Rebecca E. Irwin

Synergistic effects of floral phytochemicals against a bumble bee parasite

Abstract Floral 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.

Landscape predictors of pathogen prevalence and range contractions in US bumblebees

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.

Nectar and Pollen Phytochemicals Stimulate Honey Bee (Hymenoptera: Apidae) Immunity to Viral Infection

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.

Species-specific diagnostics of Apis mellifera trypanosomatids: A nine-year survey (2007–2015) for trypanosomatids and microsporidians in Serbian honey bees

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.

Venus Flytrap Rarely Traps Its Pollinators

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.

Interannual bumble bee abundance is driven by indirect climate effects on floral resource phenology

Climate 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 equationxa0modelling 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 8xa0years, bee abundances were driven primarily by the indirect effects of climate on the temporal distribution of floral resources. Over 43xa0years, 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.

The behavioral ecology of nectar robbing: why be tactic constant?

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.

Phenotypic selection on floral traits in an urban landscape

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.

Direct and indirect effects of episodic frost on plant growth and reproduction in subalpine wildflowers

Frost 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 inxa0situ. 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.

Pollen limitation and reproduction of three plant species across a temperature gradient in western Greenland

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.