an essential component of bee diets, and rearing bumble bees (Bombus spp.) for commercial use necessitates feeding pollen in mass quantities. This pollen is collected from honey bee (Apis mellifera L.) colonies because neither an artificial diet nor an economical, large-scale pollen collection process from flowers is available. The provenance of honey bee-collected pollen is often unknown, and in some cases has crossed international borders. Both deformed wing virus (DWV) and the fungal pathogen Ascosphaera apis (Claussen) Olive & Spiltoir (cause of chalkbrood disease); occur in honey bee-collected pollen, and infections have been observed in bumble bees. We used these pathogens as general surrogates for viruses and spore-forming fungal diseases to test the efficacy of 3 sterilization methods, and assessed whether treatment altered pollen quality for the bumble bee. Using honey bee-collected pollen spiked with known doses of DWV and A. apis, we compared gamma irradiation (GI), ozone fumigation (OZ), and ethylene oxide fumigation (EO) against an untreated positive control and a negative control. Following sterilization treatments, we tested A. apis spore viability, detected viral presence with PCR, and tested palatability to the bumble bee Bombus impatiens Cresson. We also measured bacterial growth from pollens treated with EO and GI. GI and EO outperformed OZ treatment in pathogen suppression. EO had the highest sterilizing properties under commercial conditions and retained palatability and supported bee development better than other treatments. These results suggest that EO sterilization reduces pathogen risks while retaining pollen quality as a food source for rearing bumble bees.}, number={3}, journal={Journal of Economic Entomology}, publisher={Oxford University Press (OUP)}, author={Strange, James P and Tripodi, Amber D and Huntzinger, Craig and Knoblett, Joyce and Klinger, Ellen and Herndon, James D and Vuong, Hoang Q and McFrederick, Quinn S and Irwin, Rebecca E and Evans, Jay D and et al.}, editor={Tarpy, DavidEditor}, year={2023}, month={Mar}, pages={662–673} }
 @article{heiling_irwin_morris_2023, title={Conflicting constraints on male mating success shape reward size in pollen‐rewarding plants}, volume={110}, ISSN={0002-9122 1537-2197}, url={http://dx.doi.org/10.1002/ajb2.16158}, DOI={10.1002/ajb2.16158}, abstractNote={AbstractPremisePollen‐rewarding plants face two conflicting constraints: They must prevent consumptive emasculation while remaining attractive to pollen‐collecting visitors. Small pollen packages (the quantity of pollen available in a single visit) may discourage visitors from grooming (reducing consumptive loss) but may also decrease a plant's attractiveness to pollen‐collecting visitors. What package size best balances these two constraints?MethodsWe modeled the joint effects of pollinators' grooming behaviors and package size preferences on the optimal package size (i.e., the size that maximizes pollen donation). We then used this model to examine Darwin's conjecture that selection should favor increased pollen production in pollen‐rewarding plants.ResultsWhen package size preferences are weak, minimizing package size reduces grooming losses and should be favored (as in previous theoretical studies). Stronger preferences select for larger packages despite the associated increase to grooming loss because loss associated with nonremoval of smaller packages is even greater. Total pollen donation increases with production (as Darwin suggested). However, if floral visitation declines or packages size preference increases with overall pollen availability, the fraction of pollen donated may decline as per‐plant pollen production increases. Hence, increasing production may result in diminishing returns.ConclusionsPollen‐rewarding plants can balance conflicting constraints on pollen donation by producing intermediate‐sized pollen packages. Strictly pollen‐rewarding plants may have responded to past selection to produce more pollen in total, but diminishing returns may limit the strength of that selection.}, number={6}, journal={American Journal of Botany}, publisher={Wiley}, author={Heiling, Jacob M. and Irwin, Rebecca E. and Morris, William F.}, year={2023}, month={Apr} }
 @article{prather_dalton_barr_blumstein_boggs_brody_inouye_irwin_martin_smith_et al._2023, title={Current and lagged climate affects phenology across diverse taxonomic groups}, volume={290}, ISSN={0962-8452 1471-2954}, url={http://dx.doi.org/10.1098/rspb.2022.2181}, DOI={10.1098/rspb.2022.2181}, abstractNote={The timing of life events (phenology) can be influenced by climate. Studies from around the world tell us that climate cues and species' responses can vary greatly. If variation in climate effects on phenology is strong within a single ecosystem, climate change could lead to ecological disruption, but detailed data from diverse taxa within a single ecosystem are rare. We collated first sighting and median activity within a high-elevation environment for plants, insects, birds, mammals and an amphibian across 45 years (1975–2020). We related 10 812 phenological events to climate data to determine the relative importance of climate effects on species’ phenologies. We demonstrate significant variation in climate-phenology linkage across taxa in a single ecosystem. Both current and prior climate predicted changes in phenology. Taxa responded to some cues similarly, such as snowmelt date and spring temperatures; other cues affected phenology differently. For example, prior summer precipitation had no effect on most plants, delayed first activity of some insects, but advanced activity of the amphibian, some mammals, and birds. Comparing phenological responses of taxa at a single location, we find that important cues often differ among taxa, suggesting that changes to climate may disrupt synchrony of timing among taxa.}, number={1990}, journal={Proceedings of the Royal Society B: Biological Sciences}, publisher={The Royal Society}, author={Prather, Rebecca M. and Dalton, Rebecca M. and barr, billy and Blumstein, Daniel T. and Boggs, Carol L. and Brody, Alison K. and Inouye, David W. and Irwin, Rebecca E. and Martin, Julien G. A. and Smith, Rosemary J. and et al.}, year={2023}, month={Jan} }
 @article{giacomini_adler_reading_irwin_2023, title={Differential bumble bee gene expression associated with pathogen infection and pollen diet}, volume={24}, ISSN={1471-2164}, url={http://dx.doi.org/10.1186/s12864-023-09143-5}, DOI={10.1186/s12864-023-09143-5}, abstractNote={Abstract
                Background
                Diet and parasitism can have powerful effects on host gene expression. However, how specific dietary components affect host gene expression that could feed back to affect parasitism is relatively unexplored in many wild species. Recently, it was discovered that consumption of sunflower (Helianthus annuus) pollen reduced severity of gut protozoan pathogen Crithidia bombi infection in Bombus impatiens bumble bees. Despite the dramatic and consistent medicinal effect of sunflower pollen, very little is known about the mechanism(s) underlying this effect. However, sunflower pollen extract increases rather than suppresses C. bombi growth in vitro, suggesting that sunflower pollen reduces C. bombi infection indirectly via changes in the host. Here, we analyzed whole transcriptomes of B. impatiens workers to characterize the physiological response to sunflower pollen consumption and C. bombi infection to isolate the mechanisms underlying the medicinal effect. B. impatiens workers were inoculated with either C. bombi cells (infected) or a sham control (un-infected) and fed either sunflower or wildflower pollen ad libitum. Whole abdominal gene expression profiles were then sequenced with Illumina NextSeq 500 technology.
              
                Results
                Among infected bees, sunflower pollen upregulated immune transcripts, including the anti-microbial peptide hymenoptaecin, Toll receptors and serine proteases. In both infected and un-infected bees, sunflower pollen upregulated putative detoxification transcripts and transcripts associated with the repair and maintenance of gut epithelial cells. Among wildflower-fed bees, infected bees downregulated immune transcripts associated with phagocytosis and the phenoloxidase cascade.
              
                Conclusions
                Taken together, these results indicate dissimilar immune responses between sunflower- and wildflower-fed bumble bees infected with C. bombi, a response to physical damage to gut epithelial cells caused by sunflower pollen, and a strong detoxification response to sunflower pollen consumption. Identifying host responses that drive the medicinal effect of sunflower pollen in infected bumble bees may broaden our understanding of plant-pollinator interactions and provide opportunities for effective management of bee pathogens.

              }, number={1}, journal={BMC Genomics}, publisher={Springer Science and Business Media LLC}, author={Giacomini, Jonathan J. and Adler, Lynn S. and Reading, Benjamin J. and Irwin, Rebecca E.}, year={2023}, month={Mar} }
 @article{taylor_allf_hopkins_irwin_jewell_nevo_nichols_rodríguez valerón_evans_sörensen_et al._2023, title={Nature's chefs: Uniting the hidden diversity of food making and preparing species across the tree of life}, volume={73}, ISSN={0006-3568 1525-3244}, url={http://dx.doi.org/10.1093/biosci/biad026}, DOI={10.1093/biosci/biad026}, abstractNote={AbstractThere may be no such thing as a free meal, but many species have evolved mechanisms for other species to consume the literal fruits of their labors. In the present article, inspired by a chef's recognition that such species are “nature's chefs,” we consider food-making species from the plant, animal, and fungal kingdoms, which produce food or mimic food to increase their own fitness. We identify three ways that species can produce or prepare meals—as food, drinks, or lures—and further distinguish between those providing an honest meal and those deceiving consumers with food mimics. By considering these species holistically, we highlight new hypotheses about the ecology and evolution of the widespread phenomenon of organisms that produce food for other organisms. We find surprising and useful generalities and exceptions among species as different as apple trees and anglerfish by examining species interactions across taxa, systems, and disciplines.}, number={6}, journal={BioScience}, publisher={Oxford University Press (OUP)}, author={Taylor, Brad W and Allf, Bradley and Hopkins, Skylar R and Irwin, Rebecca E and Jewell, Michelle and Nevo, Omer and Nichols, Lauren M and Rodríguez Valerón, Nabila and Evans, Joshua D and Sörensen, Pia M and et al.}, year={2023}, month={Apr}, pages={408–421} }
 @article{malfi_mcfrederick_lozano_irwin_adler_2023, title={Sunflower plantings reduce a common gut pathogen and increase queen production in common eastern bumblebee colonies}, volume={290}, ISSN={0962-8452 1471-2954}, url={http://dx.doi.org/10.1098/rspb.2023.0055}, DOI={10.1098/rspb.2023.0055}, abstractNote={
            Community diversity can reduce the prevalence and spread of disease, but certain species may play a disproportionate role in diluting or amplifying pathogens. Flowers act as both sources of nutrition and sites of pathogen transmission, but the effects of specific plant species in shaping bee disease dynamics are not well understood. We evaluated whether plantings of sunflower (
            Helianthus annuus
            ), whose pollen reduces infection by some pathogens when fed to bees in captivity, lowered pathogen levels and increased reproduction in free-foraging bumblebee colonies (
            Bombus impatiens
            ). Sunflower abundance reduced the prevalence of a common gut pathogen,
            Crithidia bombi
            , and reduced infection intensity, with an order of magnitude lower infection intensity at high sunflower sites compared with sites with little to no sunflower. Sunflower abundance was also positively associated with greater queen production in colonies. Sunflower did not affect prevalence of other detected pathogens. This work demonstrates that a single plant species can drive disease dynamics in foraging
            B. impatiens
            , and that sunflower plantings can be used as a tool for mitigating a prevalent pathogen while also increasing reproduction of an agriculturally important bee species.
          }, number={1996}, journal={Proceedings of the Royal Society B: Biological Sciences}, publisher={The Royal Society}, author={Malfi, Rosemary L. and McFrederick, Quinn S. and Lozano, Giselle and Irwin, Rebecca E. and Adler, Lynn S.}, year={2023}, month={Apr} }
 @article{figueroa_fowler_lopez_amaral_koch_stevenson_irwin_adler_2023, title={Sunflower spines and beyond: Mechanisms and breadth of pollen that reduce gut pathogen infection in the common eastern bumble bee}, volume={37}, ISSN={0269-8463 1365-2435}, url={http://dx.doi.org/10.1111/1365-2435.14320}, DOI={10.1111/1365-2435.14320}, abstractNote={Abstract


Plants have unique chemical and physical traits that can reduce infections in animals ranging from primates to caterpillars. Sunflowers (Helianthus annuus; Asteraceae) are one striking example, with pollen that suppresses infections by the trypanosomatid gut pathogen Crithidia bombi in the common eastern bumble bee (Bombus impatiens). However, the mechanism underlying this effect has remained elusive, and we do not know whether pollens from other Asteraceae species have similar effects.

We evaluated whether mechanisms mediating sunflower pollen's antipathogenic effects are physical (due to its spiny exine), chemical (due to metabolites) or both. We also evaluated the degree to which pollen from seven other Asteraceae species reduced C. bombi infection relative to pollen from sunflower and two non‐Asteraceae species, and whether pollen spine length predicted pathogen suppression.

We found that sunflower exines alone reduced infection as effectively as whole sunflower pollen, while sunflower pollen metabolites did not. Furthermore, bees fed pollen from four of seven other Asteraceae had 62%–92% lower C. bombi infections than those fed non‐Asteraceae pollen. Spine length, however, did not explain variation in bumble bee infection.

Our study indicates that sunflower pollen's capacity to suppress C. bombi is driven by its spiny exine, and that this phenomenon extends to several other Asteraceae species. Our results indicate that sunflower pollen exines are as effective as whole pollen in reducing infection, suggesting that future studies should expand to assess the effects of other species with spiny pollen on pollinator–pathogen dynamics.

Read the free Plain Language Summary for this article on the Journal blog.}, number={6}, journal={Functional Ecology}, publisher={Wiley}, author={Figueroa, Laura L. and Fowler, Alison and Lopez, Stephanie and Amaral, Victoria E. and Koch, Hauke and Stevenson, Philip C. and Irwin, Rebecca E. and Adler, Lynn S.}, year={2023}, month={Apr}, pages={1757–1769} }
 @article{campbell_price_waser_irwin_brody_2022, title={Comparative impacts of long‐term trends in snowmelt and species interactions on plant population dynamics}, volume={110}, ISSN={0022-0477 1365-2745}, url={http://dx.doi.org/10.1111/1365-2745.13875}, DOI={10.1111/1365-2745.13875}, abstractNote={Abstract


Climate change can impact plant fitness and population persistence directly through changing abiotic conditions and indirectly through its effects on species interactions. Pollination and seed predation are important biotic interactions that can impact plant fitness, but their impact on population growth rates relative to the role of direct climatic effects is unknown.

We combined 13 years of experiments on pollen limitation of seed set and pre‐dispersal seed predation in Ipomopsis aggregata, a subalpine wildflower, with a long‐term demographic study that has documented declining population growth with earlier spring snowmelt date. We determined how pollen limitation and seed predation changed with snowmelt date over 21 years and incorporated those effects into an integral projection model to assess relative impacts of biotic factors on population growth.

Both pollen limitation and the difference in stigma pollen load between pollen‐supplemented and control plants declined over years. Neither pollen limitation nor seed predation changed detectably with snowmelt date, suggesting an absence of indirect effects of that specific abiotic factor on these indices of biotic interactions. The projected biotic impacts of pollen limitation and seed predation on population growth rate were small compared to factors associated with snowmelt date. Providing full pollination would delay the projected date when earlier snowmelt will cause populations to fall below replacement by only 14 years.

Synthesis. Full pollination and elimination of seed predation would not compensate for the strong detrimental effects of early snowmelt on population growth rate, which in I. aggregata appears driven largely by abiotic environmental factors. The reduction over two decades in pollen limitation also suggests that natural selection on floral traits may weaken with continued climate change. These results highlight the value of studying both abiotic factors and biotic interactions to understand how climate change will influence plant populations.

}, number={5}, journal={Journal of Ecology}, publisher={Wiley}, author={Campbell, Diane R. and Price, Mary V. and Waser, Nickolas M. and Irwin, Rebecca E. and Brody, Alison K.}, year={2022}, month={Apr}, pages={1102–1112} }
 @article{fowler_sadd_bassingthwaite_irwin_adler_2022, title={Consuming sunflower pollen reduced pathogen infection but did not alter measures of immunity in bumblebees}, volume={377}, ISSN={0962-8436 1471-2970}, url={http://dx.doi.org/10.1098/rstb.2021.0160}, DOI={10.1098/rstb.2021.0160}, abstractNote={Certain diets can benefit bee health by reducing pathogens, but the mechanism(s) driving these medicinal effects are largely unexplored. Recent research found that sunflower (Helianthus annuus) pollen reduces the gut pathogenCrithidia bombiin the common eastern bumblebee (Bombus impatiens). Here, we tested the effects of sunflower pollen and infection on two bee immune metrics to determine whether sunflower pollen diet drives changes in host immunity that can explain this medicinal effect. Bees were infected withC. bombior not and given either sunflower or wildflower pollen. Subsequently, bees received a benign immune challenge or were left naive to test the induced and constitutive immune responses, respectively. We measured haemolymph phenoloxidase activity, involved in the melanization cascade, and antibacterial activity. Sunflower pollen reducedC. bombiinfection, but we found no significant pollen diet effect on either immune measure. Phenoloxidase activity was also not affected byC. bombiinfection status; however, uninfected bees were more likely to have measurable constitutive antibacterial activity, while infected bees had higher induced antibacterial activity. Overall, we found that sunflower pollen does not significantly affect the immune responses we measured, suggesting that the mechanisms underlying its medicinal effect do not involve these bee immune parameters.This article is part of the theme issue ‘Natural processes influencing pollinator health: from chemistry to landscapes’.}, number={1853}, journal={Philosophical Transactions of the Royal Society B: Biological Sciences}, publisher={The Royal Society}, author={Fowler, Alison E. and Sadd, Ben M. and Bassingthwaite, Toby and Irwin, Rebecca E. and Adler, Lynn S.}, year={2022}, month={May} }
 @article{pinilla-gallego_irwin_2022, title={Effects of an alternative host on the prevalence and intensity of infection of a bumble bee parasite}, volume={149}, ISSN={0031-1820 1469-8161}, url={http://dx.doi.org/10.1017/S003118202200004X}, DOI={10.1017/S003118202200004X}, abstractNote={AbstractSeveral bee parasites are transmitted through flowers, and some of them can infect multiple host species. Given the shared use of flowers by bee species, parasites can potentially encounter multiple host species, which could affect the evolution of parasite virulence. We used the trypanosomatid parasite Crithidia bombi and its host, the common eastern bumble bee (Bombus impatiens), to explore the effect of infecting an alternative host, the alfalfa leaf-cutter bee (Megachile rotundata), on parasite infectivity and ability to replicate. We conducted a serial passage experiment on primary and alternative hosts, assessing infectivity and intensity of infection during five passes. Parasite cells from each pass through the alternative host were also used to infect a group of primary hosts. We found that serial passes through the alternative host increased infectivity, but there was no effect on intensity of infection. Interestingly, both the probability and intensity of infection on the primary host increased after serial passage through the alternative host. This increase in intensity of infection could be due to maladaptation after selection of new C. bombi strains has occurred in the alternative host. This study suggests that host switching has the potential to affect the adaptation of bee parasites to their hosts.}, number={4}, journal={Parasitology}, publisher={Cambridge University Press (CUP)}, author={Pinilla-Gallego, Mario S. and Irwin, Rebecca E.}, year={2022}, month={Jan}, pages={562–567} }
 @article{pinilla-gallego_ng_amaral_irwin_2022, title={Floral shape predicts bee-parasite transmission potential}, ISSN={["1939-9170"]}, DOI={10.1002/ecy.3730}, abstractNote={AbstractThe spread of parasites is one of the primary drivers of population decline of both managed and wild bees. Several bee parasites are transmitted by the shared use of flowers, turning floral resources into potential disease hotspots. However, we know little about how floral morphology and floral species identity affect different steps of the transmission process. Here, we used the gut parasite Crithidia bombi and its primary host, bumble bees (Bombus spp.), to examine whether floral traits or species identity better predict three basic steps of parasite transmission on flowers: feces deposition on flowers, survival of the parasite on flowers, and acquisition by a new host. We also identified which traits and/or species were most strongly associated with each step in the transmission process. We found that both trait‐ and species‐based models fit the data on deposition of feces and survival of C. bombi on flowers, but that species‐based models provided a better fit compared with trait‐based ones. However, trait‐based models were better at predicting the acquisition of C. bombi on flowers. Although different species tended to support higher fecal deposition or parasite survival, we found that floral shape provided explanatory power for each of the transmission steps. When we assessed overall transmission potential, floral shape had the largest explanatory effect, with wider, shorter flowers promoting higher transmission. Taken together, our results highlight the importance of flower species identity and floral traits in disease transmission dynamics of bee parasites, and floral shape as an important predictor of overall transmission potential. Identifying traits associated with transmission potential may help us create seed mix that presents lower parasite transmission risk for bees for use in pollinator habitat.}, journal={ECOLOGY}, author={Pinilla-Gallego, Mario S. and Ng, Wee Hao and Amaral, Victoria E. and Irwin, Rebecca E.}, year={2022}, month={Jun} }
 @article{pardee_griffin_stemkovski_harrison_portman_kazenel_lynn_inouye_irwin_2022, title={Life-history traits predict responses of wild bees to climate variation}, volume={289}, ISSN={0962-8452 1471-2954}, url={http://dx.doi.org/10.1098/rspb.2021.2697}, DOI={10.1098/rspb.2021.2697}, abstractNote={Life-history traits, which are physical traits or behaviours that affect growth, survivorship and reproduction, could play an important role in how well organisms respond to environmental change. By looking for trait-based responses within groups, we can gain a mechanistic understanding of why environmental change might favour or penalize certain species over others. We monitored the abundance of at least 154 bee species for 8 consecutive years in a subalpine region of the Rocky Mountains to ask whether bees respond differently to changes in abiotic conditions based on their life-history traits. We found that comb-building cavity nesters and larger bodied bees declined in relative abundance with increasing temperatures, while smaller, soil-nesting bees increased. Further, bees with narrower diet breadths increased in relative abundance with decreased rainfall. Finally, reduced snowpack was associated with reduced relative abundance of bees that overwintered as prepupae whereas bees that overwintered as adults increased in relative abundance, suggesting that overwintering conditions might affect body size, lipid content and overwintering survival. Taken together, our results show how climate change may reshape bee pollinator communities, with bees with certain traits increasing in abundance and others declining, potentially leading to novel plant–pollinator interactions and changes in plant reproduction.}, number={1973}, journal={Proceedings of the Royal Society B: Biological Sciences}, publisher={The Royal Society}, author={Pardee, Gabriella L. and Griffin, Sean R. and Stemkovski, Michael and Harrison, Tina and Portman, Zachary M. and Kazenel, Melanie R. and Lynn, Joshua S. and Inouye, David W. and Irwin, Rebecca E.}, year={2022}, month={Apr} }
 @article{carper_warren_adler_irwin_2022, title={Pollen limitation of native plant reproduction in an urban landscape}, volume={109}, ISSN={0002-9122 1537-2197}, url={http://dx.doi.org/10.1002/ajb2.16080}, DOI={10.1002/ajb2.16080}, abstractNote={AbstractPremiseEvidence suggests that bees may benefit from moderate levels of human development. However, the effects of human development on pollination and reproduction of bee‐pollinated plants are less‐well understood. Studies have measured natural variation in pollination and plant reproduction as a function of urbanization, but few have experimentally measured the magnitude of pollen limitation in urban vs. non‐urban sites. Doing so is important to unambiguously link changes in pollination to plant reproduction. Previous work in the Southeastern United States found that urban sites supported twice the abundance of bees compared to non‐urban sites. We tested the hypothesis that greater bee abundance in some of the same urban sites translates into reduced pollen limitation compared to non‐urban sites.MethodsWe manipulated pollination to three native, wild‐growing, bee‐pollinated plants: Gelsemium sempervirens, Oenothera fruticosa, and Campsis radicans. Using supplemental pollinations, we tested for pollen limitation of three components of female reproduction in paired urban and non‐urban sites. We also measured pollen receipt as a proxy for pollinator visitation.ResultsWe found that all three plant species were pollen‐limited for some measures of female reproduction. However, opposite to our original hypothesis, two of the three species were more pollen‐limited in urban relative to non‐urban sites. We found that open‐pollinated flowers in urban sites received less conspecific and more heterospecific pollen on average than those in non‐urban sites.ConclusionsThese results suggest that even when urban sites have more abundant pollinators, this may not alleviate pollen limitation of native plant reproduction in urban landscapes.}, number={12}, journal={American Journal of Botany}, publisher={Wiley}, author={Carper, Adrian L. and Warren, Paige S. and Adler, Lynn S. and Irwin, Rebecca E.}, year={2022}, month={Oct}, pages={1969–1980} }
 @article{stemkovski_dickson_griffin_inouye_inouye_pardee_underwood_irwin_2022, title={Skewness in bee and flower phenological distributions}, volume={104}, ISSN={0012-9658 1939-9170}, url={http://dx.doi.org/10.1002/ecy.3890}, DOI={10.1002/ecy.3890}, abstractNote={AbstractPhenological distributions are characterized by their central tendency, breadth, and shape, and all three determine the extent to which interacting species overlap in time. Pollination mutualisms rely on temporal co‐occurrence of pollinators and their floral resources, and although much work has been done to characterize the shapes of flower phenological distributions, similar studies that include pollinators are lacking. Here, we provide the first broad assessment of skewness, a component of distribution shape, for a bee community. We compare skewness in bees to that in flowers, relate bee and flower skewness to other properties of their phenology, and quantify the potential consequences of differences in skewness between bees and flowers. Both bee and flower phenologies tend to be right‐skewed, with a more exaggerated asymmetry in bees. Early‐season species tend to be the most skewed, and this relationship is also stronger in bees than in flowers. Based on a simulation experiment, differences in bee and flower skewness could account for up to 14% of pairwise overlap differences. Given the potential for interaction loss, we argue that difference in skewness of interacting species is an underappreciated property of phenological change.}, number={1}, journal={Ecology}, publisher={Wiley}, author={Stemkovski, Michael and Dickson, Rachel G. and Griffin, Sean R. and Inouye, Brian D. and Inouye, David W. and Pardee, Gabriella L. and Underwood, Nora and Irwin, Rebecca E.}, year={2022}, month={Nov} }
 @article{giacomini_moore_adler_irwin_2022, title={Sunflower pollen induces rapid excretion in bumble bees: Implications for host-pathogen interactions}, volume={137}, ISSN={0022-1910}, url={http://dx.doi.org/10.1016/j.jinsphys.2022.104356}, DOI={10.1016/j.jinsphys.2022.104356}, abstractNote={Host diet can have a profound effect on host-pathogen interactions, including indirect effects on pathogens mediated through host physiology. In bumble bees (Bombus impatiens), the consumption of sunflower (Helianthus annuus) pollen dramatically reduces infection by the gut protozoan pathogen Crithidia bombi. One hypothesis for the medicinal effect of sunflower pollen is that consumption changes host gut physiological function, causing rapid excretion that flushes C. bombi from the system. We tested the effect of pollen diet and C. bombi infection on gut transit properties using a 2x2 factorial experiment in which bees were infected with C. bombi or not and fed sunflower or wildflower pollen diet. We measured several non-mutually exclusive physiological processes that underlie the insect excretory system, including gut transit time, bi-hourly excretion rate, the total number of excretion events and the total volume of excrement. Sunflower pollen significantly reduced gut transit time in uninfected bees, and increased the total number of excretion events and volume of excrement by 66 % and 68 %, respectively, in both infected and uninfected bees. Here we show that a sunflower pollen diet can affect host physiology gut function, causing more rapid and greater excretion. These results provide important insight into a mechanism that could underlie the medicinal effect of sunflower pollen for bumble bees.}, journal={Journal of Insect Physiology}, publisher={Elsevier BV}, author={Giacomini, Jonathan J. and Moore, Nicholas and Adler, Lynn S. and Irwin, Rebecca E.}, year={2022}, month={Feb}, pages={104356} }
 @article{fowler_giacomini_connon_irwin_adler_2022, title={Sunflower pollen reduces a gut pathogen in the model bee species,
            <i>Bombus impatiens
            , but has weaker effects in three wild congeners}, volume={289}, ISSN={0962-8452 1471-2954}, url={http://dx.doi.org/10.1098/rspb.2021.1909}, DOI={10.1098/rspb.2021.1909}, abstractNote={
            Commercial bumblebees have become popular models to understand stressors and solutions for pollinator health, but few studies test whether results translate to other pollinators. Consuming sunflower pollen dramatically reduces infection by the gut parasite
            Crithidia bombi
            in commercially reared
            Bombus impatiens
            . We assessed the effect of sunflower pollen on infection in wild
            B. impatiens
            ,
            Bombus griseocollis, Bombus bimaculatus
            and
            Bombus vagans
            . We also asked how pollen diet (50% sunflower pollen versus wildflower pollen) and infection (yes/no) affected performance in wild
            B. impatiens
            microcolonies. Compared to controls, sunflower pollen dramatically reduced
            Crithidia
            infection in commercial and wild
            B. impatiens,
            had similar but less dramatic effects in
            B. bimaculatus
            and
            B. vagans
            , and no effect in
            B. griseocollis
            .
            Bombus impatiens, B. bimaculatus
            and
            B. vagans
            are in the same subgenus, suggesting that responses to sunflower pollen may be phylogenetically conserved. In microcolonies, 50% sunflower pollen reduced infection compared to wildflower pollen, but also reduced reproduction. Sunflower pollen could control
            Crithidia
            infections in
            B. impatiens
            and potentially close relatives, but may hinder reproduction if other resources are scarce. We caution that research using managed bee species, such as
            B. impatiens
            , be interpreted carefully as findings may not relate to all bee species.
          }, number={1968}, journal={Proceedings of the Royal Society B: Biological Sciences}, publisher={The Royal Society}, author={Fowler, Alison E. and Giacomini, Jonathan J. and Connon, Sara June and Irwin, Rebecca E. and Adler, Lynn S.}, year={2022}, month={Feb} }
 @article{palmer-young_malfi_zhou_joyce_whitehead_van wyk_baylis_grubbs_boncristiani_evans_et al._2022, title={Sunflower-Associated Reductions in Varroa Mite Infestation of Honey Bee Colonies}, volume={116}, ISSN={0022-0493 1938-291X}, url={http://dx.doi.org/10.1093/jee/toac196}, DOI={10.1093/jee/toac196}, abstractNote={AbstractLandscapes can affect parasite epidemiology in wild and agricultural animals. Honey bees are threatened by loss of floral resources and by parasites, principally the mite Varroa destructor and the viruses it vectors. Existing mite control relies heavily on chemical treatments that can adversely affect bees. Alternative, pesticide-free control methods are needed to mitigate infestation with these ectoparasites. Many flowering plants provide nectar and pollen that confer resistance to parasites. Enrichment of landscapes with antiparasitic floral resources could therefore provide a sustainable means of parasite control in pollinators. Floral rewards of Asteraceae plants can reduce parasitic infection in diverse bee species, including honey and bumble bees. Here, we tested the effects of sunflower (Helianthus annuus) cropland and pollen supplementation on honey bee resistance to macro- and microparasites. Although sunflower had nonsignificant effects on microparasites, We found that increased sunflower pollen availability correlated with reduced Varroa mite infestation in landscapes and pollen-supplemented colonies. At the landscape level, each doubling of sunflower crop area was associated with a 28% reduction in mite infestation. In field trials, late-summer supplementation of colonies with sunflower pollen reduced mite infestation by 2.75-fold relative to artificial pollen. United States sunflower crop acreage has declined by 2% per year since 1980, however, suggesting reduced availability of this floral resource. Although further research is needed to determine whether the observed effects represent direct inhibition of mite fecundity or mite-limiting reductions in honey bee brood-rearing, our findings suggest the potential for sunflower plantings or pollen supplements to counteract a major driver of honey bee losses worldwide.}, number={1}, journal={Journal of Economic Entomology}, publisher={Oxford University Press (OUP)}, author={Palmer-Young, Evan C and Malfi, Rosemary and Zhou, Yujun and Joyce, Bryanna and Whitehead, Hannah and Van Wyk, Jennifer I and Baylis, Kathy and Grubbs, Kyle and Boncristiani, Dawn L and Evans, Jay D and et al.}, editor={Johnson, ReedEditor}, year={2022}, month={Dec}, pages={68–77} }
 @article{ledbetter_richman_irwin_bronstein_2022, title={What are the plant reproductive consequences of losing a nectar robber?}, volume={32}, ISSN={1920-7603}, url={http://dx.doi.org/10.26786/1920-7603(2022)663}, DOI={10.26786/1920-7603(2022)663}, abstractNote={Pollinator declines worldwide are detrimental for plants. Given the negative effects that antagonisitc visitors, including nectar robbers, can sometimes inflict, might declines in their populations instead confer benefits? During the 1970s, reproductive biology of the Colorado columbine, Aquilegia caerulea (Ranunculaceae), was documented near Gothic, Colorado. At that time, Bombus occidentalis, the Western Bumble bee, was one of its many pollinators, but more commonly acted as its only known nectar robber. Bombus occidentalis abundance has declined precipitously throughout the Western USA since the 1970s. In 2016, we documented floral visitors at sites near those used in the original survey. We then experimentally quantified the effects of nectar robbing, allowing us to estimate the reproductive consequences of losing B. occidentalis. We also quantified the potential pollination services of muscid flies (Muscidae, Diptera). The floral visitor community was dramatically different in 2016 compared to the 1970s. Bombus occidentalis was infrequently observed, and nectar robbing was negligible. Our experiments suggested that a high level of nectar robbing would lead to significantly reduced fruit set, although not seeds per fruit. Fly visits to flowers were dramatically higher in 2016 compared to the 1970s. In the absence of bumble bees, muscid flies significantly reduced fruit set below the self-pollination rate. The negative effect of the increase in these flies likely outweighed any positive effects A. caerulea experienced from the absence of its nectar robber. Although the field observations were conducted in a single year, when interpreted in combination with our manipulative experiments, they suggest how A. caerulea may fare in a changing visitation landscape.}, journal={Journal of Pollination Ecology}, publisher={International Commission for Plant Pollinator Relations}, author={Ledbetter, Trevor and Richman, Sarah and Irwin, Rebecca and Bronstein, Judith}, year={2022}, month={Aug}, pages={97–109} }
 @article{rixen_høye_macek_aerts_alatalo_anderson_arnold_barrio_bjerke_björkman_et al._2022, title={Winters are changing: snow effects on Arctic and alpine tundra ecosystems}, volume={8}, ISSN={2368-7460 2368-7460}, url={http://dx.doi.org/10.1139/AS-2020-0058}, DOI={10.1139/as-2020-0058}, abstractNote={ Snow is an important driver of ecosystem processes in cold biomes. Snow accumulation determines ground temperature, light conditions, and moisture availability during winter. It also affects the growing season’s start and end, and plant access to moisture and nutrients. Here, we review the current knowledge of the snow cover’s role for vegetation, plant-animal interactions, permafrost conditions, microbial processes, and biogeochemical cycling. We also compare studies of natural snow gradients with snow experimental manipulation studies to assess time scale difference of these approaches. The number of tundra snow studies has increased considerably in recent years, yet we still lack a comprehensive overview of how altered snow conditions will affect these ecosystems. Specifically, we found a mismatch in the timing of snowmelt when comparing studies of natural snow gradients with snow manipulations. We found that snowmelt timing achieved by snow addition and snow removal manipulations (average 7.9 days advance and 5.5 days delay, respectively) were substantially lower than the temporal variation over natural spatial gradients within a given year (mean range 56 days) or among years (mean range 32 days). Differences between snow study approaches need to be accounted for when projecting snow dynamics and their impact on ecosystems in future climates. }, number={3}, journal={Arctic Science}, publisher={Canadian Science Publishing}, author={Rixen, Christian and Høye, Toke Thomas and Macek, Petr and Aerts, Rien and Alatalo, Juha M. and Anderson, Jill T. and Arnold, Pieter A. and Barrio, Isabel C and Bjerke, Jarle W. and Björkman, Mats P. and et al.}, year={2022}, month={Sep}, pages={572–608} }
 @article{adler_irwin_mcart_vannette_2021, title={Floral traits affecting the transmission of beneficial and pathogenic pollinator-associated microbes}, volume={44}, ISSN={2214-5745}, url={http://dx.doi.org/10.1016/j.cois.2020.08.006}, DOI={10.1016/j.cois.2020.08.006}, abstractNote={Flowers provide resources for pollinators, and can also be transmission venues for beneficial or pathogenic pollinator-associated microbes. Floral traits could mediate transmission similarly for beneficial and pathogenic microbes, although some beneficial microbes can grow in flowers while pathogenic microbes may only survive until acquired by a new host. In spite of conceptual similarities, research on beneficial and pathogenic pollinator-associated microbes has progressed mostly independently. Recent advances demonstrate that floral traits are associated with transmission of beneficial and pathogenic microbes, with consequences for pollinator populations and communities. However, there is a near-absence of experimental manipulations of floral traits to determine causal effects on transmission, and a need to understand how floral, microbe and host traits interact to mediate transmission.}, journal={Current Opinion in Insect Science}, publisher={Elsevier BV}, author={Adler, Lynn S and Irwin, Rebecca E and McArt, Scott H and Vannette, Rachel L}, year={2021}, month={Apr}, pages={1–7} }
 @article{heiling_bronstein_irwin_2021, title={Nectar addition changes pollinator behavior but not plant reproduction in pollen‐rewarding <i>Lupinus argenteus}, volume={108}, ISSN={0002-9122 1537-2197}, url={http://dx.doi.org/10.1002/ajb2.1613}, DOI={10.1002/ajb2.1613}, abstractNote={PREMISEIn addition to its role as the male gamete, pollen is often used as a food reward for pollinators. Roughly 20,000 species of angiosperms are strictly pollen‐rewarding, providing no other rewards to their pollinators. However, the influence of this strategy on pollinator behavior and plant reproduction is poorly understood, especially relative to the nectar‐reward strategy. We performed a field experiment using the strictly pollen‐rewarding Lupinus argenteus to explore how the absence of nectar influences pollinator behavior and plant reproduction.METHODSWe added artificial nectar to Lupinus argenteus individuals to simulate a phenotype that would reward pollinators with both nectar and pollen. We compared bee pollinator behavior, via direct observation, and female reproduction between nectar‐added and nectarless control plants.RESULTSBees exhibited behavioral responses to the novel reward, collecting nectar as well as pollen and spending 27% longer per flower. Pollen transfer increased with flower visit duration. However, plants in the study population were not pollen‐limited; consequently, the observed changes in pollinator behavior did not result in changes in female components of plant reproduction.CONCLUSIONSThe addition of nectar to pollen‐rewarding plants resulted in modest increases in per‐flower pollinator visit duration and pollen transfer, but had no effect on reproduction because, at the place and time the experiment was conducted, plants were not pollen‐limited. These results suggest that a pollen‐only reward strategy may allow plants that are visited by pollen foragers to minimize some costs of reproduction by eliminating investment in other rewards, such as nectar, without compromising female plant fitness.}, number={3}, journal={American Journal of Botany}, publisher={Wiley}, author={Heiling, Jacob M. and Bronstein, Judith L. and Irwin, Rebecca E.}, year={2021}, month={Feb}, pages={402–410} }
 @article{rewcastle_henning_read_irwin_sanders_classen_2021, title={Plant removal across an elevational gradient marginally reduces rates, substantially reduces variation in mineralization}, volume={103}, ISSN={0012-9658 1939-9170}, url={http://dx.doi.org/10.1002/ecy.3546}, DOI={10.1002/ecy.3546}, abstractNote={AbstractThe loss of aboveground plant diversity alters belowground ecosystem function; yet, the mechanisms underpinning this relationship and the degree to which plant community structure and climate mediate the effects of plant species loss remain unclear. Here, we explored how plant species loss through experimental removal shaped belowground function in ecosystems characterized by different climatic regimes and edaphic properties. We measured plant community composition as well as potential carbon (C) and nitrogen (N) mineralization and microbial extracellular enzyme activity in soils collected from four unique plant removal experiments located along an elevational gradient in Colorado, USA. We found that, regardless of the identity of the removed species or the climate at each site, plant removal decreased the absolute variation in potential N mineralization rates and marginally reduced the magnitude of N mineralization rates. While plant species removal also marginally reduced C mineralization rates, C mineralization, unlike N mineralization, displayed sensitivity to the climatic and edaphic differences among sites, where C mineralization was greatest at the high elevation site that receives the most precipitation annually and contains the largest soil total C pool. Plant removal had little impact on soil enzyme activity. Removal effects were not contingent on the amount of biomass removed annually, and shifts in mineralization rates occurred despite only marginal shifts in plant community structure following plant species removal. Our results present a surprisingly simple and consistent pattern of belowground response to the loss of dominant plant species across an elevational gradient with different climatic and edaphic properties, suggesting a common response of belowground ecosystem function to plant species loss regardless of which plant species are lost or the broader climatic context.}, number={1}, journal={Ecology}, publisher={Wiley}, author={Rewcastle, Kenna E. and Henning, Jeremiah A. and Read, Quentin D. and Irwin, Rebecca E. and Sanders, Nathan J. and Classen, Aimée T.}, year={2021}, month={Nov} }
 @article{carper_richardson_irwin_bowers_2021, title={Seasonal Variation in Host Plant Chemistry Drives Sequestration in a Specialist Caterpillar}, volume={48}, ISSN={0098-0331 1573-1561}, url={http://dx.doi.org/10.1007/s10886-021-01321-7}, DOI={10.1007/s10886-021-01321-7}, number={1}, journal={Journal of Chemical Ecology}, publisher={Springer Science and Business Media LLC}, author={Carper, Adrian L. and Richardson, Leif L. and Irwin, Rebecca E. and Bowers, M. Deane}, year={2021}, month={Nov}, pages={79–88} }
 @article{richman_barker_baek_papaj_irwin_bronstein_2021, title={The Sensory and Cognitive Ecology of Nectar Robbing}, volume={9}, ISSN={2296-701X}, url={http://dx.doi.org/10.3389/fevo.2021.698137}, DOI={10.3389/fevo.2021.698137}, abstractNote={Animals foraging from flowers must assess their environment and make critical decisions about which patches, plants, and flowers to exploit to obtain limiting resources. The cognitive ecology of plant-pollinator interactions explores not only the complex nature of pollinator foraging behavior and decision making, but also how cognition shapes pollination and plant fitness. Floral visitors sometimes depart from what we think of as typical pollinator behavior and instead exploit floral resources by robbing nectar (bypassing the floral opening and instead consuming nectar through holes or perforations made in floral tissue). The impacts of nectar robbing on plant fitness are well-studied; however, there is considerably less understanding, from the animal’s perspective, about the cognitive processes underlying nectar robbing. Examining nectar robbing from the standpoint of animal cognition is important for understanding the evolution of this behavior and its ecological and evolutionary consequences. In this review, we draw on central concepts of foraging ecology and animal cognition to consider nectar robbing behavior either when individuals use robbing as their only foraging strategy or when they switch between robbing and legitimate foraging. We discuss sensory and cognitive biases, learning, and the role of a variable environment in making decisions about robbing vs. foraging legitimately. We also discuss ways in which an understanding of the cognitive processes involved in nectar robbing can address questions about how plant-robber interactions affect patterns of natural selection and floral evolution. We conclude by highlighting future research directions on the sensory and cognitive ecology of nectar robbing.}, journal={Frontiers in Ecology and Evolution}, publisher={Frontiers Media SA}, author={Richman, Sarah K. and Barker, Jessica L. and Baek, Minjung and Papaj, Daniel R. and Irwin, Rebecca E. and Bronstein, Judith L.}, year={2021}, month={Oct} }
 @article{giacomini_connon_marulanda_adler_irwin_2021, title={The costs and benefits of sunflower pollen diet on bumble bee colony disease and health}, volume={12}, ISSN={2150-8925 2150-8925}, url={http://dx.doi.org/10.1002/ecs2.3663}, DOI={10.1002/ecs2.3663}, abstractNote={AbstractPathogen transmission between domesticated and wild host species has important implications for community ecology, agriculture, and wildlife conservation. Bumble bees provide valuable pollination services that are vital for both wildflowers and agricultural production. Intense concerns about pathogen spillover from commercial bumble bees to wild bee populations, and the potential harmful effects of pathogen spillback to commercial bees, has stimulated a need for practical strategies that effectively manage bumble bee infectious diseases. Here, we assessed the costs and benefits of a medicinal sunflower pollen diet (Helianthusannuus) on whole‐colony bumble bee disease and performance using commercial colonies of the common eastern bumble bee,Bombus impatiens, and its protozoan pathogen,Crithidia bombi(Trypanosomatida). We first found that a 1:1 mixture of sunflower combined with wildflower pollen reducedC. bombiinfection prevalence and intensity within individualB. impatiensworkers by nearly 4‐fold and 12‐fold, respectively, relative to wildflower pollen. At the colony level, a 1:1 mixture of sunflower and wildflower pollen reducedC. bombiinfection prevalence by 11% averaged over a 10‐week period and infection intensity by 30% relative to wildflower pollen. Colony performance was similar between pollen diets and infection treatments, including the number of workers and immatures produced, and size and weight of workers, drones, and queens. Infection significantly reduced the probability of queen production in colonies fed a pure wildflower pollen diet, but not colonies fed a mixed sunflower pollen diet, suggesting that the medicinal benefits of a mixed sunflower pollen diet can reverse the negative effects of infection on reproductive success. This study provides evidence that sunflower pollen as part of a mixed pollen diet can reduce infection in individual bees and whole colonies with no significant nutritional trade‐offs for colony worker production and most aspects of colony reproduction. A supplemental mixed sunflower pollen diet may provide a simple and effective solution to reduce disease and improve the health of economically and ecologically important pollinators.}, number={7}, journal={Ecosphere}, publisher={Wiley}, author={Giacomini, Jonathan J. and Connon, Sara J. and Marulanda, Daniel and Adler, Lynn S. and Irwin, Rebecca E.}, year={2021}, month={Jul} }
 @article{adler_fowler_malfi_anderson_coppinger_deneen_lopez_irwin_farrell_stevenson_2020, title={Assessing Chemical Mechanisms Underlying the Effects of Sunflower Pollen on a Gut Pathogen in Bumble Bees}, volume={46}, ISSN={0098-0331 1573-1561}, url={http://dx.doi.org/10.1007/s10886-020-01168-4}, DOI={10.1007/s10886-020-01168-4}, abstractNote={Many pollinator species are declining due to a variety of interacting stressors including pathogens, sparking interest in understanding factors that could mitigate these outcomes. Diet can affect host-pathogen interactions by changing nutritional reserves or providing bioactive secondary chemicals. Recent work found that sunflower pollen (Helianthus annuus) dramatically reduced cell counts of the gut pathogen Crithidia bombi in bumble bee workers (Bombus impatiens), but the mechanism underlying this effect is unknown. Here we analyzed methanolic extracts of sunflower pollen by LC-MS and identified triscoumaroyl spermidines as the major secondary metabolite components, along with a flavonoid quercetin-3-O-hexoside and a quercetin-3-O-(6-O-malonyl)-hexoside. We then tested the effect of triscoumaroyl spermidine and rutin (as a proxy for quercetin glycosides) on Crithidia infection in B. impatiens, compared to buckwheat pollen (Fagopyrum esculentum) as a negative control and sunflower pollen as a positive control. In addition, we tested the effect of nine fatty acids from sunflower pollen individually and in combination using similar methods. Although sunflower pollen consistently reduced Crithidia relative to control pollen, none of the compounds we tested had significant effects. In addition, diet treatments did not affect mortality, or sucrose or pollen consumption. Thus, the mechanisms underlying the medicinal effect of sunflower are still unknown; future work could use bioactivity-guided fractionation to more efficiently target compounds of interest, and explore non-chemical mechanisms. Ultimately, identifying the mechanism underlying the effect of sunflower pollen on pathogens will open up new avenues for managing bee health.}, number={8}, journal={Journal of Chemical Ecology}, publisher={Springer Science and Business Media LLC}, author={Adler, Lynn S. and Fowler, Alison E. and Malfi, Rosemary L. and Anderson, Patrick R. and Coppinger, Lily M. and Deneen, Pheobe M. and Lopez, Stephanie and Irwin, Rebecca E. and Farrell, Iain W. and Stevenson, Philip C.}, year={2020}, month={Mar}, pages={649–658} }
 @article{stemkovski_pearse_griffin_pardee_gibbs_griswold_neff_oram_rightmyer_sheffield_et al._2020, title={Bee phenology is predicted by climatic variation and functional traits}, volume={23}, ISSN={1461-023X 1461-0248}, url={http://dx.doi.org/10.1111/ele.13583}, DOI={10.1111/ele.13583}, abstractNote={AbstractClimate change is shifting the environmental cues that determine the phenology of interacting species. Plant–pollinator systems may be susceptible to temporal mismatch if bees and flowering plants differ in their phenological responses to warming temperatures. While the cues that trigger flowering are well‐understood, little is known about what determines bee phenology. Using generalised additive models, we analyzed time‐series data representing 67 bee species collected over 9 years in the Colorado Rocky Mountains to perform the first community‐wide quantification of the drivers of bee phenology. Bee emergence was sensitive to climatic variation, advancing with earlier snowmelt timing, whereas later phenophases were best explained by functional traits including overwintering stage and nest location. Comparison of these findings to a long‐term flower study showed that bee phenology is less sensitive than flower phenology to climatic variation, indicating potential for reduced synchrony of flowers and pollinators under climate change.}, number={11}, journal={Ecology Letters}, publisher={Wiley}, author={Stemkovski, Michael and Pearse, William D. and Griffin, Sean R. and Pardee, Gabriella L. and Gibbs, Jason and Griswold, Terry and Neff, John L. and Oram, Ryan and Rightmyer, Molly G. and Sheffield, Cory S. and et al.}, editor={Coulson, TimEditor}, year={2020}, month={Aug}, pages={1589–1598} }
 @article{lichtenberg_irwin_bronstein_2020, title={Bumble bees are constant to nectar-robbing behaviour despite low switching costs}, volume={170}, ISSN={["1095-8282"]}, DOI={10.1016/j.anbehav.2020.09.008}, abstractNote={Individuals sometimes exhibit striking constancy to a single behaviour even when they are capable of short-term behavioural flexibility. Constancy enables animals to avoid costs such as memory constraints, but can also inflict significant opportunity costs through behaviour–environment mismatch. It is unclear when individuals should exhibit behavioural constancy and which types of costs most strongly influence such behaviour. We use a case in which individuals within a population exhibit more than one handling tactic for a single food type to investigate whether costs associated with switching among tactics constrain expression of intra-individual variation. Using wild bumble bees (Bombus spp.) that feed on nectar through flower openings (legitimate visits) or through holes at the base of flowers (robbing), we asked three questions. (1) Do individual bees exhibit tactic constancy within and across foraging bouts? (2) Are individuals willing to switch their food-handling tactics? (3) Is constancy in food-handling tactics maintained by costs associated with switching tactics? We measured energetic costs in addition to handling times. We found that bees freely foraging in meadows were highly constant to a single food-handling tactic both within and across bouts. However, experiments with individual captive bees showed that these bees were willing to switch tactics and experienced minimal costs in doing so. Thus, switching costs do not drive the observed constancy in food-handling tactics of bumble bees within and across foraging bouts.}, journal={ANIMAL BEHAVIOUR}, author={Lichtenberg, Elinor M. and Irwin, Rebecca E. and Bronstein, Judith L.}, year={2020}, month={Dec}, pages={177–188} }
 @article{tauber_tozkar_schwarz_lopez_irwin_adler_evans_2020, title={Colony-Level Effects of Amygdalin on Honeybees and Their Microbes}, volume={11}, ISBN={2075-4450}, ISSN={2075-4450}, url={http://dx.doi.org/10.3390/insects11110783}, DOI={10.3390/insects11110783}, abstractNote={Amygdalin, a cyanogenic glycoside, is found in the nectar and pollen of almond trees, as well as in a variety of other crops, such as cherries, nectarines, apples and others. It is inevitable that western honeybees (Apis mellifera) consistently consume amygdalin during almond pollination season because almond crops are almost exclusively pollinated by honeybees. This study tests the effects of a field-relevant concentration of amygdalin on honeybee microbes and the activities of key honeybee genes. We executed a two-month field trial providing sucrose solutions with or without amygdalin ad libitum to free-flying honeybee colonies. We collected adult worker bees at four time points and used RNA sequencing technology and our HoloBee database to assess global changes in microbes and honeybee transcripts. Our hypothesis was that amygdalin will negatively affect bee microbes and possibly immune gene regulation. Using a log2 fold-change cutoff at two and intraday comparisons, we show no large change of bacterial counts, fungal counts or key bee immune gene transcripts, due to amygdalin treatment in relation to the control. However, relatively large titer decreases in the amygdalin treatment relative to the control were found for several viruses. Chronic bee paralysis virus levels had a sharp decrease (−14.4) with titers then remaining less than the control, Black queen cell virus titers were lower at three time points (<−2) and Deformed wing virus titers were lower at two time points (<−6) in amygdalin-fed compared to sucrose-fed colonies. Titers of Lotmaria passim were lower in the treatment group at three of the four dates (<−4). In contrast, Sacbrood virus had two dates with relative increases in its titers (>2). Overall, viral titers appeared to fluctuate more so than bacteria, as observed by highly inconstant patterns between treatment and control and throughout the season. Our results suggest that amygdalin consumption may reduce several honeybee viruses without affecting other microbes or colony-level expression of immune genes.}, number={11}, journal={Insects}, publisher={MDPI AG}, author={Tauber, James P. and Tozkar, Cansu Ö. and Schwarz, Ryan S. and Lopez, Dawn and Irwin, Rebecca E. and Adler, Lynn S. and Evans, Jay D.}, year={2020}, month={Nov}, pages={783} }
 @article{lichtenberg_richman_irwin_bronstein_2020, title={Competition for nectar resources does not affect bee foraging tactic constancy}, volume={45}, ISSN={0307-6946 1365-2311}, url={http://dx.doi.org/10.1111/een.12866}, DOI={10.1111/een.12866}, abstractNote={1. Competition alters animal foraging, including promoting the use of alternative resources. It may also impact how animals feed when they are able to handle the same food with more than one tactic. Competition likely impacts both consumers and their resources through its effects on food handling, but this topic has received little attention.2. Bees often use two tactics for extracting nectar from flowers: they can visit at the flower opening, or rob nectar from holes at the base of flowers. Exploitative competition for nectar is thought to promote nectar robbing. If so, higher competition among floral visitors should reduce constancy to a single foraging tactic as foragers will seek food using all possible tactics. To test this prediction, field observations and two experiments involving bumble bees visiting three montane Colorado plant species (Mertensia ciliata, Linaria vulgaris, Corydalis caseana) were used under various levels of inter‐ and intra‐specific competition for nectar.3. In general, individual bumble bees remained constant to a single foraging tactic, independent of competition levels. However, bees that visited M. ciliata in field observations decreased their constancy and increased nectar robbing rates as visitation rates by co‐visitors increased.4. While tactic constancy was high overall regardless of competition intensity, this study highlights some intriguing instances in which competition and tactic constancy may be linked. Further studies investigating the cognitive underpinnings of tactic constancy should provide insight on the ways in which animals use alternative foraging tactics to exploit resources.}, number={4}, journal={Ecological Entomology}, publisher={Wiley}, author={Lichtenberg, Elinor M. and Richman, Sarah K. and Irwin, Rebecca E. and Bronstein, Judith L.}, year={2020}, month={Mar}, pages={904–909} }
 @article{ngor_palmer-young_burciaga nevarez_russell_leger_giacomini_pinilla-gallego_irwin_mcfrederick_2020, title={Cross-infectivity of honey and bumble bee-associated parasites across three bee families}, volume={147}, ISSN={0031-1820 1469-8161}, url={http://dx.doi.org/10.1017/S0031182020001018}, DOI={10.1017/S0031182020001018}, abstractNote={AbstractRecent declines of wild pollinators and infections in honey, bumble and other bee species have raised concerns about pathogen spillover from managed honey and bumble bees to other pollinators. Parasites of honey and bumble bees include trypanosomatids and microsporidia that often exhibit low host specificity, suggesting potential for spillover to co-occurring beesviashared floral resources. However, experimental tests of trypanosomatid and microsporidial cross-infectivity outside of managed honey and bumble bees are scarce. To characterize potential cross-infectivity of honey and bumble bee-associated parasites, we inoculated three trypanosomatids and one microsporidian into five potential hosts – including four managed species – from the apid, halictid and megachilid bee families. We found evidence of cross-infection by the trypanosomatidsCrithidia bombiandC. mellificae, with evidence for replication in 3/5 and 3/4 host species, respectively. These include the first reports of experimentalC. bombiinfection inMegachile rotundataandOsmia lignaria, andC. mellificaeinfection inO. lignariaandHalictus ligatus. Although inability to control amounts inoculated inO. lignariaandH. ligatushindered estimates of parasite replication, our findings suggest a broad host range in these trypanosomatids, and underscore the need to quantify disease-mediated threats of managed social bees to sympatric pollinators.}, number={12}, journal={Parasitology}, publisher={Cambridge University Press (CUP)}, author={Ngor, Lyna and Palmer-Young, Evan C. and Burciaga Nevarez, Rodrigo and Russell, Kaleigh A. and Leger, Laura and Giacomini, Sara June and Pinilla-Gallego, Mario S. and Irwin, Rebecca E. and McFrederick, Quinn S.}, year={2020}, month={Jun}, pages={1290–1304} }
 @article{adler_barber_biller_irwin_2020, title={Flowering plant composition shapes pathogen infection intensity and reproduction in bumble bee colonies}, volume={117}, ISSN={0027-8424 1091-6490}, url={http://dx.doi.org/10.1073/pnas.2000074117}, DOI={10.1073/pnas.2000074117}, abstractNote={Pathogens pose significant threats to pollinator health and food security. Pollinators can transmit diseases during foraging, but the consequences of plant species composition for infection is unknown. In agroecosystems, flowering strips or hedgerows are often used to augment pollinator habitat. We used canola as a focal crop in tents and manipulated flowering strip composition using plant species we had previously shown to result in higher or lower bee infection in short-term trials. We also manipulated initial colony infection to assess impacts on foraging behavior. Flowering strips using high-infection plant species nearly doubled bumble bee colony infection intensity compared to low-infection plant species, with intermediate infection in canola-only tents. Both infection treatment and flowering strips reduced visits to canola, but we saw no evidence that infection treatment shifted foraging preferences. Although high-infection flowering strips increased colony infection intensity, colony reproduction was improved with any flowering strips compared to canola alone. Effects of flowering strips on colony reproduction were explained by nectar availability, but effects of flowering strips on infection intensity were not. Thus, flowering strips benefited colony reproduction by adding floral resources, but certain plant species also come with a risk of increased pathogen infection intensity.}, number={21}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Adler, Lynn S. and Barber, Nicholas A. and Biller, Olivia M. and Irwin, Rebecca E.}, year={2020}, month={May}, pages={11559–11565} }
 @article{fowler_stone_irwin_adler_2020, title={Sunflower pollen reduces a gut pathogen in worker and queen but not male bumble bees}, volume={45}, ISSN={0307-6946 1365-2311}, url={http://dx.doi.org/10.1111/een.12915}, DOI={10.1111/een.12915}, abstractNote={1. Social insect castes and sexes differ in many ways, including morphology, behavior, and sometimes ploidy level. Recent studies have found that consuming sunflower pollen reduces the gut pathogen Crithidia bombi in workers of the common eastern bumble bee (Bombus impatiens). Here, this work is extended to the reproductive individuals that represent colony fitness – males and queens – to assess if the medicinal effects of sunflower pollen vary with bee caste and sex.2. This study examined the effect of sunflower pollen compared to a diverse wildflower pollen mix on infection in worker, male, and daughter queen commercial B. impatiens. Bees were infected, fed either sunflower pollen or wildflower pollen for 7 days, and then infection levels were assessed.3. Compared to wildflower pollen, sunflower pollen dramatically reduced Crithidia infection in workers and daughter queens, but not males. Infection levels were very low for both diets in males; this could be due to low pollen consumption or other mechanisms.4. Reducing Crithidia infection in young queens before they undergo hibernation is important for population dynamics since infected queens are less likely to survive hibernation, and those that do are less likely to successfully establish a nest the following spring. Because sunflowers bloom in late summer when new queens are emerging, sunflowers could provide an important dietary component for queens during this critical life stage. Deepening our understanding of how diet impacts pathogens in reproductive bees, as well as workers, is crucial to maintain healthy pollinator populations.}, number={6}, journal={Ecological Entomology}, publisher={Wiley}, author={Fowler, Alison E. and Stone, Elyse C. and Irwin, Rebecca E. and Adler, Lynn S.}, year={2020}, month={Jul}, pages={1318–1326} }
 @article{inouye_underwood_inouye_irwin_2020, title={Support early-career field researchers}, volume={368}, ISSN={0036-8075 1095-9203}, url={http://dx.doi.org/10.1126/science.abc1261}, DOI={10.1126/science.abc1261}, abstractNote={Pandemic-induced restrictions on research are now ubiquitous. We urge administrators and policy-makers to recognize that field researchers—especially those early in their careers—face unique challenges, even if restrictions last only a month or two. Bans on travel, hiring, and facility use are forcing many researchers to abandon the entire field season, losing a full year of irreplaceable data and research-training opportunities.

The loss of data is most damaging for multi-year projects, which are common in the case of field research. For example, a lost year in a demographic study renders multiple years of data uninterpretable because data on growth and survival between years are required for analysis. Similarly, in any system with lagging effects, the loss of a single season can have multi-year consequences on analyses. For long-term studies, the loss of a single year may seem less damaging, but increasing climate variance means that each season brings new insights.

The impact of lost research is most severe for scientists at early career stages. Institutions and agencies should focus on protecting graduate students and postdocs, as the loss of a year's data can affect their ability to complete dissertations or acquire jobs. We call on policy-makers and institutions to provide funding opportunities for early-career researchers to recover from such disruptions; support for salary, stipends, and tuition will be most critical. Although scientists conducting field research may be most vulnerable, these funding opportunities would certainly benefit laboratory-based scientists as well.

No one institution or agency has the resources to prevent impacts of lost research on field science or science in general. However, modest targeted funding for the most vulnerable research projects and researchers would help to preserve the quality of research and the pipeline of research training that we depend on for our next generation of scientists.}, number={6492}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Inouye, David W. and Underwood, Nora and Inouye, Brian D. and Irwin, Rebecca E.}, editor={Sills, JenniferEditor}, year={2020}, month={May}, pages={724–725} }
 @misc{irwin_youngsteadt_warren_bronstein_2020, title={The Evolutionary Ecology of Mutualisms in Urban Landscapes}, ISBN={["978-0-19-883685-8"]}, url={http://dx.doi.org/10.1093/oso/9780198836841.003.0007}, DOI={10.1093/oso/9780198836841.003.0007}, abstractNote={Abstract
               Mutualisms are critically important in maintaining the biodiversity and functioning of ecosystems. Mutualisms include a diverse array of interactions that result in reciprocal positive effects for both partners, including plant–pollinator, plant–seed disperser, and plant–rhizobia interactions. There is growing recognition that global environmental change can affect the ecological outcomes of mutualisms, but less attention has been paid to how urbanization in particular affects their evolution. This chapter builds from an ecological perspective and considers how urban landscapes may affect the evolutionary ecology of mutualism. It reviews the adaptive evolutionary processes that could affect mutualism in urban landscapes. It then surveys transportation, protection, and nutritional mutualisms to assess how urbanization may affect these mutualistic interactions in an evolutionary framework. The survey described in the chapter highlights a dearth of empirical and theoretical investigations on urban mutualisms from an evolutionary perspective despite potentially strong changes in selection pressures in urban areas. The chapter ends by outlining research directions to further the study of the evolutionary ecology of mutualisms in urban landscapes.}, journal={Urban Evolutionary Biology}, publisher={Oxford University PressOxford}, author={Irwin, Rebecca E. and Youngsteadt, Elsa and Warren, Paige S. and Bronstein, Judith L.}, year={2020}, month={May}, pages={111–129} }
 @article{prado_collazo_marand_irwin_2021, title={The influence of floral resources and microclimate on pollinator visitation in an agro-ecosystem}, volume={307}, ISSN={["1873-2305"]}, DOI={10.1016/j.agee.2020.107196}, abstractNote={As agriculture expands to meet the needs of a growing global population, natural ecosystems are threatened by deforestation and habitat fragmentation. Tropical agroforestry systems offer a sustainable alternative to traditional agriculture by providing food for production while also supporting biodiversity and ecosystem services. Previous studies have shown that these systems may even improve crop pollination, but the mechanisms of how these improvements occur are still poorly understood. Using coffee as a focal crop, we explored how microclimatic conditions affected nectar traits (sugar and caffeine concentration) important for pollinator visitation. We also studied how microclimate, floral traits, floral availability at the coffee plant level, availability of floral resources provided by other plant species in the agroecosystem ("neighborhood floral availability"), and the presence of other bees affected the amount of time bees spent foraging on coffee flowers and the proportion of coffee pollen carried on their bodies. We explored these factors using the two dominant coffee species farmed on Puerto Rico, Coffea canephora and C. arabica, under sun and shade management. We found that high nectar sugar concentration and temperature were important predictors of short floral visits (<15s), while increased numbers of bees and open coffee flowers were important predictors of longer floral visits (16–180 seconds). High nectar caffeine concentration was an important predictor of longer visits on C. arabica flowers while the opposite was observed for C. canephora flowers. For both species, high coffee floral availability was the main predicting factor for the proportion of coffee pollen on the bees' bodies. Surprisingly, neither neighborhood floral availability nor the type of coffee plantation (agroforest/shade or sun) were important predictors of bee visitation. These results suggest non-coffee flowering plants in coffee plantations were neither competitors nor facilitators of coffee plants for pollinators. Additionally, most of the bees surveyed were carrying ≥80 % pollen from one species (C. arabica or C. canephora), likely resulting in little heterospecific pollen deposition between Coffea and non-Coffea flowers. Shade trees in coffee plantations do not detract from pollinator visitation to coffee flowers, suggesting that the provision of multiple ecological and wildlife conservation benefits by shade trees is not in conflict with a grower's ability to maximize the benefits of insect pollination on fruit production.}, journal={AGRICULTURE ECOSYSTEMS & ENVIRONMENT}, author={Prado, Sara Guiti and Collazo, Jaime A. and Marand, Mariam H. and Irwin, Rebecca E.}, year={2021}, month={Feb} }
 @article{woodard_federman_james_danforth_griswold_inouye_mcfrederick_morandin_paul_sellers_et al._2020, title={Towards a US national program for monitoring native bees}, volume={252}, ISSN={["1873-2917"]}, DOI={10.1016/j.biocon.2020.108821}, abstractNote={North America has more than 4000 bee species, yet we have little information on the health, distribution, and population trends of most of these species. In the United States, what information is available is distributed across multiple institutions, and efforts to track bee populations are largely uncoordinated on a national scale. An overarching framework for monitoring U.S. native bees could provide a system that is responsive to national needs, resources, and capacities. Five major action areas and priorities for structuring a coordinated effort include: (1) Defining the scope, aims, and cost of a national native bee monitoring program; (2) Improving the national capacity in bee taxonomy and systematics; (3) Gathering and cataloging data that are standardized, accessible, and sustainable; (4) Identifying survey methods and prioritizing taxa to monitor; and (5) Prioritizing geographic areas to be monitored. Here, we detail the needs, challenges, and opportunities associated with developing a multi-layered U.S. national plan for native bee monitoring.}, journal={BIOLOGICAL CONSERVATION}, author={Woodard, S. Hollis and Federman, Sarah and James, Rosalind R. and Danforth, Bryan N. and Griswold, Terry L. and Inouye, David and McFrederick, Quinn S. and Morandin, Lora and Paul, Deborah L. and Sellers, Elizabeth and et al.}, year={2020}, month={Dec} }
 @article{pinilla-gallego_williams_davis_fitzgerald_mcart_irwin_2020, title={Within-Colony Transmission of Microsporidian and Trypanosomatid Parasites in Honey Bee and Bumble Bee Colonies}, volume={49}, ISSN={0046-225X 1938-2936}, url={http://dx.doi.org/10.1093/ee/nvaa112}, DOI={10.1093/ee/nvaa112}, abstractNote={Abstract
               Parasites are commonly cited as one of the causes of population declines for both managed and wild bees. Epidemiological models sometimes assume that increasing the proportion of infected individuals in a group should increase transmission. However, social insects exhibit behaviors and traits which can dampen the link between parasite pressure and disease spread. Understanding patterns of parasite transmission within colonies of social bees has important implications for how to control diseases within those colonies, and potentially the broader pollinator community. We used bumble bees (Bombus impatiens Cresson) (Hymenoptera: Apidae) and western honey bees (Apis mellifera L.) (Hymenoptera: Apidae) infected with the gut parasites Crithidia bombi (Lipa & Triggiani) (Trypanosomatida: Trypanosomatidae) and Nosema ceranae (Fries et al.) (Dissociodihaplophasida: Nosematidae), respectively, to understand how the initial proportion of infected individuals impacts within-colony spread and intensity of infection of the parasites. In bumble bees, we found that higher initial parasite prevalence increased both the final prevalence and intensity of infection of C. bombi. In honey bees, higher initial prevalence increased the intensity of infection in individual bees, but not the final prevalence of N. ceranae. Measures that reduce the probability of workers bringing parasites back to the nest may have implications for how to control transmission and/or severity of infection and disease outbreaks, which could also have important consequences for controlling disease spread back into the broader bee community.}, number={6}, journal={Environmental Entomology}, publisher={Oxford University Press (OUP)}, author={Pinilla-Gallego, Mario S and Williams, Emma E and Davis, Abby and Fitzgerald, Jacquelyn L and McArt, Scott H and Irwin, Rebecca E}, editor={Perlman, SteveEditor}, year={2020}, month={Sep}, pages={1393–1401} }
 @article{prado_collazo_stevenson_irwin_2019, title={A comparison of coffee floral traits under two different agricultural practices}, volume={9}, ISSN={2045-2322}, url={http://dx.doi.org/10.1038/s41598-019-43753-y}, DOI={10.1038/s41598-019-43753-y}, abstractNote={AbstractFloral traits and rewards are important in mediating interactions between plants and pollinators. Agricultural management practices can affect abiotic factors known to influence floral traits; however, our understanding of the links between agricultural practices and floral trait expression is still poorly understood. Variation in floral morphological, nectar, and pollen traits of two important agricultural species, Coffea arabica and C. canephora, was assessed under different agricultural practices (sun and shade). Corolla diameter and corolla tube length were larger and pollen total nitrogen content greater in shade plantations of C. canephora than sun plantations. Corolla tube length and anther filament length were larger in shade plantations of C. arabica. No effect of agricultural practice was found on nectar volume, sugar or caffeine concentrations, or pollen production. Pollen total nitrogen content was lower in sun than shade plantations of C. canephora, but no difference was found between sun and shade for C. arabica. This study provides baseline data on the influence of agronomic practices on C. arabica and C. canephora floral traits and also helps fill a gap in knowledge about the effects of shade trees on floral traits, which can be pertinent to other agroforestry systems.}, number={1}, journal={Scientific Reports}, publisher={Springer Science and Business Media LLC}, author={Prado, Sara Guiti and Collazo, Jaime A. and Stevenson, Philip C. and Irwin, Rebecca E.}, year={2019}, month={May} }
 @article{figueroa_blinder_grincavitch_jelinek_mann_merva_metz_zhao_irwin_mcart_et al._2019, title={Bee pathogen transmission dynamics: deposition, persistence and acquisition on flowers}, volume={286}, ISSN={0962-8452 1471-2954}, url={http://dx.doi.org/10.1098/rspb.2019.0603}, DOI={10.1098/rspb.2019.0603}, abstractNote={
            Infectious diseases are a primary driver of bee decline worldwide, but limited understanding of how pathogens are transmitted hampers effective management. Flowers have been implicated as hubs of bee disease transmission, but we know little about how interspecific floral variation affects transmission dynamics. Using bumblebees (
            Bombus impatiens
            ), a trypanosomatid pathogen (
            Crithidia bombi
            ) and three plant species varying in floral morphology, we assessed how host infection and plant species affect pathogen deposition on flowers, and plant species and flower parts impact pathogen survival and acquisition at flowers. We found that host infection with
            Crithidia
            increased defaecation rates on flowers, and that bees deposited faeces onto bracts of
            Lobelia siphilitica
            and
            Lythrum salicaria
            more frequently than onto
            Monarda didyma
            bracts
            .
            Among flower parts, bracts were associated with the lowest pathogen survival but highest resulting infection intensity in bee hosts. Additionally, we found that
            Crithidia
            survival across flower parts was reduced with sun exposure. These results suggest that efficiency of pathogen transmission depends on where deposition occurs and the timing and place of acquisition, which varies among plant species and environmental conditions. This information could be used for development of wildflower mixes that maximize forage while minimizing disease spread.
          }, number={1903}, journal={Proceedings of the Royal Society B: Biological Sciences}, publisher={The Royal Society}, author={Figueroa, Laura L. and Blinder, Malcolm and Grincavitch, Cali and Jelinek, Angus and Mann, Emilia K. and Merva, Liam A. and Metz, Lucy E. and Zhao, Amy Y. and Irwin, Rebecca E. and McArt, Scott H. and et al.}, year={2019}, month={May}, pages={20190603} }
 @article{locascio_pasquale_amponsah_irwin_adler_2019, title={Effect of timing and exposure of sunflower pollen on a common gut pathogen of bumble bees}, volume={44}, ISSN={["1365-2311"]}, DOI={10.1111/een.12751}, abstractNote={1. Several bee species are declining due to multiple factors, including pathogens. Ingestion of sunflower (Helianthus annuus) pollen can dramatically reduce the bumble bee gut pathogen Crithidia bombi, but little is known about how timing and exposure to sunflower pollen consumption affects pathogen load.2. Two experiments were carried out to investigate how exposure to sunflower pollen relative to pathogen exposure affects Crithidia bombi in Bombus impatiens. Foraging trials with pollen‐producing and male‐sterile (pollen absent) sunflower lines were performed to investigate whether sunflower pollen affected pathogen transmission in a single foraging bout, and 7‐day laboratory trials were done to investigate whether timing and duration of exposure to sunflower pollen after infection affected C. bombi.3. In foraging trials, pollen presence on inflorescences inoculated with C. bombi did not affect transmission (pathogen cell counts of foraging workers) 1 week later, suggesting that a brief experience with sunflower pollen concurrent with pathogen exposure is insufficient to reduce infection. In laboratory trials, consuming sunflower pollen for the first 3.5 days or all 7 days after infection reduced cell counts compared with a negative control pollen, but consuming sunflower pollen starting 3.5 days after infection did not. Consuming sunflower pollen for 7 days was significantly and substantially more effective than any other treatment. Thus, both duration and timing of exposure to sunflower pollen may affect pathogen load.4. These results are important for understanding ecological disease dynamics in natural settings with free‐flying bumble bees, and may inform decisions about using medicinal diets to manage bumble bee health commercially.}, number={5}, journal={ECOLOGICAL ENTOMOLOGY}, author={LoCascio, George M. and Pasquale, River and Amponsah, Eugene and Irwin, Rebecca E. and Adler, Lynn S.}, year={2019}, month={Oct}, pages={702–710} }
 @article{fowler_irwin_adler_2019, title={Parasite defense mechanisms in bees: behavior, immunity, antimicrobials, and symbionts}, volume={4}, ISSN={2397-8554 2397-8562}, url={http://dx.doi.org/10.1042/ETLS20190069}, DOI={10.1042/ETLS20190069}, abstractNote={Parasites are linked to the decline of some bee populations; thus, understanding defense mechanisms has important implications for bee health. Recent advances have improved our understanding of factors mediating bee health ranging from molecular to landscape scales, but often as disparate literatures. Here, we bring together these fields and summarize our current understanding of bee defense mechanisms including immunity, immunization, and transgenerational immune priming in social and solitary species. Additionally, the characterization of microbial diversity and function in some bee taxa has shed light on the importance of microbes for bee health, but we lack information that links microbial communities to parasite infection in most bee species. Studies are beginning to identify how bee defense mechanisms are affected by stressors such as poor-quality diets and pesticides, but further research on this topic is needed. We discuss how integrating research on host traits, microbial partners, and nutrition, as well as improving our knowledge base on wild and semi-social bees, will help inform future research, conservation efforts, and management.}, number={1}, journal={Emerging Topics in Life Sciences}, publisher={Portland Press Ltd.}, author={Fowler, Alison E. and Irwin, Rebecca E. and Adler, Lynn S.}, editor={Scott-Brown, Alison and Koch, HaukeEditors}, year={2019}, month={Dec}, pages={59–76} }
 @article{heiling_cook_lee_irwin_2019, title={Pollen and vegetative secondary chemistry of three pollen‐rewarding lupines}, volume={106}, ISSN={0002-9122 1537-2197}, url={http://dx.doi.org/10.1002/ajb2.1283}, DOI={10.1002/ajb2.1283}, abstractNote={PremiseOptimal defense theory predicts that selection should drive plants to disproportionally allocate resources for herbivore defense to tissues with high fitness values. Because pollen's primary role is the transport of gametes, plants may be expected to defend it from herbivory. However, for many animal‐pollinated plants, pollen serves a secondary role as a pollinator reward. These dual roles may present a conflict between selection to defend pollen from herbivores and selection to reward pollinators. Here, we investigate whether pollen secondary chemistry in three pollen‐rewardingLupinusspecies better reflects the need to defend pollen or reward pollinators.MethodsLupinus(Fabaceae) species are nectarless, pollen‐rewarding, and produce defensive quinolizidine and/or piperidine alkaloids throughout their tissues. We used gas chromatography to identify and quantitate the alkaloids in four aboveground tissues (pollen, flower, leaf, stem) of three western North American lupines,L. argenteus,L. bakeri, andL. sulphureus, and compared alkaloid concentrations and composition among tissues within individuals.ResultsInL. argenteusandL. sulphureus, pollen alkaloid concentrations were 11–35% of those found in other tissues. We detected no alkaloids inL. bakeripollen, though they were present in other tissues. Alkaloid concentrations were not strongly correlated among tissues within individuals. We detected fewer alkaloids in pollen compared to other tissues, and pollen contained no unique alkaloids.ConclusionsOur results are consistent with the hypothesis that, in these pollen‐rewarding species, pollen secondary chemistry may reflect the need to attract and reward pollinators more than the need to defend pollen from herbivory.}, number={5}, journal={American Journal of Botany}, publisher={Wiley}, author={Heiling, Jacob M. and Cook, Daniel and Lee, Stephen T. and Irwin, Rebecca E.}, year={2019}, month={May}, pages={643–655} }
 @article{locascio_aguirre_irwin_adler_2019, title={Pollen from multiple sunflower cultivars and species reduces a common bumblebee gut pathogen}, volume={6}, ISSN={2054-5703}, url={http://dx.doi.org/10.1098/rsos.190279}, DOI={10.1098/rsos.190279}, abstractNote={
            Pathogens are one of the factors driving pollinator declines. Diet can play an important role in mediating pollinator health and resistance to pathogens. Sunflower pollen (
            Helianthus annuus
            ) dramatically reduced a gut pathogen (
            Crithidia bombi
            ) of
            Bombus impatiens
            previously, but the breadth of this effect was unknown. We tested whether pollen from nine
            H. annuus
            cultivars, four wild
            H. annuus
            populations,
            H. petiolarus, H. argophyllus
            and two
            Solidago
            spp., reduced
            Crithidia
            in
            B. impatiens
            compared to mixed wildflower pollen and buckwheat pollen (
            Fagopyrum esculentum
            ) as controls. We also compared hand- and honeybee-collected pollen (which contains nectar) to assess whether diet effects on pathogens were due to pollen or nectar. All
            Helianthus
            and
            Solidago
            pollen reduced
            Crithidia
            by 20–40-fold compared to buckwheat pollen, and all but three taxa reduced
            Crithidia
            compared to wildflower pollen. We found no consistent differences between hand- and bee-collected pollen, suggesting that pollen alone can reduce
            Crithidia
            infection. Our results indicate an important role of pollen diet for bee health and potentially broad options within the Asteraceae for pollinator plantings to manage bee disease.
          }, number={4}, journal={Royal Society Open Science}, publisher={The Royal Society}, author={LoCascio, George M. and Aguirre, Luis and Irwin, Rebecca E. and Adler, Lynn S.}, year={2019}, month={Apr}, pages={190279} }
 @article{michaud_irwin_barber_adler_2019, title={Preinfection Effects of Nectar Secondary Compounds on a Bumble Bee Gut Pathogen}, volume={48}, ISSN={0046-225X 1938-2936}, url={http://dx.doi.org/10.1093/ee/nvz018}, DOI={10.1093/ee/nvz018}, abstractNote={Abstract Bumble bee pollinators can be exposed to pathogens when foraging on flowers previously visited by infected individuals. Infectious cells may be deposited in floral nectar, providing a site for pathogens to interact with nectar secondary compounds prior to infecting bees. Some nectar secondary compounds can reduce pathogen counts in infected bumble bees, but we know less about how exposure to these compounds directly affects pathogens prior to being ingested by their host. We exposed the trypanosomatid gut pathogen, Crithidia bombi (Lipa & Triggiani 1988) (Trypanosomatida: Trypanosomatidae), to six different compounds found in nectar (aucubin, catalpol, nicotine, thymol, anabasine, and citric acid) for 1-h prior to ingestion by Bombus impatiens (Cresson 1863) (Hymenoptera: Apidae) workers that were then reared for 1 wk on a control diet. All of these compounds except citric acid reduce pathogen levels when consumed in hosts after infection, and citric acid is a common preservative found in citrus fruits and some honeys. We found that both citric acid and aucubin reduced Crithidia cell counts compared with controls. However, catalpol, nicotine, thymol, and anabasine did not have significant effects on Crithidia levels. These results suggest that Crithidia exposure in some floral nectars may reduce cell viability, resulting in a lower risk to visiting pollinators, but this effect may not be widespread across all flowering species.}, number={3}, journal={Environmental Entomology}, publisher={Oxford University Press (OUP)}, author={Michaud, Kristen M and Irwin, Rebecca E and Barber, Nicholas A and Adler, Lynn S}, year={2019}, month={Mar}, pages={685–690} }
 @article{palmer‐young_farrell_adler_milano_egan_irwin_stevenson_2019, title={Secondary metabolites from nectar and pollen: a resource for ecological and evolutionary studies}, volume={100}, ISSN={0012-9658 1939-9170}, url={http://dx.doi.org/10.1002/ECY.2621}, DOI={10.1002/ECY.2621}, abstractNote={AbstractFloral chemistry mediates plant interactions with herbivores, pathogens, and pollinators. The chemistry of floral nectar and pollen, the primary food rewards for pollinators, can affect both plant reproduction and pollinator health. Although the existence and functional significance of nectar and pollen secondary metabolites has long been known, comprehensive quantitative characterizations of secondary chemistry exist for only a few species. Moreover, little is known about intraspecific variation in nectar and pollen chemical profiles. Because the ecological effects of secondary chemicals are dose‐dependent, heterogeneity across genotypes and populations could influence floral trait evolution and pollinator foraging ecology. To better understand within‐ and across‐species heterogeneity in nectar and pollen secondary chemistry, we undertook exhaustive LC‐MS and LC‐UV‐based chemical characterizations of nectar and pollen methanol extracts from 31 cultivated and wild plant species. Nectar and pollen were collected from farms and natural areas in Massachusetts, Vermont, and California, USA, in 2013 and 2014. For wild species, we aimed to collect 10 samples from each of three sites. For agricultural and horticultural species, we aimed for 10 samples from each of three cultivars. Our data set (1,535 samples, 102 identified compounds) identifies and quantifies each compound recorded in methanolic extracts, and includes chemical metadata that describe the molecular mass, retention time, and chemical classification of each compound. A reference phylogeny is included for comparative analyses. We found that each species possessed a distinct chemical profile; moreover, within species, few compounds were found in both nectar and pollen. The most common secondary chemical classes were flavonoids, terpenoids, alkaloids and amines, and chlorogenic acids. The most common compounds were quercetin and kaempferol glycosides. Pollens contained high concentrations of hydroxycinnamoyl‐spermidine conjugates, mainly triscoumaroyl and trisferuloyl spermidine, found in 71% of species. When present, pollen alkaloids and spermidines had median nonzero concentrations of 23,000 μmol/L (median 52% of recorded micromolar composition). Although secondary chemistry was qualitatively consistent within each species and sample type, we found significant quantitative heterogeneity across cultivars and sites. These data provide a standard reference for future ecological and evolutionary research on nectar and pollen secondary chemistry, including its role in pollinator health and plant reproduction. Data are published under a Creative Commons Attribution License (CC BY 3.0 US) and may be freely used if properly cited.}, number={4}, journal={Ecology}, publisher={Wiley}, author={Palmer‐Young, Evan C. and Farrell, Iain W. and Adler, Lynn S. and Milano, Nelson J. and Egan, Paul A. and Irwin, Rebecca E. and Stevenson, Philip C.}, year={2019}, month={Mar}, pages={e02621} }
 @article{pardee_jensen_inouye_irwin_2019, title={The individual and combined effects of snowmelt timing and frost exposure on the reproductive success of montane forbs}, volume={107}, ISSN={0022-0477 1365-2745}, url={http://dx.doi.org/10.1111/1365-2745.13152}, DOI={10.1111/1365-2745.13152}, abstractNote={Abstract


Changes from historic weather patterns have affected the phenology of many organisms world‐wide. Altered phenology can introduce organisms to novel abiotic conditions during growth and modify species interactions, both of which could drive changes in reproduction.

We explored how climate change can alter plant reproduction using an experiment in which we manipulated the individual and combined effects of snowmelt timing and frost exposure, and measured subsequent effects on flowering phenology, peak flower density, frost damage, pollinator visitation and reproduction of four subalpine wildflowers. Additionally, we conducted a pollen‐supplementation experiment to test whether the plants in our snowmelt and frost treatments were pollen limited for reproduction. The four plants included species flowering in early spring to mid‐summer.

The phenology of all four species was significantly advanced, and the bloom duration was longer in the plots from which we removed snow, but with species‐specific responses to snow removal and frost exposure in terms of frost damage, flower production, pollinator visitation and reproduction. The two early blooming species showed significant signs of frost damage in both early snowmelt and frost treatments, which negatively impacted reproduction for one of the species. Further, we recorded fewer pollinators during flowering for the earliest‐blooming species in the snow removal plots. We also found lower fruit and seed set for the early blooming species in the snow removal treatment, which could be attributed to the plants growing under unfavourable abiotic conditions. However, the later‐blooming species escaped frost damage even in the plots where snow was removed, and experienced increased pollinator visitation and reproduction.

Synthesis. This study provides insight into how plant communities could become altered due to changes in abiotic conditions, and some of the mechanisms involved. While early blooming species may be at a disadvantage under climate change, species that bloom later in the season may benefit from early snowmelt, suggesting that climate change has the potential to reshape flowering communities.

}, number={4}, journal={Journal of Ecology}, publisher={Wiley}, author={Pardee, Gabriella L. and Jensen, Isaac O. and Inouye, David W. and Irwin, Rebecca E.}, editor={Satake, AkikoEditor}, year={2019}, month={Mar}, pages={1970–1981} }
 @article{palmer‐young_farrell_adler_milano_egan_junker_irwin_stevenson_2019, title={Chemistry of floral rewards: intra‐ and interspecific variability of nectar and pollen secondary metabolites across taxa}, volume={89}, ISSN={0012-9615 1557-7015}, url={http://dx.doi.org/10.1002/ecm.1335}, DOI={10.1002/ecm.1335}, abstractNote={AbstractFloral chemistry mediates plant interactions with pollinators, pathogens, and herbivores, with major consequences for fitness of both plants and flower visitors. The outcome of such interactions often depends on compound dose and chemical context. However, chemical diversity and intraspecific variation of nectar and pollen secondary chemistry are known for very few species, precluding general statements about their composition. We analyzed methanol extracts of flowers, nectar, and pollen from 31 cultivated and wild plant species, including multiple sites and cultivars, by liquid‐chromatography–mass‐spectrometry. To depict the chemical niche of each tissue type, we analyzed differences in nectar and pollen chemical richness, absolute and proportional concentrations, and intraspecific variability. We hypothesized that pollen would have higher concentrations and more compounds than nectar, consistent with Optimal Defense Theory and pollen's importance as a male gamete. To investigate chemical correlations across and within tissues, which could reflect physiological constraints, we quantified chemical overlap between conspecific nectar and pollen, and phenotypic integration of individual compounds within tissue types. Nectar and pollen were chemically differentiated both across and within species. Of 102 compounds identified, most occurred in only one species. Machine‐learning algorithms assigned samples to the correct species and tissue type with 98.6% accuracy. Consistent with our hypothesis, pollen had 23.8‐ to 235‐fold higher secondary chemical concentrations and 63% higher chemical richness than nectar. The most common secondary compound classes were flavonoids, alkaloids, terpenoids, and phenolics (primarily phenylpropanoids including chlorogenic acid). The most common specific compound types were quercetin and kaempferol glycosides, known to mediate biotic and abiotic effects. Pollens were distinguished from nectar by high concentrations of hydroxycinnamoyl‐spermidine conjugates, which affect plant development, abiotic stress tolerance, and herbivore resistance. Although chemistry was qualitatively consistent within species and tissue types, concentrations varied across cultivars and sites, which could influence pollination, herbivory, and disease in wild and agricultural plants. Analyses of multivariate trait space showed greater overlap across sites and cultivars in nectar than pollen chemistry; this overlap reflected greater within‐site and within‐cultivar variability of nectar. Our analyses suggest different ecological roles of nectar and pollen mediated by chemical concentration, composition, and variability.}, number={1}, journal={Ecological Monographs}, publisher={Wiley}, author={Palmer‐Young, Evan C. and Farrell, Iain W. and Adler, Lynn S. and Milano, Nelson J. and Egan, Paul A. and Junker, Robert R. and Irwin, Rebecca E. and Stevenson, Philip C.}, year={2019}, month={Feb} }
 @article{richman_irwin_bosak_bronstein_2018, title={Consequences of secondary nectar robbing for male components of plant reproduction}, volume={105}, ISSN={0002-9122 1537-2197}, url={http://dx.doi.org/10.1002/ajb2.1082}, DOI={10.1002/ajb2.1082}, abstractNote={Premise of the StudyOrganisms engage in multiple species interactions simultaneously. While pollination studies generally focus on plants and pollinators exclusively, secondary robbing, a behavior that requires other species (primary robbers) to first create access holes in corollas, is common. It has been shown that secondary robbing can reduce plants' female fitness; however, we lack knowledge about its impact on male plant fitness.MethodsWe experimentally simulated primary and secondary robbing in the monocarpic perennial Ipomopsis aggregata (Polemoniaceae), quantifying indirect effects on pollinator‐mediated pollen (dye) donation. We also assessed whether continual nectar removal via the floral opening has similar effects on hummingbird‐pollinator behavior as continual secondary robbing through robber holes.Key ResultsWe found no significant indirect effects of secondary robbing on a component of Ipomopsis male fitness. Although robbing did reduce pollen (dye) donation due to avoidance of robbed plants by pollinating hummingbirds, pollen donation did not differ between the two robbing treatments. The effects of secondary robbing on hummingbird behavior resembled effects of chronic nectar removal by pollinators. Our results indicate that hummingbird pollinators may use a combination of cues, including cues given by the presence or absence of nectar, to make foraging decisions.ConclusionsCombined with prior research, this study suggests that secondary robbing is less costly to a component of male fitness than to female fitness in Ipomopsis, broadening our knowledge of the overall costs of mutualism exploitation to total plant fitness.}, number={5}, journal={American Journal of Botany}, publisher={Wiley}, author={Richman, Sarah K. and Irwin, Rebecca E. and Bosak, John T. and Bronstein, Judith L.}, year={2018}, month={May}, pages={943–949} }
 @article{lichtenberg_irwin_bronstein_2018, title={Costs and benefits of alternative food handling tactics help explain facultative exploitation of pollination mutualisms}, volume={99}, ISSN={0012-9658}, url={http://dx.doi.org/10.1002/ECY.2395}, DOI={10.1002/ECY.2395}, abstractNote={AbstractMany mutualisms are taken advantage of by organisms that take rewards from their partners but provide no benefit in return. In the absence of traits that limit exploitation, facultative exploiters (partners that can either exploit or cooperate) are widely predicted by mutualism theory to choose an exploitative strategy, potentially threatening mutualism stability. However, it is unknown whether facultative exploiters choose to exploit, and, if so, make this choice because it is the most beneficial strategy for them. We explored these questions in a subalpine plant‐insect community in which individuals of several bumble bee species visit flowers both “legitimately” (entering via the flower opening, picking up and depositing pollen, and hence behaving mutualistically) and via nectar robbing (creating holes through corollas or using an existing hole, bypassing stigmas and anthers). We applied foraging theory to (1) quantify handling costs, benefits and foraging efficiencies incurred by three bumble bee species as they visited flowers legitimately or robbed nectar in cage experiments, and (2) determine whether these efficiencies matched the food handling tactics these bee species employed in the field. Relative efficiencies of legitimate and robbing tactics depended on the combination of bee and plant species. In some cases (Bombus mixtus visiting Corydalis caseana or Mertensia ciliata), the robbing tactic permitted more efficient nectar removal. As both mutualism and foraging theory would predict, in the field, B. mixtus visiting C. caseana were observed more frequently robbing than foraging legitimately. However, for Bombus flavifrons visiting M. ciliata, the expectation from mutualism theory did not hold: legitimate visitation was the more efficient tactic. Legitimate visitation to M. ciliata was in fact more frequently observed in free‐flying B. flavifrons. Free‐flying B. mixtus also frequently visited M. ciliata flowers legitimately. This may reflect lower nectar volumes in robbed than unrobbed flowers in the field. These results suggest that a foraging ecology perspective is informative to the choice of tactics facultative exploiters make. In contrast, the simple expectation that exploiters should always have an advantage, and hence could threaten mutualism persistence unless they are deterred or punished, may not be broadly applicable.}, number={8}, journal={Ecology}, publisher={Wiley}, author={Lichtenberg, Elinor M. and Irwin, Rebecca E. and Bronstein, Judith L.}, year={2018}, month={Jun}, pages={1815–1824} }
 @article{egan_adler_irwin_farrell_palmer-young_stevenson_2018, title={Crop Domestication Alters Floral Reward Chemistry With Potential Consequences for Pollinator Health}, volume={9}, ISSN={1664-462X}, url={http://dx.doi.org/10.3389/fpls.2018.01357}, DOI={10.3389/fpls.2018.01357}, abstractNote={Crop domestication can lead to weakened expression of plant defences, with repercussions for herbivore and pathogen susceptibility. However, little is known about how domestication alters traits that mediate other important ecological interactions in crops, such as pollination. Secondary metabolites, which underpin many defence responses in plants, also occur widely in nectar and pollen and influence plant-pollinator interactions. Thus, domestication may also affect secondary compounds in floral rewards, with potential consequences for pollinators. To test this hypothesis, we chemically analysed nectar and pollen from wild and cultivated plants of highbush blueberry (Vaccinium corymbosum L.), before conducting an artificial diet bioassay to examine pollinator-pathogen interactions. Our results indicated that domestication has significantly altered the chemical composition of V. corymbosum nectar and pollen, and reduced pollen chemical diversity in cultivated plants. Of 20 plant metabolites identified in floral rewards, 13 differed significantly between wild and cultivated plants, with a majority showing positive associations with wild compared to cultivated plants. These included the amino acid phenylalanine (4.5 times higher in wild nectar, 11 times higher in wild pollen), a known bee phagostimulant and essential nutrient; and the antimicrobial caffeic acid ester 4-O-caffeoylshikimic acid (two times higher in wild nectar). We assessed the possible biological relevance of variation in caffeic acid esters in bioassays, using the commercially available 3-O-caffeoylquinic acid. This compound reduced Bombus impatiens infection by a prominent gut pathogen (Crithidia) at concentrations that occurred in wild but not cultivated plants, suggesting that domestication may influence floral traits with consequences for bee health. Appreciable levels of genetic variation and heritability were found for most floral reward chemical traits, indicating good potential for selective breeding. Our study provides the first assessment of plant domestication effects on floral reward chemistry and its potential repercussions for pollinator health. Given the central importance of pollinators for agriculture, we discuss the need to extend such investigations to pollinator-dependent crops more generally and elaborate on future research directions to ascertain wider trends, consequences for pollinators, mechanisms, and breeding solutions.}, journal={Frontiers in Plant Science}, publisher={Frontiers Media SA}, author={Egan, Paul A. and Adler, Lynn S. and Irwin, Rebecca E. and Farrell, Iain W. and Palmer-Young, Evan C. and Stevenson, Philip C.}, year={2018}, month={Sep} }
 @article{adler_michaud_ellner_mcart_stevenson_irwin_2018, title={Disease where you dine: plant species and floral traits associated with pathogen transmission in bumble bees}, volume={99}, ISSN={0012-9658 1939-9170}, url={http://dx.doi.org/10.1002/ecy.2503}, DOI={10.1002/ecy.2503}, abstractNote={AbstractHotspots of disease transmission can strongly influence pathogen spread. Bee pathogens may be transmitted via shared floral use, but the role of plant species and floral trait variation in shaping transmission dynamics is almost entirely unexplored. Given the importance of pathogens for the decline of several bee species, understanding whether and how plant species and floral traits affect transmission could give us important tools for predicting which plant species may be hotspots for disease spread. We assessed variation in transmission via susceptibility (probability of infection) and mean intensity (cell count of infected bees) of the trypanosomatid gut pathogen Crithidia bombi to uninfected Bombus impatiens workers foraging on 14 plant species, and assessed the role of floral traits, bee size and foraging behavior on transmission. We also conducted a manipulative experiment to determine how the number of open flowers affected transmission on three plant species, Penstemon digitalis, Monarda didyma, and Lythrum salicaria. Plant species differed fourfold in the overall mean abundance of Crithidia in foraging bumble bees (mean including infected and uninfected bees). Across plant species, bee susceptibility and mean intensity increased with the number of reproductive structures per inflorescence (buds, flowers and fruits); smaller bees and those that foraged longer were also more susceptible. Trait‐based models were as good or better than species‐based models at predicting susceptibility and mean intensity based on AIC values. Surprisingly, floral size and morphology did not significantly predict transmission across species. In the manipulative experiment, more open flowers increased mean pathogen abundance fourfold in Monarda, but had no effect in the other two plant species. Our results suggest that variation among plant species, through their influence on pathogen transmission, may shape bee disease dynamics. Given widespread investment in pollinator‐friendly plantings to support pollinators, understanding how plant species affect disease transmission is important for recommending plant species that optimize pollinator health.}, number={11}, journal={Ecology}, publisher={Wiley}, author={Adler, Lynn S. and Michaud, Kristen M. and Ellner, Stephen P. and McArt, Scott H. and Stevenson, Philip C. and Irwin, Rebecca E.}, year={2018}, month={Oct}, pages={2535–2545} }
 @article{rothchild_adler_irwin_sadd_stevenson_palmer‐young_2018, title={Effects of short‐term exposure to naturally occurring thymol concentrations on transmission of a bumble bee parasite}, volume={43}, ISSN={0307-6946 1365-2311}, url={http://dx.doi.org/10.1111/een.12631}, DOI={10.1111/een.12631}, abstractNote={1. Plants produce antimicrobial phytochemicals that can reduce growth and infectivity of parasites in animals. Pollinator parasites are transmitted between hosts that forage on shared flowers. Floral transmission directly exposes parasites to phytochemicals on floral surfaces and in nectar, both at flowers and, post‐ingestion, in the crop. This exposure could directly affect parasite transmission to new hosts.2. Nectar chemical analyses were combined with field and cell culture experiments to test the effects of the floral phytochemical thymol on the transmission potential of the trypanosomatid gut parasite Crithidia in Bombus impatiens. First, thymol concentrations in Thymus vulgaris nectar were measured. Second, the effect of adding thymol to floral nectaries on parasite transmission to foraging bees was tested. Third, cell cultures were used to determine direct, dose‐dependent effects of short‐term thymol exposure on subsequent in vitro parasite growth.3. A total of 26.1 ppm thymol was found in T. vulgaris nectar, five‐fold higher than previously documented in this species. However, addition of thymol to flowers of parasite‐inoculated inflorescences of four plant species did not affect acquisition of Crithidia infection during a foraging bout. Cell culture experiments showed that the thymol concentrations needed to reduce subsequent Crithidia growth by 50% (120 ppm) were 4.6‐fold higher than the highest detected nectar concentration.4. Although thymol exposure can influence Crithidia viability, Crithidia are robust to the duration and magnitude of exposure encountered during floral foraging under natural conditions. These experiments suggest that any effects of thymol alone on Crithidia–host infection dynamics probably reflect indirect, possibly host‐mediated, effects of chronic thymol ingestion.}, number={5}, journal={Ecological Entomology}, publisher={Wiley}, author={Rothchild, Kristina W. and Adler, Lynn S. and Irwin, Rebecca E. and Sadd, Ben M. and Stevenson, Philip C. and Palmer‐Young, Evan C.}, year={2018}, month={May}, pages={567–577} }
 @article{giacomini_leslie_tarpy_palmer-young_irwin_adler_2018, title={Medicinal value of sunflower pollen against bee pathogens}, volume={8}, ISSN={2045-2322}, url={http://dx.doi.org/10.1038/s41598-018-32681-y}, DOI={10.1038/s41598-018-32681-y}, abstractNote={AbstractGlobal declines in pollinators, including bees, can have major consequences for ecosystem services. Bees are dominant pollinators, making it imperative to mitigate declines. Pathogens are strongly implicated in the decline of native and honey bees. Diet affects bee immune responses, suggesting the potential for floral resources to provide natural resistance to pathogens. We discovered that sunflower (Helianthus annuus) pollen dramatically and consistently reduced a protozoan pathogen (Crithidia bombi) infection in bumble bees (Bombus impatiens) and also reduced a microsporidian pathogen (Nosema ceranae) of the European honey bee (Apis mellifera), indicating the potential for broad anti-parasitic effects. In a field survey, bumble bees from farms with more sunflower area had lower Crithidia infection rates. Given consistent effects of sunflower in reducing pathogens, planting sunflower in agroecosystems and native habitat may provide a simple solution to reduce disease and improve the health of economically and ecologically important pollinators.}, number={1}, journal={Scientific Reports}, publisher={Springer Science and Business Media LLC}, author={Giacomini, Jonathan J. and Leslie, Jessica and Tarpy, David R. and Palmer-Young, Evan C. and Irwin, Rebecca E. and Adler, Lynn S.}, year={2018}, month={Sep} }
 @article{irwin_warren_adler_2018, title={Phenotypic selection on floral traits in an urban landscape}, volume={285}, ISSN={0962-8452 1471-2954}, url={http://dx.doi.org/10.1098/rspb.2018.1239}, DOI={10.1098/rspb.2018.1239}, abstractNote={
            Native species are increasingly living in urban landscapes associated with abiotic and biotic changes that may influence patterns of phenotypic selection. However, measures of selection in urban and non-urban environments, and exploration of the mechanisms associated with such changes, are uncommon. Plant–animal interactions have played a central role in the evolution of flowering plants and are sensitive to changes in the urban landscape, and thus provide opportunities to explore how urban environments modify selection. We evaluated patterns of phenotypic selection on the floral and resistance traits of
            Gelsemium sempervirens
            in urban and non-urban sites. The urban landscape had increased florivory and decreased pollen receipt, but showed only modest differences in patterns of selection. Directional selection for one trait, larger floral display size, was stronger in urban compared to non-urban sites. Neither quadratic nor correlational selection significantly differed between urban and non-urban sites. Pollination was associated with selection for larger floral display size in urban compared to non-urban sites, due to the differences in the translation of pollination into seeds rather than pollinator selectivity. Thus, our data suggest that urban landscapes may not result in sweeping differences in phenotypic selection but rather modest differences for some traits, potentially mediated by species interactions.
          }, number={1884}, journal={Proceedings of the Royal Society B: Biological Sciences}, publisher={The Royal Society}, author={Irwin, Rebecca E. and Warren, Paige S. and Adler, Lynn S.}, year={2018}, month={Aug}, pages={20181239} }
 @article{urbanowicz_virginia_irwin_2018, title={Pollen limitation and reproduction of three plant species across a temperature gradient in western Greenland}, volume={50}, ISSN={1523-0430 1938-4246}, url={http://dx.doi.org/10.1080/15230430.2017.1414485}, DOI={10.1080/15230430.2017.1414485}, abstractNote={ABSTRACT Rapid climate change in the Arctic may increase sexual reproduction in plants because of changes in both abiotic factors, such as temperature, and biotic factors, such as pollination. Pollination may currently limit plant reproduction in the Arctic, where cold temperatures hinder pollinator activity. To understand how warming may affect pollination and plant reproduction, we studied three plant species in western Greenland. Two species were hermaphroditic and insect-pollinated (Vaccinium uliginosum and Chamerion latifolium), and one was dioecious and insect- and wind-pollinated (Salix glauca). We measured how pollinator visitation and plant reproduction varied across three temperature zones. We also conducted pollinator exclusion and pollen supplementation experiments to measure pollinator dependence and pollen limitation. Proportion of fruit set in Vaccinium and Salix was pollen limited in every temperature zone, and Vaccinium and Chamerion depended on pollinator-mediated outcrossing for maximum reproductive success. Furthermore, higher pollinator visitation to Vaccinium in the warmer temperature zones mirrored lower pollen limitation and higher fruit set, suggesting that temperature zone indirectly influenced reproduction via changes in pollination. Taken together, our results demonstrate that both abiotic factors and pollination are important in limiting reproduction in the Arctic and that plant–pollinator interactions can mediate the response of plant reproduction to warming.}, number={1}, journal={Arctic, Antarctic, and Alpine Research}, publisher={Informa UK Limited}, author={Urbanowicz, Christine and Virginia, Ross A. and Irwin, Rebecca E.}, year={2018}, month={Jan} }
 @article{hamon_youngsteadt_irwin_sorenson_2018, title={Pollination Ecology and Morphology of Venus Flytrap in Sites of Varying Time Since Last Fire}, volume={112}, ISSN={0013-8746 1938-2901}, url={http://dx.doi.org/10.1093/aesa/say032}, DOI={10.1093/aesa/say032}, abstractNote={Management of natural habitats is an important strategy for rare plant conservation. One common tool for managing natural habitats is the use of controlled fire. Rare plants in fire-dependent ecosystems often rely on frequent fires to increase nutrient availability, initiate germination, and limit cover from light competitors. Fire can also alter arthropod communities, including the pollinator communities upon which many flowering plants rely for sexual reproduction. However, it remains unclear how fire affects the pollination ecology of rare plants in fire-dependent ecosystems. Here we studied sites of varying burn history to examine the role of time since last fire on the morphology, flower visitor community, and degree of pollen limitation of seed production of Venus flytrap (Dionaea muscipula Ellis) (Caryophyllales: Droseraceae). The area occupied by blooming D. muscipula and number of traps per individual decreased with increasing time since burn. Though flower visitor richness and evenness were highest in sites of intermediate time post-burn, we found no differences in the composition of the flower visitor community in sites of different burn histories. Hand-pollinated flowers produced 8.3% more seeds per fruit than open-pollinated flowers, indicating that D. muscipula was pollen-limited, but burn history did not affect the magnitude of pollen limitation. Though we found no clear effect of burn history on the pollination ecology of D. muscipula, differences in blooming area and trap number suggest that burn history influences its distribution and growth, and affirms the benefits of frequent fires to its persistence.}, number={3}, journal={Annals of the Entomological Society of America}, publisher={Oxford University Press (OUP)}, author={Hamon, Laura E and Youngsteadt, Elsa and Irwin, Rebecca E and Sorenson, Clyde E}, year={2018}, month={Sep}, pages={141–149} }
 @article{urbanowicz_virginia_irwin_2018, title={Publisher Correction to: The response of pollen-transport networks to landscape-scale climate variation}, volume={41}, ISSN={0722-4060 1432-2056}, url={http://dx.doi.org/10.1007/S00300-018-2304-7}, DOI={10.1007/S00300-018-2304-7}, abstractNote={The above mentioned article was originally scheduled for publication in the special issue on Ecology of Tundra Arthropods with guest editors Toke T. Høye and Lauren E. Culler. Erroneously, the article was published in Polar Biology, Volume 40, Issue 11, November, 2017. The publisher sincerely apologizes to the guest editors and the authors for the inconvenience caused.}, number={8}, journal={Polar Biology}, publisher={Springer Science and Business Media LLC}, author={Urbanowicz, Christine and Virginia, Ross A. and Irwin, Rebecca E.}, year={2018}, month={Mar}, pages={1651–1651} }
 @article{prado_collazo_irwin_2018, title={Resurgence of specialized shade coffee cultivation: Effects on pollination services and quality of coffee production}, volume={265}, ISSN={0167-8809}, url={http://dx.doi.org/10.1016/j.agee.2018.07.002}, DOI={10.1016/j.agee.2018.07.002}, abstractNote={Since the early 2000s, there has been a resurgence in shade coffee production on the island of Puerto Rico. The newly restored specialized shade canopy consists of four native tree species, three of which are nitrogen fixers, and is intended to provide 30% shade cover once the trees are matured. Though much is known about the benefits of rustic and traditional shade plantations to coffee production, there is little information available for specialized shade plantations. Here, we investigate the ways in which fruit set, seed predation, bean weight, proportion of peaberries (i.e., malformed fruits), and beverage quality differ between sun and specialized shade plantations of Coffea arabica and Coffea canephora. Additionally, to assess whether coffee plants were pollen limited, we conducted a pollen supplementation experiment in which we compared pollen deposition and berry production on hand-pollinated branches to those of naturally, open-pollinated ones. We found that there was no evidence of pollen limitation on fruit set between sun and specialized shade plantations of C. arabica or C. canephora. We found that specialized shade benefits the proportion of C. arabica fruit set, without compromising bean weight or the proportion of peaberries produced. In comparison, C. canephora showed no improvement in the proportion of fruits set with specialized shade; however, beans from open-pollinated flowers weighed more in specialized shade than sun. Beverage quality was marginally better under shade, and for hand-pollinated flowers. Our results add to the limited body of work investigating the benefits of specialized shade coffee plantations on ecosystem services.}, journal={Agriculture, Ecosystems & Environment}, publisher={Elsevier BV}, author={Prado, Sara Guiti and Collazo, Jaime A. and Irwin, Rebecca E.}, year={2018}, month={Oct}, pages={567–575} }
 @article{madden_epps_fukami_irwin_sheppard_sorger_dunn_2018, title={The ecology of insect–yeast relationships and its relevance to human industry}, volume={285}, ISSN={0962-8452 1471-2954}, url={http://dx.doi.org/10.1098/rspb.2017.2733}, DOI={10.1098/rspb.2017.2733}, abstractNote={Many species of yeast are integral to human society. They produce many of our foods, beverages and industrial chemicals, challenge us as pathogens, and provide models for the study of our own biology. However, few species are regularly studied and much of their ecology remains unclear, hindering the development of knowledge that is needed to improve the relationships between humans and yeasts. There is increasing evidence that insects are an essential component of ascomycetous yeast ecology. We propose a ‘dispersal–encounter hypothesis' whereby yeasts are dispersed by insects between ephemeral, spatially disparate sugar resources, and insects, in turn, obtain the benefits of an honest signal from yeasts for the sugar resources. We review the relationship between yeasts and insects through three main examples: social wasps, social bees and beetles, with some additional examples from fruit flies. Ultimately, we suggest that over the next decades, consideration of these ecological and evolutionary relationships between insects and yeasts will allow prediction of where new yeast diversity is most likely to be discovered, particularly yeasts with traits of interest to human industry.}, number={1875}, journal={Proceedings of the Royal Society B: Biological Sciences}, publisher={The Royal Society}, author={Madden, Anne A. and Epps, Mary Jane and Fukami, Tadashi and Irwin, Rebecca E. and Sheppard, John and Sorger, D. Magdalena and Dunn, Robert R.}, year={2018}, month={Mar}, pages={20172733} }
 @article{youngsteadt_irwin_fowler_bertone_giacomini_kunz_suiter_sorenson_2018, title={Venus Flytrap Rarely Traps Its Pollinators}, volume={191}, ISSN={0003-0147 1537-5323}, url={http://dx.doi.org/10.1086/696124}, DOI={10.1086/696124}, abstractNote={Because carnivorous plants rely on arthropods as pollinators and prey, they risk consuming would-be mutualists. We examined this potential conflict in the Venus flytrap (Dionaea muscipula), whose pollinators were previously unknown. Diverse arthropods from two classes and nine orders visited flowers; 56% of visitors carried D. muscipula pollen, often mixed with pollen of coflowering species. Within this diverse, generalized community, certain bee and beetle species appear to be the most important pollinators, on the basis of their abundance, pollen load size, and pollen fidelity. Dionaea muscipula prey spanned four invertebrate classes and 11 orders; spiders, beetles, and ants were most common. At the family and species levels, few taxa were shared between traps and flowers, yielding a near-zero value of niche overlap for these potentially competing structures. Spatial separation of traps and flowers may contribute to partitioning the invertebrate community between nutritional and reproductive functions in D. muscipula.}, number={4}, journal={The American Naturalist}, publisher={University of Chicago Press}, author={Youngsteadt, Elsa and Irwin, Rebecca E. and Fowler, Alison and Bertone, Matthew A. and Giacomini, Sara June and Kunz, Michael and Suiter, Dale and Sorenson, Clyde E.}, year={2018}, month={Apr}, pages={539–546} }
 @article{heiling_ledbetter_richman_ellison_bronstein_irwin_2018, title={Why are some plant–nectar robber interactions commensalisms?}, volume={127}, ISSN={0030-1299 1600-0706}, url={http://dx.doi.org/10.1111/oik.05440}, DOI={10.1111/oik.05440}, abstractNote={Many plants that bear hidden or recessed floral nectar experience nectar robbing, the removal of nectar by a floral visitor through holes pierced in the corolla. Although robbing can reduce plant reproductive success, many studies fail to find such effects. We outline three mechanistic hypotheses that can explain when interactions between plants and nectar‐robbers should be commensal rather than antagonistic: the non‐discrimination (pollinators do not avoid robbed flowers), visitor prevalence (robber visitation is rare relative to pollinator visitation), and pollen saturation (stigmas receive sufficient pollen to fertilize all ovules with one or very few pollinator visits) hypotheses. We then explore these mechanisms in the North American subalpine, bumble bee‐pollinated and nectar‐robbed plant Corydalis caseana (Fumariaceae). We first confirmed that the effects of nectar robbing on female reproductive success were neutral in C. caseana. We then tested the three mechanisms underlying these neutral effects using a combination of observational studies and experiments. We found evidence for all three mechanisms. First, consistent with the non‐discrimination hypothesis, pollinators failed to discriminate against experimentally robbed flowers or inflorescences even though naturally robbed flowers offered significantly lower nectar rewards than unrobbed flowers. Second, C. caseana was more commonly visited by pollinators than by nectar robbers, in accordance with the visitor prevalence hypothesis. Third, stigmas of unvisited flowers as well as those visited once by pollinators were saturated with pollen, with all stigmas bearing pollen loads several orders of magnitude higher than the number of ovules per fruit, consistent with the pollen saturation hypothesis. Our investigation of the mechanisms driving the commensal outcome of nectar robbing in this system deepens our understanding of the ecology of nectar robbing and contributes to a more general understanding of the variation in the outcomes of interactions between species.}, number={11}, journal={Oikos}, publisher={Wiley}, author={Heiling, Jacob M. and Ledbetter, Trevor A. and Richman, Sarah K. and Ellison, Heather K. and Bronstein, Judith L. and Irwin, Rebecca E.}, year={2018}, month={Jul}, pages={1679–1689} }
 @article{palmer-young_hogeboom_kaye_donnelly_andicoechea_connon_weston_skyrm_irwin_adler_2017, title={Context-dependent medicinal effects of anabasine and infection-dependent toxicity in bumble bees}, volume={12}, ISSN={1932-6203}, url={http://dx.doi.org/10.1371/journal.pone.0183729}, DOI={10.1371/journal.pone.0183729}, abstractNote={Background Floral phytochemicals are ubiquitous in nature, and can function both as antimicrobials and as insecticides. Although many phytochemicals act as toxins and deterrents to consumers, the same chemicals may counteract disease and be preferred by infected individuals. The roles of nectar and pollen phytochemicals in pollinator ecology and conservation are complex, with evidence for both toxicity and medicinal effects against parasites. However, it remains unclear how consistent the effects of phytochemicals are across different parasite lineages and environmental conditions, and whether pollinators actively self-medicate with these compounds when infected. Approach Here, we test effects of the nectar alkaloid anabasine, found in Nicotiana, on infection intensity, dietary preference, and survival and performance of bumble bees (Bombus impatiens). We examined variation in the effects of anabasine on infection with different lineages of the intestinal parasite Crithidia under pollen-fed and pollen-starved conditions. Results We found that anabasine did not reduce infection intensity in individual bees infected with any of four Crithidia lineages that were tested in parallel, nor did anabasine reduce infection intensity in microcolonies of queenless workers. In addition, neither anabasine nor its isomer, nicotine, was preferred by infected bees in choice experiments, and infected bees consumed less anabasine than did uninfected bees under no-choice conditions. Furthermore, anabasine exacerbated the negative effects of infection on bee survival and microcolony performance. Anabasine reduced infection in only one experiment, in which bees were deprived of pollen and post-pupal contact with nestmates. In this experiment, anabasine had antiparasitic effects in bees from only two of four colonies, and infected bees exhibited reduced—rather than increased—phytochemical consumption relative to uninfected bees. Conclusions Variation in the effect of anabasine on infection suggests potential modulation of tritrophic interactions by both host genotype and environmental variables. Overall, our results demonstrate that Bombus impatiens prefer diets without nicotine and anabasine, and suggest that the medicinal effects and toxicity of anabasine may be context dependent. Future research should identify the specific environmental and genotypic factors that determine whether nectar phytochemicals have medicinal or deleterious effects on pollinators.}, number={8}, journal={PLOS ONE}, publisher={Public Library of Science (PLoS)}, author={Palmer-Young, Evan C. and Hogeboom, Alison and Kaye, Alexander J. and Donnelly, Dash and Andicoechea, Jonathan and Connon, Sara June and Weston, Ian and Skyrm, Kimberly and Irwin, Rebecca E. and Adler, Lynn S.}, editor={Hull, J. JoeEditor}, year={2017}, month={Aug}, pages={e0183729} }
 @article{pardee_inouye_irwin_2017, title={Direct and indirect effects of episodic frost on plant growth and reproduction in subalpine wildflowers}, volume={24}, ISSN={1354-1013 1365-2486}, url={http://dx.doi.org/10.1111/gcb.13865}, DOI={10.1111/gcb.13865}, abstractNote={AbstractFrost is an important episodic event that damages plant tissues through the formation of ice crystals at or below freezing temperatures. In montane regions, where climate change is expected to cause earlier snow melt but may not change the last frost‐free day of the year, plants that bud earlier might be directly impacted by frost through damage to flower buds and reproductive structures. However, the indirect effects of frost mediated through changes in plant–pollinator interactions have rarely been explored. We examined the direct and pollinator‐mediated indirect effects of frost on three wildflower species in southwestern Colorado, USA, Delphinium barbeyi (Ranunculaceae), Erigeron speciosus (Asteraceae), and Polemonium foliosissimum (Polemoniaceae), by simulating moderate (−1 to −5°C) frost events in early spring in plants in situ. Subsequently, we measured plant growth, and upon flowering measured flower morphology and phenology. Throughout the flowering season, we monitored pollinator visitation and collected seeds to measure plant reproduction. We found that frost had species‐specific direct and indirect effects. Frost had direct effects on two of the three species. Frost significantly reduced flower size, total flowers produced, and seed production of Erigeron. Furthermore, frost reduced aboveground plant survival and seed production for Polemonium. However, we found no direct effects of frost on Delphinium. When we considered the indirect impacts of frost mediated through changes in pollinator visitation, one species, Erigeron, incurred indirect, negative effects of frost on plant reproduction through changes in floral traits and pollinator visitation, along with direct effects. Overall, we found that flowering plants exhibited species‐specific direct and pollinator‐mediated indirect responses to frost, thus suggesting that frost may play an important role in affecting plant communities under climate change.}, number={2}, journal={Global Change Biology}, publisher={Wiley}, author={Pardee, Gabriella L. and Inouye, David W. and Irwin, Rebecca E.}, year={2017}, month={Sep}, pages={848–857} }
 @article{richman_irwin_bronstein_2017, title={Foraging strategy predicts foraging economy in a facultative secondary nectar robber}, volume={126}, ISSN={0030-1299 1600-0706}, url={http://dx.doi.org/10.1111/oik.04229}, DOI={10.1111/oik.04229}, abstractNote={In mutualistic interactions, the decision whether to cooperate or cheat depends on the relative costs and benefits of each strategy. In pollination mutualisms, secondary nectar robbing is a facultative behavior employed by a diverse array of nectar‐feeding organisms, and is thought to be a form of cheating. Primary robbers create holes in floral tissue through which they feed on nectar, whereas secondary robbers, which often lack chewing mouthparts, feed on nectar through existing holes. Because primary robbers make nectar more readily available to secondary robbers, primary robbers facilitate the behaviors of secondary robbers. However, the net effect of facilitation on secondary robber fitness has not been empirically tested: it is unknown whether the benefit secondary robbers receive is strong enough to overcome the cost of competing with primary robbers for a shared resource. We conducted foraging experiments using the bumble bee Bombus bifarius, which can alternatively forage ‘legitimately’ (from the floral opening) or secondary‐rob. We measured the relative foraging efficiencies (handling time per flower, flowers visited per minute, proportion of foraging bout spent consuming nectar) of these alternative behaviors, and tested whether the frequency of primary robbing and nectar standing crop in primary‐robbed flowers of Linaria vulgaris (Plantaginaceae) affected foraging efficiency. Surprisingly, there was no effect of primary robbing frequency on the foraging efficiency of secondary‐robbing B. bifarius. Instead, foraging strategy was a major predictor of foraging efficiency, with legitimate foraging being significantly more efficient than secondary robbing. Legitimate foraging was the more common strategy used by B. bifarius in our study; however, it is rarely used by B. bifarius foraging on L. vulgaris in nature, despite indications that it is more efficient. Our results suggest the need for deeper investigations into why bees adopt secondary robbing as a foraging strategy, specifically, the environmental contexts that promote the behavior.}, number={9}, journal={Oikos}, publisher={Wiley}, author={Richman, Sarah K. and Irwin, Rebecca E. and Bronstein, Judith L.}, year={2017}, month={Apr}, pages={1250–1257} }
 @article{ogilvie_griffin_gezon_inouye_underwood_inouye_irwin_2017, title={Interannual bumble bee abundance is driven by indirect climate effects on floral resource phenology}, volume={20}, ISSN={1461-023X 1461-0248}, url={http://dx.doi.org/10.1111/ele.12854}, DOI={10.1111/ele.12854}, abstractNote={AbstractClimate change can influence consumer populations both directly, by affecting survival and reproduction, and indirectly, by altering resources. However, little is known about the relative importance of direct and indirect effects, particularly for species important to ecosystem functioning, like pollinators. We used structural equation modelling to test the importance of direct and indirect (via floral resources) climate effects on the interannual abundance of three subalpine bumble bee species. In addition, we used long‐term data to examine how climate and floral resources have changed over time. Over 8 years, bee abundances were driven primarily by the indirect effects of climate on the temporal distribution of floral resources. Over 43 years, aspects of floral phenology changed in ways that indicate species‐specific effects on bees. Our study suggests that climate‐driven alterations in floral resource phenology can play a critical role in governing bee population responses to global change.}, number={12}, journal={Ecology Letters}, publisher={Wiley}, author={Ogilvie, Jane E. and Griffin, Sean R. and Gezon, Zachariah J. and Inouye, Brian D. and Underwood, Nora and Inouye, David W. and Irwin, Rebecca E.}, editor={Bourke, AndrewEditor}, year={2017}, month={Sep}, pages={1507–1515} }
 @article{mcart_urbanowicz_mccoshum_irwin_adler_2017, title={Landscape predictors of pathogen prevalence and range contractions in US bumblebees}, volume={284}, ISSN={0962-8452 1471-2954}, url={http://dx.doi.org/10.1098/rspb.2017.2181}, DOI={10.1098/rspb.2017.2181}, abstractNote={
            Several species of bumblebees have recently experienced range contractions and possible extinctions. While threats to bees are numerous, few analyses have attempted to understand the relative importance of multiple stressors. Such analyses are critical for prioritizing conservation strategies. Here, we describe a landscape analysis of factors predicted to cause bumblebee declines in the USA. We quantified 24 habitat, land-use and pesticide usage variables across 284 sampling locations, assessing which variables predicted pathogen prevalence and range contractions via machine learning model selection techniques. We found that greater usage of the fungicide chlorothalonil was the best predictor of pathogen (
            Nosema bombi
            ) prevalence in four declining species of bumblebees.
            Nosema bombi
            has previously been found in greater prevalence in some declining US bumblebee species compared to stable species. Greater usage of total fungicides was the strongest predictor of range contractions in declining species, with bumblebees in the northern USA experiencing greater likelihood of loss from previously occupied areas. These results extend several recent laboratory and semi-field studies that have found surprising links between fungicide exposure and bee health. Specifically, our data suggest landscape-scale connections between fungicide usage, pathogen prevalence and declines of threatened and endangered bumblebees.
          }, number={1867}, journal={Proceedings of the Royal Society B: Biological Sciences}, publisher={The Royal Society}, author={McArt, Scott H. and Urbanowicz, Christine and McCoshum, Shaun and Irwin, Rebecca E. and Adler, Lynn S.}, year={2017}, month={Nov}, pages={20172181} }
 @article{palmer-young_tozkar_schwarz_chen_irwin_adler_evans_2017, title={Nectar and Pollen Phytochemicals Stimulate Honey Bee (Hymenoptera: Apidae) Immunity to Viral Infection}, volume={110}, ISSN={0022-0493 1938-291X}, url={http://dx.doi.org/10.1093/jee/tox193}, DOI={10.1093/jee/tox193}, abstractNote={Abstract Parasites and pathogens are implicated in honey bee colony losses, and honey bees may also spread infection to wild pollinators. Bees consume nectar and pollen, which contain phytochemicals that can positively or negatively affect pollinator health. Certain phytochemicals can reduce parasite loads in humans and other animals. Understanding how phytochemicals affect honey bee infection and survival could help identify optimal forage sources and phytochemical treatments to ameliorate disease. We fed honey bees seven dietary phytochemicals to evaluate whether phytochemical consumption would treat preexisting infection in mature bees, or mitigate infection in young bees either inside or outside of their colonies. Phytochemicals were generally well-tolerated at levels documented in nectar, honey, and pollen, although clove oil and thymol increased mortality at high doses. Six of seven tested phytochemicals significantly increased antimicrobial peptide expression by 12.9 to 61-fold in older bees after 7 d consumption. Short-term (<24 h) phytochemical consumption reduced levels of Deformed wing virus (DWV) up to 500-fold in young bees released into field colonies. However, with the exception of high-dose clove oil, our phytochemical treatments did not alter infection with Lotmaria passim or Nosema ceranae. Phytochemicals also lacked antiviral effects for pollen-deprived bees reared outside the colony. Our results suggest that phytochemicals have potential therapeutic value for honey bees infected with DWV. Short-term phytochemical consumption may be sufficient to confer benefits against infection. Phytochemical concentrations that reduced disease were comparable with naturally occurring floral concentrations, suggesting that flowers could serve as seasonally varied, serially consumed pollinator medicines.}, number={5}, journal={Journal of Economic Entomology}, publisher={Oxford University Press (OUP)}, author={Palmer-Young, Evan C and Tozkar, Cansu Ö and Schwarz, Ryan S and Chen, Yanping and Irwin, Rebecca E and Adler, Lynn S and Evans, Jay D}, year={2017}, month={Jul}, pages={1959–1972} }
 @article{palmer‐young_sadd_irwin_adler_2017, title={Synergistic effects of floral phytochemicals against a bumble bee parasite}, volume={7}, ISSN={2045-7758 2045-7758}, url={http://dx.doi.org/10.1002/ece3.2794}, DOI={10.1002/ece3.2794}, abstractNote={AbstractFloral landscapes comprise diverse phytochemical combinations. Individual phytochemicals in floral nectar and pollen can reduce infection in bees and directly inhibit trypanosome parasites. However, gut parasites of generalist pollinators, which consume nectar and pollen from many plant species, are exposed to phytochemical combinations. Interactions between phytochemicals could augment or decrease effects of single compounds on parasites. Using a matrix of 36 phytochemical treatment combinations, we assessed the combined effects of two floral phytochemicals, eugenol and thymol, against four strains of the bumblebee gut trypanosome Crithidia bombi. Eugenol and thymol had synergistic effects against C. bombi growth across seven independent experiments, showing that the phytochemical combination can disproportionately inhibit parasites. The strength of synergistic effects varied across strains and experiments. Thus, the antiparasitic effects of individual compounds will depend on both the presence of other phytochemicals and parasite strain identity. The presence of synergistic phytochemical combinations could augment the antiparasitic activity of individual compounds for pollinators in diverse floral landscapes.}, number={6}, journal={Ecology and Evolution}, publisher={Wiley}, author={Palmer‐Young, Evan C. and Sadd, Ben M. and Irwin, Rebecca E. and Adler, Lynn S.}, year={2017}, month={Feb}, pages={1836–1849} }
 @article{bronstein_barker_lichtenberg_richardson_irwin_2017, title={The behavioral ecology of nectar robbing: why be tactic constant?}, volume={21}, ISSN={2214-5745}, url={http://dx.doi.org/10.1016/j.cois.2017.05.013}, DOI={10.1016/j.cois.2017.05.013}, abstractNote={How do animals forage for variable food resources? For animals foraging at flowers, floral constancy has provided a framework for understanding why organisms visit some flowers while bypassing others. We extend this framework to the flower-handling tactics that visitors employ. Nectar robbers remove nectar through holes bitten in flowers, often without pollinating. Many foragers can switch between robbing and visiting flowers legitimately to gain access to nectar. We document that even though individuals can switch foraging tactics, they often do not. We explore whether individuals exhibit constancy to either robbing or visiting legitimately, which we term tactic constancy. We then extend hypotheses of floral constancy to understand when and why visitors exhibit tactic constancy and raise questions for future research.}, journal={Current Opinion in Insect Science}, publisher={Elsevier BV}, author={Bronstein, Judith L and Barker, Jessica L and Lichtenberg, Elinor M and Richardson, Leif L and Irwin, Rebecca E}, year={2017}, month={Jun}, pages={14–18} }
 @article{urbanowicz_virginia_irwin_2017, title={The response of pollen-transport networks to landscape-scale climate variation}, volume={40}, ISSN={0722-4060 1432-2056}, url={http://dx.doi.org/10.1007/s00300-017-2138-8}, DOI={10.1007/s00300-017-2138-8}, number={11}, journal={Polar Biology}, publisher={Springer Science and Business Media LLC}, author={Urbanowicz, Christine and Virginia, Ross A. and Irwin, Rebecca E.}, year={2017}, month={Jun}, pages={2253–2263} }
 @article{palmer-young_sadd_stevenson_irwin_adler_2016, title={Bumble bee parasite strains vary in resistance to phytochemicals}, volume={6}, ISSN={2045-2322}, url={http://dx.doi.org/10.1038/srep37087}, DOI={10.1038/srep37087}, abstractNote={AbstractNectar and pollen contain diverse phytochemicals that can reduce disease in pollinators. However, prior studies showed variable effects of nectar chemicals on infection, which could reflect variable phytochemical resistance among parasite strains. Inter-strain variation in resistance could influence evolutionary interactions between plants, pollinators, and pollinator disease, but testing direct effects of phytochemicals on parasites requires elimination of variation between bees. Using cell cultures of the bumble bee parasite Crithidia bombi, we determined (1) growth-inhibiting effects of nine floral phytochemicals and (2) variation in phytochemical resistance among four parasite strains. C. bombi growth was unaffected by naturally occurring concentrations of the known antitrypanosomal phenolics gallic acid, caffeic acid, and chlorogenic acid. However, C. bombi growth was inhibited by anabasine, eugenol, and thymol. Strains varied >3-fold in phytochemical resistance, suggesting that selection for phytochemical resistance could drive parasite evolution. Inhibitory concentrations of thymol (4.53–22.2 ppm) were similar to concentrations in Thymus vulgaris nectar (mean 5.2 ppm). Exposure of C. bombi to naturally occurring levels of phytochemicals—either within bees or during parasite transmission via flowers—could influence infection in nature. Flowers that produce antiparasitic phytochemicals, including thymol, could potentially reduce infection in Bombus populations, thereby counteracting a possible contributor to pollinator decline.}, number={1}, journal={Scientific Reports}, publisher={Springer Science and Business Media LLC}, author={Palmer-Young, Evan C. and Sadd, Ben M. and Stevenson, Philip C. and Irwin, Rebecca E. and Adler, Lynn S.}, year={2016}, month={Nov} }
 @article{schaeffer_mei_andicoechea_manson_irwin_2016, title={Consequences of a nectar yeast for pollinator preference and performance}, volume={31}, ISSN={0269-8463 1365-2435}, url={http://dx.doi.org/10.1111/1365-2435.12762}, DOI={10.1111/1365-2435.12762}, abstractNote={Summary


Pollinators utilize floral resources that vary in colour, scent and reward quality. Variation in such traits, including nectar rewards, in addition to cues associated with their quality, can influence pollinator foraging decisions with consequences for pollinator reproductive success. Nectar is commonly subject to colonization by micro‐organisms capable of affecting a suite of traits important for pollinator attraction and fitness; yet, links between microbial presence and changes in pollinator preference and performance remain few.

Here, we evaluated the effects of a nectar‐inhabiting micro‐organism on pollinator foraging behaviour and reproduction using the common eastern bumblebee Bombus impatiens and the cosmopolitan nectar yeast Metschnikowia reukaufii. Using a combination of choice and no‐choice behavioural and feeding assays, we manipulated the presence and viability of M. reukaufii in nectar and assessed bumblebee foraging and reproductive responses.

Bombus impatiens workers responded positively to the presence of yeasts. Foragers trained to associate yeast presence with flower colour visited a significantly greater proportion of flowers inoculated with yeast when subject to a colour discrimination test. Moreover, foragers naïve to nectar yeasts incorporated more yeast‐inoculated flowers into initial foraging bouts when presented with a novel floral array. In addition, bees spent significantly longer foraging on yeast‐inoculated flowers compared to yeast‐free flowers. However, when we manipulated yeast presence and viability in microcolonies of queenless workers, we found no effect of yeast on components of bumblebee reproduction, such as initiation of egg laying and number of eggs laid. This lack of an effect of yeast persisted even under conditions of pollen limitation.

Taken together, these results suggest that nectar yeasts can enhance floral signalling and alter pollinator foraging behaviour at individual flowers, though they may not directly affect pollinator performance. Thus, nectar yeasts may play a significant role in mediating pollinator foraging behaviour, with consequences for plant fitness and evolution of floral traits.

}, number={3}, journal={Functional Ecology}, publisher={Wiley}, author={Schaeffer, Robert N. and Mei, Yu Zhu and Andicoechea, Jonathan and Manson, Jessamyn S. and Irwin, Rebecca E.}, editor={Kudo, GakuEditor}, year={2016}, month={Sep}, pages={613–621} }
 @article{carper_adler_irwin_2016, title={Effects of florivory on plant-pollinator interactions: Implications for male and female components of plant reproduction}, volume={103}, ISSN={["1537-2197"]}, DOI={10.3732/ajb.1600144}, abstractNote={PREMISE OF THE STUDY:Florivory could have direct negative effects on plant fitness due to consumption of floral organs, and indirect effects mediated through changes in traits important to pollination. These effects likely vary with plant sexual system, depending on sex‐ or morph‐specific patterns of damage. We investigated the direct and indirect effects of simulated florivory on male and female components of reproduction in the native, distylous vine Gelsemium sempervirens.METHODS:We crossed floral damage and supplemental pollination treatments in a common garden array and tracked pollinator behavioral responses. We also estimated male function using fluorescent dye as an analog for pollen transfer, and measured both fruit and seed production.KEY RESULTS:The effects of floral damage varied by floral morph, the genus of floral visitor, and the component of reproduction measured. Damage reduced the number of pollinator visits to pin but not thrum plants, and increased the time some pollinators spent per flower in thrum but not pin plants. Flowers of damaged plants transferred more dye particles to recipient plants compared to undamaged plants, but only later in the season when the majority of dye transfer occurred. Damage had no effect on female reproduction.CONCLUSION:These results suggest that florivory can have positive indirect effects on estimated male plant reproduction through changes in different pollinators’ behavior at flowers, but the effects of floral damage vary with male vs. female function. These results underscore the importance of other species’ interactions at flowers in driving pollinator behavior and pollen transfer dynamics.}, number={6}, journal={AMERICAN JOURNAL OF BOTANY}, author={Carper, Adrian L. and Adler, Lynn S. and Irwin, Rebecca E.}, year={2016}, month={Jun}, pages={1061–1070} }
 @article{richman_irwin_nelson_bronstein_2017, title={Facilitated exploitation of pollination mutualisms: fitness consequences for plants}, volume={105}, ISSN={0022-0477 1365-2745}, url={http://dx.doi.org/10.1111/1365-2745.12657}, DOI={10.1111/1365-2745.12657}, abstractNote={Summary


Mutualisms are only rarely one‐to‐one interactions: each species generally interacts with multiple mutualists. Exploitation is ubiquitous in mutualisms, and we would therefore expect that each mutualist interacts with multiple exploiters as well. Exploiter species may also interact with one another. For example, the action of one exploiter species might open the opportunity for exploitation by a second species.

Exploitation is common in many plant–pollinator mutualisms: ‘primary’ nectar robbers feed through holes they make in flowers, which can be subsequently used by ‘secondary’ nectar robbers unable to create holes themselves. The overall effect of nectar robbing on plant fitness is often (although not always) negative. No study has separated the effects of interacting with primary vs. secondary robbers.

Here, we examine the effects of primary vs. secondary nectar robbing on pollinator visitation rate and female fitness in Ipomopsis aggregata. Manipulating the type of nectar robbing that flowers experienced, we found that secondary nectar robbing inflicted fitness costs to plants beyond that inflicted by primary robbing alone. Secondary nectar robbing significantly reduced pollen receipt to flowers, as well as fruit and seed production. Although the causes are elusive, the effect may be attributed to changes in pollinator behaviour at these plants.

Synthesis. Our findings provide evidence that interacting with multiple exploiters can lead to increased negative effects for mutualists, and highlight the importance of incorporating multiple exploiters into the conceptual framework of mutualism.

}, number={1}, journal={Journal of Ecology}, publisher={Wiley}, author={Richman, Sarah K. and Irwin, Rebecca E. and Nelson, Cherie J. and Bronstein, Judith L.}, editor={Bartomeus, IgnasiEditor}, year={2017}, month={Jan}, pages={188–196} }
 @article{conroy_palmer-young_irwin_adler_2016, title={Food Limitation Affects Parasite Load and Survival of <i>Bombus impatiens</i>  (Hymenoptera: Apidae) Infected With<i>Crithidia</i>(Trypanosomatida: Trypanosomatidae)}, volume={45}, ISSN={0046-225X 1938-2936}, url={http://dx.doi.org/10.1093/ee/nvw099}, DOI={10.1093/ee/nvw099}, abstractNote={Bumble bees (genus Bombus) are globally important insect pollinators, and several species have experienced marked declines in recent years. Both nutritional limitation and pathogens may have contributed to these declines. While each of these factors may be individually important, there may also be synergisms where nutritional stress could decrease pathogen resistance. Understanding interactions between bumble bees, their parasites, and food availability may provide new insight into the causes of declines. In this study, we examined the combined impacts of pollen and nectar limitation on Crithidia, a common gut parasite in Bombus impatiens Cresson. Individual worker bees were inoculated with Crithidia and then assigned in a factorial design to two levels of pollen availability (pollen or no pollen) and two nectar sugar concentrations (high [30%] or low [15%] sucrose). We found that lack of pollen and low nectar sugar both reduced Crithidia cell counts, with the most dramatic effect from lack of pollen. Both pollen availability and nectar sugar concentration were also important for bee survival. The proportion of bees that died after seven days of infection was ∼25% lower in bees with access to pollen and high nectar sugar concentration than any other treatment. Thus, nectar and pollen availability are both important for bee survival, but may come at a cost of higher parasite loads. Our results illustrate the importance of understanding environmental context, such as resource availability, when examining a host-parasite interaction.}, number={5}, journal={Environmental Entomology}, publisher={Oxford University Press (OUP)}, author={Conroy, Taylor J. and Palmer-Young, Evan C. and Irwin, Rebecca E. and Adler, Lynn S.}, year={2016}, month={Aug}, pages={1212–1219} }
 @article{adler_leege_irwin_2016, title={Geographic variation in resistance to nectar robbing and consequences for pollination}, volume={103}, ISSN={["1537-2197"]}, DOI={10.3732/ajb.1600114}, abstractNote={PREMISE OF THE STUDY:Floral evolution is frequently ascribed to selection by pollinators, but may also be shaped by antagonists. However, remarkably few studies have examined geographic mosaics in resistance to floral antagonists or the consequences for other floral interactions.METHODS:Gelsemium sempervirens experiences frequent nectar robbing in northern Georgia, but rarely in southern Georgia. We conducted common‐garden experiments in both locations using genotypes from each region and measured robbing, pollinator attraction, floral attractive and defensive traits, and plant reproduction.KEY RESULTS:Nectar robbing was more than four times higher in the north vs. south, and pollinator visits did not differ between gardens. Across both gardens, northern genotypes were half as likely to be nectar‐robbed but received half as many pollinator visits as southern genotypes, suggesting evolution of resistance to robbing at a cost of reduced pollinator attraction. Plant‐level traits, such as height and number of flowers, were more closely associated with resistance to robbing than floral size, shape, or chemistry. Northern genotypes had lower female and estimated male reproduction compared to southern genotypes at both locations, which could be due to costs of resistance to nectar robbing, or costs of adaptations to other biotic or abiotic differences between regions.CONCLUSIONS:Our study indicates that geographic variation can play a strong role structuring interactions with floral antagonists and mutualists and provides evidence consistent with the hypothesis that local resistance to nectar robbing imposes costs in terms of decreased pollinator attraction and reproduction.}, number={10}, journal={AMERICAN JOURNAL OF BOTANY}, author={Adler, Lynn S. and Leege, Lissa M. and Irwin, Rebecca E.}, year={2016}, month={Oct}, pages={1819–1828} }
 @article{gezon_inouye_irwin_2016, title={Phenological change in a spring ephemeral: implications for pollination and plant reproduction}, volume={22}, ISSN={1354-1013 1365-2486}, url={http://dx.doi.org/10.1111/gcb.13209}, DOI={10.1111/gcb.13209}, abstractNote={AbstractClimate change has had numerous ecological effects, including species range shifts and altered phenology. Altering flowering phenology often affects plant reproduction, but the mechanisms behind these changes are not well‐understood. To investigate why altering flowering phenology affects plant reproduction, we manipulated flowering phenology of the spring herb Claytonia lanceolata (Portulacaceae) using two methods: in 2011–2013 by altering snow pack (snow‐removal vs. control treatments), and in 2013 by inducing flowering in a greenhouse before placing plants in experimental outdoor arrays (early, control, and late treatments). We measured flowering phenology, pollinator visitation, plant reproduction (fruit and seed set), and pollen limitation. Flowering occurred approx. 10 days earlier in snow‐removal than control plots during all years of snow manipulation. Pollinator visitation patterns and strength of pollen limitation varied with snow treatments, and among years. Plants in the snow removal treatment were more likely to experience frost damage, and frost‐damaged plants suffered low reproduction despite lack of pollen limitation. Plants in the snow removal treatment that escaped frost damage had higher pollinator visitation rates and reproduction than controls. The results of the array experiment supported the results of the snow manipulations. Plants in the early and late treatments suffered very low reproduction due either to severe frost damage (early treatment) or low pollinator visitation (late treatment) relative to control plants. Thus, plants face tradeoffs with advanced flowering time. While early‐flowering plants can reap the benefits of enhanced pollination services, they do so at the cost of increased susceptibility to frost damage that can overwhelm any benefit of flowering early. In contrast, delayed flowering results in dramatic reductions in plant reproduction through reduced pollination. Our results suggest that climate change may constrain the success of early‐flowering plants not through plant‐pollinator mismatch but through the direct impacts of extreme environmental conditions.}, number={5}, journal={Global Change Biology}, publisher={Wiley}, author={Gezon, Zachariah J. and Inouye, David W. and Irwin, Rebecca E.}, year={2016}, month={Feb}, pages={1779–1793} }
 @article{cook_slominski_gardner_pfister_irwin_2016, title={Seasonal variation in the secondary chemistry of foliar and reproductive tissues of Delphinium nuttallianum}, volume={65}, ISSN={["1873-2925"]}, DOI={10.1016/j.bse.2016.02.006}, abstractNote={Plant secondary compounds are critical in affecting interactions between plants and their herbivores. The norditerpene alkaloids are secondary compounds in Delphinium (larkspur) species which are divided into two classes: the N-(methylsuccinimido) anthranoyllycoctonine (MSAL-type) and non MSAL-type, and are known to be toxic to herbivorous insects and livestock. Alkaloid concentrations were measured in a whole plant context in vegetative and reproductive tissues in Delphinium nuttallianum at different stages of plant maturity at two locations to explore how plant maturity affected alkaloid concentrations within a growing season. Alkaloid concentrations differed between vegetative and reproductive tissues, with vegetative tissues having significantly lower alkaloid concentrations than reproductive tissues. However, no systematic differences in alkaloid concentrations were observed at different plant maturity stages across the growing season. Based on the data we suggest that alkaloid allocation in different plant parts of D. nuttallianum is influenced by life history of the plant, consistent with plant defense theory. At one location, as pods mature the qualitative alkaloid composition changed through structural diversification of the alkaloids present. The ecological significance of this structural diversification awaits further exploration.}, journal={BIOCHEMICAL SYSTEMATICS AND ECOLOGY}, author={Cook, Daniel and Slominski, Anthony and Gardner, Dale R. and Pfister, James A. and Irwin, Rebecca E.}, year={2016}, month={Apr}, pages={93–99} }
 @article{stevanovic_schwarz_vejnovic_evans_irwin_glavinic_stanimirovic_2016, title={Species-specific diagnostics of Apis mellifera trypanosomatids: A nine-year survey (2007-2015) for trypanosomatids and microsporidians in Serbian honey bees}, volume={139}, ISSN={["1096-0805"]}, DOI={10.1016/j.jip.2016.07.001}, abstractNote={In this study, honey bees collected in Serbia over 9 consecutive years (2007–2015) were retrospectively surveyed to determine the prevalence of eukaryotic gut parasites by molecular screening of archival DNA samples. We developed species-specific primers for PCR to detect the two known honey bee trypanosomatid species, Crithidia mellificae and the recently described Lotmaria passim. These primers were validated for target specificity under single and mixed-species conditions as well as against the bumblebee trypanosomatid Crithidia bombi. Infections by Nosema apis and Nosema ceranae (Microsporidia) were also determined using PCR. Samples from 162 colonies (18 from each year) originating from 57 different localities were surveyed. L. passim was detected in every year with an overall frequency of 62.3% and annual frequencies ranging from 38.9% to 83.3%. This provides the earliest confirmed record to date for L. passim and the first report of this species in Serbia. N. ceranae was ubiquitous, occurring in every year and at 95.7% overall frequency, ranging annually from 83.3% to 100%. The majority of colonies (60.5%) were co-infected with L. passim and N. ceranae, but colony infections by each species were statistically independent of one another over the nine years. Although C. mellificae and N. apis have both been reported recently at low frequency in Europe, neither of these species was detected in Serbia. These results support the hypothesis that L. passim has predominated over C. mellificae in A. mellifera during the past decade.}, journal={JOURNAL OF INVERTEBRATE PATHOLOGY}, author={Stevanovic, Jevrosima and Schwarz, Ryan S. and Vejnovic, Branislav and Evans, Jay D. and Irwin, Rebecca E. and Glavinic, Uros and Stanimirovic, Zoran}, year={2016}, month={Sep}, pages={6–11} }
 @article{hung_ascher_gibbs_irwin_bolger_2015, title={Effects of fragmentation on a distinctive coastal sage scrub bee fauna revealed through incidental captures by pitfall traps}, volume={19}, ISSN={1366-638X 1572-9753}, url={http://dx.doi.org/10.1007/S10841-015-9763-8}, DOI={10.1007/S10841-015-9763-8}, number={1}, journal={Journal of Insect Conservation}, publisher={Springer Science and Business Media LLC}, author={Hung, Keng-Lou James and Ascher, John S. and Gibbs, Jason and Irwin, Rebecca E. and Bolger, Douglas T.}, year={2015}, month={Feb}, pages={175–179} }
 @article{richardson_bowers_irwin_2016, title={Nectar chemistry mediates the behavior of parasitized bees: consequences for plant fitness}, volume={97}, ISSN={0012-9658 1939-9170}, url={http://dx.doi.org/10.1890/15-0263.1}, DOI={10.1890/15-0263.1}, abstractNote={AbstractPlants produce an array of secondary metabolites that play important ecological roles as anti‐herbivore and anti‐pathogen defenses. Many herbivores experience physiological costs when they consume secondary metabolites, yet some also benefit, for example when these chemicals confer resistance to parasites and predators. Secondary metabolites are often present in nectar and pollen, which is paradoxical given that floral rewards are important in the attraction of mutualists rather than deterrence of antagonists. Motivated by studies of interactions among plants, herbivores, and parasites, as well as research showing that secondary metabolites can reduce bee disease, we characterized the occurrence of two iridoid glycosides, aucubin and catalpol, in floral rewards and other tissues of the bee pollinated plant, Chelone glabra. We then experimentally investigated effects of nectar iridoid glycoside concentrations on the foraging behavior of bumble bee pollinators naturally afflicted by a parasitoid fly and a protozoan intestinal parasite, and subsequent effects on an estimate of plant reproduction. We found that floral nectar had lower iridoid glycoside concentrations than leaves, pollen, and corollas, and that, compared to those plant parts, the relative ratio of the two primary iridoid glycosides, aucubin and catalpol, was reversed in nectar. Whether bees carried parasitoid fly larvae did not affect their response to nectar chemistry; however, there was a significant interaction between protozoan parasite infection and nectar treatment, with infected bees foraging longer at flowers with high compared to low nectar iridoid glycoside concentrations. Parasitized bees were also more likely to return to inflorescences with high iridoid glycoside nectar. Consequently, flowers in the high iridoid glycoside nectar treatment donated significantly more pollen to conspecific stigmas than did flowers in the low iridoid glycoside treatment, suggesting an increase in male plant fitness. Taken together, these results demonstrate that nectar secondary metabolites can mediate the behavior of pollinators with subsequent benefits for estimates of plant reproduction.}, number={2}, journal={Ecology}, publisher={Wiley}, author={Richardson, Leif L. and Bowers, M. Deane and Irwin, Rebecca E.}, year={2016}, month={Feb}, pages={325–337} }
 @article{schaeffer_vannette_irwin_2015, title={Nectar yeasts in Delphinium nuttallianum (Ranunculaceae) and their effects on nectar quality}, volume={18}, ISSN={1754-5048}, url={http://dx.doi.org/10.1016/J.FUNECO.2015.09.010}, DOI={10.1016/J.FUNECO.2015.09.010}, abstractNote={Microorganisms colonize the nectar of many angiosperms. Variable diversity and spatio-temporal dynamics of nectar-inhabiting microorganisms (e.g., yeasts) may drive variation in nectar sugar composition and subsequent plant–pollinator interactions. We assessed yeast frequency of occurrence and density in the nectar of the perennial herb, Delphinium nuttallianum, across multiple spatio-temporal scales, including flower lifetime and sex-phase transition, flowering season, populations, and years. We tested the hypothesis that pollinators vector yeasts by comparing densities between virgin flowers and those open to visitation. Finally, we identified yeasts using molecular methods and tested for an association between yeast density and nectar composition using ultra-performance liquid chromatography. Yeasts were frequent colonists of Delphinium nectar, occurring in all populations and years sampled. Yeast frequency of occurrence and density varied across most spatio-temporal scales examined. Pollinators were vectors of yeast: virgin flowers remained yeast-free, while those open to visitation became inoculated. Nectar samples were species-poor, with a majority colonized by Metschnikowia reukaufii. Finally, increasing yeast density was correlated with a decrease in sucrose and an increase in monosaccharides. Our results document that yeasts form species-poor communities in populations of this hermaphroditic perennial, in addition to highlighting their spatio-temporal dynamics and effects on nectar quality. Spatio-temporal variation in frequency of occurrence, density, and changes in nectar may have important implications for the nature and strength of interactions between Delphinium and its pollinators.}, journal={Fungal Ecology}, publisher={Elsevier BV}, author={Schaeffer, Robert N. and Vannette, Rachel L. and Irwin, Rebecca E.}, year={2015}, month={Dec}, pages={100–106} }
 @article{richardson_irwin_2015, title={Pollination ecology and floral visitor spectrum of turtlehead (<i>Chelone glabra</i> L.; Plantaginaceae)}, volume={17}, ISSN={1920-7603}, url={http://dx.doi.org/10.26786/1920-7603(2015)18}, DOI={10.26786/1920-7603(2015)18}, abstractNote={Many flowering plants engage in mutualistic interactions with animals in order to sexually reproduce, exchanging food rewards such as nectar and pollen for the service of pollen transfer between flowers. Floral reward variation strongly influences visitation patterns of both pollinating mutualists and non-mutualist consumers, with consequences for both male and female components of plant reproductive success. Despite the importance of pollination to ecological systems, the pollination ecology of many plants is poorly known. At seven sites over three years, we studied the mating system, floral visitors and pollen limitation of turtlehead (Chelone glabra L.), an eastern North America wetland herb. We found that the plant is autogamous, but requires pollinator visitation to set seed. C. glabra flowers are protandrous, with floral rewards that vary between male and female sex phases. We found diurnal variation in reward presentation that was a function of both floral phenology and consumer behavior. Bombus vagans Smith, the most common visitor to C. glabra flowers, removed a large fraction of available pollen (>36%) in single visits to newly opened flowers, and compared to other flower visitors, passively transported more pollen on flights between flowers and deposited more to conspecific stigmas, suggesting it was the most effective pollinator. The solitary bee Hylaeus annulatus L. made frequent visits to flowers, but contributed little to pollination due to morphological mismatch and because it avoided male-phase flowers. Despite high bee visitation rates, flowers were pollen limited for seed production, possibly indicating a negative effect of non-pollinating flower visitors on plant reproductive success.}, journal={Journal of Pollination Ecology}, publisher={International Commission for Plant Pollinator Relations}, author={Richardson, Leif L. and Irwin, Rebecca E.}, year={2015}, month={Nov}, pages={132–144} }
 @article{biller_adler_irwin_mcallister_palmer-young_2015, title={Possible Synergistic Effects of Thymol and Nicotine against Crithidia bombi Parasitism in Bumble Bees}, volume={10}, ISSN={1932-6203}, url={http://dx.doi.org/10.1371/journal.pone.0144668}, DOI={10.1371/journal.pone.0144668}, abstractNote={Floral nectar contains secondary compounds with antimicrobial properties that can affect not only plant-pollinator interactions, but also interactions between pollinators and their parasites. Although recent work has shown that consumption of plant secondary compounds can reduce pollinator parasite loads, little is known about the effects of dosage or compound combinations. We used the generalist pollinator Bombus impatiens and its obligate gut parasite Crithidia bombi to study the effects of nectar chemistry on host-parasite interactions. In two experiments we tested (1) whether the secondary compounds thymol and nicotine act synergistically to reduce parasitism, and (2) whether dietary thymol concentration affects parasite resistance. In both experiments, uninfected Bombus impatiens were inoculated with Crithidia and then fed particular diet treatments for 7 days, after which infection levels were assessed. In the synergism experiment, thymol and nicotine alone and in combination did not significantly affect parasite load or host mortality. However, the thymol-nicotine combination treatment reduced log-transformed parasite counts by 30% relative to the control group (P = 0.08). For the experiment in which we manipulated thymol concentration, we found no significant effect of any thymol concentration on Crithidia load, but moderate (2 ppm) thymol concentrations incurred a near-significant increase in mortality (P = 0.054). Our results tentatively suggest the value of a mixed diet for host immunity, yet contrast with research on the antimicrobial activity of dietary thymol and nicotine in vertebrate and other invertebrate systems. We suggest that future research evaluate genetic variation in Crithidia virulence, multi-strain competition, and Crithidia interactions with the gut microbe community that may mediate antimicrobial activities of secondary compounds.}, number={12}, journal={PLOS ONE}, publisher={Public Library of Science (PLoS)}, author={Biller, Olivia Masi and Adler, Lynn S. and Irwin, Rebecca E. and McAllister, Caitlin and Palmer-Young, Evan C.}, editor={Rodriguez-Saona, CesarEditor}, year={2015}, month={Dec}, pages={e0144668} }
 @article{irwin_howell_galen_2015, title={Quantifying direct vs. indirect effects of nectar robbers on male and female components of plant fitness}, volume={103}, ISSN={0022-0477 1365-2745}, url={http://dx.doi.org/10.1111/1365-2745.12476}, DOI={10.1111/1365-2745.12476}, abstractNote={Summary


Plants interact simultaneously with both mutualists and antagonists. While webs of plant–animal interactions in natural systems can be highly complex, most interactions can be simplified into those that are either direct (mediated through pairwise interactions) or indirect (mediated through third‐party species). Mechanistic studies of the direct and indirect pathways by which foliar herbivores affect plants have been well explored; however, mechanistic explorations of how floral herbivores, such as nectar robbers, affect total plant fitness via direct vs. indirect pathways have received less attention.

The goal of this study was to assess the importance of direct vs. pollinator‐mediated indirect effects of a floral antagonist on female and male components of plant fitness. We focused on the hummingbird‐pollinated plant scarlet gilia, Ipomopsis aggregata, which is nectar‐robbed by the bumblebee Bombus occidentalis. Prior studies have found evidence for pollinator‐mediated indirect effects of robbing on female and male components of I. aggregata fitness, but the mechanisms by which these indirect effects occur, and experimental evidence supporting or refuting direct effects of robbing, have been lacking.

We found no evidence for direct effects of robbing on plant fitness. Robbers did not act as pollinators of I. aggregata nor did they directly affect seed production by making nectar‐robber holes or removing nectar in hand‐pollinated flowers. Moreover, robbing had no direct effect on pollen production per flower or the ability of pollen from robbed flowers to sire seeds in hand pollinations.

However, nectar robbing had indirect effects on plant reproduction mediated through per‐visit pollinator effectiveness at depositing pollen in robbed vs. unrobbed flowers. A simple model of a plant‐robber‐pollinator system suggested that robbing effects in general may occur through more indirect mechanisms when nectar removal by robbers is high relative to nectar replenishment, and that compensation for robbing is then more profitable through the production of additional flowers.

Synthesis. Our results highlight the importance of indirect effects in mediating the fitness consequences of species interactions.

}, number={6}, journal={Journal of Ecology}, publisher={Wiley}, author={Irwin, Rebecca E. and Howell, Paige and Galen, Candace}, editor={Bonser, StephenEditor}, year={2015}, month={Oct}, pages={1487–1497} }
 @article{richardson_adler_leonard_andicoechea_regan_anthony_manson_irwin_2015, title={Secondary metabolites in floral nectar reduce parasite infections in bumblebees}, volume={282}, ISSN={0962-8452 1471-2954}, url={http://dx.doi.org/10.1098/rspb.2014.2471}, DOI={10.1098/rspb.2014.2471}, abstractNote={
            The synthesis of secondary metabolites is a hallmark of plant defence against herbivores. These compounds may be detrimental to consumers, but can also protect herbivores against parasites. Floral nectar commonly contains secondary metabolites, but little is known about the impacts of nectar chemistry on pollinators, including bees. We hypothesized that nectar secondary metabolites could reduce bee parasite infection. We inoculated individual bumblebees with
            Crithidia bombi
            , an intestinal parasite, and tested effects of eight naturally occurring nectar chemicals on parasite population growth. Secondary metabolites strongly reduced parasite load, with significant effects of alkaloids, terpenoids and iridoid glycosides ranging from 61 to 81%. Using microcolonies, we also investigated costs and benefits of consuming anabasine, the compound with the strongest effect on parasites, in infected and uninfected bees. Anabasine increased time to egg laying, and
            Crithidia
            reduced bee survival. However, anabasine consumption did not mitigate the negative effects of
            Crithidia
            , and
            Crithidia
            infection did not alter anabasine consumption. Our novel results highlight that although secondary metabolites may not rescue survival in infected bees, they may play a vital role in mediating
            Crithidia
            transmission within and between colonies by reducing
            Crithidia
            infection intensities.
          }, number={1803}, journal={Proceedings of the Royal Society B: Biological Sciences}, publisher={The Royal Society}, author={Richardson, Leif L. and Adler, Lynn S. and Leonard, Anne S. and Andicoechea, Jonathan and Regan, Karly H. and Anthony, Winston E. and Manson, Jessamyn S. and Irwin, Rebecca E.}, year={2015}, month={Mar}, pages={20142471} }
 @article{anthony_palmer-young_leonard_irwin_adler_2015, title={Testing Dose-Dependent Effects of the Nectar Alkaloid Anabasine on Trypanosome Parasite Loads in Adult Bumble Bees}, volume={10}, ISSN={1932-6203}, url={http://dx.doi.org/10.1371/journal.pone.0142496}, DOI={10.1371/journal.pone.0142496}, abstractNote={The impact of consuming biologically active compounds is often dose-dependent, where small quantities can be medicinal while larger doses are toxic. The consumption of plant secondary compounds can be toxic to herbivores in large doses, but can also improve survival in parasitized herbivores. In addition, recent studies have found that consuming nectar secondary compounds may decrease parasite loads in pollinators. However, the effect of compound dose on bee survival and parasite loads has not been assessed. To determine how secondary compound consumption affects survival and pathogen load in Bombus impatiens, we manipulated the presence of a common gut parasite, Crithidia bombi, and dietary concentration of anabasine, a nectar alkaloid produced by Nicotiana spp. using four concentrations naturally observed in floral nectar. We hypothesized that increased consumption of secondary compounds at concentrations found in nature would decrease survival of uninfected bees, but improve survival and ameliorate parasite loads in infected bees. We found medicinal effects of anabasine in infected bees; the high-anabasine diet decreased parasite loads and increased the probability of clearing the infection entirely. However, survival time was not affected by any level of anabasine concentration, or by interactive effects of anabasine concentration and infection. Crithidia infection reduced survival time by more than two days, but this effect was not significant. Our results support a medicinal role for anabasine at the highest concentration; moreover, we found no evidence for a survival-related cost of anabasine consumption across the concentration range found in nectar. Our results suggest that consuming anabasine at the higher levels of the natural range could reduce or clear pathogen loads without incurring costs for healthy bees.}, number={11}, journal={PLOS ONE}, publisher={Public Library of Science (PLoS)}, author={Anthony, Winston E. and Palmer-Young, Evan C. and Leonard, Anne S. and Irwin, Rebecca E. and Adler, Lynn S.}, editor={Nieh, James C.Editor}, year={2015}, month={Nov}, pages={e0142496} }
 @article{gezon_wyman_ascher_inouye_irwin_2015, title={The effect of repeated, lethal sampling on wild bee abundance and diversity}, volume={6}, ISSN={2041-210X 2041-210X}, url={http://dx.doi.org/10.1111/2041-210X.12375}, DOI={10.1111/2041-210X.12375}, abstractNote={Summary


Bee pollinators provide a critical ecosystem service to wild and agricultural plants but are reported to be declining world‐wide due to anthropogenic change. Long‐term data on bee abundance and diversity are scarce, and the need for additional quantitative sampling using repeatable methods has been emphasized. Recently, monitoring programmes have begun using a standardized method that employs a combination of pan traps and sweep netting, resulting in lethal sampling of bees. This standardized method can remove a large number of bees from sites during each sampling day, raising concern that the sampling itself could have a negative effect on bee populations.

We conducted an experiment to assess whether lethal sampling for bees using pan traps and netting affected bee abundance and diversity when done every two weeks throughout a season and over multiple years. We compared bee abundance, richness, evenness and functional group composition between sites that had been sampled every two weeks from 2009 to 2012 to similar sites not previously sampled.

We found that the standardized method for sampling bees, with specimens from 132 morphospecies, did not affect bee communities in terms of abundance, rarefied richness, evenness, or functional group composition. Thus, our results indicate that the bee communities we sampled are robust to such sampling efforts, despite removing an average of 2862 bees per season.

We discuss several explanations for why sampling did not affect bee abundance or community structure, including a density‐dependent response to reduced competition for resources.

These results suggest that bee monitoring programmes sampling once every two weeks with pan traps and netting will not affect bee community structure. We urge researchers monitoring bees to utilize standardized protocols so that results can be compared across space and time.

}, number={9}, journal={Methods in Ecology and Evolution}, publisher={Wiley}, author={Gezon, Zachariah J. and Wyman, Eli S. and Ascher, John S. and Inouye, David W. and Irwin, Rebecca E.}, editor={Vamosi, JanaEditor}, year={2015}, month={Apr}, pages={1044–1054} }
 @article{thorburn_adler_irwin_palmer-young_2015, title={Variable effects of nicotine and anabasine on parasitized bumble bees}, volume={4}, ISSN={2046-1402}, url={http://dx.doi.org/10.12688/f1000research.6870.1}, DOI={10.12688/f1000research.6870.1}, abstractNote={Secondary metabolites in floral nectar have been shown to reduce parasite load in two common bumble bee species. Previous studies on the effects of nectar secondary metabolites on parasitized bees have focused on single compounds in isolation; however, in nature, bees are simultaneously exposed to multiple compounds. We tested for synergistic effects of two alkaloids found in the nectar of Nicotiana spp. plants, nicotine and anabasine, on parasite load and mortality in bumble bees (Bombus impatiens) infected with the intestinal parasite Crithidia bombi. Adult worker bees inoculated with C. bombi were fed nicotine and anabasine diet treatments in a factorial design, resulting in four nectar treatment combinations:  2 ppm nicotine, 5 ppm anabasine, 2ppm nicotine and 5 ppm anabasine together, or a control alkaloid-free solution. We conducted the experiment twice: first, with bees incubated under variable environmental conditions (‘Variable’; temperatures varied from 10-35°C); and second, under carefully controlled environmental conditions (‘Controlled’; 27°C incubator, constant darkness). In ‘Variable’, each alkaloid alone significantly decreased parasite loads, but this effect was not realized with the alkaloids in combination, suggesting an antagonistic interaction. Nicotine but not anabasine significantly increased mortality, and the two compounds had no interactive effects on mortality. In ‘Controlled’, nicotine significantly increased parasite loads, the opposite of its effect in ‘Variable’. While not significant, the relationship between anabasine and parasite loads was also positive. Interactive effects between the two alkaloids on parasite load were non-significant, but the pattern of antagonistic interaction was similar to that in the variable experiment. Neither alkaloid, nor their interaction, significantly affected mortality under controlled conditions. Our results do not indicate synergy between Nicotiana nectar alkaloids; however, they do suggest a complex interaction between secondary metabolites, parasites, and environmental variables, in which secondary metabolites can be either toxic or medicinal depending on context.}, journal={F1000Research}, publisher={F1000 Research Ltd}, author={Thorburn, Lukas P. and Adler, Lynn S. and Irwin, Rebecca E. and Palmer-Young, Evan C.}, year={2015}, month={Sep}, pages={880} }
 @article{mcart_koch_irwin_adler_2014, title={Arranging the bouquet of disease: floral traits and the transmission of plant and animal pathogens}, volume={17}, ISSN={1461-023X 1461-0248}, url={http://dx.doi.org/10.1111/ele.12257}, DOI={10.1111/ele.12257}, abstractNote={AbstractSeveral floral microbes are known to be pathogenic to plants or floral visitors such as pollinators. Despite the ecological and economic importance of pathogens deposited in flowers, we often lack a basic understanding of how floral traits influence disease transmission. Here, we provide the first systematic review regarding how floral traits attract vectors (for plant pathogens) or hosts (for animal pathogens), mediate disease establishment and evolve under complex interactions with plant mutualists that can be vectors for microbial antagonists. Attraction of floral visitors is influenced by numerous phenological, morphological and chemical traits, and several plant pathogens manipulate floral traits to attract vectors. There is rapidly growing interest in how floral secondary compounds and antimicrobial enzymes influence disease establishment in plant hosts. Similarly, new research suggests that consumption of floral secondary compounds can reduce pathogen loads in animal pollinators. Given recent concerns about pollinator declines caused in part by pathogens, the role of floral traits in mediating pathogen transmission is a key area for further research. We conclude by discussing important implications of floral transmission of pathogens for agriculture, conservation and human health, suggesting promising avenues for future research in both basic and applied biology.}, number={5}, journal={Ecology Letters}, publisher={Wiley}, author={McArt, Scott H. and Koch, Hauke and Irwin, Rebecca E. and Adler, Lynn S.}, editor={Gurevitch, JessicaEditor}, year={2014}, month={Feb}, pages={624–636} }
 @article{carper_adler_warren_irwin_2014, title={Effects of Suburbanization on Forest Bee Communities}, volume={43}, ISSN={0046-225X 1938-2936}, url={http://dx.doi.org/10.1603/en13078}, DOI={10.1603/en13078}, abstractNote={ABSTRACT 
 Urbanization is a dominant form of land-use change driving species distributions, abundances, and diversity. Previous research has documented the negative impacts of urbanization on the abundance and diversity of many groups of organisms. However, some organisms, such as bees, may benefit from moderate levels of development, depending on how development alters the availability of foraging and nesting resources. To determine how one type of low-intensity human development, suburbanization, affects bee abundance and diversity and the mechanisms involved, we surveyed bees across suburban and natural forests in the Raleigh-Durham area of North Carolina. We sampled for bees using a combination of bee bowls and hand-netting from March through July of 2008 and 2009. We found higher bee abundance in suburban than natural forests, and although observed species richness was greater in suburban than natural forests, there were no significant differences in rarefied richness or evenness estimates in either year. In addition, the effects of suburbanization were similar across bee species of varying ecological and life-history characteristics. At the local scale, bee abundance and species richness were both positively related to the abundance and richness of flowering species within forests, while the proportion of surrounding developed open areas, such as yards and roadsides, was a strong positive predictor of both bee abundance and richness at the landscape scale. These results suggest that open habitats and the availability of floral resources in suburban sites can support abundant and diverse bee communities and underscore the potential for native bee conservation in urban habitats.}, number={2}, journal={Environmental Entomology}, publisher={Oxford University Press (OUP)}, author={Carper, Adrian L. and Adler, Lynn S. and Warren, Paige S. and Irwin, Rebecca E.}, year={2014}, month={Apr}, pages={253–262} }
 @article{schaeffer_phillips_duryea_andicoechea_irwin_2014, title={Nectar Yeasts in the Tall Larkspur Delphinium barbeyi (Ranunculaceae) and Effects on Components of Pollinator Foraging Behavior}, volume={9}, ISSN={1932-6203}, url={http://dx.doi.org/10.1371/journal.pone.0108214}, DOI={10.1371/journal.pone.0108214}, abstractNote={Microorganisms frequently colonize the nectar of angiosperm species. Though capable of altering a suite of traits important for pollinator attraction, few studies exist that test the degree to which they mediate pollinator foraging behavior. The objective of our study was to fill this gap by assessing the abundance and diversity of yeasts associated with the perennial larkspur Delphinium barbeyi (Ranunculaceae) and testing whether their presence affected components of pollinator foraging behavior. Yeasts frequently colonized D. barbeyi nectar, populating 54–77% of flowers examined depending on site. Though common, the yeast community was species-poor, represented by a single species, Metschnikowia reukaufii. Female-phase flowers of D. barbeyi were more likely to have higher densities of yeasts in comparison to male-phase flowers. Pollinators were likely vectors of yeasts, as virgin (unvisited) flowers rarely contained yeasts compared to flowers open to pollinator visitation, which were frequently colonized. Finally, pollinators responded positively to the presence of yeasts. Bombus foragers both visited and probed more flowers inoculated with yeasts in comparison to uninoculated controls. Taken together, our results suggest that variation in the occurrence and density of nectar-inhabiting yeasts have the potential to alter components of pollinator foraging behavior linked to pollen transfer and plant fitness.}, number={10}, journal={PLoS ONE}, publisher={Public Library of Science (PLoS)}, author={Schaeffer, Robert N. and Phillips, Cody R. and Duryea, M. Catherine and Andicoechea, Jonathan and Irwin, Rebecca E.}, editor={Huang, Shuang-QuanEditor}, year={2014}, month={Oct}, pages={e108214} }
 @article{irwin_cook_richardson_manson_gardner_2014, title={Secondary Compounds in Floral Rewards of Toxic Rangeland Plants: Impacts on Pollinators}, volume={62}, ISSN={0021-8561 1520-5118}, url={http://dx.doi.org/10.1021/JF500521W}, DOI={10.1021/JF500521W}, abstractNote={The study of plant secondary chemistry has been essential in understanding plant consumption by herbivores. There is growing evidence that secondary compounds also occur in floral rewards, including nectar and pollen. Many pollinators are generalist nectar and pollen foragers and thus are exposed to an array of secondary compounds in their diet. This review documents secondary compounds in the nectar or pollen of poisonous rangeland plants of the western United States and the effects of these compounds on the behavior, performance, and survival of pollinators. Furthermore, the biochemical, physiological, and behavioral mechanisms by which pollinators cope with secondary compound consumption are discussed, drawing parallels between pollinators and herbivores. Finally, three avenues of future research on floral reward chemistry are proposed. Given that the majority of flowering plants require animals for pollination, understanding how floral reward chemistry affects pollinators has implications for plant reproduction in agricultural and rangeland habitats.}, number={30}, journal={Journal of Agricultural and Food Chemistry}, publisher={American Chemical Society (ACS)}, author={Irwin, Rebecca E. and Cook, Daniel and Richardson, Leif L. and Manson, Jessamyn S. and Gardner, Dale R.}, year={2014}, month={May}, pages={7335–7344} }
 @article{schaeffer_irwin_2014, title={Yeasts in nectar enhance male fitness in a montane perennial herb}, volume={95}, ISSN={0012-9658 1939-9170}, url={http://dx.doi.org/10.1890/13-1740.1}, DOI={10.1890/13-1740.1}, abstractNote={Floral nectar of many plant species is prone to colonization by microbial organisms such as yeasts. Their presence and metabolism of nectar chemical components have the potential to modify a suite of floral traits important for pollinator attraction, including nectar quality and scent. However, studies on the direct and indirect effects of nectar‐inhabiting microorganisms on pollinator behavior and plant reproductive success remain rare. To determine their potential to affect pollinator behavior and plant fitness, we experimentally manipulated the common nectar‐inhabiting yeast Metschnikowia reukaufii in the nectar of Delphinium nuttallianum, a short‐lived montane perennial herb. We detected positive, indirect, pollinator‐mediated effects of yeasts on male plant fitness measured as pollen donation using powdered fluorescent dyes. However, we detected no direct or indirect effects on components of female fitness. Matching effects on male plant fitness, pollinators responded positively to the presence of yeasts, removing more nectar from flowers treated with M. reukaufii. Our results provide evidence of effects of nectar‐inhabiting yeasts on male plant fitness and highlight the importance of microorganisms in mediating plant–pollinator interactions and subsequent plant fitness.}, number={7}, journal={Ecology}, publisher={Wiley}, author={Schaeffer, Robert N. and Irwin, Rebecca E.}, year={2014}, month={Jul}, pages={1792–1798} }
 @article{manson_cook_gardner_irwin_2013, title={Dose‐dependent effects of nectar alkaloids in a montane plant–pollinator community}, volume={101}, ISSN={0022-0477 1365-2745}, url={http://dx.doi.org/10.1111/1365-2745.12144}, DOI={10.1111/1365-2745.12144}, abstractNote={Summary


Although secondary metabolites are prevalent in floral nectar, the ecological consequences for pollinators and pollination remain relatively unexplored. While often deterrent to pollinators at high concentrations, secondary metabolite concentrations in nectar tend to be much lower than secondary metabolite concentrations in leaves and flowers; yet, they may still affect the maintenance of pollination mutualisms.

Delphinium barbeyi, a common montane herb, contains norditerpene alkaloids in its nectar but at concentrations that are substantially lower than those found in its leaves or flowers. By manipulating nectar alkaloid concentrations in the field and laboratory, we assessed the degree to which varying concentrations of alkaloids in nectar influenced pollinator behaviour and activity and plant reproduction.

In the field, nectar alkaloids significantly reduced both the number of flower visits and the time spent per flower by free‐flying bumblebee pollinators, but we only observed effects at alkaloid concentrations 50 times that of natural nectar. When we supplemented D. barbeyi nectar with alkaloids at concentrations almost 15 times that of natural nectar, we found no evidence for direct or pollinator‐mediated indirect effects on female plant reproduction.

In the laboratory, the direct consumptive effects of nectar alkaloids on bumblebee pollinators were also concentration dependent. Bumblebees exhibited reduced mobility and vigour but only at alkaloid concentrations more than 25 times higher than those found in natural nectar.

Synthesis. We found that nectar alkaloids have dose‐dependent effects on pollinator behaviour and activity. While concentrations of nectar alkaloids rivalling those found in leaves would negatively affect pollinator behaviour and pollination services, the natural concentrations of nectar alkaloids in D. barbeyi have no negative direct or pollinator‐mediated indirect effects on plant reproduction. These results provide experimental insight into the dose‐dependent ecological consequences of nectar secondary metabolites for pollinators and pollination, suggesting that low nectar alkaloid concentrations incurred no ecological costs for D. barbeyi.

}, number={6}, journal={Journal of Ecology}, publisher={Wiley}, author={Manson, Jessamyn S. and Cook, Daniel and Gardner, Dale R. and Irwin, Rebecca E.}, editor={Heil, MartinEditor}, year={2013}, month={Aug}, pages={1604–1612} }
 @article{cook_manson_gardner_welch_irwin_2013, title={Norditerpene alkaloid concentrations in tissues and floral rewards of larkspurs and impacts on pollinators}, volume={48}, ISSN={0305-1978}, url={http://dx.doi.org/10.1016/j.bse.2012.11.015}, DOI={10.1016/j.bse.2012.11.015}, abstractNote={Plant secondary compounds mediate interactions with insects and other animals. The norditerpene alkaloids are significant secondary compounds in Delphinium (larkspur) species which are divided into two classes: the 7, 8-methylenedioxylycoctonine (MDL-type) and N-(methylsuccinimido) anthranoyllycoctonine (MSAL-type), and are known to be toxic to herbivorous insects and livestock. Alkaloid concentrations were measured in a whole plant context in vegetative and floral tissues as well as rewards (pollen and nectar) in Delphinium barbeyi and Delphinium nuttallianum. Alkaloid concentrations differed between vegetative tissues, floral tissues and floral rewards. Alkaloid concentrations in floral parts were consistent with optimal defense theory, with tissues more closely tied to plant fitness, such as fruits, being more heavily defended than foliage. However, alkaloid concentrations were significantly lower in nectar compared to other tissues. The norditerpene alkaloids influenced the activity of bumble bees, the dominant pollinator of larkspur, but the effects were concentration dependent. Alkaloids in nectar are found at concentrations that have no effect on bee activity; however, if alkaloid concentrations in nectar were similar to those in foliage bee activity would be reduced significantly. These results suggest that nectar with low alkaloid concentrations may be beneficial to plant fitness by limiting adverse effects on pollinator activity.}, journal={Biochemical Systematics and Ecology}, publisher={Elsevier BV}, author={Cook, Daniel and Manson, Jessamyn S. and Gardner, Dale R. and Welch, Kevin D. and Irwin, Rebecca E.}, year={2013}, month={Jun}, pages={123–131} }
 @article{irwin_warren_carper_adler_2014, title={Plant–animal interactions in suburban environments: implications for floral evolution}, volume={174}, ISSN={0029-8549 1432-1939}, url={http://dx.doi.org/10.1007/S00442-013-2797-2}, DOI={10.1007/S00442-013-2797-2}, abstractNote={Plant interactions with mutualists and antagonists vary remarkably across space, and have played key roles in the ecology and evolution of flowering plants. One dominant form of spatial variation is human modification of the landscape, including urbanization and suburbanization. Our goal was to assess how suburbanization affected plant-animal interactions in Gelsemium sempervirens in the southeastern United States, including interactions with mutualists (pollination) and antagonists (nectar robbing and florivory). Based on differences in plant-animal interactions measured in multiple replicate sites, we then developed predictions for how these differences would affect patterns of natural selection, and we explored the patterns using measurements of floral and defensive traits in the field and in a common garden. We found that Gelsemium growing in suburban sites experienced more robbing and florivory as well as more heterospecific but not conspecific pollen transfer. Floral traits, particularly corolla length and width, influenced the susceptibility of plants to particular interactors. Observational data of floral traits measured in the field and in a common garden provided some supporting but also some conflicting evidence for the hypothesis that floral traits evolved in response to differences in species interactions in suburban vs. wild sites. However, the degree to which plants can respond to any one interactor may be constrained by correlations among floral morphological traits. Taken together, consideration of the broader geographic context in which organisms interact, in both suburban and wild areas, is fundamental to our understanding of the forces that shape contemporary plant-animal interactions and selection pressures in native species.}, number={3}, journal={Oecologia}, publisher={Springer Science and Business Media LLC}, author={Irwin, Rebecca E. and Warren, Paige S. and Carper, Adrian L. and Adler, Lynn S.}, year={2014}, month={Nov}, pages={803–815} }
 @article{mcdermott_irwin_taylor_2013, title={Using economic instruments to develop effective management of invasive species: insights from a bioeconomic model}, volume={23}, ISSN={1051-0761 1939-5582}, url={http://dx.doi.org/10.1890/12-0649.1}, DOI={10.1890/12-0649.1}, abstractNote={Economic growth is recognized as an important factor associated with species invasions. Consequently, there is increasing need to develop solutions that combine economics and ecology to inform invasive species management. We developed a model combining economic, ecological, and sociological factors to assess the degree to which economic policies can be used to control invasive plants. Because invasive plants often spread across numerous properties, we explored whether property owners should manage invaders cooperatively as a group by incorporating the negative effects of invader spread in management decisions (collective management) or independently, whereby the negative effects of invasive plant spread are ignored (independent management). Our modeling approach used a dynamic optimization framework, and we applied the model to invader spread using Linaria vulgaris. Model simulations allowed us to determine the optimal management strategy based on net benefits for a range of invader densities. We found that optimal management strategies varied as a function of initial plant densities. At low densities, net benefits were high for both collective and independent management to eradicate the invader, suggesting the importance of early detection and eradication. At moderate densities, collective management led to faster and more frequent invader eradication compared to independent management. When we used a financial penalty to ensure that independent properties were managed collectively, we found that the penalty would be most feasible when levied on a property's perimeter boundary to control spread among properties. At the highest densities, the optimal management strategy was “do nothing” because the economic costs of removal were too high relative to the benefits of removal. Spatial variation in L. vulgaris densities resulted in different optimal management strategies for neighboring properties, making a formal economic policy to encourage invasive species removal critical. To accomplish the management and enforcement of these economic policies, we discuss modification of existing agencies and infrastructure. Finally, a sensitivity analysis revealed that lowering the economic cost of invader removal would strongly increase the probability of invader eradication. Taken together, our results provide quantitative insight into management decisions and economic policy instruments that can encourage invasive species removal across a social landscape.}, number={5}, journal={Ecological Applications}, publisher={Wiley}, author={McDermott, Shana M. and Irwin, Rebecca E. and Taylor, Brad W.}, year={2013}, month={Jul}, pages={1086–1100} }
 @article{schaeffer_manson_irwin_2012, title={Effects of abiotic factors and species interactions on estimates of male plant function: a meta‐analysis}, volume={16}, ISSN={1461-023X 1461-0248}, url={http://dx.doi.org/10.1111/ele.12044}, DOI={10.1111/ele.12044}, abstractNote={AbstractThe majority of angiosperms are hermaphroditic with total fitness comprised of both male and female components of reproduction. However, most studies examining the effects of abiotic factors and species interactions on fitness have focussed on female reproduction, potentially biasing our understanding of the consequences of environmental factors on total fitness. Here, we use meta‐analysis to test how environmental factors affect male function. We obtained 278 effect sizes from 96 studies that measured male function responses to manipulated environmental factors. We found significant effects of abiotic factors and species interactions on estimates of male function, with responses varying depending on environmental factor identity. Male and female responses were correlated for abiotic factor manipulations, but varied based on the type of species interaction (antagonistic or mutualistic). This suggests that measuring only female function may misrepresent whole‐plant reproduction depending on context. Finally, we found differences amongst components of male function in response to environmental factors, suggesting that some male function estimates may fail to capture the effects of environmental factors on male fitness. Our results demonstrate the importance of incorporating male function into ecological and evolutionary studies to provide a more accurate understanding of the effects of environmental factors on total fitness.}, number={3}, journal={Ecology Letters}, publisher={Wiley}, author={Schaeffer, Robert N. and Manson, Jessamyn S. and Irwin, Rebecca E.}, editor={Gurevitch, JessicaEditor}, year={2012}, month={Dec}, pages={399–408} }
 @misc{irwin_2012, title={The role of trait-mediated indirect interactions for multispecies plant–animal mutualisms}, url={http://dx.doi.org/10.1017/cbo9780511736551.018}, DOI={10.1017/cbo9780511736551.018}, abstractNote={Organisms experience myriad interactions with both antagonists and mutualists. There is widespread recognition that these multispecies interactions are not independent and that community membership can have important consequences for host fitness as well as patterns of natural selection (Strauss and Irwin 2004; Morris et al. 2007). For example, herbivore feeding can influence plant interactions with other herbivores or mutualists (e.g., pollinators), which can have subsequent effects on host plant fitness (Karban and Baldwin 1997; Mothershead and Marquis 2000; Strauss et al. 2001). Moreover, traits involved in these multispecies interactions can represent an adaptive compromise due to host interactions with antagonists and mutualists (Galen and Cuba 2001). While the effects of antagonist–antagonist and antagonist–mutualist interactions on hosts have received attention from both theoreticians and empiricists, the ecological and evolutionary consequences of host interactions with multiple mutualists have received less study (Hoeksema and Bruna 2000). That the study of multispecies mutualisms has lagged behind other suites of multispecies interactions is not surprising, given that mutualisms in general receive less study than competition and predation (Bronstein 1994). However, because many species interact with multiple mutualists either simultaneously or sequentially throughout their lifetimes (Janzen 1985) and mutualisms can have powerful impacts on host fitness and evolution (Bronstein et al. 2006), it is germane to ask how these multispecies mutualisms affect the ecology and evolution of their shared hosts (also see Stanton 2003).}, journal={Trait-Mediated Indirect Interactions}, publisher={Cambridge University Press}, author={Irwin, Rebecca E.}, year={2012}, month={Dec}, pages={257–277} }
 @article{adler_irwin_2012, title={What you smell is more important than what you see? Natural selection on floral scent}, volume={195}, ISSN={0028-646X 1469-8137}, url={http://dx.doi.org/10.1111/j.1469-8137.2012.04229.x}, DOI={10.1111/j.1469-8137.2012.04229.x}, abstractNote={The notion that floral traits are under phenotypic selection is widely recognized in evolutionary ecology, and myriad studies have documented strong selection on traits such as flower number, flower size, color, and shape (reviewed in Parachnowitsch & Kessler, 2010). Indeed, some of the most striking examples of presumed phenotypic selection come from floral morphological traits, such as the nectar spurs of Madagascar Star Orchids pollinated by hawkmoths with impressively long tongues (reviewed in Whittall & Hodges, 2007). However, despite the often overpowering smell of many flowers, few studies have measured phenotypic selection on floral scent. Scent traits are notoriously difficult to measure and analyze compared with many other floral traits, in part due to the technical skills needed to collect and analyze scent, and in part because ‘scent’ is a very complex trait. Moreover, measuring phenotypic selection on floral traits, including scent, often involves hundreds of plant replicates, requiring a heavy investment in plant chemistry. Thus, the work presented by Parachnowitsch et al. in this issue of New Phytologist (pp. 667–675) provides a significant step forward in our understanding of phenotypic selection on floral traits by showing that floral scent can be under stronger selection than more traditionally measured floral morphological traits, such as floral size and color.}, number={3}, journal={New Phytologist}, publisher={Wiley}, author={Adler, Lynn S. and Irwin, Rebecca E.}, year={2012}, month={Jul}, pages={510–511} }
 @article{brody_irwin_2012, title={When resources don't rescue: flowering phenology and species interactions affect compensation to herbivory in <i>Ipomopsis aggregata}, volume={121}, ISSN={0030-1299 1600-0706}, url={http://dx.doi.org/10.1111/j.1600-0706.2012.20458.x}, DOI={10.1111/j.1600-0706.2012.20458.x}, abstractNote={The ability of plants to tolerate, or compensate for, herbivore damage is highly variable and has been the subject of much research. Although many plants can compensate for herbivore damage, and some even overcompensate, we cannot yet generalize about the conditions that promote a positive response to damage. Here, we asked how abiotic resources (i.e. plant nutrient status) coupled with biotic interactions – i.e. subsequent interactions with pollinators, seed predators and nectar robbing bumble bees – affect the compensatory ability of Ipomopsis aggregata, a monocarpic herb that has been the subject of much previous debate. We hypothesized that compensation to herbivore damage in I. aggregata (Polemoniaceae) would depend first on plants having an ample supply of resources and, second, on the outcome of subsequent interactions with mutualist pollinators and enemy pre‐dispersal seed predators and nectar robbing bumble bees. We used a fully‐factorial experiment in which plants were watered, fertilized or left as unmanipulated controls, crossed with clipping to simulate herbivore damage to the apical meristem. Resource addition enhanced both male and female components of fitness, but resource enhancement did not provide the means for plants to fully compensate for simulated herbivory. Clipped plants produced significantly more inflorescences, but at the expense of a delay in flowering and fewer total flowers. Clipping significantly reduced losses to dipteran pre‐dispersal seed predators by delaying flowering time, but early flowering plants produced higher numbers of seeds despite incurring higher rates of predation. Clipped plants incurred a higher risk to nectar robbers in one of two years. Overall, clipped plants suffered severe reductions (a nearly 50% reduction in total seed set) in female success, but clipping combined with nutrient addition enhanced male function through increases in per‐flower pollen production. However, because clipped plants produced significantly fewer flowers than unclipped plants, whole‐plant pollen production was significantly reduced by clipping. Pollinator visitation and nectar robbing were variable between clipping treatments and between years and (nectar robbing) among sites. Our results demonstrate that the variability in plant response to herbivory can, at least in part, be driven by plant interactions with mutualists and enemies. Thus, accounting for such interactions and their variability is important to fully understanding plant compensation for herbivore damage and will likely go far to explain variation in plant response that appears to be independent of resources.}, number={9}, journal={Oikos}, publisher={Wiley}, author={Brody, Alison K. and Irwin, Rebecca E.}, year={2012}, month={May}, pages={1424–1434} }
 @article{irwin_brody_2011, title={Additive effects of herbivory, nectar robbing and seed predation on male and female fitness estimates of the host plant Ipomopsis aggregata}, volume={166}, ISSN={0029-8549 1432-1939}, url={http://dx.doi.org/10.1007/s00442-010-1898-4}, DOI={10.1007/s00442-010-1898-4}, abstractNote={Many antagonistic species attack plants and consume specific plant parts. Understanding how these antagonists affect plant fitness individually and in combination is an important research focus in ecology and evolution. We examined the individual and combined effects of herbivory, nectar robbing, and pre-dispersal seed predation on male and female estimates of fitness in the host plant Ipomopsis aggregata. By examining the effects of antagonists on plant traits, we were able to tease apart the direct consumptive effects of antagonists versus the indirect effects mediated through changes in traits important to pollination. In a three-way factorial field experiment, we manipulated herbivory, nectar robbing, and seed predation. Herbivory and seed predation reduced some male and female fitness estimates, whereas plants tolerated the effects of robbing. The effects of herbivory, robbing, and seed predation were primarily additive, and we found little evidence for non-additive effects of multiple antagonists on plant reproduction. Herbivory affected plant reproduction through both direct consumptive effects and indirectly through changes in traits important to pollination (i.e., nectar and phenological traits). Conversely, seed predators primarily had direct consumptive effects on plants. Our results suggest that the effects of multiple antagonists on estimates of plant fitness can be additive, and investigating which traits respond to damage can provide insight into how antagonists shape plant performance.}, number={3}, journal={Oecologia}, publisher={Springer Science and Business Media LLC}, author={Irwin, Rebecca E. and Brody, Alison K.}, year={2011}, month={Jan}, pages={681–692} }
 @article{adler_irwin_2012, title={Nectar alkaloids decrease pollination and female reproduction in a native plant}, volume={168}, ISSN={0029-8549 1432-1939}, url={http://dx.doi.org/10.1007/S00442-011-2153-3}, DOI={10.1007/S00442-011-2153-3}, abstractNote={The evolution of floral traits may be shaped by a community of floral visitors that affect plant fitness, including pollinators and floral antagonists. The role of nectar in attracting pollinators has been extensively studied, but its effects on floral antagonists are less understood. Furthermore, the composition of non-sugar nectar components, such as secondary compounds, may affect plant reproduction via changes in both pollinator and floral antagonist behavior. We manipulated the nectar alkaloid gelsemine in wild plants of the native perennial vine Gelsemium sempervirens. We crossed nectar gelsemine manipulations with a hand-pollination treatment, allowing us to determine the effect of both the trait and the interaction on plant female reproduction. We measured pollen deposition, pollen removal, and nectar robbing to assess whether gelsemine altered the behavior of mutualists and antagonists. High nectar gelsemine reduced conspecific pollen receipt by nearly half and also reduced the proportion of conspecific pollen grains received, but had no effect on nectar robbing. Although high nectar gelsemine reduced pollen removal, an estimate of male reproduction, by one-third, this effect was not statistically significant. Fruit set was limited by pollen receipt. However, this effect varied across sites such that the sites that were most pollen-limited were also the sites where nectar alkaloids had the least effect on pollen receipt, resulting in no significant effect of nectar alkaloids on fruit set. Finally, high nectar gelsemine significantly reduced seed weight; however, this effect was mediated by a mechanism other than pollen limitation. Taken together, our work suggests that nectar alkaloids are more costly than beneficial in our system, and that relatively small-scale spatial variation in trait effects and interactions could determine the selective impacts of traits such as nectar composition.}, number={4}, journal={Oecologia}, publisher={Springer Science and Business Media LLC}, author={Adler, Lynn S. and Irwin, Rebecca E.}, year={2012}, pages={1033–1041} }
 @article{zhang_irwin_wang_he_yang_duan_2011, title={Selective seed abortion induced by nectar robbing in the selfing plant <i>Comastoma pulmonarium}, volume={192}, ISSN={0028-646X 1469-8137}, url={http://dx.doi.org/10.1111/j.1469-8137.2011.03785.x}, DOI={10.1111/j.1469-8137.2011.03785.x}, abstractNote={• Self-pollination often provides plants with the benefit of reproductive assurance; thus, it is generally assumed that species' interactions that alter floral attractiveness or rewards, such as nectar robbing, will have little effect on the seed production of selfing species. We challenge this view with experimental data from Comastoma pulmonarium, a selfing annual experiencing a high ratio of nectar robbing in the Qinghai-Tibet Plateau. • We manipulated robbing (robbed or netted) and pollination mode (hand-selfed or hand-outcrossed) in a factorial design and measured the number of developing ovules and mature seeds, together with seed weight and seed germination, in each treatment. • Robbing decreased the number of mature seeds, but not the number of developing ovules, suggesting a negative influence of robbers through indirect effects via selective seed abortion. We found no evidence for early-acting inbreeding depression, but found later-acting inbreeding depression. Our data also suggested that later-acting inbreeding depression of progeny from robbed flowers could be reduced in comparison with that from unrobbed flowers. • We suggest that nectar robbing can have both negative and positive effects on the quantity and quality, respectively, of progeny produced in selfing plants, and challenge the view that robbing has no effect on selfing species.}, number={1}, journal={New Phytologist}, publisher={Wiley}, author={Zhang, Chan and Irwin, Rebecca E. and Wang, Yun and He, Ya‐Ping and Yang, Yong‐Ping and Duan, Yuan‐Wen}, year={2011}, month={Jun}, pages={249–255} }
 @article{burkle_irwin_2010, title={Beyond biomass: measuring the effects of community‐level nitrogen enrichment on floral traits, pollinator visitation and plant reproduction}, volume={98}, ISSN={0022-0477 1365-2745}, url={http://dx.doi.org/10.1111/j.1365-2745.2010.01648.x}, DOI={10.1111/j.1365-2745.2010.01648.x}, abstractNote={Summary1. Nitrogen (N) limits primary productivity in many systems and can have dramatic effects on plant–herbivore interactions, but its effects on mutualistic interactions at the community level are not well‐understood. The reproduction of many plants depends on both soil N and pollination, and N may affect floral traits, such as flower number or size, which are important for pollinator attraction to plant individuals and communities.2. Thus, N may influence plant biomass and reproduction directly as well as indirectly via changes in pollination. The degree to which the effects of N enrichment scale from plant individuals to assemblages through emerging community‐level changes in species interactions, like pollination, is relatively unknown.3. For 4 years, we tested how N addition to subalpine plant assemblages in Colorado, USA, affected primary productivity and species diversity, floral traits and plant–pollinator interactions, and components of female and male plant reproduction.4. At the community level, we found that high‐N addition favoured the biomass and seed production of grasses, whereas low‐N addition promoted forb growth, flower production and pollinator visitation. However, using a pollen supplementation experiment, we found no evidence that N addition altered patterns of pollen limitation of seed production. Pollinators distributed themselves evenly across floral resources such that per‐flower visitation rate did not differ among N treatments. Thus, individual plants did not incur any extra benefit or cost from community‐level changes in plant–pollinator interactions that resulted from N enrichment, and the effects of N on forb reproduction were direct.5. Synthesis. Understanding how mutualistic and antagonistic species interactions influence individual and community responses to abiotic resources may provide insight to the dominant forces structuring communities and is especially important in the context of predicting the effects of environmental change. In this case, the direct effects of N addition on plants were stronger than the indirect effects mediated through plant–pollinator interactions, thus supporting the concept of bottom‐up resource limitation controlling plant response.}, number={3}, journal={Journal of Ecology}, publisher={Wiley}, author={Burkle, Laura A. and Irwin, Rebecca E.}, year={2010}, month={Apr}, pages={705–717} }
 @article{irwin_2010, title={Evolutionary Ecology: When Pollinators Are Also Herbivores}, volume={20}, ISSN={0960-9822}, url={http://dx.doi.org/10.1016/j.cub.2009.12.005}, DOI={10.1016/j.cub.2009.12.005}, abstractNote={Plants often face a dilemma in attracting mutualists versus deterring antagonists. This dilemma may be exceptionally challenging when the mutualist and antagonist are the same visitor. It has now been demonstrated how plants can resolve this conflict through a novel change in flowering traits.}, number={3}, journal={Current Biology}, publisher={Elsevier BV}, author={Irwin, Rebecca E.}, year={2010}, month={Feb}, pages={R100–R101} }
 @article{irwin_bronstein_manson_richardson_2010, title={Nectar Robbing: Ecological and Evolutionary Perspectives}, volume={41}, ISSN={1543-592X 1545-2069}, url={http://dx.doi.org/10.1146/annurev.ecolsys.110308.120330}, DOI={10.1146/annurev.ecolsys.110308.120330}, abstractNote={ Not all floral visitors attracted to flowers are pollinators. Instead, some visitors circumvent the floral opening, usually removing nectar without contacting the anthers and/or stigma. Here we review the evolutionary ecology of nectar robbing from both the plant and animal perspective. Effects of robbing on female and male components of plant reproduction range from negative to positive. Their underlying mechanisms are diverse, including direct effects and indirect effects mediated through changes in pollination. We detail how plants may be able to deter robbers through morphological and chemical traits. For the evolutionary ecology of robbing to move beyond a phytocentric perspective, studies must also address the causes of robbing and the consequences for both robbers and pollinators. We use an energetics approach to evaluate these causes and consequences. Finally, we highlight unanswered questions in need of further research. }, number={1}, journal={Annual Review of Ecology, Evolution, and Systematics}, publisher={Annual Reviews}, author={Irwin, Rebecca E. and Bronstein, Judith L. and Manson, Jessamyn S. and Richardson, Leif}, year={2010}, month={Dec}, pages={271–292} }
 @article{mitchell_irwin_flanagan_karron_2009, title={Ecology and evolution of plant–pollinator interactions}, volume={103}, ISSN={1095-8290 0305-7364}, url={http://dx.doi.org/10.1093/aob/mcp122}, DOI={10.1093/aob/mcp122}, abstractNote={BACKGROUND
Some of the most exciting advances in pollination biology have resulted from interdisciplinary research combining ecological and evolutionary perspectives. For example, these two approaches have been essential for understanding the functional ecology of floral traits, the dynamics of pollen transport, competition for pollinator services, and patterns of specialization and generalization in plant-pollinator interactions. However, as research in these and other areas has progressed, many pollination biologists have become more specialized in their research interests, focusing their attention on either evolutionary or ecological questions. We believe that the continuing vigour of a synthetic and interdisciplinary field like pollination biology depends on renewed connections between ecological and evolutionary approaches.


SCOPE
In this Viewpoint paper we highlight the application of ecological and evolutionary approaches to two themes in pollination biology: (1) links between pollinator behaviour and plant mating systems, and (2) generalization and specialization in pollination systems. We also describe how mathematical models and synthetic analyses have broadened our understanding of pollination biology, especially in human-modified landscapes. We conclude with several suggestions that we hope will stimulate future research. This Viewpoint also serves as the introduction to this Special Issue on the Ecology and Evolution of Plant-Pollinator Interactions. These papers provide inspiring examples of the synergy between evolutionary and ecological approaches, and offer glimpses of great accomplishments yet to come.}, number={9}, journal={Annals of Botany}, publisher={Oxford University Press (OUP)}, author={Mitchell, Randall J. and Irwin, Rebecca E. and Flanagan, Rebecca J. and Karron, Jeffrey D.}, year={2009}, month={Jun}, pages={1355–1363} }
 @article{elliott_irwin_2009, title={Effects of flowering plant density on pollinator visitation, pollen receipt, and seed production in <i>Delphinium barbeyi</i> (Ranunculaceae)}, volume={96}, ISSN={0002-9122 1537-2197}, url={http://dx.doi.org/10.3732/ajb.0800260}, DOI={10.3732/ajb.0800260}, abstractNote={Variation in flowering plant density can have conflicting effects on pollination and seed production. Dense flower patches may attract more pollinators, but flowers in those patches may also compete for pollinator visits and abiotic resources. We examined how natural and experimental conspecific flowering plant density affected pollen receipt and seed production in a protandrous, bumble bee‐pollinated wildflower, Delphinium barbeyi (Ranunculaceae). We also compared floral sex ratios, pollinator visitation rates, and pollen limitation of seed set from early to late in the season to determine whether these factors mirrored seasonal changes in pollen receipt and seed production. Pollen receipt increased with natural flowering plant density, while seed production increased across lower densities and decreased across higher flower densities. Experimental manipulation of flowering plant density did not affect pollinator visitation rate, pollen receipt, or seed production. Although pollinator visitation rate increased 10‐fold from early to late in the season, pollen receipt and seed set decreased over the season. Seed set was never pollen‐limited. Thus, despite widespread effects of flowering plant density on plant reproduction in other species, the effects of conspecific flowering plant density on D. barbeyi pollination and seed production are minor.}, number={5}, journal={American Journal of Botany}, publisher={Wiley}, author={Elliott, Susan E. and Irwin, Rebecca E.}, year={2009}, month={May}, pages={912–919} }
 @article{burkle_irwin_2009, title={Nectar Sugar Limits Larval Growth of Solitary Bees (Hymenoptera: Megachilidae)}, volume={38}, ISSN={0046-225X 1938-2936}, url={http://dx.doi.org/10.1603/022.038.0441}, DOI={10.1603/022.038.0441}, abstractNote={ABSTRACT The bottom-up effects of plant food quality and quantity and affect the growth, survival, and reproduction of herbivores. The larvae of solitary bee pollinators, consumers of nectar and pollen, are also herbivores. Although pollen quantity and quality are known to be important for larval growth, little is known about how nectar quality limits solitary bee performance. By adding different levels of nectar sugar directly to solitary bee provisions in the subalpine of Colorado, we tested the degree to which larval performance (development time, mass, and survival) was limited by nectar sugar. We found that larval growth increased with nectar sugar addition, with the highest larval mass in the high nectar-sugar addition treatment (50% honey solution). The shortest larval development time was observed in the low nectar-sugar addition treatment (25% honey solution). Neither low nor high nectar-sugar addition affected larval survival. This study suggests that, in addition to pollen, nectarsugar concentration can limit solitary bee larval growth and development, and nectar should be considered more explicitly as a currency governing foraging decisions related to producing optimally sized offspring. The availability and sugar content of nectar may scale up to affect bee fitness, population dynamics, and plant-pollinator mutualisms.}, number={4}, journal={Environmental Entomology}, publisher={Oxford University Press (OUP)}, author={Burkle, Laura and Irwin, Rebecca}, year={2009}, month={Aug}, pages={1293–1300} }
 @article{irwin_2009, title={Realized tolerance to nectar robbing: compensation to floral enemies in Ipomopsis aggregata}, volume={103}, ISSN={1095-8290 0305-7364}, url={http://dx.doi.org/10.1093/aob/mcp056}, DOI={10.1093/aob/mcp056}, abstractNote={BACKGROUND AND AIMS
Although the ecological and evolutionary consequences of foliar herbivory are well understood, how plants cope with floral damage is less well explored. Here the concept of tolerance, typically studied within the context of plant defence to foliar herbivores and pathogens, is extended to floral damage. Variation in tolerance to floral damage is examined, together with some of the mechanisms involved.


METHODS
The study was conducted on Ipomopsis aggregata, which experiences floral damage and nectar removal by nectar-robbing bees. High levels of robbing can reduce seeds sired and produced by up to 50 %, an indirect effect mediated through pollinator avoidance of robbed plants. Using an experimental common garden with groups of I. aggregata, realized tolerance to robbing was measured. Realized tolerance included both genetic and environmental components of tolerance. It was hypothesized that both resource acquisition and storage traits, and traits involved in pollination would mitigate the negative effects of robbers.


KEY RESULTS
Groups of I. aggregata varied in their ability to tolerate nectar robbing. Realized tolerance was observed only through a component of male plant reproduction (pollen donation) and not through components of female plant reproduction. Some groups fully compensated for robbing while others under- or overcompensated. Evidence was found only for a pollination-related trait, flower production, associated with realized tolerance. Plants that produced more flowers and that had a higher inducibility of flower production following robbing were more able to compensate through male function.


CONCLUSIONS
Variation in realized tolerance to nectar robbing was found in I. aggregata, but only through an estimate of male reproduction, and traits associated with pollination may confer realized tolerance to robbing. By linking concepts and techniques from studies of plant-pollinator and plant-herbivore interactions, this work provides insight into the role of floral traits in pollinator attraction as well as plant defence.}, number={9}, journal={Annals of Botany}, publisher={Oxford University Press (OUP)}, author={Irwin, Rebecca E.}, year={2009}, month={Mar}, pages={1425–1433} }
 @article{burkle_irwin_2009, title={The importance of interannual variation and bottom–up nitrogen enrichment for plant–pollinator networks}, volume={118}, ISSN={0030-1299 1600-0706}, url={http://dx.doi.org/10.1111/j.1600-0706.2009.17740.x}, DOI={10.1111/j.1600-0706.2009.17740.x}, abstractNote={Striking changes in food web structure occur with alterations in resource supply. Like predator–prey interactions, many mutualisms are also consumer–resource interactions. However, no studies have explored how the structure of plant–pollinator networks may be affected by nutrient enrichment. For three years, we enriched plots of subalpine plant communities with nitrogen and observed subsequent effects on plant–pollinator network structure. Although nitrogen enrichment affects floral abundance and rates of pollinator visitation, we found no effects of nitrogen enrichment on the core group of generalist plants and pollinators or on plant–pollinator network structure parameters, such as network topology (the identity and frequency of interactions) and the degree of nestedness. However, individual plant and pollinator taxa were packed into the nested networks differently among nitrogen treatments. In particular, pollinators visited different numbers and types of plants in the nested networks, suggesting weak, widespread effects of nitrogen addition on individual taxa. Independent of nitrogen enrichment, there were large interannual differences in network structure and interactions, due to species turnover among years and flexibility in interacting with new partners. These data suggest that the community structure of small‐scale mutualistic networks may be relatively robust to short‐term bottom–up changes in the resource supply, but sensitive to variation in the opportunistic behavior and turnover of plant and pollinator species among years.}, number={12}, journal={Oikos}, publisher={Wiley}, author={Burkle, Laura and Irwin, Rebecca}, year={2009}, month={Nov}, pages={1816–1829} }
 @article{wilke_irwin_2010, title={Variation in the phenology and abundance of flowering by native and exotic plants in subalpine meadows}, volume={12}, ISSN={1387-3547 1573-1464}, url={http://dx.doi.org/10.1007/s10530-009-9649-3}, DOI={10.1007/s10530-009-9649-3}, number={7}, journal={Biological Invasions}, publisher={Springer Science and Business Media LLC}, author={Wilke, Brook J. and Irwin, Rebecca E.}, year={2010}, pages={2363–2372} }
 @article{sloan_duell_shi_irwin_andrew_williams_moore_2009, title={Ecogeographic genetic epidemiology}, volume={33}, ISSN={0741-0395 1098-2272}, url={http://dx.doi.org/10.1002/gepi.20386}, DOI={10.1002/gepi.20386}, abstractNote={AbstractComplex diseases such as cancer and heart disease result from interactions between an individual's genetics and environment, i.e. their human ecology. Rates of complex diseases have consistently demonstrated geographic patterns of incidence, or spatial “clusters” of increased incidence relative to the general population. Likewise, genetic subpopulations and environmental influences are not evenly distributed across space. Merging appropriate methods from genetic epidemiology, ecology and geography will provide a more complete understanding of the spatial interactions between genetics and environment that result in spatial patterning of disease rates. Geographic information systems (GIS), which are tools designed specifically for dealing with geographic data and performing spatial analyses to determine their relationship, are key to this kind of data integration. Here the authors introduce a new interdisciplinary paradigm, ecogeographic genetic epidemiology, which uses GIS and spatial statistical analyses to layer genetic subpopulation and environmental data with disease rates and thereby discern the complex gene‐environment interactions which result in spatial patterns of incidence. Genet. Epidemiol. 2009. © 2008 Wiley‐Liss, Inc.}, number={4}, journal={Genetic Epidemiology}, publisher={Wiley}, author={Sloan, Chantel D. and Duell, Eric J. and Shi, Xun and Irwin, Rebecca and Andrew, Angeline S. and Williams, Scott M. and Moore, Jason H.}, year={2009}, month={May}, pages={281–289} }
 @article{egan_irwin_2008, title={Evaluation of the field impact of an adventitious herbivore on an invasive plant, yellow toadflax, in Colorado, USA}, volume={199}, ISSN={1385-0237 1573-5052}, url={http://dx.doi.org/10.1007/s11258-008-9415-0}, DOI={10.1007/s11258-008-9415-0}, number={1}, journal={Plant Ecology}, publisher={Springer Science and Business Media LLC}, author={Egan, J. Franklin and Irwin, Rebecca E.}, year={2008}, month={Mar}, pages={99–114} }
 @article{irwin_galen_rabenold_kaczorowski_mccutcheon_2008, title={MECHANISMS OF TOLERANCE TO FLORAL LARCENY IN TWO WILDFLOWER SPECIES}, volume={89}, ISSN={0012-9658 1939-9170}, url={http://dx.doi.org/10.1890/08-0081.1}, DOI={10.1890/08-0081.1}, abstractNote={Tolerance of foliar damage is widely recognized as an effective defense against herbivores and pathogens. However, tolerance of the impacts of antagonists on pollination success is less well understood. Here, we extend the framework of tolerance to foliar damage to understand how plants mitigate the pollination and fitness costs of floral larceny (i.e., the consumption of floral nectar often without pollination). We focused on two mechanisms: high nectar rewards per flower to feed all floral visitors and high flower production to compensate for reproductive losses under reduced pollination and seed set. We compared the efficacy of these mechanisms in two plant species:Polemonium viscosumandIpomopsis aggregata. InPolemonium, ants acting as larcenists reduce nectar accumulation but do not completely empty flowers. When nectar reserves were augmented, ant consumption increased, negating the efficacy of this putative tolerance mechanism. Similarly, inIpomopsis, nectar addition had little effect on tolerance to larceny by bumble bees, perhaps because residual intact flowers do not have enough nectar to compensate for lost rewards. Flower production in both species mitigated some of the negative impacts of larceny on seed set. InPolemonium, flower number was not plastic in response to larceny, but large inflorescences enhanced female fitness only when larcenists were present, suggesting that “surplus” flowers in large inflorescences can function to replace reproductive losses due to larceny. InIpomopsis, high rates of larceny induced flower production, but the fecundity benefits of making more flowers declined inversely to larcenist intensity. Overall, our results suggest (1) that tolerance to floral larceny involves “banking” extra flowers to replace lost reproduction rather than maintaining pollination of ones with larceny, and (2) that the efficacy of flower production as a tolerance mechanism varies inversely to larceny rate.}, number={11}, journal={Ecology}, publisher={Wiley}, author={Irwin, Rebecca E. and Galen, Candace and Rabenold, Jessica J. and Kaczorowski, Rainee and McCutcheon, Meghan L.}, year={2008}, month={Nov}, pages={3093–3104} }
 @article{irwin_adler_2008, title={NECTAR SECONDARY COMPOUNDS AFFECT SELF-POLLEN TRANSFER: IMPLICATIONS FOR FEMALE AND MALE REPRODUCTION}, volume={89}, ISSN={0012-9658}, url={http://dx.doi.org/10.1890/07-1359.1}, DOI={10.1890/07-1359.1}, abstractNote={Pollen movement within and among plants affects inbreeding, plant fitness, and the spatial scale of genetic differentiation. Although a number of studies have assessed how plant and floral traits influence pollen movement via changes in pollinator behavior, few have explored how nectar chemical composition affects pollen transfer. As many as 55% of plants produce secondary compounds in their nectar, which is surprising given that nectar is typically thought to attract pollinators. We tested the hypothesis that nectar with secondary compounds may benefit plants by encouraging pollinators to leave plants after visiting only a few flowers, thus reducing self-pollen transfer. We used Gelsemium sempervirens, a plant whose nectar contains the alkaloid gelsemine, which has been shown to be a deterrent to foraging bee pollinators. We found that high nectar alkaloids reduced the total and proportion of self-pollen received by one-half and one-third, respectively. However, nectar alkaloids did not affect female reproduction when we removed the potential for self-pollination (by emasculating all flowers on plants). We then tested the assumption that self-pollen in combination with outcrossed pollen depresses seed set. We found that plants were weakly self-compatible, but self-pollen with outcrossed pollen did not reduce seed set relative to solely outcrossed flowers. Finally, an exponential model of pollen carryover suggests that high nectar alkaloids could benefit plants via increased pollen export (an estimate of male function), but only when pollinators were efficient and abundant and plants had large floral displays. Results suggest that high nectar alkaloids may benefit plants via increased pollen export under a restricted set of ecological conditions, but in general, the costs of high nectar alkaloids in reducing pollination balanced or outweighed the benefits of reducing self-pollen transfer for estimates of female and male reproduction.}, number={8}, journal={Ecology}, publisher={Wiley}, author={Irwin, Rebecca E. and Adler, Lynn S.}, year={2008}, month={Aug}, pages={2207–2217} }
 @article{irwin_mitchell_karron_2008, title={Pre-meeting Conference; The Ecology and Evolution of Plant–Pollinator Interactions}, volume={89}, ISSN={0012-9623}, url={http://dx.doi.org/10.1890/0012-9623(2008)89[481:pteaeo]2.0.co;2}, DOI={10.1890/0012-9623(2008)89[481:pteaeo]2.0.co;2}, abstractNote={A conference organized by Jeffrey D. Karron, Randall J. Mitchell, and Rebecca E. Irwin prior to the 2008 ESA Annual Meeting in Milwaukee, Wisconsin, with support from the Ecological Society of America and the Annals of Botany Corporation. For over two centuries, pollination biology has enjoyed a rich history of study by both ecologists and evolutionary biologists, and has fascinated natural historians, gardeners, and environmental enthusiasts. Studies in pollination biology have provided insight into animal cognition and behavior, mutualism, exploitation, mating biology, and some of the best-known examples of evolution and co-evolution by natural selection (reviewed in Thompson 1994, Chittka and Thomson 2001, Harder and Barrett 2006). Like many disciplines in biology, innovation in the study of pollination has often involved specialization in a particular subdiscipline (McPeek 2006), such as botanical vs. zoological aspects (Waser and Price 1998) or plant-mating system vs. pollination ecology focus areas (Lloyd and Barrett 1996). However, this specialization may cause fragmentation of understanding and conceptual frameworks, which can hamper progress if unaddressed. The study of pollination biology has experienced a recent surge of growth in two related fields. On the one hand, studies in community pollination ecology are breaking new ground in research addressing webs of species interactions and the repercussions of disturbance, land-use change, and invasion to community dynamics (Waser and Ollerton 2006). On the other hand, evolutionary pollination biologists are now armed with advanced molecular and genomic tools that enable them to delve into the processes and consequences underlying the dynamics of pollen transport, the evolution of obligate mutualisms and plant mating patterns, and the genetics of floral evolution (Harder and Barrett 2006). The goal of this conference was to highlight exciting recent advances in community and evolutionary pollination biology, and to foster interaction among pollination biologists. We aimed to encourage a unified framework for the study of community and evolutionary approaches, and draw attention to largely unexplored questions at the intersection of community and evolutionary pollination biology to inspire future research. The two-day conference featured 23 speakers from eight countries, as well as a poster session with 85 participants. The conference drew more than 200 attendees from 17 nations. Oral presentations were organized into four half-day sessions, two each on evolutionary and community approaches in pollination biology. The conference opened with six talks on evolutionary approaches. Three talks focused on the adaptive nature of floral traits, including how close traits are to their adaptive optimum and why populations depart from their adaptive optimum (S. Armbruster), the roles of integration and constraint on anther-position evolution within the context of a diverse pollinator assemblage (J. Conner), and the effect of flower color and correlated traits on pollinator visitation preferences (D. Campbell). Three additional talks explored theoretical, molecular, and experimental approaches (L. Harder, J. Brunet, and J. Karron) to investigating plant mating patterns and the causes and consequences of pollen dispersal by diverse pollinator assemblages. One common thread through all of the talks was the importance of community composition (both of the plants and the pollinators) to mating and fitness outcomes, providing a direct link between the ecology of the plant–pollinator community and evolutionary implications in terms of mating patterns, gene flow, and selection on floral traits. These talks also emphasized the need for more research quantifying male components of reproductive success. The next set of talks highlighted the importance of nonpollinating species to the ecology and evolution of plant–pollinator interactions. A surprising number of organisms interact with flowers but do not act as pollinators; these nonpollinating floral visitors may have powerful effects on the ecology and evolution of plant–pollinator interactions via both direct and indirect mechanisms. C. Herrera highlighted the patterns and mechanisms driving microbial communities in floral nectar. Yeasts are common in floral nectar across a diversity of habitats and may shape (and be shaped by) pollinator visitation, with implications for plant fitness and floral evolution. J. Bronstein and R. Irwin offered empirical insight into how multispecies interactions shape plant fitness and natural selection on floral traits, including plant interactions with ants, nectar robbers, and other co-flowering plants. One common theme running through these studies is that these nonpollinating floral visitors may impose selection on floral traits that may conflict with or strengthen pollinator-mediated selection. Plant–pollinator interactions occur within the context of a changing world. The next three talks highlighted how anthropogenic factors may affect the ecology of plant–pollinator interactions, with implications for seed production in wild and agricultural plants. T. Knight focused on pollen limitation in invasive vs. native flowering species, using both empirical studies and a meta-analysis. M. Aizen and C. Kremen investigated plant–pollinator interactions in agricultural landscapes. Approximately 35% of crops worldwide require pollinators for production (Kremen et al. 2002). At a global scale, M. Aizen investigated the evidence concerning pollinator shortages in agricultural systems, and how increasing reliance on crops that require pollinators may affect future crop yield. At a local scale, C. Kremen used empirical studies to assess pollen limitation in agricultural systems and discussed the development of a model of pollination services to generate a pollinator source map. The first day of oral presentations was followed by an evening mixer and poster session. The mixer and poster session provided many opportunities for participants to share diverse research perspectives and view some of the most exciting new work in pollination biology. Many of these posters may also be viewed online at the conference web site http://www3.uakron.edu/biology/pollination/ The opening talks on the second day addressed pollinator communities and their host plants. There is growing recognition that plant–pollinator interactions are generalized in nature (Waser et al. 1996) and web-like in structure (Memmott 1999). The Pollination Syndrome Concept, which has drawn much controversy in recent years (Waser et al. 1996, Johnson and Steiner 2000, Fenster et al. 2004), describes convergent sets of floral characters that are presumed to be adaptations to specific types of pollinators. N. Waser developed the framework for a quantitative test of the Pollination Syndrome Concept, and provided an empirical test of the model from six plant–pollinator communities on three continents. J. Ollerton used a biogeographic and phylogenetic approach to the study of plant–pollinator interactions, focusing on a diverse plant genus (Ceropegia, Apocynaceae) and the diversity of flies that pollinate them. Continuing with the exploration of generalization and specialization in pollination systems, T. Roulston and T.-L. Ashman investigated pollinator redundancy across space and time and across studies with implications for pollinator efficiency and pollen limitation of seed production. The next series of talks focused on webs of plant–pollinator interactions and the factors that may determine the structure of the webs, including floral and insect morphology (M. Stang) as well as plant and insect abundance, phenology, and space (D. Vazquez). The conference closed with a series of talks on evolutionary pollination biology with a focus on spatial structure and community composition. While many studies in ecology focus on small spatial scales, pollination biologists must incorporate the spatial structure at which pollinators forage. This spatial structure was convincingly incorporated in studies on trap-lining bees (J. Thomson and K. Ohashi), flowering phenology and pollination success at the landscape scale (G. Kudo), the effects of habitat fragmentation on pollination and outcrossing (R. Whelan), and the ecological and evolutionary implications of competition for pollinators in mixed-species plant stands (R. Mitchell). S. Barrett took a different approach to the study of pollination than many talks in the conference by focusing on the ecology and evolution of wind pollination, shattering many of the conventional wisdoms typically associated with wind pollination. Finally, R. Mitchell tied the conference together by synthesizing the diversity of ecological and evolutionary approaches used and questions addressed, demonstrating the fundamental importance of plant–pollinator interactions to ecology and evolution and the link between ecological and evolutionary disciplines from both the plant's and the pollinator's perspective. The goal of the conference was to unite themes from evolutionary and community disciplines in pollination biology. While the talks themselves were organized into thematic sections, calls for action did emerge that will continue to unite evolutionary and community approaches to the study of pollination biology. We note the following three topic areas, although many others were also discussed: (1) the implications of diverse pollinator communities and behaviors to plant mating patterns and selection on traits; (2) the evolutionary consequences of global environmental change via changes in plant–pollinator interactions; and (3) the importance of temporally and spatially varying interaction webs for (co)evolution among partners. A separate vein of agreement was the recognition of the growing international nature of modern pollination biology. The many excellent international speakers and participants at this meeting highlighted the rapidly growing strength of the science. We encourage readers who would like to read more about this conference to view a forthcoming special issue of Annals of Botany on the Ecology and Evolution of Plant–Pollinator Interactions.}, number={4}, journal={Bulletin of the Ecological Society of America}, publisher={Wiley}, author={Irwin, Rebecca E. and Mitchell, Randall J. and Karron, Jeffrey D.}, year={2008}, month={Oct}, pages={481–484} }
 @article{burkle_irwin_2009, title={The effects of nutrient addition on floral characters and pollination in two subalpine plants, Ipomopsis aggregata and Linum lewisii}, volume={203}, ISSN={1385-0237 1573-5052}, url={http://dx.doi.org/10.1007/s11258-008-9512-0}, DOI={10.1007/s11258-008-9512-0}, number={1}, journal={Plant Ecology}, publisher={Springer Science and Business Media LLC}, author={Burkle, Laura A. and Irwin, Rebecca E.}, year={2009}, pages={83–98} }
 @article{elliott_irwin_adler_williams_2008, title={The nectar alkaloid, gelsemine, does not affect offspring performance of a native solitary bee, <i>Osmia lignaria</i> (Megachilidae)}, volume={33}, ISSN={0307-6946 1365-2311}, url={http://dx.doi.org/10.1111/j.1365-2311.2007.00974.x}, DOI={10.1111/j.1365-2311.2007.00974.x}, abstractNote={Abstract1. The ecology and evolution of foliar‐feeding insects are thought to be closely tied to plant secondary compounds. Although secondary compounds are also abundant in floral nectar, their role in mediating pollinator preference and performance remains relatively unexplored.2. This study tested the effects of an alkaloid, gelsemine, found in the nectar of Carolina jessamine (Gelsemium sempervirensL., Loganiaceae), on the performance of a native solitary bee (Osmia lignaria lignariaSay, Megachilidae). Nectar gelsemine reduces visits from pollinators, includingO. lignaria lignaria, and gelsemine is toxic to vertebrates and possibly non‐native honey bees (Apis melliferaL., Apidae). To test the hypothesis that the deterrent effects of nectar gelsemine reflect negative consequences for pollinator performance,O. lignaria lignariaoffspring provisions were supplemented with nectar containing different gelsemine concentrations. Effects on larval development time, prepupa cocoon mass, adult emergence, and adult mass were measured.3. Nectar gelsemine had no effect on any measure of offspring performance. Thus, although gelsemine deters foraging by adult bees, this behaviour did not optimize offspring performance under the experimental conditions of this study. In contrast, sugar added to nectar treatments increased offspring mass.4. While adult pollinators may avoid nectar with secondary compounds, this could hinder offspring performance by reducing sugar in provisions if nectar is limiting in the environment. Preference‐performance trade‐offs, which are studied extensively with foliar herbivores, have seldom been tested for pollinating plant consumers. Future studies of nectar secondary compounds and insect pollinator preference and performance may help to integrate studies of foliage‐consuming insect herbivores with nectar‐consuming insect pollinators.}, number={2}, journal={Ecological Entomology}, publisher={Wiley}, author={Elliott, Susan E. and Irwin, Rebecca E. and Adler, Lynn S. and Williams, Neal M.}, year={2008}, month={Feb}, pages={298–304} }
 @article{brody_irwin_mccutcheon_parsons_2008, title={Interactions between nectar robbers and seed predators mediated by a shared host plant, Ipomopsis aggregata}, volume={155}, ISSN={0029-8549 1432-1939}, url={http://dx.doi.org/10.1007/s00442-007-0879-8}, DOI={10.1007/s00442-007-0879-8}, abstractNote={Animals that consume plant parts or rewards but provide no services in return are likely to have significant impacts on the reproductive success of their host plants. The effects of multiple antagonists to plant reproduction may not be predictable from studying their individual effects in isolation. If consumer behaviors are contingent on each other, such interactions may limit the ability of the host to evolve in response to any one enemy. Here, we asked whether nectar robbing by a bumblebee (Bombus occidentalis) altered the likelihood of pre-dispersal seed predation by a fly (Hylemya sp.) on a shared host plant, Ipomopsis aggregata (Polemoniaceae). We estimated the fitness consequences of the combined interactions using experimental manipulations of nectar robbing within and among sites. Within sites, nectar robbing reduced the percentage of fruits destroyed by Hylemya. However, the negative effects of robbing on seed production outweighed any advantages associated with decreased seed predation in robbed plants. We found similar trends among sites when we manipulated robbing to all plants within a local population, although the results were not statistically significant. Taken together, our results suggest that seed predation is not independent of nectar robbing. Thus, accounting for the interactions among species is crucial to predicting their ecological effects and plant evolutionary response.}, number={1}, journal={Oecologia}, publisher={Springer Science and Business Media LLC}, author={Brody, Alison K. and Irwin, Rebecca E. and McCutcheon, Meghan L. and Parsons, Emily C.}, year={2008}, pages={75–84} }
 @misc{irwin_2007, title={Plant-Pollinator Interactions: From Specialization to Generalization N. M. Waser, J. Ollerton . 2006. Plant-Pollinator Interactions: From Specialization to Generalization. University of Chicago Press.<i>xii</i>+. 445 15 × 23 cm, softcover, US$45.00. ISBN: 0-226-87400-1.}, volume={14}, ISSN={1195-6860}, url={http://dx.doi.org/10.2980/1195-6860(2007)14[135:pifstg]2.0.co;2}, DOI={10.2980/1195-6860(2007)14[135:pifstg]2.0.co;2}, number={1}, journal={Ecoscience}, publisher={Informa UK Limited}, author={Irwin, Rebecca E.}, year={2007}, month={Mar}, pages={135–136} }
 @article{burkle_irwin_newman_2007, title={Predicting the effects of nectar robbing on plant reproduction: implications of pollen limitation and plant mating system}, volume={94}, ISSN={0002-9122 1537-2197}, url={http://dx.doi.org/10.3732/ajb.94.12.1935}, DOI={10.3732/ajb.94.12.1935}, abstractNote={The outcome of species interactions is often difficult to predict, depending on the organisms involved and the ecological context. Nectar robbers remove nectar from flowers, often without providing pollination service, and their effects on plant reproduction vary in strength and direction. In two case studies and a meta‐analysis, we tested the importance of pollen limitation and plant mating system in predicting the impacts of nectar robbing on female plant reproduction. We predicted that nectar robbing would have the strongest effects on species requiring pollinators to set seed and pollen limited for seed production. Our predictions were partially supported. In the first study, natural nectar robbing was associated with lower seed production inDelphinium nuttallianum, a self‐compatible but non‐autogamously selfing, pollen‐limited perennial, and experimental nectar robbing reduced seed set relative to unrobbed plants. The second study involvedLinaria vulgaris, a self‐incompatible perennial that is generally not pollen limited. Natural levels of nectar robbing generally had little effect on estimates of female reproduction inL. vulgaris, while experimental nectar robbing reduced seed set per fruit but not percentage of fruit set. A meta‐analysis revealed that nectar robbing had strong negative effects on pollen‐limited and self‐incompatible plants, as predicted. Our results suggest that pollination biology and plant mating system must be considered to understand and predict the ecological outcome of both mutualistic and antagonistic plant–animal interactions.}, number={12}, journal={American Journal of Botany}, publisher={Wiley}, author={Burkle, Laura A. and Irwin, Rebecca E. and Newman, Daniel A.}, year={2007}, month={Dec}, pages={1935–1943} }
 @article{irwin_adler_2006, title={Correlations among traits associated with herbivore resistance and pollination: implications for pollination and nectar robbing in a distylous plant}, volume={93}, ISSN={0002-9122 1537-2197}, url={http://dx.doi.org/10.3732/ajb.93.1.64}, DOI={10.3732/ajb.93.1.64}, abstractNote={Plants interact simultaneously with a diversity of visitors, including herbivores and pollinators. Correlations among traits associated with herbivory and pollination may constrain the degree to which plants can evolve in response to any one interactor. Using the distylous plant, Gelsemium sempervirens, we tested the hypothesis that traits typically associated with pollination (distyly) and herbivore resistance (secondary compounds) were phenotypically correlated and examined how these traits influenced plant interactions with floral visitors. The flowers of G. sempervirens are visited by pollinators and a nectar robber, and the leaves and flowers express gelsemine, an alkaloid that is deterrent and sometimes toxic to visitors. Using an observational approach across five populations, we found the thrum floral morph (short‐styled) expressed more leaf gelsemine than the pin morph (long‐styled). Leaf gelsemine concentrations were positively correlated with flower gelsemine; however, there were no correlations between gelsemine and other floral morphological traits. Trait expression influenced pollination more so than robbing. Thrums received two times less pollen than pins. Moreover, across both morphs, pollen receipt was lower in plants that expressed higher levels of leaf gelsemine in two sites. These results imply that traits associated with pollination and herbivore resistance may not be independent.}, number={1}, journal={American Journal of Botany}, publisher={Wiley}, author={Irwin, Rebecca E. and Adler, Lynn S.}, year={2006}, month={Jan}, pages={64–72} }
 @article{mccall_irwin_2006, title={Florivory: the intersection of pollination and herbivory}, volume={9}, ISSN={1461-023X 1461-0248}, url={http://dx.doi.org/10.1111/j.1461-0248.2006.00975.x}, DOI={10.1111/j.1461-0248.2006.00975.x}, abstractNote={AbstractPlants interact with many visitors who consume a variety of plant tissues. While the consequences of herbivory to leaves and shoots are well known, the implications of florivory, the consumption of flowers prior to seed coat formation, have received less attention. Herbivory and florivory can yield different plant, population and community outcomes; thus, it is critical to distinguish between these two types of consumption. Here, we consider the ecological and evolutionary consequences of florivory. A growing number of studies recognize that florivory is common in natural systems and in some cases surpasses leaf herbivory in magnitude and impact. Florivores can affect male and female plant fitness via direct trophic effects and through altered pathways of species interactions. In particular, florivory can affect pollination and have consequences for plant mating and floral sexual system evolution. Plants are not defenceless against florivore damage. Concepts of resistance and tolerance can be applied to plant–florivore interactions. Moreover, extant theories of plant chemical defence, including optimal defence theory, growth rate hypothesis and growth differentiation–balance hypothesis, can be used to make testable predictions about when and how plants should defend flowers against florivores. The majority of the predictions remain untested, but they provide a theoretical foundation on which to base future experiments. The approaches to studying florivory that we outline may yield novel insights into floral and defence traits not illuminated by studies of pollination or herbivory alone.}, number={12}, journal={Ecology Letters}, publisher={Wiley}, author={McCall, Andrew C. and Irwin, Rebecca E.}, year={2006}, month={Oct}, pages={1351–1365} }
 @article{irwin_2006, title={The Consequences of Direct versus Indirect Species Interactions to Selection on Traits: Pollination and Nectar Robbing in <i>Ipomopsis aggregata}, volume={167}, ISSN={0003-0147 1537-5323}, url={http://dx.doi.org/10.1086/499377}, DOI={10.2307/3844755}, abstractNote={Organisms experience a complex suite of species interactions. Although the ecological consequences of direct versus indirect species interactions have received attention, their evolutionary implications are not well understood. I examined selection on floral traits through direct versus indirect pathways of species interactions using the plant Ipomopsis aggregata and its pollinators and nectar robber. Using path analysis and structural equation modeling, I tested competing hypotheses comparing the relative importance of direct (pollinator‐mediated) versus indirect (robber‐mediated) interactions to trait selection through female plant function in 2 years. The hypothesis that provided the best fit to the observed data included robbing and pollination, suggesting that both interactors are important in driving selection on some traits; however, the direction and intensity of selection through robbing versus pollination varied between years. I then increased my scope of inference by assessing traits and species interactions across more years. I found that the potential for temporal variation in the direction and intensity of selection was pronounced. Taken together, results suggest that assessing the broader context in which organisms evolve, including both direct and indirect interactions and across multiple years, can provide increased mechanistic understanding of the diversity of ways that animals shape floral and plant evolution.}, number={3}, journal={The American Naturalist}, publisher={University of Chicago Press}, author={Irwin, Rebecca E.}, year={2006}, month={Mar}, pages={315–328} }
 @article{adler_irwin_2005, title={Comparison of Pollen Transfer Dynamics by Multiple Floral Visitors: Experiments with Pollen and Fluorescent Dye}, volume={97}, ISSN={1095-8290 0305-7364}, url={http://dx.doi.org/10.1093/aob/mcj012}, DOI={10.1093/aob/mcj012}, abstractNote={BACKGROUND AND AIMS
Most plant species are visited by a diversity of floral visitors. Pollen transfer of the four most common pollinating bee species and one nectar-robbing bee of the distylous plant Gelsemium sempervirens were compared.


METHODS
Naturally occurring pollen loads carried by the common floral visitor species of G. sempervirens were compared. In addition, dyed pollen donor flowers and sequences of four emasculated recipient flowers in field cages were used to estimate pollen transfer, and the utility of fluorescent dye powder as an analogue for pollen transfer was determined.


KEY RESULTS
Xylocopa virginica, Osmia lignaria and Habropoda laboriosa carried the most G. sempervirens pollen on their bodies, followed by Bombus bimaculatus and Apis mellifera. However, B. bimaculatus, O. lignaria and H. laboriosa transferred significantly more pollen than A. mellifera. Nectar-robbing X. virginica transferred the least pollen, even when visiting legitimately. Dye particles were strongly correlated with pollen grains on a stigma, and therefore provide a good analogue for pollen in this system. The ratio of pollen : dye across stigmas was not affected by bee species or interactions between bee species and floral morphology. However, dye transfer was more sensitive than pollen transfer to differences in floral morphology.


CONCLUSIONS
The results from this study add to a growing body of literature highlighting that floral visitors vary in pollination effectiveness, and that visitors carrying the most pollen on their bodies may not always be the most efficient at depositing pollen on stigmas. Understanding the magnitude of variability in pollinator quality is one important factor for predicting how different pollinator taxa may influence the evolution of floral traits.}, number={1}, journal={Annals of Botany}, publisher={Oxford University Press (OUP)}, author={Adler, Lynn S. and Irwin, Rebecca E.}, year={2005}, month={Nov}, pages={141–150} }
 @article{adler_irwin_2005, title={ECOLOGICAL COSTS AND BENEFITS OF DEFENSES IN NECTAR}, volume={86}, ISSN={0012-9658}, url={http://dx.doi.org/10.1890/05-0118}, DOI={10.1890/05-0118}, abstractNote={The nectar of many plant species contains defensive compounds that have been hypothesized to benefit plants through a variety of mechanisms. However, the rela- tionship between nectar defenses and plant fitness has not been established for any species. We experimentally manipulated gelsemine, the principal alkaloid of Carolina jessamine (Gelsemium sempervirens ), in nectar to determine its effect on pollinator visitation, nectar robber visitation, and male and female plant reproduction. We found that nectar robbers and most pollinators probed fewer flowers and spent less time per flower on plants with high compared to low nectar alkaloids. High alkaloids decreased the donation of fluorescent dye, an analogue of pollen used to estimate male plant reproduction, to neighboring plants by one-third to one-half. However, nectar alkaloids did not affect female plant reproduction, measured as pollen receipt, fruit set, seed set, and seed mass. The weak effects of nectar alkaloids on female reproduction could represent a balance between the altered behavior of nectar robbers and pollinators, or it could be that neither of these interactions affected plant reproduction. Taken together, these results suggest that secondary compounds in nectar may have more costs than benefits for plants.}, number={11}, journal={Ecology}, publisher={Wiley}, author={Adler, Lynn S. and Irwin, Rebecca E.}, year={2005}, month={Nov}, pages={2968–2978} }
 @article{irwin_strauss_2005, title={Flower Color Microevolution in Wild Radish: Evolutionary Response to Pollinator‐Mediated Selection}, volume={165}, ISSN={0003-0147 1537-5323}, url={http://dx.doi.org/10.1086/426714}, DOI={10.2307/3473147}, abstractNote={Evolutionary ecologists are fundamentally interested in how species interactions affect evolutionary change. We tested the degree to which plant‐pollinator interactions affect the frequency of flower color morphs of Raphanus sativus. Petal color in R. sativus is determined by two independently assorting loci, producing four petal colors (yellow, white, pink, and bronze). We assessed the impact of pollinator discrimination on changes in flower color variation by comparing the frequency of colors produced in the presence (open pollination) versus absence (null pollination) of pollinator discrimination. We also assessed the impact of postpollination and developmental effects on progeny colors using equal pollinations with all four color morphs. Our results from open pollinations found an overrepresentation of yellow progeny in the next generation, when compared with both null pollinations and cumulative ratios based on Hardy‐Weinberg and linkage equilibria assumptions. When these results were combined with those from equal pollinations, the overrepresentation of yellow could be attributed to selection from pollinators. Yet, surveys in the field the following year found no flower color frequency changes in the next generation. These results illustrate that flower color microevolution can be driven by both pollinator discrimination and other nonpollinator selective forces acting during the seed‐to‐adult transition, countering selection imposed by pollinators.}, number={2}, journal={The American Naturalist}, publisher={University of Chicago Press}, author={Irwin, Rebecca E. and Strauss, Sharon Y.}, year={2005}, month={Feb}, pages={225–237} }
 @article{price_waser_irwin_campbell_brody_2005, title={TEMPORAL AND SPATIAL VARIATION IN POLLINATION OF A MONTANE HERB: A SEVEN-YEAR STUDY}, volume={86}, ISSN={0012-9658}, url={http://dx.doi.org/10.1890/04-1274}, DOI={10.1890/04-1274}, abstractNote={Pollination by animals is critical to sexual reproduction of most angiosperms. However, little is known about variation in pollination service to single plant species. We report results of a long-term study of Ipomopsis aggregata, a semelparous montane herb whose flowers are visited by hummingbird and insect pollinators as well as “floral larcenists.” We censused flower visitors over seven summers at permanent study sites separated by several hundred meters, and counted pollen delivered to flowers on a subset of plants observed for visitation. The species composition of the community of visitors varied significantly across years and within the flowering season; sites varied significantly only in the magnitude of parallel annual changes in the visitor community. Rates of flower visitation fluctuated over an order of magnitude or more. Variation in mean stigma pollen load among plants flowering in the same site and year was explained by a causal path model in which visitation rates by pollinators and larcen...}, number={8}, journal={Ecology}, publisher={Wiley}, author={Price, Mary V. and Waser, Nickolas M. and Irwin, Rebecca E. and Campbell, Diane R. and Brody, Alison K.}, year={2005}, month={Aug}, pages={2106–2116} }
 @article{irwin_adler_agrawal_2004, title={Community and Evolutionary Ecology of Nectar<sup>1}, volume={85}, ISSN={0012-9658}, url={http://dx.doi.org/10.1890/03-0717}, DOI={10.1890/03-0717}, abstractNote={EcologyVolume 85, Issue 6 p. 1477-1478 Special Features Community and Evolutionary Ecology of Nectar† R. E. Irwin, R. E. Irwin Guest Editor University of GeorgiaSearch for more papers by this authorL. S. Adler, L. S. Adler Guest Editor Virginia Tech UniversitySearch for more papers by this authorA. A. Agrawal, A. A. Agrawal Special Features Editor University of TorontoSearch for more papers by this author R. E. Irwin, R. E. Irwin Guest Editor University of GeorgiaSearch for more papers by this authorL. S. Adler, L. S. Adler Guest Editor Virginia Tech UniversitySearch for more papers by this authorA. A. Agrawal, A. A. Agrawal Special Features Editor University of TorontoSearch for more papers by this author First published: 01 June 2004 https://doi.org/10.1890/03-0717Citations: 6Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL No abstract is available for this article.Citing Literature Volume85, Issue6June 2004Pages 1477-1478 RelatedInformation}, number={6}, journal={Ecology}, publisher={Wiley}, author={Irwin, R. E. and Adler, L. S. and Agrawal, A. A.}, year={2004}, month={Jun}, pages={1477–1478} }
 @article{cariveau_irwin_brody_garcia‐mayeya_von der ohe_2004, title={Direct and indirect effects of pollinators and seed predators to selection on plant and floral traits}, volume={104}, ISSN={0030-1299 1600-0706}, url={http://dx.doi.org/10.1111/j.0030-1299.2004.12641.x}, DOI={10.1111/j.0030-1299.2004.12641.x}, abstractNote={Although flowering traits are often assumed to be under strong selection by pollinators, significant variation in such traits remains the norm for most plant species. Thus, it is likely that the interactions among plants, mutualists, and other selective agents, such as antagonists, ultimately shape the evolution of floral and flowering traits. We examined the importance of pollination vs pre‐dispersal seed predation to selection on plant and floral characters via female plant‐reproductive success in Castilleja linariaefolia (Scrophulariaceae). C. linariaefolia is pollinated by hummingbirds and experiences high levels of pre‐dispersal seed predation by plume moth and fly larvae in the Rocky Mountains of Colorado, USA, where this work was conducted. We first examined whether female reproduction in C. linariaefolia was limited by pollination. Supplemental pollination only marginally increased components of female reproduction, likely because seed predation masked, in part, the beneficial effects of pollen addition. In unmanipulated populations, we measured calyx length, flower production, and plant height and used path analysis combined with structural equation modeling to quantify their importance to relative seed set through pathways involving pollination vs seed predation. We found that the strength of selection on calyx length, flower production, and plant height was greater for seed predation pathways than for pollination pathways, and one character, calyx length, experienced opposing selection via pollination vs seed predation. These results suggest that the remarkable intraspecific variation in plant and floral characters exhibited by some flowering plants is likely the result of selection driven, at least in part, by pollinators in concert with antagonists, such as pre‐dispersal seed predators. This work highlights the subtle but complex interactions that shape floral and vegetative design in natural ecosystems.}, number={1}, journal={Oikos}, publisher={Wiley}, author={Cariveau, Daniel and Irwin, Rebecca E. and Brody, Alison K. and Garcia‐Mayeya, Lucero Sevillano and Von Der Ohe, Andrea}, year={2004}, month={Jan}, pages={15–26} }
 @article{strauss_irwin_2004, title={Ecological and Evolutionary Consequences of Multispecies Plant-Animal Interactions}, volume={35}, ISSN={1543-592X 1545-2069}, url={http://dx.doi.org/10.1146/annurev.ecolsys.35.112202.130215}, DOI={10.1146/annurev.ecolsys.35.112202.130215}, abstractNote={▪ Abstract  Ecologists and evolutionary biologists are broadly interested in how the interactions among organisms influence their abundance, distribution, phenotypes, and genotypic composition. Recently, we have seen a growing appreciation of how multispecies interactions can act synergistically or antagonistically to alter the ecological and evolutionary outcomes of interactions in ways that differ fundamentally from outcomes predicted by pairwise interactions. Here, we review the evidence for criteria identified to detect community-based, diffuse coevolution. These criteria include (a) the presence of genetic correlations between traits involved in multiple interactions, (b) interactions with one species that alter the likelihood or intensity of interactions with other species, and (c) nonadditive combined effects of multiple interactors. In addition, we review the evidence that multispecies interactions have demographic consequences for populations, as well as evolutionary consequences. Finally, we explore the experimental and analytical techniques, and their limitations, used in the study of multispecies interactions. Throughout, we discuss areas in particular need of future research.}, number={1}, journal={Annual Review of Ecology, Evolution, and Systematics}, publisher={Annual Reviews}, author={Strauss, Sharon Y. and Irwin, Rebecca E.}, year={2004}, month={Dec}, pages={435–466} }
 @article{taylor_irwin_2004, title={Linking economic activities to the distribution of exotic plants}, volume={101}, ISSN={0027-8424 1091-6490}, url={http://dx.doi.org/10.1073/pnas.0405176101}, DOI={10.1073/pnas.0405176101}, abstractNote={The human enterprise is flooding Earth's ecosystems with exotic species. Human population size is often correlated with species introductions, whereas more proximate mechanisms, such as economic activities, are frequently overlooked. Here we present a hypothesis that links ecology and economics to provide a causal framework for the distribution of exotic plants in the United States. We test two competing hypotheses (the population-only and population-economic models) using a national data set of exotic plants, employing a statistical framework to simultaneously model direct and indirect effects of human population and ecological and economic variables. The population-only model included direct effects of human population and ecological factors as predictors of exotics. In contrast, the population-economic model included the direct effects of economic and ecological factors and the indirect effects of human population as predictors of exotics. The explicit addition of economic activity in the population-economic model provided a better explanation for the distribution of exotics than did the population-only model. The population-economic model explained 75% of the variation in the number of exotic plants in the 50 states and provided a good description of the observed number of exotic plants in the Canadian provinces and in other nations in 85% of the cases. A specific economic activity, real estate gross state product, had the strongest positive effect on the number of exotics. The strong influence of economics on exotics demonstrates that economics matter for resolving the exotic-species problem because the underlying causes, and some of the solutions, may lie in human-economic behaviors.}, number={51}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Taylor, Brad W. and Irwin, Rebecca E.}, year={2004}, month={Dec}, pages={17725–17730} }
 @article{strauss_irwin_lambrix_2004, title={Optimal defence theory and flower petal colour predict variation in the secondary chemistry of wild radish}, volume={92}, ISSN={0022-0477 1365-2745}, url={http://dx.doi.org/10.1111/j.1365-2745.2004.00843.x}, DOI={10.1111/j.1365-2745.2004.00843.x}, abstractNote={1 The presence, concentration and composition of plant secondary compounds, which confer plant resistance to herbivores and pathogens, vary greatly both within and among individuals. Optimal defence theory predicts that plant tissues most closely tied to plant fitness should be most defended at the constitutive level, and that more expendable tissues should be inducible with damage. 2 We examined variation in glucosinolate content between leaves and petals, as well as among four petal colour morphs of wild radish, Raphanus sativus . We predicted greater levels of constitutive defences in petals, and greater inducibility of glucosinolates in leaves, based on previous studies that could relate leaves and petals to plant fitness. 3 While, overall, optimal defence predictions were supported, individual glucosinolates differed in both their degree of inducibility as well as in their distribution between tissue types. 4 Petal colour variants differed in their induced responses to damage, but not in their constitutive levels of compounds. Yellow and white morphs, which are preferred by the dominant bee pollinators as well as by herbivores, were generally less inducible than anthocynanin‐containing pink and bronze petal morphs. 5 Pleiotropic effects between petal colour and defence loci, or tight linkage between these loci, may allow pollinators to maintain variation in secondary chemistry, as well as allow herbivores to influence colour morph fitness and prevalence.}, number={1}, journal={Journal of Ecology}, publisher={Wiley}, author={Strauss, Sharon Y. and Irwin, Rebecca E. and Lambrix, Virginia M.}, year={2004}, month={Jan}, pages={132–141} }
 @article{irwin_adler_brody_2004, title={THE DUAL ROLE OF FLORAL TRAITS: POLLINATOR ATTRACTION AND PLANT DEFENSE}, volume={85}, ISSN={0012-9658}, url={http://dx.doi.org/10.1890/03-0390}, DOI={10.1890/03-0390}, abstractNote={Plants are under siege from a diversity of enemies that consume both leaf and floral parts. Plants resist damage to leaves in a variety of ways, and we now have a rich literature documenting how plants defend themselves against herbivore attack. In con- trast, the mechanisms by which plants resist enemies that consume floral parts or resources are much less known, even though damage to floral tissue usually has tighter links to plant fitness than damage to leaf tissue. Many plants experience nectar robbing, whereby floral visitors remove nectar from flowers, often without pollinating. Nectar robbers can reduce plant fitness to degrees comparable to, or even surpassing, reduction by herbivores. How- ever, because nectar attracts both pollinators and nectar robbers, plants face a dilemma in defending against nectar robbers without also deterring pollinators. Here, we extend the conceptual framework of resistance to herbivores to include resistance to nectar robbers, focusing on nectar traits. We review published data and find that an array of nectar traits may deter robbers without deterring pollinators. Although resistance traits against robbers have been broadly identified, the costs and benefits of these traits in terms of plant fitness remain poorly understood. We present data showing that a nectar trait (dilute nectar) might directly, as well as indirectly, benefit plant fitness by deterring nectar-robbing bumble bees of Ipomopsis aggregata without deterring hummingbird pollinators. However, the magni- tude of any plant fitness benefit will depend on the degree to which plants are pollen- vs. resource-limited in a given year. The results of our work offer both conceptual and empirical insight into how plants cope with attack by nonpollinating floral visitors through a relatively unexplored trait, nectar.}, number={6}, journal={Ecology}, publisher={Wiley}, author={Irwin, Rebecca E. and Adler, Lynn S. and Brody, Alison K.}, year={2004}, month={Jun}, pages={1503–1511} }
 @article{irwin_2003, title={Attraction and defense: the role of floral traits for scarlet gilia}, journal={Rocky Mountain Biological Laboratory Newsletter}, author={Irwin, R.E.}, year={2003} }
 @article{irwin_2003, title={IMPACT OF NECTAR ROBBING ON ESTIMATES OF POLLEN FLOW: CONCEPTUAL PREDICTIONS AND EMPIRICAL OUTCOMES}, volume={84}, ISSN={0012-9658}, url={http://dx.doi.org/10.1890/0012-9658(2003)084[0485:ionroe]2.0.co;2}, DOI={10.1890/0012-9658(2003)084[0485:ionroe]2.0.co;2}, abstractNote={Pollen movement within and among plants affects levels of inbreeding and plant fitness as well as the spatial scale of genetic differentiation. Pollen movement has primarily been studied as a function of the direct relationships between plants and pollinators; however, nonpollinating floral visitors, such as some nectar robbers, may have indirect effects on pollen dispersal by altering plant–pollinator interactions. Theory predicts that nectar robbing should have indirect positive effects on plants by increasing pollen dispersal distance and reducing self-pollen transfer (geitonogamy) and inbreeding through changes in pollinator behavior associated with reduced nectar rewards. Here I experimentally tested the indirect effects of the nectar-robbing bumble bee, Bombus occidentalis, on the distance of pollen movement among plants and levels of pollen movement within plants (estimated using powdered fluorescent dyes as pollen analogues) using the self-incompatible, hummingbird-pollinated host, Ipomopsis aggre...}, number={2}, journal={Ecology}, publisher={Wiley}, author={Irwin, Rebecca E.}, year={2003}, month={Feb}, pages={485–495} }
 @article{cayenne engel_irwin_2003, title={Linking pollinator visitation rate and pollen receipt}, volume={90}, ISSN={0002-9122 1537-2197}, url={http://dx.doi.org/10.3732/ajb.90.11.1612}, DOI={10.3732/ajb.90.11.1612}, abstractNote={The majority of flowering plants require animals for pollination, a critical ecosystem service in natural and agricultural systems. However, quantifying useful estimates of pollinator visitation rates can be nearly impossible when pollinator visitation is infrequent. We examined the utility of an indirect measure of pollinator visitation, namely pollen receipt by flowers, using the hummingbird‐pollinated plant, Ipomopsis aggregata (Polemoniaceae). Our a priori hypothesis was that increased pollinator visitation should result in increased pollen receipt by stigmas. However, the relationship between pollinator visitation rate and pollen receipt may be misleading if pollen receipt is a function of both the number of pollinator visits and variation in pollinator efficiency at depositing pollen, especially in the context of variable floral morphology. Therefore, we measured floral and plant characters known to be important to pollinator visitation and/or pollen receipt in I. aggregata (corolla length and width and plant height) and used path analysis to dissect and compare the effect of pollinator visitation rate vs. pollinator efficiency on pollen receipt. Of the characters we measured, pollinator visitation rate (number of times plants were visited multiplied by the mean percentage of flowers probed per visit) had the strongest direct positive effect on pollen receipt, explaining 36% of the variation in pollen receipt. Plant height had a direct positive effect on pollinator visitation rate and an indirect positive effect on pollen receipt. Despite the supposition that floral characters would directly affect pollen receipt as a result of changes in pollinator efficiency, corolla length and width only weakly affected pollen receipt. These results suggest a direct positive link between pollinator visitation rate and pollen receipt across naturally varying floral morphology in I. aggregata. Understanding the relationship between pollinator visitation rate and pollen receipt may be of critical importance in systems where pollinator visitation is difficult to quantify.}, number={11}, journal={American Journal of Botany}, publisher={Wiley}, author={Cayenne Engel, E. and Irwin, Rebecca E.}, year={2003}, month={Nov}, pages={1612–1618} }
 @article{irwin_strauss_storz_emerson_guibert_2003, title={THE ROLE OF HERBIVORES IN THE MAINTENANCE OF A FLOWER COLOR POLYMORPHISM IN WILD RADISH}, volume={84}, ISSN={0012-9658}, url={http://dx.doi.org/10.1890/0012-9658(2003)084[1733:trohit]2.0.co;2}, DOI={10.1890/0012-9658(2003)084[1733:trohit]2.0.co;2}, abstractNote={Plant species exhibiting polymorphisms with respect to flower color are widespread. Our understanding of the selection pressures that may maintain these color polymorphisms has primarily been confined to one set of organisms-pollinators. Yet, selection on flower color may also be driven by other agents, such as herbivores, especially in cases where pollinators and herbivores are using the same or correlated traits to select plants. A wealth of studies have documented pollinator preference for anthocyanin-recessive color morphs (A-; yellow and white flowers) of wild radish, Raphanus sativus, over anthocyanin-dominant morphs (A+; pink and bronze flowers); yet, differences in pollination alone do not explain the maintenance of the flower color polymorphism. Here, we ask whether variation in flower color in R. sativus influences the preference and performance of herbivores for A- flower color morphs vs. A+ flower color morphs in four types of herbivores (generalist and specialist Lepidoptera, slugs, aphids, and thrips). We found that all herbivores except for aphids and thrips preferred flowering A- color morphs compared to A+ morphs of R. sativus. Furthermore, all herbivores except larvae of specialist and generalist Lepidoptera performed better on A- color morphs. Differences in plant secondary chemistry may play a role in differential herbivore preference and performance on the anthocyanin flower color morphs. Chemical analyses of leaf secondary compounds (indole glucosinolates) revealed that A+ color morphs produced higher concentrations of indole glucosinolates than A- morphs in the presence of herbivore damage. Therefore, herbivores may exhibit lower preference for A+ color morphs, and these morphs may support lower herbivore performance because they are heavily defended once damaged. This is the first study, to our knowledge, to document differential preference and performance of herbivores for different flower color morphs. Previous studies have shown that increased herbivore damage can have profound negative direct and indirect effects on the reproduction of R. sativus. The data presented here suggest that differential preference and performance of herbivores for R. sativus color morphs may counter selection on flower color exerted by pollinators.}, number={7}, journal={Ecology}, publisher={Wiley}, author={Irwin, Rebecca E. and Strauss, Sharon Y. and Storz, Shonna and Emerson, Aimee and Guibert, Genevieve}, year={2003}, month={Jul}, pages={1733–1743} }
 @misc{irwin_2002, title={Alpine plants of North America}, volume={49}, number={2}, journal={Plant Science Bulletin}, author={Irwin, R.}, year={2002}, pages={68–69} }
 @article{strauss_rudgers_lau_irwin_2002, title={Direct and ecological costs of resistance to herbivory}, volume={17}, ISSN={0169-5347}, url={http://dx.doi.org/10.1016/s0169-5347(02)02483-7}, DOI={10.1016/s0169-5347(02)02483-7}, abstractNote={Herbivores can consume significant amounts of plant biomass in many environments. Yet plants are not defenseless against such attack. Although defenses might benefit plants in the presence of herbivores, herbivore attack varies both spatially and temporally, and the expression of plant resistance to herbivores can be costly in the absence of plant enemies. Costs can be described as allocation costs, resource-based tradeoffs between resistance and fitness, or as ecological costs, decreases in fitness resulting from interactions with other species. Here, we update the seminal 1996 Bergelson and Purrington review of resistance costs and find that many more studies have documented costs of resistance (sensu lato) than found during the 1996 survey. Eighty-two percent of studies in which genetic background is controlled, demonstrate significant fitness reductions associated with herbivore resistance. We categorize studies by type of resistance, induced or constitutive, by type of cost, and also by the degree to which investigators controlled for genetic background. Recent work has commonly detected both direct resistance costs, such as resource-based tradeoffs, and ecological costs, which depend on interactions with other species.}, number={6}, journal={Trends in Ecology & Evolution}, publisher={Elsevier BV}, author={Strauss, Sharon Y. and Rudgers, Jennifer A. and Lau, Jennifer A. and Irwin, Rebecca E.}, year={2002}, month={Jun}, pages={278–285} }
 @misc{irwin_2002, title={Pollination Biology—Linking Botany and Zoology}, volume={83}, DOI={10.1890/0012-9658(2002)083[1168:PBLBAZ]2.0.CO;2}, abstractNote={EcologyVolume 83, Issue 4 p. 1168-1169 Book Review Pollination Biology—Linking Botany and Zoology Rebecca E. Irwin, Rebecca E. Irwin University of Georgia Institute of Ecology Ecology Building Athens, Georgia 30602 E-mail: rirwin@arches.uga.eduSearch for more papers by this author Rebecca E. Irwin, Rebecca E. Irwin University of Georgia Institute of Ecology Ecology Building Athens, Georgia 30602 E-mail: rirwin@arches.uga.eduSearch for more papers by this author First published: 01 April 2002 https://doi.org/10.1890/0012-9658(2002)083[1168:PBLBAZ]2.0.CO;2Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinkedInRedditWechat No abstract is available for this article. Volume83, Issue4April 2002Pages 1168-1169 RelatedInformation}, number={4}, journal={Ecology}, author={Irwin, R.}, year={2002}, month={Apr}, pages={1168–1169} }
 @article{irwin_maloof_2002, title={Variation in nectar robbing over time, space, and species}, volume={133}, ISSN={0029-8549 1432-1939}, url={http://dx.doi.org/10.1007/s00442-002-1060-z}, DOI={10.1007/s00442-002-1060-z}, number={4}, journal={Oecologia}, publisher={Springer Science and Business Media LLC}, author={Irwin, Rebecca E. and Maloof, Joan E.}, year={2002}, month={Dec}, pages={525–533} }
 @article{irwin_dorsett_2002, title={Volatile Production by Buds and Corollas of Two Sympatric, Confamilial Plants, Ipomopsis aggregata and Polemonium foliosissimum}, volume={28}, DOI={10.1023/A:1014596129601}, journal={Journal of Chemical Ecology}, author={Irwin, R.E. and Dorsett, B.}, year={2002}, pages={565–578} }
 @article{irwin_2001, title={Field and allozyme studies investigating optimal mating success in two sympatric spring-ephemeral plants, Trillium erectum and T. grandiflorum}, volume={87}, ISSN={0018-067X 1365-2540}, url={http://dx.doi.org/10.1046/j.1365-2540.2001.00896.x}, DOI={10.1046/j.1365-2540.2001.00896.x}, abstractNote={A combination of field experiments and allozyme studies was used to test whether two spring-ephemeral plants growing in eastern North America, Trillium erectum and T. grandiflorum (Liliaceae), exhibited an optimal outcrossing distance for fruit and seed production. Furthermore, the spatial genetic structure of the Trillium populations was examined in light of the outcrossing results. In field experiments, recipient plants were pollinated with either self pollen or with pollen from donors growing 1 m, 10 m, 100 m, and 1500 m away. These distances represented crosses between individuals growing within the same population (1 m, 10 m, and 100 m crosses) and between individuals growing in different populations (1500 m crosses). Self-pollinated T. erectum and T. grandiflorum produced 71% and 89% fewer seeds, respectively, than all other outcrossing treatments. However, there were no significant differences among outcrossing treatments for fruit or seed production. As neither T. erectum nor T. grandiflorum exhibited an optimal outcrossing distance for fruit or seed production, it was predicted that populations of the two would not demonstrate strong spatial genetic structure or isolation by distance. The allozyme results only partially supported the patterns revealed in the outcrossing treatments. Populations of T. erectum and T. grandiflorum showed moderate spatial genetic differentiation based on F-statistics, and only T. grandiflorum exhibited significant isolation by distance based on spatial autocorrelation analyses. The lack of optimal outcrossing distances and the patterns of allozyme variation in T. erectum and T. grandiflorum populations may be attributed to a number of factors, including active seed dispersal by ants, rare long-distance gene-flow events, post-pollination and post-fertilization selection, and/or the severity of inbreeding depression.}, number={2}, journal={Heredity}, publisher={Springer Science and Business Media LLC}, author={Irwin, Rebecca E}, year={2001}, month={Aug}, pages={178–189} }
 @misc{irwin_2001, title={Invasive Plants of California Wildlands}, volume={47}, number={4}, journal={Plant Science Bulletin}, author={Irwin, R.}, year={2001}, pages={161–162} }
 @article{irwin_brody_waser_2001, title={The impact of floral larceny on individuals, populations, and communities}, volume={129}, ISSN={0029-8549 1432-1939}, url={http://dx.doi.org/10.1007/s004420100739}, DOI={10.1007/s004420100739}, number={2}, journal={Oecologia}, publisher={Springer Science and Business Media LLC}, author={Irwin, Rebecca E. and Brody, Alison K. and Waser, Nickolas M.}, year={2001}, month={Oct}, pages={161–168} }
 @article{irwin_brody_2000, title={CONSEQUENCES OF NECTAR ROBBING FOR REALIZED MALE FUNCTION IN A HUMMINGBIRD-POLLINATED PLANT}, volume={81}, ISSN={0012-9658}, url={http://dx.doi.org/10.1890/0012-9658(2000)081[2637:CONRFR]2.0.CO;2}, DOI={10.2307/177481}, abstractNote={EcologyVolume 81, Issue 9 p. 2637-2643 Article CONSEQUENCES OF NECTAR ROBBING FOR REALIZED MALE FUNCTION IN A HUMMINGBIRD-POLLINATED PLANT Rebecca E. Irwin, Rebecca E. Irwin Biology Department, Marsh Life Science Building, University of Vermont, Burlington, Vermont 05405 USA and The Rocky Mountain Biological Laboratory, PO Box 519, Crested Butte, Colorado 81224 USA Present address: Section of Evolution and Ecology, 2320 Starer Hall, One Shields Avenue, University of California, Davis, California 95616 USA. E-mail: reirwin@ucdavis.eduSearch for more papers by this authorAlison K. Brody, Alison K. Brody Biology Department, Marsh Life Science Building, University of Vermont, Burlington, Vermont 05405 USA and The Rocky Mountain Biological Laboratory, PO Box 519, Crested Butte, Colorado 81224 USASearch for more papers by this author Rebecca E. Irwin, Rebecca E. Irwin Biology Department, Marsh Life Science Building, University of Vermont, Burlington, Vermont 05405 USA and The Rocky Mountain Biological Laboratory, PO Box 519, Crested Butte, Colorado 81224 USA Present address: Section of Evolution and Ecology, 2320 Starer Hall, One Shields Avenue, University of California, Davis, California 95616 USA. E-mail: reirwin@ucdavis.eduSearch for more papers by this authorAlison K. Brody, Alison K. Brody Biology Department, Marsh Life Science Building, University of Vermont, Burlington, Vermont 05405 USA and The Rocky Mountain Biological Laboratory, PO Box 519, Crested Butte, Colorado 81224 USASearch for more papers by this author First published: 01 September 2000 https://doi.org/10.1890/0012-9658(2000)081[2637:CONRFR]2.0.CO;2Citations: 54 Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinkedInRedditWechat Abstract The effects of nectar robbers on plants and their mutualistic pollinators are poorly understood due, in part, to the paucity of studies examining male reproductive success in nectar-robbed plants. Here we measured the effects of a nectar-robbing bumblebee, Bombus occidentalis, on realized male reproductive success (seeds sired) in a hummingbird-pollinated plant, Ipomopsis aggregata. To determine the effects of nectar robbing on paternity, we used a series of experimental populations of plants containing a known allozyme marker. In each population, we experimentally controlled the levels of nectar robbing on each I. aggregata plant by cutting a hole in the corolla with dissecting scissors and removing nectar with a micro-capillary tube. We measured hummingbird-pollinator foraging behavior and fruit and seed production (maternal function) for each plant. We then genotyped seeds for the allozyme marker to determine the number of seeds sired by plants with known levels of robbing. Heavy nectar robbing (> 80% of flowers robbed) significantly reduced the number of seeds sired, as well as the number of seeds produced due to pollinator avoidance of heavily robbed plants. Total plant reproduction, both male and female contributions, were reduced by 50% due to high levels of robbing. To date, no other studies have measured the effects of nectar robbing on realized male function (number of seeds sired). Ours is the first study to demonstrate that robbing can simultaneously decrease realized male reproductive success as well as female reproductive success, and that the effects are incurred indirectly through pollinator avoidance of robbed plants. Citing Literature Volume81, Issue9September 2000Pages 2637-2643 RelatedInformation}, number={9}, journal={Ecology}, publisher={Wiley}, author={Irwin, Rebecca E. and Brody, Alison K.}, year={2000}, month={Sep}, pages={2637–2643} }
 @article{irwin_2000, title={Hummingbird avoidance of nectar‐robbed plants: spatial location or visual cues}, volume={91}, ISSN={0030-1299 1600-0706}, url={http://dx.doi.org/10.1034/j.1600-0706.2000.910311.x}, DOI={10.1034/j.1600-0706.2000.910311.x}, abstractNote={Broad‐tailed and rufous hummingbirds avoid plants and flowers that have recently been visited by nectar‐robbing bees. However, the cues the hummingbirds use to make such choices are not known. To determine the proximate cues hummingbirds use to avoid visiting nectar‐robbed plants, I conducted multiple field experiments and one aviary study using the nectar‐robbed, hummingbird‐pollinated plant Ipomopsis aggregata. In the first field experiment, free‐flying hummingbirds were presented with plants in which I manipulated nectar volume and the presence of nectar‐robber holes. Hummingbirds visited significantly more plants with nectar and probed more available flowers on those plants, regardless of the presence of nectar‐robber holes. Thus, I hypothesized that hummingbirds may avoid robbed plants based on their spatial memory of unrewarding plants and/or visual cues that nectar absence provides. In an aviary study, I removed spatial cues by re‐randomizing the position of plants after each hummingbird‐foraging bout, but hummingbirds still selected plants with nectar. Nectar may provide a visual cue in I. aggregata flowers because corollas are translucent, and nectar is visible through the side of the corolla. To determine if hummingbirds use this visual cue to avoid plants with no nectar, I masked corolla translucence in a field study by painting flowers with acrylic paint. Hummingbirds still visited significantly more plants with nectar and probed more flowers on those plants, whether or not the corollas were painted. These results suggest that hummingbirds use nectar as a proximate cue to locate and avoid non‐rewarding, nectar‐robbed plants, even in the absence of spatial cues and simple visual cues.}, number={3}, journal={Oikos}, publisher={Wiley}, author={Irwin, Rebecca E.}, year={2000}, month={Dec}, pages={499–506} }
 @article{irwin_2000, title={Morphological variation and female reproductive success in two sympatric <i>Trillium</i> species: evidence for phenotypic selection in <i>Trillium erectum</i> and <i>Trillium grandiflorum</i> (Liliaceae)}, volume={87}, ISSN={0002-9122 1537-2197}, url={http://dx.doi.org/10.2307/2656907}, DOI={10.2307/2656907}, abstractNote={I investigated the mating systems and phenotypic variation of two sympatric spring ephemerals, Trillium erectum and T. grandiflorum (Liliaceae), and phenotypic selection acting through female reproductive success for 11 morphological characters in five sympatric populations of the two species. I examined the degree of self‐compatibility, pollinator‐visitation rates, and pollen limitation of fruit and seed production in both species. Both Trillium species were self‐compatible, but outcrossed flowers produced more successful fruits and seeds than self‐pollinated flowers. Pollinator‐visitation rates to the two species were low compared to other insect‐pollinated spring ephemerals. In addition, both T. erectum and T. grandiflorum experienced pollen limitation in fruit and/or seed production; however, levels of fecundity in both species may be influenced by resource availability as well. I found significant phenotypic variation in 11 morphological characters within and among the five study populations. The sizes of all morphological characters were positively correlated. In general, larger T. erectum and T. grandiflorum produced more seeds. Phenotypic selection analysis revealed that direct and indirect selection acted on the size of morphological characters for both species. But there was no detectable selection acting on plant shape. This study reveals that variation in plant size exists within and among populations of both species, and this variation is associated with variance in female reproductive success. Spatial and temporal variation in pollinator and/or resource abundance may play a role in the phenotypic variation exhibited by both Trillium species.}, number={2}, journal={American Journal of Botany}, publisher={Wiley}, author={Irwin, Rebecca E.}, year={2000}, month={Feb}, pages={205–214} }
 @article{irwin_brody_1999, title={Nectar-Robbing Bumble Bees Reduce the Fitness of Ipomopsis aggregata (Polemoniaceae)}, volume={80}, ISSN={0012-9658}, url={http://dx.doi.org/10.2307/176558}, DOI={10.2307/176558}, number={5}, journal={Ecology}, publisher={Wiley}, author={Irwin, Rebecca E. and Brody, Alison K.}, year={1999}, month={Jul}, pages={1703} }
 @article{jones_reithel_irwin_1998, title={A trade-off between the frequency and duration of bumblebee visits to flowers}, volume={117}, ISSN={0029-8549 1432-1939}, url={http://dx.doi.org/10.1007/s004420050644}, DOI={10.1007/s004420050644}, number={1-2}, journal={Oecologia}, publisher={Springer Science and Business Media LLC}, author={Jones, Kristina N. and Reithel, Jennifer S. and Irwin, Rebecca E.}, year={1998}, month={Nov}, pages={161–168} }
 @article{irwin_brody_1998, title={Nectar robbing in Ipomopsis aggregata  : effects on pollinator behavior and plant fitness}, volume={116}, ISSN={0029-8549 1432-1939}, url={http://dx.doi.org/10.1007/s004420050617}, DOI={10.1007/s004420050617}, number={4}, journal={Oecologia}, publisher={Springer Science and Business Media LLC}, author={Irwin, Rebecca E. and Brody, Alison K.}, year={1998}, month={Oct}, pages={519–527} }
 @misc{irwin, title={Of birds and bees: feuds over nectar}, journal={The Hummingbird Connection.}, publisher={The Hummingbird Connection}, author={Irwin, R.E.} }