Climate change increases flowering duration, driving phenological reassembly and elevated co-flowering richness.

Changes to flowering phenology are a key response of plants to climate change. However, we know little about how these changes alter temporal patterns of reproductive overlap (i.e. phenological reassembly). We combined long-term field (1937-2012) and herbarium records (1850-2017) of 68 species in a flowering plant community in central North America and used a novel application of Bayesian quantile regression to estimate changes to flowering season length, altered richness and composition of co-flowering assemblages, and whether phenological shifts exhibit seasonal trends. Across the past century, phenological shifts increased species' flowering durations by 11.5 d on average, which resulted in 94% of species experiencing greater flowering overlap at the community level. Increases to co-flowering were particularly pronounced in autumn, driven by a greater tendency of late season species to shift the ending of flowering later and to increase flowering duration. Our results demonstrate that species-level phenological shifts can result in considerable phenological reassembly and highlight changes to flowering duration as a prominent, yet underappreciated, effect of climate change. The emergence of an autumn co-flowering mode emphasizes that these effects may be season-dependent.

Resource Availability Affects Seasonal Trajectories of Population-Level Learning.

AbstractEnvironmental effects on learning are well known, such as cognition that is mediated by nutritional consumption. Less known is how seasonally variable environments affect phenological trajectories of learning. Here, we test the hypothesis that nutritional availability affects seasonal trajectories of population-level learning in species with developmentally plastic cognition. We test this in bumble bees (Apidae: Bombus), a clade of eusocial insects that produce individuals at different time points across their reproductive season and exhibit organ developmental plasticity in response to nutritional consumption. To accomplish this, we develop a theoretical model that simulates learning development across a reproductive season for a colony parameterized with observed life history data. Our model finds two qualitative seasonal trajectories of learning: (1) an increase in learning across the season and (2) no change in learning across the season. We also find these two qualitative trajectories revealed by empirical learning data; the proportion of workers successfully completing a learning test increases across a season for two bumble bee species (Bombus auricomus, Bombus pensylvanicus) but does not change for another three (Bombus bimaculatus, Bombus griseocollis, Bombus impatiens). This study supports the novel consideration that resources affect seasonal trajectories of population-level learning in species with developmentally plastic cognition.

Beyond the usual climate? Factors determining flowering and fruiting phenology across a genus over 117 years.

PREMISE: Although changes in plant phenology are largely attributed to changes in climate, the roles of other factors such as genetic constraints, competition, and self-compatibility are underexplored. METHODS: We compiled >900 herbarium records spanning 117 years for all eight nominal species of the winter-annual genus Leavenworthia (Brassicaceae). We used linear regression to determine the rate of phenological change across years and phenological sensitivity to climate. Using a variance partitioning analysis, we assessed the relative influence of climatic and nonclimatic factors (self-compatibility, range overlap, latitude, and year) on Leavenworthia reproductive phenology. RESULTS: Flowering advanced by ~2.0 days and fruiting by ~1.3 days per decade. For every 1°C increase in spring temperature, flowering advanced ~2.3 days and fruiting ~3.3 days. For every 100 mm decrease in spring precipitation, each advanced ~6-7 days. The best models explained 35.4% of flowering variance and 33.9% of fruiting. Spring precipitation accounted for 51.3% of explained variance in flowering date and 44.6% in fruiting. Mean spring temperature accounted for 10.6% and 19.3%, respectively. Year accounted for 16.6% of flowering variance and 5.4% of fruiting, and latitude for 2.3% and 15.1%, respectively. Nonclimatic variables combined accounted for <11% of the variance across phenophases. CONCLUSIONS: Spring precipitation and other climate-related factors were dominant predictors of phenological variance. Our results emphasize the strong effect of precipitation on phenology, especially in the moisture-limited habitats preferred by Leavenworthia. Among the many factors that determine phenology, climate is the dominant influence, indicating that the effects of climate change on phenology are expected to increase.

Climate change is associated with increased allocation to potential outcrossing in a common mixed mating species.

PREMISE: Although the balance between cross- and self-fertilization is driven by the environment, no long-term study has documented whether anthropogenic climate change is affecting reproductive strategy allocation in species with mixed mating systems. Here, we test whether the common blue violet (Viola sororia; Violaceae) has altered relative allocation to the production of potentially outcrossing flowers as the climate has changed throughout the 20th century. METHODS: Using herbarium records spanning from 1875 to 2015 from the central United States, we quantified production of obligately selfing cleistogamous (CL) flowers and potentially outcrossing chasmogamous (CH) flowers by V. sororia, coupled these records with historic temperature and precipitation data, and tested whether changes to the proportion of CL flowers correlate with temporal climate trends. RESULTS: We find that V. sororia progressively produced lower proportions of CL flowers across the past century and in environments with lower mean annual temperature and higher total annual precipitation. We also find that both CL and CH flower phenology has advanced across this time period. CONCLUSIONS: Our results suggest that V. sororia has responded to lower temperatures and greater water availability by shifting reproductive strategy allocation away from selfing and toward potential outcrossing. This provides the first long-term study of how climate change may affect relative allocation to potential outcrossing in species with mixed mating systems. By revealing that CL flowering is associated with low water availability and high temperature, our results suggest the production of obligately selfing flowers is favored in water limited environments.

Intraspecific Variation in Worker Body Size Makes North American Bumble Bees (Bombus spp.) Less Susceptible to Decline.

Population declines have been documented in approximately one-third of bumble bee species. Certain drivers of these declines are known; however, less is known about the interspecific trait differences that make certain species more susceptible to decline. Two traits that have implications for responding to rapidly changed environments may be particularly consequential for bumble bee populations: intraspecific body size variation and brain size. Bumble bee body size is highly variable and is likely adaptive at the colony level, and brain size correlates with cognitive traits (e.g., behavioral plasticity) in many groups. Trait variation and plasticity may buffer species against negative effects of rapidly changed environments. Using phylogenetically controlled analyses of 31 North American bumble bee species, we find that higher intraspecific body size variation is associated with species having increased their relative abundance over time. However, this variation does not significantly interact with tongue length, another trait thought to influence bees' decline susceptibility. Head size, a proxy for brain size, is not correlated with change in relative abundance. Our results support the hypothesis that variation in body size makes species less susceptible to decline in rapidly altered environments and suggests that this variation is important to the success of bumble bee populations.

Bumble bees exhibit body size clines across an urban gradient despite low genetic differentiation.

Environmental heterogeneity resulting from human-modified landscapes can increase intraspecific trait variation. However, less known is whether such phenotypic variation is driven by plastic or adaptive responses to local environments. Here, we study five bumble bee (Apidae: Bombus) species across an urban gradient in the greater Saint Louis, Missouri region in the North American Midwest and ask: (1) Can urban environments induce intraspecific spatial structuring of body size, an ecologically consequential functional trait? And, if so, (2) is this body size structure the result of plasticity or adaptation? We additionally estimate genetic diversity, inbreeding, and colony density of these species-three factors that affect extinction risk. Using ≥ 10 polymorphic microsatellite loci per species and measurements of body size, we find that two of these species (Bombus impatiens, Bombus pensylvanicus) exhibit body size clines across the urban gradient, despite a lack of population genetic structure. We also reaffirm reports of low genetic diversity in B. pensylvanicus and find evidence that Bombus griseocollis, a species thought to be thriving in North America, is inbred in the greater Saint Louis region. Collectively, our results have implications for conservation in urban environments and suggest that plasticity can cause phenotypic clines across human-modified landscapes.

Equivalent learning, but unequal participation: Male bumble bees learn comparably to females, but participate in cognitive assessments at lower rates.

Sex-specific cognitive abilities are well documented. These can occur when sexes engage in different ecological contexts. Less known is whether different ecological contexts can also drive sex-specific participation rates in behavioral tests. Here, we explore this question in bumble bees, a group of eusocial insects where worker females and males exhibit stark socioecological differences. Among myriad colony maintenance tasks, workers forage for themselves and developing brood, while males forage only for themselves while mate-searching. Following upon previous studies suggesting no sex differences in bumble bee learning, we test the hypothesis that despite having equivalent associative learning abilities, males participate in cognitive assessments offering nutritional rewards at lower rates. Testing > 500 bees from nine colonies in a differential conditioning protocol, we find support for our hypothesis. An equivalent proportion of workers and males successfully completed our cognitive assessment, while a significantly lower proportion of males participated in the entire protocol. Unequal participation is a perennial issue in the behavioral sciences, limiting sample size and potentially biasing results. Our results suggest that to understand the true range of variation in cognition, sex-differences in participation must be accounted for.